Conservation By Proxy

conservation by proxy

Large mammalian carnivores, such as this jaguar, are used as proxy species to pursue many different agendas in conservation.

Conservation by Proxy indicator, umbrella, keystone, flagship, and other surrogate species

Tim Caro Illustrated by Sheila Girling

Washington | Covelo | London

Copyright © 2010 Island Press All rights reserved under International and Pan-American Copyright Conventions. No part of this book may be reproduced in any form or by any means without permission in writing from the publisher: Island Press, 1718 Connecticut Avenue NW, Suite 300, Washington, DC 20009. Island Press is a trademark of The Center for Resource Economics.

Library of Congress Cataloging-in-Publication Data Caro, T. M. (Timothy M.) Conservation by Proxy : Indicator, umbrella, keystone, flagship, and other surrogate species / Tim Caro ; Illustrated by Sheila Girling. p. cm. Includes bibliographical references and index. ISBN-13: 978-1-59726-192-0 (cloth : alk. paper) ISBN-10: 1-59726-192-0 (cloth : alk. paper) ISBN-13: 978-1-59726-193-7 (pbk. : alk. paper) ISBN-10: 1-59726-193-9 (pbk. : alk. paper) 1. Conservation of natural resources. 2. Environmental protection. 3. Globalization. I. Girling, Sheila. II. Title. S936.C37 2010 333.95′16—dc22 2010008855

Design and typesetting by Karen Wenk Font: Galliard Printed on recycled, acid-free paper

Manufactured in the United States of America 10 9 8 7 6 5 4 3 2 1

You can’t always get what you want But if you try sometimes you just might find You get what you need. —Mick Jagger and Keith Richards

table of contents

xv

Preface INTRODUCTION Chapter 1

Buzzwords in Conservation Biology Shortcuts Biodiversity Usage Documentation Remarkable species Scale Surrogate species in systematic conservation Taxonomy of surrogate species Other terms Difficulties in surrogate typology Loose definitions Lax terminology Multiple applications and purpose Using the same species for two surrogate tasks Hidden agendas and research displacement activities Summary

1 1 3 3 8 8 9 13 15 16 17 17 22 23 26 26 27

DISTRIBUTION OF BIODIVERSITY Chapter 2

Species Indicators of Biodiversity at a Large Scale A big picture Congruency of species richness Environmental surrogates Higher taxa Congruency of endemism Congruency of rarity Congruency of threatened species

31 31 32 36 37 39 42 43

x Table of Contents Complementarity and congruency Concordance between different measures of biodiversity Global scale Continental scale Complementarity Biodiversity distribution and protected areas Practical application Summary

45 50 50 51 53 53 57 58

RESERVE SITE SELECTION Chapter 3

Species Indicators of Biodiversity in Reserve Selection A smaller scale Cross-taxon congruence of species richness Within-taxon congruence of species richness Taxon subsets Higher taxa Morphospecies Congruency of endemism, congruency of rarity, and congruency of threatened species Concordance between measures of biodiversity Species richness and endemism Species richness and rarity Species richness and threatened species Biodiversity metrics Congruency of complementarity Species richness Other biodiversity measures Persistence Higher taxa Protected area coverage Marine reserve prioritization Environmental surrogates Combining environmental and taxonomic surrogates Practical issues Summary

61 61 62 66 68 68 71 72 74 74 76 78 78 79 79 82 83 84 86 89 90 94 95 96

RESERVE DESIGN AND MANAGEMENT Chapter 4

Umbrella Species and Landscape Species Three conservation goals

99 99

Table of Contents xi Lambeck’s insight Umbrella species by taxon Plants Invertebrates Mammals Birds Choosing an appropriate umbrella species Problems with umbrella species Management implications Landscape species Summary

Chapter 5

Keystone, Engineering, and Foundation Species The keystone species concept Classic keystone species Wider scope Mesopredator release in temperate ecosystems Ecological meltdown in the neotropics Keystone introductions Removing invasive species Problems with using keystone species as a conservation tool Reasons for continuing to use keystone species Ecosystem engineers Mechanisms of habitat modification Examples of ecosystem engineers Difficulties in using ecosystem engineers in conservation Advantages of ecosystem engineers Foundation species Management issues Summary

102 103 103 105 106 108 113 117 119 120 125

127 127 127 129 132 134 136 138 139 142 143 144 146 151 153 153 154 156

SPECIES INDICATORS OF ANTHROPOGENIC CHANGE Chapter 6

Environmental Indicator Species Ecosystem health and biological integrity Environmental indicators Sentinel species Examples of the uses of environmental indicator species Marine pollution Freshwater pollution River modification Marine fisheries

159 159 162 167 169 169 171 174 177

xii Table of Contents

Chapter 7

Climate change in marine ecosystems Proliferation and obfuscation of terms Summary

181 184 185

Ecological-Disturbance Indicator Species

189

Effects of disturbance Proposed criteria for indicator species Single species and species-groups as indicators of disturbance Single species Species-groups Examples of the use of species-groups in documenting effects of land-use change Forest fragmentation: BDFFP Countryside biogeography Tropical plantations Exurban USA Changes in populations over time Determining the number of species-groups Management pointers Summary

Chapter 8

Cross-Taxon-Response Indicator Species Habitat alteration Fora for cross-taxon-response indicator species Land-use changes Agricultural landscapes Management areas Intraguild-response indicator species Population changes Management indicator species Difficulties with the MIS concept Early warnings Substitute species Problems with cross-taxon-response indicator species Summary

189 190 194 194 196 197 197 203 206 209 210 211 213 214

217 217 219 219 224 227 228 229 230 233 234 238 239 242

PROMOTING CONSERVATION Chapter 9

Flagship Species Characteristics of flagship species Multiple objectives

245 245 246

Table of Contents xiii Are flagship species successful? Public awareness Raising funds Reserve establishment Qualities of flagship species Iconic species What next? Summary

249 249 251 251 257 258 259 260

SUMMARY OF CONCEPTS AND COST-EFFECTIVENESS Chapter 10 Surrogate Species in the Real World Surrogate categories Synopsis Multi-surrogacy Predictive power of surrogate species Distribution of biodiversity Reserve site selection Reserve design and management Species indicators of anthropogenic change Promoting conservation Wrap-up Summary

263 263 264 268 270 271 274 277 278 281 283 284

References

287

Scientific Names of Species Mentioned in the Text

355

Subject Index

365

California blue mussels completely cover littoral-zone rock faces, providing shelter for many species of marine invertebrates and microorganisms. Protecting these influential engineering species consequently conserves habitat used by numerous other species. (Drawing by Sheila Girling.)

preface

Mention “umbrella species” or “flagship species” and people will nod their heads sagely, but ask them to tell you what these phrases mean and they will mumble something incoherent. Talk to nature reserve managers about “keystone species” and they will expostulate about important species in the ecosystem. Go to a conservation conference and you will hear “focal” and “indicator species” as catchwords thrown about with panache but little substance. Everyone is using these species-terms as shortcuts to achieving conservation goals, but few really know what they signify or whether they are of any real use as conservation tools. I wanted to write a book about surrogate species—that is, species that are used to represent other species or aspects of the environment to obtain a conservation objective—for three reasons. First, I wished to be clear as to what these buzzwords mean. Beginning in 1999, I had written several papers about surrogate species but had never completely clarified the differences and overlap among these terms. I knew that I was confused, and I suspected others might be too. Second, I wanted to help people evaluate whether conservation shortcuts had sound biological foundations. It is important to clarify what conservation tools can and cannot achieve, because political decisions with long-lasting ramifications for conservation are being made using these ideas and so we need to know their biological limitations. I had a nagging feeling that buzzwords are often used in conservation because they are fashionable and attract attention, but I wanted to see whether they really represented underlying biological patterns. Third, I wanted to remind conservation practitioners of the conservation settings in which these terms are most commonly used, so that they could immediately place them in context when they heard them next. In short, my objective was to write a concise reference book in which conservation biologists and conservation managers could consult theory and evidence underlying surrogate species concepts. The book is timely because of the increasing use and proliferation of surrogate buzzwords in conservation biology, the absence of any central clearing house that defines and

xv

xvi Preface

scrutinizes their usefulness, and the urgent necessity to understand whether decision makers can go on employing these concepts with confidence. I am particularly grateful to Toby Gardner for many e-mail discussions and for reading and commenting on the whole manuscript; the book is much better as a consequence. I also thank Monique Borgerhoff Mulder and Tim Davenport for after-dinner advice; the University of California Davis library system for enabling me to read their reprints from the other side of the world; Barbara Dean, Mike Fleming, Erin Johnson, Maureen Gately, and Sharis Simonian at Island Press for guidance; Thomas Sears for help with the figures; my mother, Sheila Girling, for the charming drawings; the Tanzania Wildlife Research Institute and Commission for Science and Technology for making it possible to live in Tanzania; and the people of Msasani and members of the Gymkhana Squash Club, Dar es Salaam, and regulars at the Drop Shot Bar there for their hospitality while I wrote this book. Tim Caro March 1, 2010

Confusion bedevils surrogate species terminology. Focal species, for instance, is used in a well-defined, specific sense but is also used to refer to any species that is being studied, such as this gray wolf. (Drawing by Sheila Girling.)

Chapter 1

Buzzwords in Conservation Biology

Shortcuts The goal of conservation biology is to stop or delay the extinction of plant and animal populations and to prevent or slow habitat destruction. As populations, species, and habitats are under threat in so many places, we are forced to make difficult decisions about where to focus conservation attention. Ideally, detailed study should precede important decisions, especially those that have long-term ramifications for conservation, but four factors prohibit this: the complexity of nature prevents accurate appraisal of all its aspects, the scale of the biodiversity crisis is vast, political decisions must be made rapidly, and there is a severe shortage of funds. Consequently, conservation scientists are compelled to take shortcuts to identify and solve problems. These involve using satellite imagery to monitor environmental change, modeling population responses to anthropogenic pressure, interviewing people about their activities, garnering expert opinion about species’ distributions and the threats they face, and monitoring subsets of species. Subsets may act as proxies for the presence of others, and may help us in deciding where to set up protected areas, in measuring plant and animal community responses to anthropogenic change, and in raising conservation awareness. They are called surrogate species or surrogate taxa, which I define as “species that are used to represent other species or aspects of the environment to attain a conservation objective” (see also Wiens et al. 2008). 1

2 conservation by proxy

Surrogates may be species that represent the whole pool of species, or those that represent subsets of the species pool, or they may be speciesgroups that represent the species pool (see Fig. 1-1). All of these fall under the rubric of surrogate species in this book. Broadly, surrogates are likely to be most useful when the number of species being protected or monitored is uncertain, or the spatial extent of the task is intermediate in size (Wiens et al. 2008). When the area or number of species is very small, individual species can sometimes be considered one by one, and when the area or number of species is very large, surrogate species may be unable to represent the variety of taxa or habitats present and so may not be helpful. Spatial scale is thus very important in the science of surrogate species. At its heart, the surrogate species concept relies on extrapolation, from group A to group B, from area A to area B, from subgroup to group, from smaller to larger scale, sample to inventory, habitat to inventory, and so on (Hammond 1995). The key issue is whether such extrapolations are valid. Until we know this, the surrogate species concept is a risky gambit because we may be making unreliable approximations of the larger picture. Nevertheless, perhaps because surrogate terms are catchy shorthand expressions and have now become conservation buzzwords, unreliable and ill-conceived surrogate species continue to be proposed in conservation workshops, in meetings, and in the literature, potentially affecting important management decisions without careful thought as to what such terms really signify in nature and without considering the burden that they carry for conserving species and habitats. Moreover, surrogate concepts are often interchanged,

Figure 1-1. The hierarchical relation between the species pool of interest, species groups, and surrogate species. Surrogate species may be used either to represent the species pool as a whole or to represent subsets of that pool designated by species groups, or the groups themselves may be used as distillations of the larger species pool. (Reprinted from Wiens et al. 2008.)

Buzzwords in Conservation Biology 3

elided, or just used incorrectly, generating a loose terminology that is confusing to laypersons, wildlife managers, and conservation scientists alike. In short, buzzwords in conservation are useful only if they are clearly defined, address clear objectives, and prove themselves to be effective. I start this chapter by introducing issues of biodiversity and scale, then outline the variety of ways surrogate species are used in conservation, and present five different problems in their application. This chapter provides a sketch of how surrogate concepts are brought into play and misused in conservation science.

Biodiversity Usage Biological diversity or biodiversity (Wilson 1992; Harper & Hawksworth 1995) “means the variability among living organisms from all sources including, inter alia, terrestrial, marine, and other aquatic systems, and the ecological complexes of which they are part; this includes diversity within species, between species, and of ecosystems” (Heywood 1995, 8; see also OTA 1987; Hunter 1996; Hubbell 2001; Groves et al. 2002; and Magurran 2004). The concept captures variability in biological systems from genes to communities but in practice centers on species richness (i.e., the number of species present) in an area. Species richness is reasonably precise (at least for animals), relatively easy to measure, and is generally assumed to play a positive role in ecosystem dynamics. Some people erroneously equate species richness with α diversity (i.e., the number of species in a homogeneous habitat), but it can also refer to β diversity, the difference in composition of species between habitats located in close proximity in the same landscape (also referred to as species turnover or community dissimilarity, Whittaker 1960; Su et al. 2004). Measures of β diversity can be quantified in several ways, using Jaccard’s coefficient or percentage similarity, for example. Alpha diversity increases with the size of the area sampled, whereas β diversity declines because fewer new species are encountered; γ diversity refers to the total number of species in a given region. Biodiversity is also measured using combinatorial measures of richness and abundance (Maclaurin & Sterelny 2008), allowing species community structure and composition to be assessed using measures such as the Q statistic, Simpson’s index, and Generalized Dissimilarity Modeling (Ferrier et al. 2007).

4 conservation by proxy

Biodiversity is used in other senses as well. Endemic species have relatively small geographic ranges (e.g., an average of 64,561 km2 for 147 endemic Mexican mammals versus 427,183 km2 for 314 nonendemics, Ceballos et al. 1998). They may be restricted to an ecoregion, such as mangrove forests, or to a country—bonobos are endemic to the Democratic Republic of Congo, for instance. Species with narrow geographic ranges are especially susceptible to extinction from disease, invasive species, sustained habitat degradation, climate change, or political instability (Usher 1986; Pimm et al. 1995). Rarity is a component of biodiversity, too. It is important in conservation because rare species are prone to extinction. Rarity can be measured in three orthogonal ways—a wide or narrow geographic distribution, a broad or restricted habitat specificity, or a local population size that is somewhere large or everywhere small (Rabinowitz et al. 1986). These can be combined together to produce seven different forms of rarity and one form of commonness, although in practice rare species are frequently defined by their limited geographic distribution—often as the lowest quartile of species based on their representation on a geographic grid (Gaston 1994; Flather & Sieg 2007)—so in this sense they are similar to narrow endemics. They are also defined as species with absolutely or relatively small population sizes (Andelman & Fagan 2000). Other definitions include habitat specialists and, confusingly, threatened species, although these need not be synonymous (Freitag & van Jaarsveld 1997), as well as combinations of measures (Cofre & Marquet 1999; Marcot & Flather 2007). In ecological surveys, rare species can denote species of which only a single individual is recorded (Novotny & Basset 2000), or those found at only one site (Longino et al. 2002)—such rarity can be more apparent than real because it is affected by sampling effort. Threatened species are yet another aspect of biodiversity. Threat refers to processes that drive loss of biodiversity, such as logging and mining. It can be considered in terms of exposure, or probability of a threatening process affecting an area, or intensity or magnitude, or the impact or outcome of the threat. Vulnerability is a closely related term that often refers to species and populations but also relates to the area of occupancy (Wilson et al. 2005). Conventionally, the extent to which a species is vulnerable is measured using the International Union of Nature and Natural Resources (IUCN) categorization of threatened and endangered species (see Table 1-1a) in which species are ascribed categories using several criteria (see Table 1-1b); sometimes these categories are assigned ordinal measures (e.g., Rey Benayas & de la Montana 2003). The method is transparent and

Not evaluated (NE)

Data deficient (DD)

Least concern (LC)

Near threatened (NT)

Vulnerable (VU)

Extinct (EX) Extinct in the Wild (EW) Critically endangered (CR) Endangered (EN)

(a)

When there is no reasonable doubt that last individual has died. When the species is known only to survive in cultivation, in captivity, or as a naturalized population(s) outside the past range. When the best available evidence indicates that it meets any of the criteria A–E for CR and is therefore thought to be facing an extremely high risk of extinction in the wild. When the best available evidence indicates that it meets any of the criteria A–E for EN and is therefore thought to be facing an extremely high risk of extinction in the wild. When the best available evidence indicates that it meets any of the criteria A–E for VU and is therefore thought to be facing an extremely high risk of extinction in the wild. When it has been evaluated against the criteria but does not qualify for CR, EN, or VU now, but is close to qualifying for or is likely to qualify for a threatened category in the near future. When it has been evaluated against the criteria and does not qualify for CR, EN, VU, or NT. Widespread and abundant taxa are included in this category. When there is inadequate information to make a direct, or indirect, assessment of its risk of extinction based on its distribution and/or population status. When a species has not yet been evaluated against the criteria.

Table 1-1. (a) IUCN Red List categories, (b) a simplified overview of the IUCN Red List Criteria that are used to categorize critically endangered, endangered, and vulnerable species (from Rodrigues et al. 2006; IUCN 2008).

74-cm dbh trees and understory Vaccinium cover, each of which are easier to measure than the squirrels themselves! This raises an important and somewhat obvious issue, namely that it may be easier to identify old-growth forests through direct measurement. Certainly, forest structural diversity can be assessed by measuring

234 c o n s e r v a t i o n b y p r o x y

heterogeneity (i.e., the relative abundance of structural components in the vertical and horizontal planes), complexity (i.e., the absolute abundance of individual structural components), and scale (i.e., variation as a result of the size of the area). These give some indication of the number of niches for microbial plant and animal communities (Ferris & Humphrey 1999). Documenting forest structure itself is relatively straightforward and involves recording the number of trees of different sizes classes, the number of tree species, the size and height of canopy, stand density and amount of deadwood, and so on—deadwood, in particular, is recognized as a key indicator in forests because it fosters a wide range of species (Franklin et al. 1981). Nonetheless, as in the case of MIS, there are shortcomings: habitat variables are often poor predictors of species abundance (Lindenmayer et al. 2002), and they are greatly affected by the rules chosen to classify habitat. The coarse-grained land-cover maps favored by managers explain very little variance in bird abundance, for example. Moreover, some bird guilds are well explained by a given habitat classification, whereas others are explained with little confidence (Cushman et al. 2008). To discover that red wattlebirds are more likely to be found where eucalypt cover is consolidated while crimson rosellas are found where the same cover is dispersed is sobering (Lindenmayer et al. 2002). In reality, identifying forests of high biodiversity requires knowledge not only of species composition, vascular plants, bryophytes, lichens, fungi, butterflies, carabid beetles, woodpeckers, and so forth (Ferris & Humphrey 1999), but also forest structural and functional components; so it may be most expeditious to measure abundance of a few selected species in combination with some structural elements (Noss 1990; chapter 10).

Early Warnings There is a special sort of cross-taxon-response indicator species that, in theory, would be extraordinarily useful in conservation: indicators that could give early warning of an impending problem for other species. One hundred years ago, canaries (actually lemon-breasted seedeaters) were taken down into coal mines to inform miners working underground that carbon monoxide levels had risen to lethal levels that would soon endanger their health; when the canary stopped singing it was time to leave the mine (Burrell & Seibert 1916). The concept has been borrowed for assessing ecosystem health by ecotoxicologists (see chapter 6), but conservation biologists would also like to find analogous species to provide an early warning of en-

Cross-Taxon-Response Indicator Species 235

vironmental disturbance that will soon affect populations of other species over space or time. There are very few concrete examples of these extra-sensitive species, again sometimes called sentinel species (borrowing and changing the term from ecotoxicology and medicine), that can predict in advance sympatric species’ responses to environmental change. One example is the percentage of grass cover being an early warning of desertification in the Chihuahuan desert (de Soyza et al. 1998). Usually, however, the logical sequence of events runs in other directions (see Table 8-4). Often, for example, declines are noticed in some populations, as was the case in southern Asia with populations of oriental white-backed, long-billed, and slender-billed vultures that have declined by more that 95 percent since the early 1990s (Oaks et al. 2004). Later these were followed by declines in Egyptian and redheaded vultures (Cuthbert et al. 2006), and other species such as marabou storks are now suspected of being in trouble (Cuthbert et al. 2007). These declines were caused by scavenging from livestock carcasses treated with diclofenac, a non-steroid anti-inflammatory drug, and, to a lesser extent,

Table 8-4. Common causal chains in uncovering a conservation problem. Early warning species are shown at the bottom. First event

Second event

Species found to be declining.

Populations of other species found to be declining. Species found to be Environmental declining. change acknowledged. Environmental Populations found change recognized. to be declining.

Environmental Species identified change recognized. as likely to be at risk. Environmental Species found to change anticipated. be declining.

Measures

Example

Steps taken to stop all declines.

Asian vultures

Steps taken to identify specific aspects of change. Specific aspects of change specified and restoration initiated. Legal steps taken to protect them.

Amphibians

Steps taken to stop decline of that and other species.

European farm birds

Polar bear


carpofen and fluinixen, shortly before the cow died. Further research has now identified meloxicam as a veterinary alternative to diclofenac that does not result in kidney damage, visceral gout, and death in vultures, and the Indian Government has banned the sale of diclofenac (Swan et al. 2006). Another alternative sequence of events is the simultaneous discovery of several species in decline and then making concerted attempts to uncover the cause. A current disturbing example is the global decline in amphibians (Lips et al. 2006; Pounds et al. 2006), which has resulted in nine species of amphibian becoming extinct since 1980 and another 113 possibly extinct. This crisis led to intense research that uncovered the pathogen chytridiomycosis as being an important source of mortality (Rachowicz et al. 2005), although several other factors, including climate change, contribute as well (Collins & Storfer 2003). At present the most promising short-term solution is captive breeding and reintroductions (Griffiths & Pavajeau 2008). A third avenue is simultaneously recognizing that environmental change is underway and that some populations are in decline, and then, through research, linking the two to determine the specific aspects of change that are responsible in the hope of ameliorating them. Changing farming practices in Britain, coupled with declines in farmland birds, drove research that showed that loss of nest sites and reduction in winter seeds and summer invertebrates for feeding nestlings were responsible for lowered avian reproduction and survival. This further led to Biodiversity Action Plans for individual species and schemes to increase wet habitats (Bradbury & Kirby 2006) and provide supplemental winter seed (Siriwardena et al. 2007). A fourth route is where well-understood environmental changes are predicted to affect certain species that then become a focus of conservation attention. There are a number of transformations anticipated as a consequence of climate change for ice-obligate mammals that rely on sea-ice platforms, ice-associated cetaceans that are adapted to sea-ice-dominated ecosystems, and seasonally migrant species for which sea ice can act as a barrier (see Table 8-5). Melting arctic ice due to global warming has resulted in the listing of the polar bear under the Endangered Species Act, although little can be done about stemming its decline in the short term. Thus, although early-warning species would be a tremendous asset in theory—forecasting cross-taxon responses in advance at the ecological scale—in practice the sequence of discovery is more convoluted. If we knew that a particular target species was likely to decline in the near future despite having healthy populations now, we would have an op-


Table 8-5. Anticipated climate-related changes for ice-obligate, iceassociated, and seasonally migrant marine mammals in the arctic (from Moore & Huntingdon 2008). Species category Species

Ice-obligate Polar bear Walrus Bearded seal Ringed seal Ice-associated Bowhead whale Beluga Narwhal Seasonally migrant Gray whale Harbor seal

Anticipated change

Declines in recruitment and body condition

Migration alteration and occupation of new feeding areas

Novel occupation of Arctic latitudes and longer residence times

portunity to protect it or to address the factors that we suspect will affect it adversely. There is now some opportunity to do this—but only for taxa for which we have good life-history and ecological data. The opportunity presents itself because extinction risk is not only a reflection of extrinsic anthropogenic drivers but of species’ intrinsic biological attributes. For example, carnivores and primates that occupy small geographic ranges, occur at low population densities, occupy a high trophic level, and exhibit low reproductive rates are prone to extinction (Purvis et al. 2000). The importance of intrinsic factors varies even within mammalian clades (Fisher et al. 2003), so if traits such as these evolve along branches of a phylogenetic tree, then close relatives of threatened species are expected to be at greater risk than distant relatives, allowing us to make predictions about extinction risk in the absence of data on levels of extrinsic threat (Mace et al. 2003). It is helpful to think of this as a discrepancy between predicted extinction risk and present extinction risk. Cardillo and others (2006) converted the World Conservation Union Red List into a 0 to 5 scale using only species listed under criterion A—those that have a recent or ongoing decline in population size (see Table 1-1). This they correlated with numerous life-history and ecological variables, such as gestation length and arboreality, for all major mammalian clades, using phylogenetically independent contrasts, which


yielded a set of independent biological predictors of extinction risk. They then fitted the same set of predictors in standard non-phylogenetic regressions and used these to calculate predicted values of extinction risk. Latent extinction risk was calculated as predicted-minus-current risk of extinction based on the Red List. It can be thought of as the potential of a species to decline rapidly if subject to the human impact equivalent to the average that other species experience. When they plotted the geographic ranges of those terrestrial mammals with high latent extinction risks on a world map, two areas stood out: northern boreal forests of the New World, and an arc of islands from the Andaman and Nicobar Islands through Indonesia, New Guinea, and Melanesia. These are areas where human impact is arguably low but where mammal species are inherently sensitive to human disturbance. Similar algorithms have been applied to other groups and have yielded surprising results. Hylid and Bufonid frogs both seem predisposed to chytridiomycosis infections and climate change, with the former clade concentrated in Central and South America and Australia (Corey & Waite 2008). Given the population declines in closely related British birds, the now-common blackbird seems destined for an imminent population reduction (Thomas 2008). Based on projected human population increases, African viverrids seem particularly susceptible to risk of extinction because of their life-history traits (Cardillo et al. 2004). Now there is an argument for watching these species currently listed as “of least concern” or “greenlisted species” very carefully indeed because of these early warnings.

Substitute Species Some researchers have proposed using behavioral indicators of environmental change in common species as substitutes for parallel behavioral changes in other, rarer species. Behavioral responses are common outcome variables in ecotoxicological studies and are usually observed in species thought to be under environmental stress, but here it is proposed that the behavior of one species is used as an indicator of behavioral responses in others. This is because it may be difficult to locate and observe rare or narrow endemics, sample sizes may be inadequate, and conducting experimental tests on endangered species may be problematic. Substitute species have been defined (very broadly) as “species or populations that are studied on the assumption that they show how populations of conservation concern might respond to environmental disturbance” (Caro et al. 2005, 1822) and


are therefore cross-taxon-response indicators but the focus is on behavioral rather than population change. Substitute species are chosen either on the basis of genetic or ecological similarity to the target so as to approximate its response to disturbance; or they may be chosen because they are members of a group of species along with the target (see Dearborn et al. 2001) and so can provide a consensus response close to that of the target. Or they may be chosen because they help identify a relationship between the response and some aspect of the phenotype. A practical example comes from using the presence of the relatively common bronze darter to predict the response of the amber darter, a species that is restricted to just two rivers in the southeastern United States, to aspects of urbanization (Wenger 2008). The difficulty with substitute species is that the endangered species is likely to be subject to greater disturbance than other, more-common species or is more sensitive to a given level of disturbance (Caro et al. 2005). In fact, the number of studies showing that different species exhibit differential sensitivity (whether behavioral or not) to landscape change is enormous—insects (Collinge 2000) or carnivores (Gehring & Swihart 2003; Riley et al. 2003) in fragmented North American landscapes, to mention only two. Therefore the use of cross-taxon-response behavioral indicators may be limited.

Problems with Cross-Taxon-Response Indicator Species There is a conundrum: on one hand, “the concept of indicator species remains an appealing and potentially important one because of the impossibility of monitoring everything” (Lindemayer et al. 2000, 945); on the other hand, there are a great many difficulties in using indicators at the species or species-group level. For convenience, we can classify these conceptual problems into those that pertain within a single habitat and those that apply across habitats. First, it is difficult to believe that two species should respond in exactly the same fashion to environmental change. Species are influenced by disease, predation, weather, refuge availability, breeding sites, and inter- and intraspecific competition, but to differing degrees, so it seems improbable that any two species would respond in exactly the same way to a given environmental challenge. Species’ responses to climate change are a case in point (Root & Schneider 2002; Lindenmayer & Fischer 2003; Root et al. 2003; Jonzen et al. 2006).


Nonetheless, there are situations where populations do change in parallel, such as declining European farmland birds, because constellations of species are similarly limited, some by shortage of nest sites, others by shortage of winter feed, others by shortage of food for offspring—often these species belong to the same foraging guild. Similar to Lambeck’s focal species, the challenge is to choose cross-taxon-response indicator species knowing that the limiting factors are shared by other sympatric species and suspecting that one of these factors is changing for the worse. Therefore, considerable background knowledge is required, which limits the usefulness of the cross-taxon indicator as a shortcut. Second, given that so many different factors affect populations, managing an area for a particular species in the hope that benign environmental conditions will be maintained for others is optimistic, especially if the management protocol becomes overly focused on a particular species’ requirements (Landres 1992). In brief, suggesting that the demands of a single species might satisfy those of an entire community is wishful thinking (Cairns 1986). Moving on to the idea of using the same cross-taxon-response indicator species or species-group in different habitats, there are additional conceptual difficulties. First, different populations of the same species respond to multiple independent factors in different ways at different locations. Of 47 bird species recorded in the North American Breeding Bird Survey that occurred in more than one region in the United States, 77 percent showed a decline in at least one region but increases in at least one other. Only 23 percent showed consistent increases or consistent declines across all regions in which they were found. Just as worrying, in 77 percent of 22 regions, there were statistically significant increases in at least one species but significant declines in at least one other. These findings question whether there can ever be a common species that we can always rely on to monitor effects of environmental disturbance on other species (Taper et al. 1995). Second, in comparing disturbance regimes, species nestedness can be important because sensitive species that drop out of the community early should be good candidates for assessing the presence of others. Yet in those studies that have examined the consistency of nestedness there are queries related to both space and time. Among amphibians in Ontario, Canada, or bryophytes and lichens in coniferous spruce forests in Norway, species nested at one set of sites have a low probability of being nested at other sites (Hecnar & M’Closkey 1997; Saetersdal et al. 2005). Saetersdal and coresearchers volunteer two reasons for this lack of consistency: enormous variation in individual species’ population densities across a landscape and poor dispersal ability, both resulting in some species not being present at a


given site. Both factors would produce inconsistencies in nestedness. In a separate appraisal, repeated inventories of butterflies over time in Nevada, USA, revealed no change in overall nestedness but the degree of nestedness of individual species did change (Fleishman et al. 2000b). Third, there is the issue of scale when attempting to generalize whether cross-taxon-response indicator species are effective across sites. As area increases, empirical data show that rates at which new species from different taxa are added together differs. Consequently, correlations between species vary from place to place and decline with increasing area (Weaver 1995), making it problematic to use the same cross-taxon-response indicator at different scales (see also Murphy & Wilcox 1986; Flather et al. 1997). Fourth, cross-taxon indicators are task specific. Around the Great Lakes region of Ontario, Canada, sites suffering from air pollution from smelter and mining activities, but now naturally recovering, showed different species associations than sites enjoying active restoration that involved fertilizing, seeding, and planting native and nonnative species (Anand et al. 2005). In naturally recovering sites, vascular-plant richness was correlated with other groups, as was the vascular- and non-vascular-plant Shannon diversity index, but in restored sites none were significant (see Table 8-6). Vascular plants therefore predict overall diversity but only in natural environments, raising the possibility that surrogates may be less than useful in monitoring progress of restoration projects. Landres ended his 1992 article thus: “The current use of ecological indicators to assess population trends and habitat quality for other species of interest is financially not practical, conceptually inappropriate, and empirically unsupported, potentially leading to inaccurate long-term management and assessment decisions” (1313). Cross-taxon-response indicators of

Table 8-6. Correlations between diversity of taxonomic groups in naturally recovering and restored sites (from Anand et al. 2005). Naturally recovering sites

Vascular plants/nonvascular plants Vascular plants/bryophytes Vascular plants/lichen Bryophytes/lichens * p < 0.05, ** p < 0.02, ***p < 0.001

Restored sites

Taxa richness

Shannon diversity

Taxa richness

Shannon diversity

0.96*** 0.37*** 0.56*** 0 ***

0.96*** 0.83*** 0.77*** 0.44***

0.29 0.01 0.09 0.21

0.15 0.11 0.23 0.15


disturbance have a shaky conceptual scientific basis but are nonetheless embedded in agency management and conservation practice. Recognizing this, Landres advised always stating management goals clearly, using (crosstaxon-response) indicator species only as a last resort, and choosing them only if they are in accord with assessment goals, which requires knowledge of the biology of the indicator species in advance. At present, the field is an awkward marriage of administrative inertia using unsubstantiated science and the necessity of developing monitoring schemes as new environmental problems appear. Management projects that plan on using cross-taxonresponse indicators need to be very circumspect.

Summary By focusing on one or a few species, conservationists may be able to assess many species’ responses to anthropogenic activities, but examination of empirical data suggests that this is tricky. First, species’ responses to land degradation and urbanization are idiosyncratic. Second, species sensitive to habitat change can predict responses of species that are less sensitive to habitat change—but not vice versa. Third, some studies in agricultural landscapes demonstrate cross-taxon-response congruency, but they are scale-dependent. Last, areas under various sorts of legal management affect different taxonomic groups in dissimilar ways. Despite these difficulties, there is evidence that bird-community types predict structural vegetation changes inherent in forestry practice and in agricultural intensification. Management Indicator Species (MIS) are used in forestry management to maintain biodiversity, to identify old forests, and to try to maintain suitable harvests; there are five classes of MIS. Scrutiny of the MIS concept has raised doubts about its utility in predicting other aspects of forestcommunity diversity, and it may instead be more judicious to measure a few selected species and forest structural elements together. It would be expeditious if certain species could give advance warning of declines in other species. In reality, however, it is more common for conservation biologists to discover a species declining, thus alerting them to a broader problem of other species backsliding at the same time, or to changes in the environment. In other situations, environmental changes are recognized and populations are then found to be in decline or else are predicted to decline shortly. Some advance predictions can be made, however, because closely related species share traits, some of which make them susceptible to extinction. Thus, common species with threatened relatives may


be at risk. Sometimes behavioral responses to environmental change in common species are used as a substitute for examining behavioral changes in endangered species, but this strategy is questionable. Cross-taxon congruency in response to environmental change is somewhat improbable where change is not too harsh—sympatric populations are not necessarily expected to change in parallel, given that they are subject to so many different abiotic and biotic influences. Also, across habitats, species show idiosyncratic population trajectories; species nestedness is inconsistent; increasing area reduces correlations between sites; and congruency varies even between naturally recovering and actively restored sites. Thus, the science underpinning the use of cross-taxon-response indicator species is not well substantiated, but administrative inertia ensures that these species will continue to be used.

The jaguar is an interesting example of a flagship species because it has been used in at least two capacities—to set up reserves in the neotropics and to raise money for conservation organizations in the developed world. (Drawing by Sheila Girling.)

Chapter 9

Flagship Species

Characteristics of Flagship Species When a local conservation group, NGO, or government wants to educate the public about conservation or promote a conservation program, or when a conservation organization or zoological institution aims to raise its profile, increase its membership, or obtain funds, it will often use a single charismatic species as an emblem and rallying point for the conservation campaign, as a catalyst for conservation action, and for its power to draw in money. The underlying reason for using just a single species, or occasionally a small collection of species, is that the public is assumed to have inadequate knowledge of ecological or biodiversity complexities (Leader-Williams & Dublin 2000), or has a short attention span. The reason for choosing certain species over others is that they have particular ecological, aesthetic, or visceral appeal (Lorimer 2007) and are thus attractive and memorable. These are flagship species, “chosen for their charisma, to increase public awareness of conservation issues and rally support for the protection of that species’ habitat. Protection of other species is accomplished through the umbrella effect of the flagship species” (Favreau et al. 2006, 3,951; see also Heywood 1995; Meffe & Carroll 1997; Simberloff 1998). Flagship species are usually homeotherms—large, endangered, toppredatory mammals, or else piscivorous or omnivorous large birds (Clucas et al. 2008; see also Ward et al. 1998; Gunnthorsdottir 2001; White et al. 245


2001). Presumably these are the traits that resonate with the public (in both the industrialized and developing world), as many people are in awe of large bird and mammal species out of respect or fear; in the urban sectors of the industrialized world, at least, people are thrilled by witnessing an act of predation, and they are concerned about species disappearance. Indeed, 8 out of the top 12 species featured on U.S. conservation and nature magazine covers over a decade were of large carnivores (Clucas et al. 2008). Nevertheless, occasionally poikilotherm vertebrates (Walpole & LeaderWilliams 2002), invertebrates (Samways 1994), or plants (Farjon et al. 2004) are chosen as flagship species. Here I discuss the different ways in which flagship species are used as surrogates in conservation, efforts to measure their success, and their principal characteristics.

Multiple Objectives User groups employ flagship species to deliver subtly different conservation messages. First, NGOs or local conservation organizations try to raise public awareness about habitat and species losses by using striking and memorable species. In billboards, posters, brochures, or stickers, eye-catching pictures are interwoven with short texts about the ecology of an area or the habits of a species. For instance, the Natural Resources Defense Council has used the white “ghost” or “spirit” bear (actually a white morph of brown bears) as a symbol for conserving temperate rainforest along the coast of British Columbia, Canada. Conservation groups mounted a local awareness campaign using the golden lion tamarin to increase awareness of this species and its dwindling Atlantic rainforest habitat in Rio de Janeiro and São Paulo, Brazil (Dietz et al. 1994). The Colobus Trust in southeast Kenya uses the Angolan black and white colobus as an emblem to conserve habitat for primate species and to advertise its willingness to give veterinary attention to primates hit by vehicles (Anderson et al. 2007). The target audience for these educational tools or advertisements can also be the wider international community. For example, Greenpeace uses whales to educate the public in industrialized nations about whaling, to build support for a boycott of nations that continue to whale (such as Norway), and to raise funds for their efforts to halt whaling and to support other Greenpeace activities. Also, flagship taxa such as butterflies are used to educate the public about biodiversity—insects, for example (New 1995). Second, and related to conservation enlightenment as discussed above, governments use flagship species to symbolize a country’s natural heritage and to increase environmental awareness. For instance, almost every coun-

Flagship Species 247

try has a national bird or mammal that is protected by law (e.g., Uganda has the crowned crane). When the Government of India mounted “Project Tiger” in 1972, annexing 15 tiger reserves that aimed to conserve the species, its prey, and its habitat, they were doing this in part to save a quintessential Indian species (Panwar 1982). Third, NGOs focus attention on their own organizations using flagship species. For example, the Worldwide Fund for Nature (WWF) uses the giant panda as its logo (Dietz et al. 1994), while the Flora and Fauna Preservation Society’s logo is the Arabian oryx—their most famous project was “Operation Oryx,” which reintroduced this species back to the Arabian peninsula (Ostrowski et al. 1998). Flagship species featured in conservation organizations’ magazines are used to maintain the public’s interest in ongoing projects. Fourth, flagship species are enlisted to raise money for a conservation organization by capitalizing on a high-profile species with which donors sympathize. For example, Defenders of Wildlife uses stories of wolf persecution in its fund-raising efforts to run its offices and legal projects. Also, zoological institutions like to exhibit high-profile species such as giant pandas, or to breed attractive species, such as cheetahs, for the purposes of promoting themselves, attracting more visitors, and raising money (Christie 2007). Related to this, flagship species may be used to encourage tourists to visit particular places (Kruger 2005; Verissimo et al. 2009) Fifth, flagship species are used to establish reserves (see Table 9-1). If the population of a charismatic species is thought to be worthy of protection for its own sake, and a reserve is especially set up for this purpose, the reserve will necessarily harbor other species; consequently these flagship species assume an umbrella role. For example, mountain tapirs have been used to set up reserves in the high Andes (Downer 1986). In the marine realm, some conservation efforts use charismatic megafauna, such as whales, seals, and migratory seabirds, as flagship species to identify where to set up marine protected areas. (Often these species occupy distinctive habitats whose communities are substantially different from the surround, [Roff & Evans 2002]). Interestingly, some characteristics of flagship species, such as large body size and being a predator, overlap with useful traits of umbrella species—large species are likely to have large home ranges, for instance (see chapter 4). Writers sometimes apply the terms flagship species and umbrella species interchangeably or attribute both meanings to the same species (e.g., Johnsingh & Joshua 1994), although originally flagship species were a public relations tool while classic umbrella species had an ecological basis (Simberloff 1988; Caro & O’Doherty 1999). To avoid semantic quibbles, I


Table 9-1. Use of flagship species in establishing reserves (from Caro et al. 2004). Species

Reserve

Plants Redwoods

Avenue of Giants Redwood State and National Parks, California, USA

Arthropods Monarch butterflies

El Rosario Monarch Butterfly Sanctuary, Michoacan, Mexico

Birds Brown pelicans Flamingoes

Pelican Island National Wildlife Reserve, Florida, USA Lake Nakuru National Park, Kenya

Mammals Jaguar Tiger Javan rhinoceros and Javan tiger African elephant Baird’s tapir

Cockscomb Jaguar Nature Reserve, Belize 15 reserves in India Ujung Kulon National Park, Indonesia Addo National Park, South Africa Tapir Mountain Nature Reserve, Belize

Table 9-2. Principal proponents and objectives for which flagship species are used. Promote conservation awareness

NGOs/Local groups Zoos Governments

X X

Selfpromotion

Raise funds

Set up a reserve

X X

X X

X X

X shows that the objective is relevant.

will simply call these flagship umbrella species; I cover them in this chapter rather than chapter 4 only for convenience; the emphasis on the first and second word in the term depends simply on the use to which the species is put in a particular project. In summary, flagship species are used to achieve at least four objectives in conservation (see Table 9-2), and species that are useful in one arena may not necessarily be useful in another.


Are Flagship Species Successful? Public Awareness Case studies provide anecdotal evidence that flagship species do enhance public awareness. Dietz and coworkers (1994) describe how three liontamarin species (golden-headed, golden lion, and black lion tamarins), all rare, were used to build public support for a habitat-conservation plan in Brazil. The project focused on residents of Rio de Janeiro and São Paulo who were purchasing wild animals illegally and on government bureaucrats and politicians. The program educated them about environmental protection, tamarins, and reserve establishment. Results after two years were impressive (see Table 9-3) because people had generalized their environmental awareness, suggesting that conservation-education programs centered on individual species helped to change local attitudes about forest conservation. In other examples, captive Asian elephants were used in Aceh, Indonesia, to raise awareness in villages and thereby encourage people to patrol forests, detect illegal logging, and control crop-raiding by wild elephants.

Table 9-3. Responses to some questions used in interviews of adults before and after two years of the golden lion tamarin conservationeducation project (from Dietz et al. 1994). Responses to questions

Question

Before project activities

After project activities

What is the name of this animal? (photo of golden lion tamarin)

Correct

59% (518)a

79% (497)

How does the tamarin live?

Correct

24% (140)

55% (406)

Is the golden lion tamarin important or beneficial?

Don’t know Yes

77% (515) 14%

22% (400) 62%

What would you do with a little bird you found in the woods?

Raise at home Leave it alone

55% (512) 44%

29% (499) 69%

What would you do with a snake you found in the woods?

Kill it Leave it alone

73% (512) 25%

55% (499) 32%

a

Number of responses.


On Pemba Island, Tanzania, the endemic Pemba flying fox was used as a symbol to educate children about habitat conservation and to change hunting regulations. In southern Belize, the ceiba or kapok tree that plays a central role in the folklore of Mayan communities was used as an emblem to conserve forest in the Golden Stream Corridor Reserve. All three projects were apparently successful (Bowen-Jones & Entwistle 2002). In contrast, Linnell and others (2000) report that attempts to use large carnivores as flagship species in Sweden were problematic because hunters viewed wolves and brown bears as competitors for ungulate prey, while sheep farmers and reindeer herders complained about predation. Linnell and colleagues argue that negative attitudes of rural inhabitants mean that large carnivores are inappropriate flagship species in this part of Scandinavia. Actually, much has been made of context in choosing flagship species. Species that are attractive for urban folk far removed from wilderness areas may be unattractive for rural populations living near these animals; species respected in the industrialized world may be scorned in the developing world (Leader-Willams & Dublin 2000; Woodroffe et al. 2005). For example, schoolchildren in rural Guyana are most concerned about the huge Arapaima fish that are eaten locally, while tapirs, anacondas, jaguars, harpy eagles, giant anteaters, and red howler monkeys— attractive to people from industrialized nations—were classified in the same category as tarantulas, black caimans, frogs, freshwater stingrays, and bullet ants (Borgerhoff-Mulder et al. 2009). Flagship species in the developing world must be chosen carefully. Writing about what they term culturally defined “keystone species,” which from their definition can be construed as flagship species—“plant and animal species whose existence and symbolic value are essential to the stability of a cultural group over time”(3)—Cristancho and Vining (2004) stipulated seven conditions for their successful use in conservation. The story of the species’ origin is tied to the myths, ancestors, or origins of the culture; the species is central to the transmission of cultural knowledge; it is indispensable in the major rituals on which the community’s stability depends; it is either related to or used in activities intended to supply the basic needs of the community such as getting food, constructing shelters, and curing illnesses; the species has significant spiritual or religious value for the culture in which it is embedded; it exists physically within the territory that the cultural group inhabits or to which it has access; and the cultural group refers to the species as one of the most important species. Possible examples include coca for the Letuama Indians, the jaguar for the Tukano Indians, and pigs for Tsembaga of New Guinea. As many of these species are likely to be


domesticates—for instance, corn for the Hopi Indians—the merit of conserving culturally defined species must lie indirectly in helping to preserve the well-being of indigenous communities that are caring for local native species.

Raising Funds Surveys and willingness-to-pay (WTP) analyses show that flagship species can be enlisted to raise conservation funding (Kontoleon & Swanson 2003; Verissimo et al. 2009). In parts of the industrialized world, the public values species that provide ecological services (Montgomery 2002), as well as endangered species (Tisdell et al. 2007) and endemic species (Meuser et al. 2009), suggesting these are useful attributes for flagship species. For instance, correspondents are willing to pay reasonable sums of money to conserve North American threatened and endangered species (see Table 9-4) and would pay more by means of a one-off payment than they would annually, more if they have visited places where the species lived, and more for marine mammals (Loomis & White 1996). Flagship species can be specifically used to raise money for habitat conservation. Kontoleon and Swanson (2003) asked 305 non-Chinese correspondents whether they would be willing to pay for conservation of the giant panda. Respondents were informed about the plight of the carnivore and that its best hope for survival lay in the Wolong Reserve, where 200 free-living and caged pandas are found. People were given the option of contributing money toward boosting the population by 300 animals that were either to be kept in 100-m2 cages, in 5,000-m2 pens, or in their natural habitat. Mean WTP was $3.90, $8.43, and $14.86, respectively, showing that people not only wanted to conserve pandas but to protect them in situ, thereby contributing to habitat conservation.

Reserve Establishment High-profile species have been used to set up protected areas. A prominent example of these flagship umbrella species is the northern spotted owl, which has come to symbolize North American old-growth forest. Studies conducted in Washington, Oregon, and California showed that owls nest and roost in conifer-dominated stands characterized by large, old trees and closed canopies that are less fragmented than are surrounding landscapes.


Table 9-4. Review of 20 studies reporting economic values of rare, threatened, or endangered species using WTP estimates (in 1993 US$) (from Loomis & White 1996).

Species

Studies reporting annual WTP Northern spotted owl Pacific salmon/steelhead Grizzly bear Whooping crane Red-cockaded woodpecker Sea otter Gray whale Bald eagle Bighorn sheep Sea turtle Atlantic salmon Squawfish Striped shiner Studies reporting lump sum WTP Bald eagle Humpback whale Monk seal Gray wolf Arctic grayling/Cutthroat trout

Low value

High value

$44 31

$95 88

10

15

17 15 12

33 33 30

7

8

178

254

16 13

118 17

Average of all studies

$70 63 46 35 13 29 24 24 21 13 8 8 6

216 173 120 67 15

There is great variation in home-range size: 450 ha in California and up to 3,200 ha in Washington (Hunter et al. 1995; Lehmkuhl & Raphael 1993; Ripple et al. 1996), which relates to abundance of medium-sized prey and dusky-footed and bushy-tailed woodrats (although home-range size decreases with increasing old-growth forest in areas where owls eat northern flying squirrels [Carey et al. 1992]). Knowledge of home-range size and habitat attributes was used to model owl population sizes under various tree-harvest regimes, resulting in a number of proposals (USDA [90], USDI [93]): maintaining 40-ha reserves around known nesting sites; 46–91-m riparian buffers along all streams; dispersal corridors where 50 percent of the land needs to hold tree diameters >28 cm and canopy clo-


sure of >40 percent; and so on. Although it has been very difficult to reach a consensus on tree-cutting practices in this region of the United States, owls are both a flagship for remaining old-growth forests and an umbrella for undisturbed or lightly disturbed redwood forests. Some studies have specifically tried to assess whether flagship umbrella species could prove useful in reserve establishment either at a local scale or at a regional or continental scale. (Almost all focus is on the presence or absence of background species, not on their population sizes or viability.) In the central-eastern Italian Alps, numbers of avian species, vulnerable bird species, and tree diversity, as well as the total number of birds and butterflies, were greater in six avian predator species’ breeding territories than at control sites (Sergio et al. 2005a, 2006; see Figure 4-3). In contrast, a study of goshawks in Hokkaido, Japan, found no association between their home ranges and bird, butterfly, carabid beetle, and forest-floor plant species richness or abundance, except that goshawk avian-prey abundance was higher in their home ranges (Ozaki et al. 2006; see also Roth & Weber 2008). Certainly, one could argue that top avian predators are charismatic and could be called flagship species, and in Italy they seem to be associated with some aspects of biodiversity and so could aid in conserving wildlife at a local scale. Switching to mammals, species that are used as flagships in other public relations contexts have been noted as having wide ramifications for ecosystems. Ripple and Beschta (2006) reported that the cougar population in Zion National Park, Utah, USA, declined as a consequence of increased tourist traffic. This resulted in an increase in mule deer densities, higher browsing intensities, and reduced recruitment of cottonwood trees, leading to bank erosion and reductions in terrestrial and aquatic species abundance. Similarly, Berger and colleagues (2001) found that wolf and grizzly bear extinction in the southern Greater Yellowstone Ecosystem triggered an eruption of the moose population that caused a decline in vegetation density, particularly that of willow. This was in turn associated with a reduction in breeding-bird densities. In both cases, this cascade is in line with keystone ideas advanced for large carnivores (Terborgh et al. 1999; Ray et al. 2005). Other studies have reached opposing conclusions. Caro and colleagues (2004) tried to determine whether flagship umbrella species could be useful tools in establishing small reserves in subtropical rainforest in Belize, specifically asking whether locations where flagships were commonly seen were areas that harbored high vertebrate biodiversity. They identified 1-km2 areas where flagship species—jaguar and Baird’s tapir—were frequently seen and


two other 1-km2 areas where non-flagship large mammals—white-lipped peccary and spider monkey—were seen. To examine whether flagship centers of activity coincided with vertebrate diversity, species richness and abundance of frogs, phyllostomatid bats, small terrestrial mammals, scansorial mammals, and birds were sampled at the four sites. They found no significant differences in species richness across sites for any taxon except that more frog species were found at the tapir site along the river. Similarly, there were no strong differences in abundance of taxa except that more frogs were found at the tapir site and fewest frog, bat, and bird individuals at the spidermonkey site. The message to emerge was that no small area chosen due to flagship species usage was substantially better at incorporating vertebrate species richness or abundance than any other area. A similar study that focused on flagship species’ daily activity, this time of European otters, was conducted in western France. Areas of the river that had been frequented by otters for the previous 20 years did not support greater bird-, amphibian-, and mollusk-species richness than areas that were not frequented by otters (Bifolchi & Lode 2005). Finally, in this list of ecological tests of flagship umbrella species, Berger (1997) asked whether a black rhinoceros population of 50 individuals in the Namib desert, Namibia, could encompass sufficiently large populations of background species. He found that dry-season population sizes of gemsbok, zebra, kudu, giraffe, and ostrich did not reach 250 individuals in the area used by rhinoceroses, indicating that the size and characteristics of the area were inappropriate for long-term viability of these background species. This study is particularly interesting because population sizes of background species, rather than presence/absence, was the outcome variable, speaking directly to merits of long-term capacity of a reserve to support populations. There have also been attempts to fathom how flagship species’ presence predicts biodiversity at a larger scale. Andelman and Fagan (2000) examined overlap between biodiversity and flagship species presence in 785 25km2 areas in the coastal sage-scrub communities in southern California, in 1,241 sites across five U.S. states in the Columbia River area of the northwest United States, and at 2,856 sites across U.S. counties. They defined flagships in two ways: large carnivores and unspecified charismatic species. Results were disappointing. Large carnivores protected less than 50 percent of background species in the sage-scrub and Columbia plateau data sets, although close to 90 percent across the country. Their charismatic species showed similar patterns of poor overlap with background species in the three areas. In most cases, overlap figures were lower than that of 20 species


chosen randomly as representative candidates for the presence of other species. In a hypothetical money-saving enterprise, the number of sites was reduced to protecting one, three, five, or ten occurrences of charismatic species or big carnivores, rather than every occurrence, but now invariably less than 20 percent of background species coincided with them. Andelman and Fagan concluded that flagships do not serve in a competent umbrella capacity across these three scales. In another large-scale analysis, Kerr (1997) examined large 2.5° × 2.5° quadrats covering North America to determine whether large-carnivore presence predicted invertebrate diversity. Only four quadrats contained large carnivores and, if protected, they would conserve 51.9 percent of Lasiglossum, 77.8 percent of Papilionidae, and 31.4 percent of Plusinae species, or only 43.5 percent of invertebrate diversity in total. Again, hardly impressive. Working with an African database, Williams and colleagues (2000a) investigated a data set of large-mammal and bird distributions in 1° grid cells across the continent. They picked two different sets of flagship species, the first being “well-known” species (two species of rhinoceros, elephant, gorilla, common chimpanzee, and bonobo); the second being the classic sportsmen’s bag of the “big five” (lion, leopard, buffalo, elephant, and [two species of] rhinoceros), and determined whether the presence of these species in a grid cell coincided with species richness. They discovered rather poor species representation in cells covered by each sort of charismatic species compared to what was actually on the ground. They attributed this failure to considerable overlap in flagship species’ distributions, particularly in African savannah and woodland biomes. Indeed, the best surrogate species for mammal and bird diversity was a combined distribution of a bat, gerbil, rat, crake, barn owl, and oriole—hardly charismatic taxa (see Table 9-5). In a similar vein, but here using Primates, Carnivora, Proboscidae, Perissodactyla, and Artiodactyla flagship taxa (228 mammal species in total), Williams and colleagues (2000b) found that these overlapped the distribution of only 50 percent or 54 percent of the other 937 African mammal species, depending on whether the top 50 species-rich grid squares were considered, or whether the top 50 grid squares with endemic flagship species were used (endemic being defined as the top 25 percent of species with the most restricted ranges). Neither method performed better than species chosen at random. To summarize, there are now a handful of quantitative empirical studies that have attempted to see whether the presence of flagship umbrella species in an area, or combined individual home ranges of a subpopulation


Table 9-5. Patterns of co-occupancy of grid cells (overlap) for species within the groups of six species used to select areas together with numbers of species of all sub-Saharan mammals and breeding birds in example sets of 50 grid cells selected using the hotspotscomplementary-richness method (from Williams et al. 2000a).

Groups of 6 species used for area selection

“Well-known” species “Big Five” species “Best” 6 species from random draws Totala a

Number of ecoregions within combined range of 6 species

Mean number of background species per cell from the group of 6 species

Median number of mammal and bird species represented using repeated runs

125 757

81 95

1.50 2.63

1,755 1,675

13 1,961

94 98

1.35 6.00

2,121 2,687

Median range size (cells)

Gives an estimate of data if everything were counted.

of flagship umbrella species, or daily activities of individuals of a flagship umbrella species overlap with large numbers of other species, or many individuals of other species (see chapter 4). The majority of these studies has found no strong associations, exceptions being that the presence of certain raptors and some North American carnivores can signal local species richness at an ecological scale, and so are worth examining. There are several possibilities as to why top predators in temperate regions might be associated with species richness: (a) Raptors might select breeding sites on the basis of ecosystem productivity that is associated with high biodiversity in some ecosystems (Worm et al. 2003). (b) Top predators have large area requirements that encompass territories of less-demanding species (the classic umbrella species argument). (c) Apex predators may be sensitive to ecosystem dysfunction so that their continued presence signifies a functioning ecosystem. (d) Top predators select sites with high topographic and habitat complexity that favors high biodiversity. And (e) they feed on a variety of prey species that must be present (Gaston 1996a; Carroll et al. 2001; Gittleman et al. 2001; Sergio et al. 2006). Alternatively, top predators might themselves be responsible for maintaining high biodiversity (Sergio et al. 2008). For example, they (a) can provide carrion for sympatric species (Wilmers et al. 2003); (b) can protect lower trophic levels by keeping other predators out of the area (Quinn &


Kokorev 2002); (c) can alter the environment, thereby providing refuges for other species (Craighead 1968); and (d) be responsible for trophic cascades (Palomares et al. 1995; Rogers & Caro 1998; Soule et al. 1988; Estes et al. 1998; Crooks & Soule 1999; Berger et al. 2001, Ripple & Beschta 2006; chapter 5). Given these possible mechanisms, it seems strange that so few investigations of flagship umbrella species have been positive.

Qualities of Flagship Species Attempts have been made to list criteria that make a successful flagship species (Bowen-Jones & Entwistle 2002; Farjon et al. 2004), but there is no consensus (Favreau et al. 2006). In part, the criteria must depend on conservation goals that should be specified in advance (see Table 9-6). When a flagship species is used to raise awareness of conservation issues in the

Table 9-6. Helpful features for different uses of flagship species. Raise awareness in

Features

Well known Well liked Homeotherm Large Carnivore Charismatic Endangered Culturally significant Requires large area Important ecologically Confined to one habitat Indicates species richness Sensitive to disturbance Utility Scientific uniqueness

industrialized world

developing world

X X X

X

X X X

Self-promotion or raise money in industrialized world

Help establish reserve

X X X X X X X X

X X

X X X X

X

X X X

X denotes applicable to use (from Dietz et al. 1994; Caro & O’Doherty 1999; LeaderWilliams & Dublin 2000; Zacharias & Roff 2001; Bowen-Jones & Entwistle 2002; Caro et al. 2004; Farjon et al. 2004; Sergio et al. 2006; Clucas et al. 2008; Verissimo et al. 2009).


industrialized world, it should attract attention by being charismatic and should live in one sort of habitat with which it can be easily associated. It may have additional significance and educational value if it plays an important ecological role in a specified habitat or is sensitive to disturbance (as discussed in chapters 5 through 7). In the developing world, flagship species should be well known and liked (more likely if the species also have utilitarian value); they should be charismatic, possibly endangered (although many national emblems are not), and culturally significant, especially if used locally. Utility and scientific uniqueness can help sell the conservation idea. When a flagship species is used to raise funds in the industrialized world it should be well known and liked—this often means a homeotherm that is large; is a carnivore, making it charismatic; typically has a vulnerable or endangered conservation status, perhaps due to endemism; likely requires a large area if it is a large mammal or bird; and perhaps is sensitive to disturbance. These traits are some of the classic hallmarks of a flagship species. Finally, if flagships are being employed to set up reserves, subpopulations should require a large area in which to live so that they encompass sufficient area to protect viable populations of background species. Some conservationists have even argued that flagship species should be migratory (Zacharias & Roff 2001). They should overlap with a large amount of biodiversity, perhaps because they are in a commanding ecological position that structures the ecological community. From a pragmatic standpoint, species that are culturally significant will be better placed in helping to establish a reserve.

Iconic Species Species that are famous because of peculiar traits, because they live in particular habitats, or are closely associated with a certain country (often a combination of these) are sometimes called iconic species (see Table 9-7). The duck-billed platypus is renowned because it is a mammal that lays eggs, has a singular snout, and is restricted to Australia. The polar bear has a uniform white pelage and lives in the arctic. The Beccariophoenix madagascarensis palm is a large, majestic, and critically endangered tree and is endemic to Madagascar. Iconic status can also come about because a species is extraordinarily rare or has been the object of repeated expeditions to find it. An air of mystery surrounds the ivory-billed woodpecker, believed until very recently to be extinct (Hill 2007). In conservation, iconic status can be used to attract public attention that will help save the species itself, as in the case of trying to mitigate the


Table 9-7. Examples of species that have been termed iconic in the literature. Species

Traits

Habitat

American chestnut Beccariophoenix madagascarensis Salt-water crocodile

Large, majestic

Eastern forests

Large, majestic Very large

Salt water

Duck-billed platypus Tasmanian devil Polar bear

Egg-laying Carnivorous Largest bear, white Flightless

Kaka

Country

Source

USA

1

Madagascar Australia and New Guinea Australia Tasmania

2 3

New Zealand

7

Arctic

4 5 6

1. Wheeler & Sederoff 2009; 2. Shapcott et al. 2007; 3. Bradshaw et al. 2006; 4. Grutzner et al. 2008; 5. Jones et al. 2008; 6. O’Neill et al. 2008; 7. Leech et al. 2008.

impact of fatal facial tumor disease in Tasmanian devils (Jones et al. 2008). Alternatively, it can be used to marshal public attention to the habitat in which the species lives—for example, the fate of polar bears is largely dependent on summer arctic sea ice, which is disappearing (Slocum 2004). As with flagship species, there are no distinct categories of iconic and non-iconic species, and iconic status is promulgated by biologists intent on attributing added importance to their study animal. There is no quantitative evidence that iconic status increases likelihood of funding or public awareness. Iconic species are only useful if they are extant. The iconic dodo is extinct and of questionable help to conservation efforts. Mythical animals such as the yeti, unicorn, or phoenix are of no conservation service because arguments to conserve the habitat in which they “live” are baseless.

What Next? In the developing world there is a clear need to educate the public about habitat loss and species’ declines, and if this task is accomplished more easily by using figureheads than by explaining complex conservation issues and anthropogenic pressures in detail, then flagship species are a conservation necessity. Inevitably, this means that the public will continue to have to


swallow simplistic prose accompanied by pictures and logos of charismatic species. The need to dumb down the quality and quantity of information is taken as given (Leader-Williams & Dublin 2000). Public conservation education is not keeping up with advances in conservation biology and management, which recognizes the importance of community-based conservation organizations and working with plantation industries to find compromises to biodiversity loss, to take just two examples. The utility of using species to perform double duty as emblems and umbrella species is mixed. On one hand, there is a suggestion that top predators may serve as local umbrella species for species diversity in terrestrial ecosystems. On the other hand, these species receive undue conservation attention. Listings of species under the U.S. Endangered Species Act (ESA) are slanted heavily toward birds and mammals with, in order, the bald eagle, northern spotted owl, Florida scrub jay, West Indian manatee, redcockaded woodpecker, Florida panther, grizzly or brown bear, Least Bell’s vireo, American peregrine falcon, and whooping crane receiving 54 percent of the total U.S. Federal and state ESA spending between 1989 and 1991, and each species receiving >$10 million. Being large, endangered, and taxonomically unique, or being a bird, a mammal, a reptile, or an amphibian, all increased the likelihood of being listed; while being large and being a mammal were associated with greater spending (Metrick & Weitzman 1996). Given that listing depends in part on the amount of background research carried out on a species, and that, in the main, researchers prefer to work on attractive species (Lorimer 2007), and that Federal spending is a zero-sum game, implicitly or explicitly the U.S. government is concentrating on conserving species with flagship species qualities. There are complaints about the disproportionate use of large birds and mammals in conservation at the expense of non-charismatic species (Wilson 1987; Munoz 2007), so there is a burden of proof on conservationists to demonstrate clear benefits of using flagship species in an umbrella role in conservation, not just for fund raising and education.

Summary Flagship species are popular charismatic species that serve as symbols and rallying points to stimulate conservation awareness and action. They are used to educate the public about conservation, to advertise conservation NGOs, to raise funds for conservation organizations and zoos, and to facilitate the establishment of reserves. The entities that use flagship spe-


cies are local conservation groups, zoological institutions, NGOs, and governments. The success of flagship species has been assessed in two contexts: as public-relations tools and in the establishment of reserves. Willingness-topay studies and largely anecdotal case histories suggest that flagship species have been important in conservation education and awareness building, but also that flagship species must be chosen with care—human perceptions of species differ geographically. Studies in Italy show that biodiversity is higher in raptor territories although the mechanistic basis for this is unclear; and the absence of charismatic large carnivores has detrimental effects on lower trophic levels in North American ecosystems. In contrast, studies of jaguars, tapirs, European otters, and black rhinoceroses did not find an association between centers of flagship species activity and various biodiversity measures of background species. At a larger scale, the presence of flagship species such as large carnivores or apes was not associated with greater numbers of background species across North America or Africa, so the benefits of using flagship species in reserve design are not assured. Iconic species are famous because of their unique traits or well-known endemism.

Rainforests have been used to attract public attention to habitat destruction in the tropics and can supplement or replace the use of surrogate species as tools to raise conservation awareness. (Drawing by Sheila Girling.)

Chapter 10

Surrogate Species in the Real World

Surrogate Categories Two key points emerge from this book. The first is that there are several shortcuts to achieving conservation goals. Surrogate species can be broadly divided into three major categories with little overlap in objectives: those that can help to identify the location of areas of conservation significance, those that can help to document the effects of environmental change on biological systems; and those that can be used in public-relations exercises. Within the first major category, there are surrogates employed at a large global or continental scale, others at a regional or national level, and still others at a more local level that are used to help define the shape and size of reserves. There are two orthogonal divisions here: between global prioritization, national reserve selection, or local reserve design; and between using a taxonomic group or a single species. In the second major category, there is a historical scientific divide between indicators of perturbation in aquatic and in terrestrial ecosystems, and another division between species or taxa that document environmental change directly and those that reflect the responses of other taxa to environmental change. The third major category is relatively straightforward: single species chosen to excite public interest. The second point is that the biological foundations of surrogate species are insecure. There are very few arenas in which we can say that studies have 263


unequivocally demonstrated that certain surrogate species or speciesgroups represent the distribution of other taxa, or the responses of other taxa to environmental change. In this chapter, I first briefly revisit surrogate typology with a view to clarifying the different objectives for which they are used. Next, I examine conceptually awkward but useful situations where species can be used for several conservation tasks simultaneously. In the second part, I try to suggest future directions in using surrogate species, focusing especially on how environmental and economic information is being drawn into conservation surrogacy.

Synopsis Indicators of biodiversity may be used to determine large areas of current biological significance at a global or continental scale using one taxonomic group (table 10-1). The targets are other taxonomic groups whose distributions or identities are more difficult to ascertain, considered either separately or combined together. A second class of biodiversity indicators is used to identify smaller areas of conservation concern at a regional or national level, again using one taxonomic group. Less commonly, one or a few species are used—called local umbrella species—although other sorts of umbrella species have different objectives. When the conservation goal is to plan the shape and size of a reserve most appropriate for other species, a single species, often with a large home range or specific habitat requirements, may be used as a proxy for the distribution of populations of other species (classic umbrella species, or landscape species), or several species may be used ( focal species, sensu Lambeck). When the objective is to maintain a functional community in or outside a reserve, species with disproportionate ecological influence may need inclusion in the plan (keystone, engineering, or foundation species). Similarly, certain species may be appropriate as a central point of management attention because of their large impact on local ecology (management umbrella, keystone, engineering, and foundation species). The second major category of surrogate species are indicators of environmental change; nowadays this is almost entirely rapid, anthropogenically induced change. Thus the word indicator is unfortunately used in two senses—in relation to the distribution of biodiversity, and with regard to environmental transformation. Anthropogenic change in freshwater systems is frequently caused by pollution. Indicators of aquatic pollution are well established in ecotoxicology and range from the cellular to community

Keystone species

Engineering species

Conserve populations

Classic umbrella species Focal species sensu Lambeckb Management umbrella species Landscape species

One taxon

Regional biodiversity indicator Local umbrella species

One or few species

One species

One or few populations One or few populations Populations of several species One or few populations A few species

One taxon

Taxonomic group used

Biodiversity indicator

Surrogate species

Identify location, size of reserve and manage it Conserve populations

Identify areas of biological significance Identify areas of biological significance Identify location, size, shape of a reserve Determine size and shape of a reserve Determine most limiting factors Manage populations

Principal conservation objective

Table 10-1. Surrogate species in conservation biology.

Other taxa, all other taxa Other taxa, all other taxa Other taxa, all other taxa Other species’ populations Other species’ populations Other species’ populations Other species, & populations Other species or populations Other species or populations

Target or background species

(P)

National

Regional

Regional

(A)

(A)

(A)

A, P

National

Regional, national

(A)

A, (P)

A, (P)

A

Principal applicationa

National

National

Regional, national

Global, continental

Spatial scale

Assess other species’ responses to environmental change Assess effects of management on that species and others Assess other species’ responses to environmental change Usually one species

Substitute speciesg

One or few species

Several species

One or few species

Ecologicaldisturbance indicator species Cross-taxon-response indicator speciese

Assess effects of disturbance on species

Usually one species

One or few species

One species

Taxonomic group used

Management indicator speciesf

Environmental indicatorc species Sentinel speciesd

Assess extent of disturbance

Assess extent of disturbance

Foundation species

Surrogate species

Conserve populations

Principal conservation objective

Table 10-1. Continued

Behavior of other species

That or other species’ populations

Other species

Other species or populations Environmental change Environmental or change other species Environmental change

Target or background species

Land-use system

Terrestrial ecosystem

Terrestrial ecosystem

Land-use system

Aquatic or terrestrial ecosystem

Aquatic ecosystem

Regional

Spatial scale

(A)

P

(A)

A, (P)

(A)

P

(A)

Principal applicationa

Habitat

One species

One species

Iconic species

Habitat, that species

Habitat

One species

Flagship umbrella speciesh Flagship species

Regional, national

Regional, national, local Global, regional, national, local

(P)

P

(P)

b

A, usually academic; (A), academic but used infrequently; P, usually practical; (P), practical but used infrequently. , easily abused term; c, used in pollution studies; d, similar to environmental indicator species; e, subset of ecological-disturbance indicator species; f, similar to ecological-disturbance indicator species, cross-taxon-response indicator species, management umbrella species; g, similar to cross-taxon-response indicator species; h, similar to classic umbrella species.

a

Raise political will for a reserve Raise conservation awareness and funds Raise conservation awareness and funds


level. Anthropogenic change in terrestrial ecosystems is usually due to forms of land conversion, and several species may be monitored at once to assess how such disturbance affects biological systems. Sentinel species is an ill-defined term used in both pollution and habitat-alteration contexts that sometimes refers to classic environmental- or ecological-disturbance indicator species, or to species that are particularly sensitive to anthropogenic change. Confusingly, there is another type of (cross-taxon-response) indicator species that may be indicative of both habitat disturbance and other species’ responses to habitat disturbance. Management indicator species are chosen with a hodgepodge of objectives, including monitoring that and other species’ responses to management activities. Substitute species focus on the behavior of one species being a marker for anthropogenically induced behavioral change in other species. Charismatic species employed in public relations, the third major category, are called flagship species. They are used to educate the public, raise money, or to establish a protected area—those involved in the last task I call flagship umbrella species. Iconic species are single species famous because of their biological characteristics or geographic location.

Multi-Surrogacy One source of confusion over the terminology of surrogate species is that some species can be legitimately used for several conservation objectives simultaneously. Large, charismatic, wide-ranging, threatened species—many large whales, for instance—are sometimes variously called flagship, classic umbrella, and ecological-disturbance indicator species at the same time (see Noss et al. 1996; Dalerum et al. 2008; Sergio et al. 2008). To take a specific example, in an attempt to identify marine protected area sites in the ScotiaFundy Region of Canada, King and Beazley (2005) consulted with experts and used the literature to identify 29 species that were endangered, threatened, or of special concern according to Canadian authorities, and were subject to known threats or limiting factors. Grouping them into keystone, umbrella, indicator, vulnerable and sensitive, or flagship categories, they found that many of these species fill several roles (see Table 10-2). King and Beazley singled out the North Atlantic right whale and deep-sea corals as being particularly well spread across surrogate categories. These therefore carry considerable weight when conservationists design a marine protectedarea network. Large mammalian carnivores are used in multiple surrogate roles as well. Cougars, jaguars, tigers, grizzly bears, and giant pandas are

Table 10-2. Characteristics of species identified for representing potential marine protected areas in Nova Scotia, Canada (from King & Beazley 2005). Speciesab

Keystone Presence is critical to maintaining community organization and diversity. Functionally important predator, prey, plant, link, or modifier. Umbrella Require large amounts of habitat or several specific habitat types. Established habitat association. Indicator Sensitive to human activities. Presence implies pristine or undisturbed habitat. Vulnerable and sensitive Vulnerable Listed as endangered, threatened, or of special concern by COSEWIC. c Listed as a species at risk by an international body (e.g., IUCN). Reduced or declining population size. Sensitive Low genetic variation. Poor dispersal ability. Low fecundity. Dependent on patchy or unpredictable resources. Congregate in large groups. Long-distance migrations. Long-lived. Large-bodied.

M, N, V, X K, M, N, O, P, Q, T, X

A, C, E, F, K, L, O, S, T, b, c B, F, N, W, X,

A, B, D, F, G, H, I, J, K, L, M, O, Q, R, S, T, U, V, Y, b, c F, V

A, B, C, D, E, F, G, H, I, J, K, Y, b A, B, C, D, E, F, K, O, Q, S, U, b, c A, B, C, D, E, F, G, H, I, J, K, O, Q, R, T, U, V, W, Y, b, c A, B, C, D, Y A, B, C, E, S, T, U, Y, Z, a, b, c A, C, E, Y, b, c A, F, K, L, M, N, O, P, R, W, X, Z, a, c A, C, E, F, L, M, S, T, U, Y, Z, a, b, c A, B, C, E, I, Q, S, T, U, V, W, b, c A, B, C, D, E, I, Q, S, T, U, b, c


Table 10-2. Continued Speciesab

Flagship Charismatic species. Large vertebrate.

A, B, C, D, E, F, V, b, c A, B, C, D, E, F, G, H, J, K, O, P, Q, R, S, T, U, b, c

Commercial or recreational harvested species.

F, H, I, J, K, L, M, O, P, Q, R, S, T, W

a

Species (followed by total number of affirmative consensus responses in brackets). Mammals: A, North Atlantic right whale (14); B, northern bottlenose whale (11); C, blue whale (12); D, harbor porpoise (8); E, fin whale (11). Fish: F, Atlantic salmon (12); G, spotted wolfish (4); H, northern wolfish (5); I, cusk (6); J, Atlantic wolfish (5); K, Atlantic cod (9); L, American shad (5); M, Atlantic herring (6); N, northern sand lance (4); O, haddock (8); P, pollock (4); Q, Atlantic halibut (8); R, winter flounder (4); S, spiny dogfish shark (10); T, porbeagle shark (7); U, barndoor shark (8). Invertebrates: V, deep-sea corals (6); W, sea scallop (5); X, krill (4). Birds: Y, roseate tern (7); Z, red-necked phalarope (3); a, razorbill (3). Reptiles: b, leatherback turtle (12); c, loggerhead turtle (12). b Absence may be due to lack of knowledge rather than the species not displaying the characteristic. c Committee on the Status of Endangered Wildlife in Canada.

frequently touted as fulfilling several objectives by conservation organizations—ecological-disturbance indicators, keystone, flagship, and umbrella species (but see Linnell et al. 2000). It is advantageous to use the same species for different conservation objectives because there is an economy of scale—radio-tracking of cougars, for instance, can yield information on ranging (umbrella) and food habits (keystone), and is appealing research (flagship characteristics). Problems arise when some stakeholders view the species as fulfilling one conservation goal while others regard it as a relatively unhelpful tool in another context—leopards are alluring but poor indicators of anthropogenic disturbance. An additional problem is miscommunication over the precise conservation objectives for which the species is being used (as discussed in chapter 1).

Predictive Power of Surrogate Species The typology of surrogate species in Table 10-1 may change as new objectives arise and new buzzwords are added to the conservation lexicon. To

Surrogate Species in the Real World 271

date, however, there is surprisingly little hard evidence that surrogate species taken as a whole have a great deal of predictive power about biological systems, despite an extensive amount of research. In a qualitative and limited review of surrogate species conducted in 2004, no firm conclusions could be drawn about where and when surrogate species, meaning flagship, focal (sensu Lambeck), indicator (ecological-disturbance and cross-taxonresponse types), keystone, and classic umbrella species were effective in achieving conservation goals (Favreau et al. 2006). The difficulty was that the methods, temporal scales, geographic contexts, and taxonomic groups were all so diverse. Instead, it was suggested that methods be established to facilitate comparisons between studies, that data-rich areas be mined for multi-scale case studies and at varying temporal scales, and that long-term post-implementation monitoring be initiated. The issues notwithstanding, some positive highlights have emerged in the last two decades. These are (i) Large-scale investigations consistently identify the same areas of the globe where biodiversity is high. (ii) Endemic species in one taxon, especially birds, coincide with those in other taxa at a large scale. (iii) Families and genera predict species richness at large and small scales. (iv) Cross-taxon congruence in species richness is high when a network of regional reserves is chosen with the goal of representing all the species in sympatric taxa. (v) Fish and invertebrate communities predict environmental pollution and perturbation in freshwater habitats. (vi) Landuse change is best monitored using many taxa simultaneously. (vii) Bird communities are good predictors of structural changes in vegetation in forest and agricultural landscapes, and have power to predict responses of other bird species within the same guild. (viii) Flagship species are likely to help raise conservation funds. In conclusion, the search for reliable surrogates has been keen but has not yielded striking breakthroughs. Yet our inability to find consistent and hence reliable associations may matter less as economic concerns and dwindling conservation opportunities take a more prominent role in conservation planning, reserve management, ecological monitoring, and fund raising.

Distribution of Biodiversity In this section I show how conservation objectives can be pursued without recourse to using surrogate species. Already there is a strong precedent for using environmental variables to pinpoint important areas of biodiversity,


thus circumventing uncertainties of using surrogate species. A handful of ambitious non-species-based approaches have been made to identify terrestrial areas of conservation significance at a global scale, such as WWF’s Global Ecoregion Project, in which 223 areas were classified by their biological distinctiveness as globally outstanding, regionally outstanding, bioregionally outstanding, or locally important (Olson et al. 2001); Conservation International’s Wilderness Areas of >10,000 km2 with 70 percent intactness (Mittermeier et al. 2004); and the Wildlife Conservation Society’s Last of the Wild exercise, which mapped the most remote 10 percent of the globe, based on human population density, land transformation, accessibility, and electrical power infrastructure (Sanderson et al. 2002c). There is a good deal of consensus—areas such as the Eastern Arc Mountains, Tropical Andes, Madagascar, and Indonesia occur repeatedly in these priority-setting exercises that are conducted without recourse to using species inventories or surrogate taxa. Similarly, many measures of threat rely on habitat information rather than impending species’ extinctions. For example, it is now possible to calculate, at a 1-km2 grain, the proportion of different biomes turned over to cultivation or that are managed: nearly 50 percent of temperate grasslands, tropical dry forest, and temperate broadleaf forests have been converted so far, with remarkably small proportions of them under protection. Biomes with very high and very low levels of habitat conversion have only limited protection (see Figure 10-1). Surprisingly, temperate grasslands and Mediterranean forests are under greater threat than tropical moist forests— another finding made without recourse to relying on species data. Other measures, such as hotspots identified by Conservation International, melded species-inventory information with quantitative measures of habitat loss (Myers et al. 2000). In conclusion, large-scale conservation priority-setting has been successfully carried out on land, and now the most promising avenue of research in global prioritization exercises is matching areas of importance to networks of existing protected areas in order to show where new reserves need to be established to conserve threatened species (Hoekstra et al. 2005). These ventures can be performed with existing plant and vertebrate data sets and do not need to incorporate species surrogacy to move forward. In the marine biome, however, rather little progress has been made on prioritization, and surrogate taxa could be extremely useful in pinpointing locations of high biodiversity, given that it is difficult to sample marine taxa systematically. Therefore, there is a call to investigate between-taxon con-


Figure 10-1. Habitat conversion and protection in the world’s 13 terrestrial biomes. Biomes are ordered by their Conversion Risk Index. (CRI is the ratio of the percent area converted to the percent area protected—an index of relative risk of biome-wide biodiversity loss.) (Reprinted from Hoekstra et al. 2005.)

gruency in species richness within oceans (lack of data makes it difficult to gather information on endemism or rarity). Turning to economics, reserve planners have, until recently, focused on the benefits of protecting species in terms of complementary species richness, or conserving hotspots of rarity, and so on, either minimizing the


number of reserve sites but encompassing all species, or maximizing coverage subject to constraints. But protection costs money—at the start of the century it was estimated as $6–6.5 billion globally (James et al. 2001), with a funding shortfall of perhaps $1.3 billion in developing countries (Bruner et al. 2004). Expanding the protected-area network, the central goal of reserve selection and design studies, incurs survey, transaction, social, acquisition, damage, opportunity, management, and stewardship costs, which vary independently (Naidoo et al. 2006), and these are now being incorporated into models of reserve selection planning, at least at the regional scale, with a key element being recognition that all of these costs vary spatially. In conclusion, there is a noticeable shift in emphasis from biodiversity inventories to cost evaluation.

Reserve Selection Reserve site selection can benefit from incorporating environmental variables into planning. For example, forest type, structural diversity, treespecies richness, vegetation density, and canopy cover are fairly standard environmental surrogates describing species richness and species rarity of diverse insect groups (Fraser et al. 2009), so there is a precedent for broadening the use of these environmental measures to predict other forest fauna. It is the acknowledgment of economics, however, that is transforming reserve-selection procedures. At a national level, it has been recognized for some time that biodiversity surveys are costly but nonetheless economically worthwhile. Collating national surveys from eight countries, Balmford and Gaston (1999) showed that biodiversity surveys paid off in economic terms. They calculated costs of land purchase in 1990 $US and costs of reserve maintenance discounted into the future at annual rates of 5, 10, or 20 percent. Assuming that a survey allowed reserve networks to be planned in a complementary fashion rather than based on land purchased simply because of species richness or availability, and assuming too that this amounted to a minimum of 5 percent in purchase savings, they reckoned that savings averaged $1,320/km2 for five developing countries and $5,946/ km2 for three industrialized countries, far greater values than average survey costs calculated from three developing countries or two industrialized countries ($333/km2 and $753/km2, respectively). At a regional scale, there are also recognized gains in efficiency from incorporating the spatial distribution of costs when planning reserve networks. For example, Ando and colleagues (1998) reanalyzed Dobson and


collaborators’ 1997 data on 2,851 U.S. county-level tallies of 911 endangered species, but they also put county-by-county land-use values into the mix in order to compare the costs of covering the same number of species under a budget-constrained versus a site-constrained approach. The budget-constrained method was more efficient; for example, 453 species could be covered at 30 percent of the cost of achieving the same species coverage through minimizing the number of sites. Similar results have been arrived at using land acquisition prices in Oregon, USA (Polasky et al. 2001, 2008), in Africa (Moore et al. 2004), and in Southeast Asia (Wilson et al. 2006). These are welcome steps toward starting to place ivory-tower reserve-planning exercises into a more realistic economic framework. An additional injection of realism comes from the recognition that reserves are not all acquired simultaneously, because there are normally insufficient funds to put all reserve sites under protection at once (Pressey & Taffs 2001). Unprotected sites may be targeted by property developers in the interim, so it may be worth protecting a relatively valueless reserve at high risk rather than a species-rich reserve at low risk. Existing reserveselection algorithms ignore uncertainty about the fate of as-yet unprotected areas, and this is exacerbated in complementary scenarios because choosing the next reserve depends not only on the species pool in already-protected sites but also the pool in unprotected sites if the goal is, say, to represent each species once within the reserve network. Uncertainty about unprotected areas can be incorporated into reservenetwork planning using stochastic dynamic programming that looks at the whole period over which choices are made, or using an “informed myopic” algorithm that accounts for the possibility of development following each round of choice (Costello & Polasky 2004; Drechsler 2005). Some of these exercises are sophisticated: Meir and colleagues (2004), using stochastic dynamic programming, built an idealized bird-reserve network on the Columbia Plateau, USA, that incorporated the probability of sites becoming available for acquisition, the probability of species being extirpated at a site, and two levels of site costs. They concluded that simple rules of thumb, such as protect the available site with the highest amount of irreplaceability or the greatest species richness, were most effective (see also Turner & Wilcove 2006). Other models are able to incorporate incomplete species inventories (Grantham et al. 2008), additional parcels becoming available in the future (Grantham et al. 2009; McDonald-Madden et al. 2009), spatial constraints in site selection (Hof & Bevers 1998), trade-offs with other non-conservation objectives (Hof & Joyce 1992), and off-reserve proenvironmental management activities (Wilson et al. 2007).


Socioeconomic factors and the realism that they bring to the table are gaining greater ascendancy in conservation decision making because monetary costs are usually easier to estimate than species totals. Moreover, planners can incorporate species into reserves with greater cost-efficiency than selection procedures that eschew financial accounting (Perhans et al. 2008). For example, in an interesting exercise, Bode and colleagues (2008) determined efficient funding-allocation schedules for each of 34 of the world’s terrestrial biodiversity hotspots by integrating conservation costs of establishing new protected areas and habitat-loss rates from quantitative predictions of extinction risk for endemic vertebrates, and by using seven different surrogate taxonomic groups within a dynamic decision making framework. On average, two-thirds of funds based on any particular taxon would be allocated in the same way whichever surrogate taxon was considered (see Table 10-3). Five hotspots—areas with low cost and high threat— were given funds no matter which taxon was used as a biodiversity surrogate. When threat and cost were ignored (as they have been in so many reserve-selection models of the last decade), conservation schedules were

Table 10-3. Similarity of different funding schedules based on the taxa shown in each row and column, measured as the proportion of funding that is directed to the same hotspots in both schedules, expressed as a percentage. Top lines: funding schedules that include socioeconomic data and biodiversity variation. Bottom lines: funding schedules that do not consider regional variation in socioeconomic factors (from Bode et al. 2008).

Mammals Birds Amphibians Reptiles Freshwater fishes Tiger beetles

Birds

Amphibians

Reptiles

Freshwater fishes

Tiger beetles

Vascular plants

73.7 38.2 — — — — — — — — — —

73.2 8.8 90.6 8.8 — — — — — — — —

53.4 0. 54.5 14.7 54.2 67.7 — — — — — —

57.3 0. 48.3 0. 57.0 23.6 64.2 0. — — — —

64.5 0. 55.8 14.7 64.7 23.6 71.5 21.2 76.0 78.8 — —

78.9 0. 81.4 32.5 81.0 0 55.8 21.2 49.4 0. 64.2 21.2


now hugely affected by choice of taxon (see Table 10-3): only 20.5 percent, on average, shared funding, with no hotspot being allocated money using more than four of the seven taxa. If these results hold up with models incorporating other forms of realism, and at smaller regional scales, the need for effective species-indicators of biodiversity may be less pressing than was previously supposed.

Reserve Design and Management Environmental variables are very effective in capturing the distributions of species and communities at a regional level (Lindenmayer et al. 2002). Hess and colleagues (2006) compared the effectiveness of forest plans in the Triangle Region of North Carolina that were devised in four different ways. The first used six focal species (sensu Lambeck)—bobcat, eastern box turtle, barred owl, ovenbird, broad-winged hawk, and pileated woodpecker—chosen because they were extremely sensitive to area, dispersal, resources, or processes (see Table 10-4). The second mapped areas close to wetlands and riparian areas. The third located diverse forest types—wetland, mixed, evergreen, and deciduous. The fourth simply found large forest patches. Using North Carolina’s Natural Heritage Program, which contains point locations of species and natural communities, the effectiveness of each plan could be evaluated in three different ways (see Table 10-4).

Table 10-4. Three measures of effectiveness for focal species and environmental plans: the proportion of species and communities of conservation concern captured at least once (representation), the proportion of element occurrences captured (completeness), and the proportion of land in the inventory-based plan that was included (overlap) (from Hess et al. 2006).

Plan (area)

Focal species Close wetlands and riparian areas Diverse forest types Largest forested patches

Representation: species and communities captured (%)

Completeness: element occurrences captured (%)

Overlap: area of inventorybased plan captured

87 90 94 84

68 81 86 64

58 49 52 50


Certainly, all four methods were equivalent in terms of the proportion of species and communities that occurred at least once in the 2,446-km2 area (see representation). Interestingly, places close to water or with diverse forest types had a greater proportion of forest species and community occurrences than areas chosen using focal species (completeness). Focal species outperformed other methods with regard to the proportion of significant Natural Heritage area land that was covered, but not greatly (overlap). Umbrella species, focal species (sensu Lambeck), and landscape species need to be assessed with regard to how they promote financially sensible decision making. For instance, careful accounting shows that conserving wild dogs in large protected areas is far more cost-efficient than setting up a meta-population on private reserves (Lindsey et al. 2005), a finding that suggests that wild dogs would have use as a landscape species. Whether a species has keystone or engineering properties is so dependent on spatial and temporal context that there may be little point in formally incorporating these concepts explicitly into reserve design. In contrast, managers need to pay attention to population sizes of these species because they can, in some circumstances, dramatically affect ecological community structure, and this will demand sensitive monitoring of the protected area on a case-by-case basis. Foundation, keystone, and engineering species may have an as-yet undetermined role in public relations.

Species Indicators of Anthropogenic Change Environmental, ecological-disturbance, and management indicator species can sometimes be bypassed by using environmental measures to assess pollution, species presence, or sustainable forest management. Respectively, robust measures of the effects of pollution include indices of biological integrity that combine environmental metrics, limited species richness and composition, trophic composition, fish abundance, and condition (Karr 1991); forest structural, functional, and compositional attributes including canopy cover and age structure that can predict plant and animal biodiversity (e.g., Smith et al. 2008); and logging intensity, length of rotation cycle, area of native forest, and fragmentation are standard forestry metrics (Gardner 2010). Noss (1990, 1999) made a forceful case for monitoring not only species in order to assess environmental changes but for monitoring environmental factors, too. Since we know some of the adverse affects of fragmentation on species diversity, and the effects of habitat patch size on


population size, it is an obvious step simply to use aerial photography and satellite technology and GIS to monitor regional landscape change. On the ground, forest conditions, for example, can be measured by recording tree age-class ratios, structural complexity, blocks of continuous forest, road networks, exotic species, their abundances, or even recreational use of forests. Recently, the financial costs of biological surveys have been carefully documented in an effort to make species-monitoring more effective. For instance, radio telemetry and transect surveys can both be applied to determine habitat selection in birds. In a study of lesser kestrels in a Portuguese agricultural landscape, Franco and colleagues (2007) found that although telemetry set-up costs were higher than conducting transects, and day-today activities more expensive in terms of time and money, the area covered was larger and was unconstrained by access to roads (see Table 10-5).

Table 10-5. Cost-benefit analysis of radio-telemetry and transect surveys for foraging and habitat selection studies of lesser kestrels (from Franco et al. 2007). Costs/requirements

Field work period Number of field days Number of people needed per day Survey time per day per person (h) Surveyed area (km2) Access requirements (roads) Species handling/disturbance Identification skills and experience Factors affecting locations error Total number of points obtained People required for set up Set up time (days per person) =) Set up cost (C Set up knowledge =) (based on 0.25= Daily cost (C C /km) Time cost spent (h) =) Total costs (set up and daily cost) (C Significant differences obtained Time spent per significant difference (h) =) Cost per significant difference (C

Telemetry

Transcects

13 Mar–10 Jun 22 2 4 63 Small Yes No Weather 195 2 17 5,850 Large 3.7 312 8,115 26

8 Mar–10 Jun 24 1 4 34.6 Large No Yes Observer 209 1 2 790 Small 10 112 1,815 22

12 312

5 82.5


Assessing biodiversity-survey costs across three forest types in Brazil— primary, secondary, and eucalypt plantations—Gardner and coworkers (2008a) took stock of the monetary cost of sampling different taxa by adding up costs of equipment and salaries of field assistants, relative time invested including worker hours in laboratory and field, and expertise needed to identify specimens. The last measure varied hugely with some groups such as birds, large mammals, and bats being identified to the species level, others such as arachnids being identified mostly to morphospecies; for some taxa, species-level guides were available; for some there were many experts (e.g., for fruit-feeding butterflies), for others such as orchid bees, only a handful of experts (see Table 10-6). Examining costs of surveying each taxon in each of the habitats (sampling only the equivalent number of individuals to that of the least effectively sampled taxon) revealed that small mammals were consistently expensive to survey every-

Table 10-6. Study taxa (vertebrates, invertebrates, trees, and lianas) sampled in Jari, northeast Brazilian Amazonia (from Gardner et al. 2008a). Number of Taxon

Leaf-litter amphibians Lizards Large mammals Small mammals Bats Birds Scavenger flies Fruit-feeding butterflies Dung beetles Epigeic arachnids Fruit flies Orchid bees Moths Trees and lianasc a,b

individuals

1,739 1,937 280 219 4,125 6,865 5,365 10,588 9,203 3,176 5,085 2,363 1,848 7,600

% morphospecies species

23 30 19 32 54 255 30 130 85 116 38 22 335 219

8.6 3.3 0. 9.4 0. 0. 20.0 0.8 35.3 75.9 5.3 18.2 50.7 NA

Species guide?

No Yes Yes No No Yes No No No No No Yes No NA

Experts globala

Brazilb

20 10 20–30 8 >250 >150 20 10 30 10 >50 15–20 NA 5 >50 20 3 1 30 20 4 3 30 10 15 3 NA NA

Estimate of the number of experts (a) in the world, or (b) in Brazil who would be able to identify samples of their taxonomic group from Jari to the level of species or morphospecies without extensive consultation with reference material or other scientists. c Only genus-level information included for trees and lianas.


where, as to a lesser extent were moths and arachnids, while expenses for some taxa, such as fruit flies, depended on the habitat in which they were sampled. Using the IndVal method to assess ecological-indicator value, or average correlation coefficients between species’ abundance matrices for each taxon and all the remaining others, no one taxon was clearly superior in reflecting response patterns of others to different types of forest (although some were poorer, such as amphibians, bats, and arachnids, depending on the method). There was a strong negative relationship between taxonspecific cost and benefit for each forest type, however. Taxa that were cheapest to survey, such as birds and dung beetles, were the most effective ecological indicators, whereas expensive-to-survey taxa such as small mammals and moths were poor at discriminating other taxa’s responses to habitat modification (see Figure 10-2)—an optimistic finding. Furthermore, knowing taxon-specific costs allowed cost reductions of up to 16 percent by surveying certain taxa simultaneously—leaf-litter amphibians and lizards, small mammals and herpetofauna, arachnids and herpetofauna, and dung beetles and blow flies. Information about net-indicator benefits and doubling up on field surveys gives a fresh and tighter focus to the choices that survey teams can make regarding indicator taxa.

Promoting Conservation Large charismatic rare species continue to attract the attention of the public and are used to galvanize political will to set up reserves. Flagship species are not the sole vehicle to promote conservation, however—threatened biomes such as the warming arctic and disappearing rainforest are familiar hooks to attract public attention in the industrialized world. Specific habitats such as the Everglades or the Serengeti plains appear to work well as conservation rallying points, too. The idea of focusing attention on habitats using environmentally memorable features rather than using species proxies is not new. In lieu of the fact that the public is becoming more sophisticated in its understanding of conservation problems through increasing media attention, it would be instructive to know how much detailed conservation knowledge different sectors of society can assimilate and respond to, and how much NGOs need to worry about viewer fatigue with regard to using the same species repeatedly and the same stories of doom and gloom.

12

(a)

10

BI DB

Significant ecological indicator species (indicator species as % of total for a given taxon, averaged across forests)

8

LI BU TR

6

SF OB

4

LM

BA AM FF AR

2

MO

SM

0

12

(b)

10

DB

8 6

BI

TR

BU AM

SF OB

4

LI LM BA

FF

AR

2

MO

SM

0 12

(c)

10

BI DB

8 6 4

LI

BU BA AM

SF OB

FF

2 0 100

AR MO

1000

SM 10000

Standardized survey cost (US $)

Figure 10-2. Cost-effectiveness of surveying 14 higher taxa in the Brazilian Amazon. The relationship between the standardized cost and ecological-indicator value of a variety of focal taxa sampled in (a) primary, (b) secondary, and (c) plantation forests. Note log scale on x-axis. BI, birds; DB, dung beetles; LI, lizards; TR, trees and lianas; BU, butterflies; AM, amphibians; BA, bats; SF, scavenger flies; LM, large mammals; OB, orchid bees; FF, fruit flies; AR, arachnids; MO, moths; SM, small mammals. (Reprinted from Gardner et al. 2008a.)


Effective conservation public relations needs to move from conventional wisdom to evidence-based strategizing. Some evidence suggests that flagship species do not transfer easily from the industrialized- to the developing-world. Research is needed into national perceptions and receptivity to conservation messages in the developing world. Furthermore, it is not clear whether the flagship-species concept works well in human communities that live in contact with flagship species, given wildlife-human conflict and opportunities for exploitation (Woodroffe et al. 2005).

Wrap-Up Surrogate species are a necessary shortcut to pursuing conservation objectives, given the shortage of conservation funding and time, coupled with the complexities of species distributions and the complicated way that different species respond to environmental perturbation. The efficacy of surrogate species and surrogate taxa therefore needs to be assessed carefully in a world where strategic conservation planning is now paramount. Twenty years ago few would have guessed how much thought, computer time, and researchers’ salaries would have been spent on finessing surrogate methods, especially in regards to reserve-site selection and environmental indicators—effort and money that could arguably have been directed toward practical solutions. While some recognize that conservation science is in an “implementation crisis” and needs to move into planning and management phases (Knight et al. 2006), much of the surrogate-species literature is still firmly entrenched in the ivory tower of academia—“journals like Ecology still packed with papers describing more and more sophisticated analyses applied to more and more trivial problems” (Ehrlich 1997, 111). The next step must be to apply studies to real-life situations by working with stakeholders and land-use planners—work that involves socioeconomic knowledge, flexibility, and sensitivity. It is sad that the science of surrogate species is still a cottage industry of scientific-paper production with only sporadic relevance to solving conservation challenges successfully in the real world. Hopefully, pleas for relevance in conservation science (Salafsky et al. 2002; Sutherland et al. 2004; Cleary 2006; Ferraro & Pattanayak 2006) will galvanize practical application of surrogate species concepts.


Summary Surrogate-species terminology can be clarified by qualifying surrogatespecies phrases more precisely and by stating conservation objectives more clearly. Some species can be used for different conservation goals simultaneously. In general, surrogate species or species-groups do not have a great deal of power to predict the presence of target taxa or their responses to environmental change, although there are some encouraging exceptions. The distribution of terrestrial biodiversity can be mapped globally using environmental variables without recourse to using surrogate taxa, although the latter may still be necessary for mapping marine biodiversity. Reserveplanning procedures now incorporate costs of reserve acquisition and uncertainty about reserve availability in the future, and these factors can relieve the pressure on choosing appropriate surrogate taxa. Environmental variables can be used with great effect in reserve design and in signifying anthropogenic change. Ecological monitoring and surveys can be made more cost-effective with simple financial auditing. Conservation can be promoted using biomes and habitats as well as single species. Therefore, environmental and economic considerations hold promise for bypassing the use of surrogate species as conservation tools.

Large beetle larvae are a delicacy among the Pimbwe people of western Tanzania. They risk arrest to go into Katavi National Park to find Acacia trees where these larvae—called madime in the Kipimbwe language—are found. This raises questions about which species might best foster a conservation ethic in the area and more generally about culturally appropriate flagship species. (Drawing by Sheila Girling.)

references

Abbitt, R. J. F., J. M. Scott, and D. S. Wilcove. 2000. The geography of vulnerability: incorporating species geography and human development patterns into conservation planning. Biological Conservation 96:169–75. Ackery, P. R., and R. I. Vane-Wright. 1984. Milkweed Butterflies. Cornell: Cornell University Press. Adams, S. M. 2002., ed. Biological Indicators of Aquatic Ecosystem Stress. Bethseda, MD: American Fisheries Society. Aebischer, N. J., A. D. Evans, P. V. Price, and J. A. Vickery. 2000. Ecology and Conservation of Lowland Farmland Birds. Tring, UK: British Ornithologists Union. Aguilar-Amuchastegui, N., and Henebry, G. M. 2007. Assessing sustainability indicators for tropical forests: spatio-temporal heterogeneity, logging intensity, and dung beetle communities. Forest Ecology and Management 253:56–67. Airame, S., J. E. Dugan, K. D. Laferty, H. Leslie, D. A. McArdle, and R. R. Warner. 2003. Applying ecological criteria to marine reserve design: a case study from the California Channel Islands. Ecological Applications 13:S170–84. Allen, A. P., T. R. Whittier, D. P. Larsen, P. R. Kaufmann, R. J. O’Connor, R. M. Hughes, R. S. Stemberger, S. S. Dixit, R. O. Brinhurst, A. T. Hirlihy, and S. G. Paulsen. 1999. Concordance of taxonomic richness patterns across multiple assemblages in lakes of the north-eastern United States. Canadian Journal of Fish and Aquatic Sciences 56:739–47. Altieri, A. H., and J. D. Witman. 2006. Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem. Ecology 87:717–30. Alves da Mata, R., M. McGeoch, and R. Tidon. 2008. Drosophilid assemblages as a bioindicator system of human disturbance in the Brazilian savanna. Biodiversity and Conservation 17:2899–916. Anand, M., S. Laurence, and B. Rayfield. 2005. Diversity relationships among taxonomic groups in recovering and restored forests. Conservation Biology 19:955–62. Andelman, S. J., and W.F. Fagan. 2000. Umbrellas and flagships: efficient conservation surrogates or expensive mistakes? Proceedings of the National Academy of Sciences 97:5954–59. Andelman, S. J., and M. R. Willig. 2003. Present patterns and future prospects for biodiversity in the Western Hemisphere. Ecology Letters 6:818–24.

287

288 References Andersen, A. N. 1995. Measuring more of biodiversity: genus richness as a surrogate for species richness in Australian ant faunas. Biological Conservation 73:39– 43. Anderson, J., J. M. Rowcliffe, and G. Cowlishaw. 2007. The Angola black-andwhite colobus (Colobus angolensis palliates) in Kenya: historical range contraction and current conservation status . American Journal of Primatology 69:664– 80. Ando, A., J. Camm, S. Polasky, and A. Solow. 1998. Species distribution, land values, and efficient conservation. Science 279:2126–28. Angermeier, P. L., and J. R. Karr. 1994. Biological integrity versus biological diversity as policy directives. BioScience 44:690–97. Armstrong, D. 2002. Focal and surrogate species: getting the language right. Conservation Biology 16:285–86. Arrigo, K. R., C. W. Sullivan, and J. N. Kremer. 1991. A bio-optical model of Antarctic sea lice. Journal of Geophysical Research 96 C6:10581–92. Araujo, M. B., C. J. Humphries, P. J. Densham, R. Lampinen, W. J. M. Hagemeijer, A. J. Mitchell-Jones, and J. P. Gase. 2001. Would environmental diversity be a good surrogate for species diversity? Ecography 24:103–10. Araujo, M. B., P. J. Densham, and P. H. Williams. 2004. Representing species in reserves from patterns of assemblage diversity. Journal of Biogeography 31:1037– 50. Asquith, N. M., S. J. Wright, and M. J. Claus. 1997. Does mammal community composition control seedling recruitment in neotropical forests? Evidence from islands in central Panama. Ecology 78:941–46. Atauri, J. A., and J. V. de Lucio. 2001. The role of landscape structure in species richness distribution of birds, amphibians, reptiles and lepidoterans in Mediterranean landscapes. Landscape Ecology 16:147–59. Attrill, M. J. 2002. Community-level indicators of stress in aquatic ecosystems. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 473–508. Bethseda, MD: American Fisheries Society. Awad, A. A., C. L. Griffiths, and J. K. Turpie. 2002. Distribution of South African marine benthic invertebrates applied to the selection of priority conservation areas. Diversity and Distributions 8:129–45. Awimbo, J. A., D. A. Norton, and F. B. Overmars. 1996. An evaluation of representativeness for nature conservation, Hokitika Ecological District, New Zealand. Biological Conservation 75:177–86. Ball, S. M. J. 2004. Stocks and exploitation of East African blackwood Dalbergia melanoxylon: a flagship species for Tanzania’s Miombo woodlands? Oryx 38:266–72. Balmford, A., and K. J. Gaston. 1999. Why biodiversity surveys are good value. Nature 398:204–5. Balmford, A., M. J. B. Green, and M. G. Murray. 1996a. Using higher-taxon rich-

References 289 ness as a surrogate for species richness: I. Regional tests. Proceedings of the Royal Society London B 263:1267–74. Balmford, A., A. H. M. Jayasuriya, and M. J. B. Green 1996b. Using higher-taxon richness as a surrogate for species richness: II. Local applications. Proceedings of the Royal Society of London B 263:1571–75. Balmford, A., and A. Long. 1995. Across-country analyses of biodiversity congruence and current conservation effort in the tropics. Conservation Biology 9:1539–47. Balmford, A., A. J. E. Lyon, and R. M. Lang. 2000. Testing the higher-taxon approach to conservation planning in a megadiverse group: the macrofungi. Biological Conservation 93:209–17. Bangert, R. K., and C. N. Slobodchikoff. 2006. Conservation of prairie dog ecosystem engineering may support arthropod beta and gamma diversity. Journal of Arid Environments 67:100–115. Bani, L., M. Baietto, L. Bottoni, and R. Massa. 2002. The use of focal species in designing a habitat network for a lowland area of Lombardy, Italy. Conservation Biology 16:826–31. Bani, L., D. Massimino, L. Bottoni, and R. Massa. 2006. A multiscale method for selecting indicator species and priority conservation areas: a case study for broadleaved forests in Lombardy, Italy. Conservation Biology 20:512–26. Barkai, A., and C. McQuaid. 1988. Predator-prey role reversal in a marine benthic ecosystem. Science 242:62–64. Barlow, J., W. L. Overal, I. S. Araujo, T. A. Gardner, and C. A. Peres. 2007c. The value of primary, secondary and plantation forests for fruit-feeding butterflies in the Brazilian Amazon. Journal of Applied Ecology 44:1001–12. Barlow, J., T. A. Gardner, A. I. Araujo, T. C. Avila-Pires, A. B. Bonaldo, J. E. Costa, M. C. Esposito, L. V. Ferreira, J. Hawes, M. I. M. Hernandez, M. S. Hoogmoed, R. N. Leite, N. F. Lo-Man-Hung, J. R. Malcolm, M. B. Martins, L. A. M. da Silva, C. da Silva Motta, and C. A. Peres. 2007d. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences 104:18555–60. Barlow, J., T. A. Gardner, L. V. Ferreira, and C. A. Peres. 2007a. Litter fall and decomposition in primary, secondary and plantation forests in the Brazilian Amazon. Forest Ecology and Management 247:91–97. Barlow, J., L. A. M. Maestre, T. A. Gardner, and C. A. Peres. 2007b.The value of primary, secondary and plantation forests for Amazonian birds. Biological Conservation 136:212–31. Barlow, J., I. S. Araujo, W. L. Overal, T. A. Gardner, F. da Silva Mendes, I. R. Lake, C. A. Peres. 2008. Diversity and composition of fruit-feeding butterflies in tropical Eucalyptus plantations. Biodiversity and Conservation 17:1089–104. Barton, B. A., J. D. Morgan, and M. M. Vijayan. 2002. Physiological and condition-related indicators of environmental stresses in fish. In Biological Indicators

290 References of Aquatic Ecosystem Stress, ed. S. M. Adams, 111–48. Bethseda, MD: American Fisheries Society. Basset, Y., E. Charles, D. S. Hammond, and V. K. Brown. 2001. Short-term effects of canopy openness on insect herbivores in a rain forest in Guyana. Journal of Applied Ecology 38:1045–58. Basset, Y., J. F. Mavoungou, J. B. Mikissa, O. Mikissa, S. E. Miller, R. L. Kitching, and A. Alonso. 2004. Discriminatory power of different arthropod data sets for the biological monitoring of anthropogenic disturbance in tropical forests. Biodiversity and Conservation 13:709–32. Basset, Y., O. Missa, A. Alonso, S. E. Miller, G. Curletti, M. de Meyer, C. Eardley, O. T. Lewis, M. W. Mansell, V. Novotny, and T. Wagner. 2008. Changes in arthropod assemblages along a wide gradient of disturbance in Gabon. Conservation Biology 22:1552–63. Beazley, K., and N. Cardinal. 2004. A systematic approach for selecting focal species for conservation in the forests of Nova Scotia and Maine. Environmental Conservation 31:91–101. Bedward, M., R. L. Pressey, and D. A. Keith. 1992. A new approach for selecting fully representative reserve networks: addressing efficiency, reserve design and land suitability with an iterative analysis. Biological Conservation 62:115–25. Beeby, A. 2001. What do sentinels stand for? Environmental Pollution 112:285–98. Beger, M., G. P. Jones, and P. L. Munday. 2003. Conservation of coral reef biodiversity: a comparison of reserve selection procedures for corals and fishes. Biological Conservation 111:53–62. Beger, M., S. A. McKenna, and H. P. Possingham. 2007. Effectiveness of surrogate taxa in the design of coral reef reserve systems in the Indo-Pacific. Conservation Biology 21:1584–93. Begon, M., J. L. Harper, and C. R. Townsend. 1990. Ecology, Individuals, Populations and Communities (2nd ed). Oxford, UK: Blackwell. Belbin, L. 1993. Environmental representativeness: regional partitioning and reserve selection. Biological Conservation 66:223–30. Bellwood, D. R., A. S. Hoey, J. L. Ackerman, and M. Depczynski. 2006. Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Global Change Biology 12:1587–94. Benton, T. G., D. M. Bryant, L. Cole, and H. Q. P. Crick. 2002. Linking agricultural practice to insect and bird populations: a historical study over three decades. Journal of Applied Ecology 39:673–87. Berg, A., and M. Tjernberg. 1996. Common and rare Swedish vertebrates—distribution and habitat preferences. Biodiversity and Conservation 5:101–28. Bergamini, A., C. Sheidegger, S. Stofer, P. Carvalho, S. Davey, M. Dietrich, F. Dubs, E. Farkas, U. Groner, K. Karkkainen, C. Keller, L. Lokos, S. Lommi, C. Maguas, R. Mitchell, P. Pinho, V. J. Rico, G. Aragon, A.-M. Truscott, P. Wolseley, and A. Watt. 2005. Performance of macrolichens and lichen genera

References 291 as indicators of lichen species richness and composition. Conservation Biology 19:1051–62. Berger, J. 1997. Population constraints associated with the use of black rhinos as an umbrella species for desert herbivores. Conservation Biology 11:69–78. Berger, J., P. B. Stacey, L. Bellis, and M. P. Johnson. 2001. A mammalian predatorprey imbalance: grizzly bear and wolf extinction affect avian neotropical migrants. Ecological Applications 11:947–60. Berger, K. M., and E. M. Gese. 2007. Does intereference competition with wolves limit the distribution and abundance of coyotes? Journal of Animal Ecology 76:1075–85. Berger, K. M., E. M. Gese, and J. Berger. 2008. Indirect effects and traditional trophic cascades: a test involving wolves, coyotes, and pronghorn. Ecology 89:818–28. Berkman, H. E., C. F. Rabeni, and T. P. Boyle. 1986. Biomonitors of stream quality in agricultural areas: fish versus invertebrates. Environmental Management 10:413–19. Bertness, M. D. 1984. Habitat and community modification by an introduced herbivorous snail. Ecology 65:370–81. Bertness, M. D., and S. D. Hacker. 1994. Physical stress and positive associations among marsh plants. American Naturalist 144:363–72. Beschta, R. L. 2003. Cottonwoods, elk, and wolves in the Lamar Valley of Yellowstone National Park. Ecological Applications 13:1295–309. Betrus, C. J., E. Fleishman, and R. B. Blair. 2005. Cross-taxonomic potential and spatial transferability of an umbrella species index. Journal of Environmental Management 74:79–87. Bhagwat, S.A., K.J. Willis, H.J.B. Birks, and R.J. Whittaker. 2008. Agroforestry: a refuge for tropical biodiversity? Trends in Ecology and Evolution 23:261–267. Bibby C. J., N. J. Collar, M. J. Crosby, M. F. Heath, Ch. Imboden, T. H. Johnson, A. J. Long, A. J. Stattersfield, and S. J. Thirgood.1992. Putting Biodiversity on the Map: Priority Areas for Global Conservation. Cambridge, UK: International Council for Bird Preservation. Bifolchi, A., and T. Lode. 2005. Efficiency of conservation shortcuts: an investigation with otters as umbrella species. Biological Conservation 126:523–27. Billeter, R., J. Liira, D. Bailey, R. Bugter, P. Arens, I Augenstein, S. Aviron, J. Baudry, R. Bukacek, F. Burel, M. Cerney, G. De Blust, R, De Cock, T. Diekotter, H. Dietz, J. Dirksen, C. Dormann, W. Durka, M. Frenzel, R. Hamersky, F. Hendrickx, F. Herzog, S. Klotz, B. Koolstra, A. Lausch, D. Le Coeur, J. P. Maelfait, P. Opdam, M. Roubalova, A. Schermann, N. Schermann, T. Schmidt, O. Schweiger, M. J. M. Smulders, M. Speelmans, P. Simova, J. Verboom, W. K. R. E. van Wingereden, M. Zobel, and P. J. Edwards. 2008. Indicators for biodiversity in agricultural landscapes: a pan-European study. Journal of Applied Ecology 45:141–50.

292 References Bilton, D. T., L. Mcabendroth, A. Bedford, and P. M. Ramsay. 2006. How wide to cast the net? Cross-taxon congruence of species richness, community similarity and indicator taxa in ponds. Freshwater Biology 51:578–90. Bishop, J. A., and W. L. Myers. 2005. Associations between avian functional guild response and regional landscape properties for conservation planning. Ecological Indicators 5:33–48. Bladt, J., F. W. Larsen, and C. Rahbek. 2008. Does taxonomic diversity in indicator groups influence their effectiveness in identifying priority areas for species conservation? Animal Conservation 11:546–54. Blair, R. B. 1996. Land use and avian species diversity along an urban gradient. Ecological Applications 6:506–19. Blair, R. B. 1999. Birds and butterflies along an urban gradient: surrogate taxa for assessing biodiversity? Ecological Applications 9:164–70. Bode, M., K. A. Wilson, T. M. Brooks, W. R. Turner, R. A. Mittermeier, M. F. McBride, E. C. Underwood, and H. P. Possingham. 2008. Cost-effective global conservation spending is robust to taxonomic group. Proceedings of the the National Academy of Sciences 105:6498–501. Bohning-Gaese, K. 1997. Determinants of avian species richness at different spatial scales. Journal of Biogeography 24:49–60. Bond, W. J. 1994. Keystone species. In Biodiversity and Ecosystem Function, ed. E.-D. Schulze and H. A. Mooney, 237–53. Berlin: Springer-Verlag. Bonn, A., and K. J. Gaston 2005. Capturing biodiversity: selecting priority areas for conservation using different criteria. Biodiversity and Conservation 14:1083– 1100. Bonn, A., A. S. L. Rodrigues, and K. J. Gaston. 2002. Threatened and endemic species: are they good indicators of patterns of biodiversity on a national scale? Ecology Letters 5:733–41. Bonn, A., and B. Schroder. 2001. Habitat models and their transfer for single and multi species groups: a case study of carabids in an alluvial forest. Ecography 24:483–96. Borgerhoff-Mulder, M., R. Schacht, T. Caro, J. Schacht, and B. Caro. 2009. Knowledge and attitudes of children of the Rupununi: implications for conservation in Guyana. Biological Conservation 142:879–87. Boulton, A. J. 1999. An overview of river health assessment: philosophies, practice, problems and prognosis. Freshwater Biology 41:469–79. Bowen-Jones, E., and A. Entwistle. 2002. Identifying appropriate flagship species: the importance of culture and local contexts. Oryx 36:189–95. Boyd, S. E., H. L. Rees, and C. A. Richardson. 2000. Nematodes as sensitive indicators of change at dredge material disposal sites. Estuarine, Coastal, and Shelf Science 51:805–19. Bradbury, R. B., and W. B. Kirby. 2006. Farmland birds and resource protection in the UK: cross-cutting solutions for multi-functional farming? Biological Conservation 129:530–42.

References 293 Bradshaw, C. J. A., Y. Fukuda, M. Letnic, and B. W. Brook. 2006. Incorporating known sources of uncertainty to determine precautionary harvests of saltwater crocodiles. Ecological Applications 16:1436–48. Breininger, D. R., V. L. Larson, B. W. Duncan, R. B. Smith, D. M. Oddy, and M. F. Goodchild. 1995. Landscape patterns of Florida scrub jay habitat use and demographic success. Conservation Biology 9:1442–53. Bried, J. T., B. D. Herman, and G. N. Ervin. 2007. Umbrella potential of plants and dragonflies for wetland conservation: a quantitative case study using the umbrella index. Journal of Applied Ecology 44:833–42. Brook, B. W., C. J. A. Bradshaw, L. P. Koh, and N. S. Sodhi. 2006. Momentum drives the crash: mass extinction in the tropics. Biotropica 38:302–5. Brook, B. W., N. S. Sodhi, and C. J. A. Bradshaw. 2008. Synergies among extinction drivers under global change. Trends in Ecology and Evolution 23:453–60. Brooks, T., A. Balmford, N. Burgess, J. Fjeldsa, L. A. Hansen, J. Moore, C. Rahbek, and P. Williams. 2001. Toward a blueprint for conservation in Africa. BioScience 51:613–24. Brooks, T., G. A. B. da Fonseca, and A. S. L. Rodrigues. 2004. Species, data, and conservation planning. Conservation Biology 18:1682–88. Brooks, T. M., R. A. Mittermeier, G. A. B. da Fonseca, J. Gerlach, M. Hoffmann, J. F. Lamoreux, C. G. Mittermeier, J. D. Pilgrim, and A. S. L. Rodrigues. 2006. Global biodiversity conservation priorities. Science 313:58–61. Brown, C. 2000. The global outlook for present and future wood supply from forest plantation. Working Paper No. GFPOS/WP/03. FAO. Brown, J. H. 1971. Mammals on mountaintops: non-equilibrium insular biogeography. American Naturalist 105:467–78. Brown, J. H., and E. J. Heske. 1990. Control of a desert-grassland transition by a keystone rodent guild. Science 250:1705–7. Brown, K. S. and A. V. L. Freitas. 2000. Atlantic forest butterflies: indicators for landscape conservation. Biotropica 32:934–56. Brummitt, N., and E. N. Lughadha. 2003. Biodiversity: where’s hot and where’s not? Conservation Biology 17:1442–48. Bruner, A. G., R. E. Gullison, and A. Balmford. 2004. Financial costs and shortfalls of managing and expanding protected-area systems in developing countries. BioScience 54:1119–26. Bruno, J. F., and M. I. O’Connor. 2005. Cascading effects of predator diversity and omnivory in a marine food web. Ecology Letters 8:1048–56. Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18:119–25. Buchman, N., K. Cuddington, and J. Lambrinos. 2007. A historical perspective on ecosystem engineering. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 25–46. Amsterdam: Elsevier. Bunn, S. E., and A. H. Arthington. 2002. Basic principles and ecological

294 References consequences of altered flow regimes for aquatic biodiversity. Environmental Management 30:492–507. Burgess, N. D., C. Rahbek, F. W. Larsen, P. Williams, and A. Balmford. 2002. How much of the vertebrate diversity of sub-Saharan Africa is catered for by recent conservation proposals? Biological Conservation 107:327–39. Burrell, G. A., and F. M. Seibert. 1916. Gases found in coal mines. Miners’ Circular 14. Washington, DC: Bureau of Mines, Department of the Interior. Buse, J., T. Ranius, and T. Assmann. 2008. An endangered longhorn beetle associated with old oaks and its possible role as an ecosystem engineer. Conservation Biology 22:329–37. Butchart, S. H. M., A. J. Stattersfield, J. Baillie, L. A. Bennun, S. N. Stuart, H. R. Akcakaya, C. Hilton-Taylor, and G. M. Mace. 2005. Using Red List Indices to measure progress towards the 2010 target and beyond. Philosophical Transactions of the Royal Society of London B 360:255–68. Butler, R. A., and W. F. Laurance. 2008. New strategies for conserving tropical forests. Trends in Ecology and Evolution 23:469–72. Byers, J.E., K. Cuddington, C.G. Jones, T.S.Talley, A Hastings, J.G. Lambrinos, J.A. Crookks, and W.G. Wilson. 2006. Using ecosystem engineers to restore ecological systems. Trends in Ecology and Evolution 21:493–500. Cabeza, M., A. Arponen, and A. Van Teeffelen. 2008. Top predators: hot or not? A call for systematic assessment of biodiversity surrogates. Journal of Applied Ecology 45:976–980. Cabeza, M., and A. Moilanen. 2001. Design of reserve networks and the persistence of biodiversity. Trends in Ecology and Evolution 16:242–48. Cairns, J., Jr. 1986. The myth of the most sensitive species. BioScience 36:670–72. Cairns, J., P. V. McCormick, and B. R. Niederlehner. 1993. A proposed framework for developing indicators of ecosystem health. Hydrobiologica 236:1–44. Cairns, J., Jr., and J. R. Pratt. 1993. A history of biological monitoring using benthic macroinvertebrates. In Freshwater Biomonitoring and Benthic Macroinvertebrates, eds. D. M. Rosenberg and V. H. Resh, 10–27. New York: Chapman & Hall. Cairns, J., Jr., and W. H. van der Schalie. 1980. Biological monitoring Part I—early warning systems. Water Research 14:1179–96. Canterbury, G. E., T. E. Martin, D. R. Petit, L. J. Petit, and D. F. Bradford. 2000. Bird communities and habitat as ecological indicators of forest condition in regional monitoring. Conservation Biology 14:544–58. Cantu, C., R. G. Wright, J. M. Scott, and E. Strand. 2004. Assessment of current and proposed nature reserves of Mexico based on their capacity to protect geophysical features and biodiversity. Biological Conservation 115:411–17. Cardillo, M., G. M. Mace, J. L. Gittleman, and A. Purvis. 2006. Latent extinction risk and the future battlegrounds of mammal conservation. Proceedings of the National Academy of Sciences 103:4157–61. Cardillo, M., A. Purvis, W. Sechrest, J. L. Gittleman, J. Bielby, and G. M. Mace.

References 295 2004. Human population density and extinction risk in the world’s carnivores. PLoS Biology 2:909–13. Cardoso, P., I. Silva, N. G. de Oliveira, and A. R. M. Serrano. 2004a. Indicator taxa of spider (Araneae) diversity and their efficiency in conservation. Biological Conservation 120:517–24. Cardoso, P., I. Silva, N. G. de Oliveira, and A. R. M. Serrano. 2004b. Higher taxa surrogates of spider (Araneae) diversity and their efficiency in conservation. Biological Conservation 117:453–59. Carey, A. B., S. P. Horton, and B. L. Biswell. 1992. Northern spotted owls: influence of prey base and landscape character. Ecological Monographs 62:223–50. Carignan, V., and M.-A. Villard. 2002. Selecting indicator species to monitor ecological integrity: a review. Environmental Monitoring and Assessment 78:45–61. Caro, T. M. 2000. Focal species. Conservation Biology 14:1569–70. Caro, T. M. 2001. Species richness and abundance of small mammals inside and outside an African national park. Biological Conservation 98:251–57. Caro, T. M. 2002a. Focal and surrogate species: getting the language right. Conservation Biology 16:286–87. Caro, T. M. 2002b. Factors affecting the small mammal community inside and outside Katavi National Park, Tanzania. Biotropica 34:310–18. Caro, T. M. 2003. Umbrella species: critique and lessons from East Africa. Animal Conservation 6:171–81. Caro, T. 2007. The Pleistocene rewilding gambit. Trends in Ecology and Evolution 22:281–83. Caro, T., J. Eadie, and A. Sih. 2005. Use of substitute species in conservation biology. Conservation Biology 19:1821–26. Caro, T., A. Engilis Jr., E. Fitzherbert, and T. Gardner 2004. Preliminary assessment of the flagship species concept at a small scale. Animal Conservation 7:63–70. Caro, T. M., and G. O’Doherty. 1999. On the use of surrogate species in conservation biology. Conservation Biology 13:805–14. Carrillo, E., G. Wong, and A. D. Cuaron. 2000. Monitoring mammal populations in Costa Rican protected areas under different hunting restrictions. Conservation Biology 14:1580–91. Carroll, C., R. F. Noss, and P. C. Paquet. 2001. Carnivores as focal species for conservation planning in the Rocky Mountain region. Ecological Applications 11:961–80. Carroll, C., R. F. Noss, P. C. Paquet, and N. H. Schumaker. 2003. Use of population viability analysis and reserve selection algorithms in regional conservation plans. Ecological Applications 13:1773–89. Carroll, S. S., and D. L. Pearson. 1998. Spatial modeling of butterfly species richness using tiger beetles (Cicindelidae) as a bioindicator taxon. Ecological Applications 8:534–43. Carson, R. 1962. Silent Spring. Boston, MA: Houghton Mifflin. Carwardine, J., C. J. Klein, K. A. Wilson, R. L. Pressey, and H. Possingham. Hitting

296 References the target and missing the point: target-based conservation planning in context. Conservation Letters 2:3–10. Caughley, G., and A. Gunn. 1996. Conservation Biology in Theory and Practice. Cambridge, MA: Blackwell Science. Caughley, H. 1976. The elephant problem—an alternative hypothesis. East African Wildlife Journal 14:265–83. Ceballos, G., and P. R. Ehrlich. 2006. Global mammal distributions, biodiversity hotspots, and conservation. Proceedings of the National Academy of Sciences 103:19374–79. Ceballos, G., P. R. Ehrlich, J. Soberon, I. Salazar, and J. P. Fay. 2005. Global mammal conservation: what must we manage? Science 309:603–7. Ceballos, G., P. Rodriguez, and R. A. Medellin. 1998. Assessing conservation priorities in megadiverse Mexico: mammalian diversity, endemicity, and endangerment. Ecological Applications 8:8–17. Chase, J. M. 2000. Are there real differences among aquatic and terrestrial food webs? Trends in Ecology and Evolution 15:408–12. Chase, M. K., W. B. Kristan III, A. J. Lynam, M. V. Price, and J. T. Rotenberry. 2000. Single species as indicators of species richness and composition in California coastal sage scrub birds and small mammals. Conservation Biology 14:474–87. Chiarucci, A., F. D’Auria, V. de Dominicis, A. Lagana, C. Perini, and E. Salerni. 2005. Using vascular plants as a surrogate taxon to maximize species richness in reserve design. Conservation Biology 19:1644–52. Christie, S. 2007. Zoo-based fundraising for in situ wildlife conservation. In Zoos in the 21st Century: Catalysts for Conservation? eds. A. Zimmermann, M. Hatchwell, L. Dickie, and C. West, 257–74. Cambridge, UK: Cambridge University Press. Cincotta, R. P., J. Wisnewski, and R. Engelman. 2000. Human population in the biodiversity hotspots. Nature 404:990–92. Claisse, D. 1989. Chemical contamination of French coasts—the results of a tenyear mussel watch. Marine Pollution Bulletin 20:523–28. Clarke, G. M. 1993. Fluctuations asymmetry of invertebrate populations as a biological indicator of environmental quality. Environmental Pollution 82:207–11. Clarke, K. R. 1990. Comparisons of dominance curves. Journal of Experimental Marine Biology and Ecology 138:143–57. Clarke, K. R., and R. M. Warwick 1998. A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35:523–31. Claudet, J., D. Pelletier, J.-Y. Jouvenel, F. Bachet, and R. Galzin. 2006. Assessing the effects of marine protected area (MPA) on a reef fish assemblage in a northwestern Mediterranean marine reserve: identifying community-based indicators. Biological Conservation 130:349–69. Cleary, D. 2006. The questionable effectiveness of science spending by international conservation organizations in the tropics. Conservation Biology 20:733–38.

References 297 Clements, W. H., and M. C. Newman. 2002. Community Ecotoxicology. Chichester, Sussex: John Wiley & Sons. Clucas, B., K. McHugh, and T. Caro. 2008. Use of flagship species by U.S. conservation and nature magazines. Biodiversity and Conservation. 17:1517–28. Cochrane, M. A., and W. F. Laurance 2002. Fire as large-scale edge effect in Amazonian forests. Journal of Tropical Ecology 18:311–25. Code of Federal Regulations 1985. Title 36, Code of Federal Regulations, Chapter II. Part 219.19, subpart 64. Washington, DC: U.S. Government Printing Office. Cofre, H., and P. A. Marquet. 1999. Conservation status, rarity, and geographic priorities for conservation of Chilean mammals: an assessment. Biological Conservation 88:53–68. Coleman, F. C., and S. L. Williams. 2002. Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends in Ecology and Evolution 17:40–44. Collinge, S. K. 2000. Effects of grassland fragmentation on insect species loss, colonization, and movement patterns. Ecology 81:2211–26. Collinge, S. K. 2009. Ecology of Fragmented Landscapes. Baltimore, MD: Johns Hopkins University Press. Collins, J. P., and A. Storfer. 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98. Colwell, R. K., and J. A. Coddington. 1994. Estimating terrestrial biodiversity. Philosophical Transactions of the Royal Society of London B 345:101–8. Constanza, R. 1992. Can ecosystems be healthy? Critical consideration of concepts. Journal of Aquatic Ecosystem Health 1:1–15. Conway, W. G. 1989. The prospects for sustaining species and their evolution. In Conservation for the Twenty-first Century, eds. D. Western and M. C. Pearl, 199– 209. New York: Oxford University Press. Coppolillo, P., H. Gomez, F. Maisels, and R. Wallace. 2004. Selection criteria for suites of landscape species as a basis for site-based conservation. Biological Conservation 115:419–30. Corey, S. J., and T. A. Waite. 2008. Phylogenetic autocorrelation of extinction threat in globally imperiled amphibians. Diversity and Distributions 14:614–29. Cornutt, J., J. Lockwood, H. Luh, P. Nott, and G. Russell. 1994. Hotspots and species diversity. Nature 367:326–27. Costello, C., and S. Polasky. 2004. Dynamic reserve site selection. Resource and Energy Economics 26:157–74. Cowling, R. M., A. T. Knight, D. P. Faith, S. Ferrier, A. T. Lombard, A. Driver, M. Rouget, K. Maze, and P. G. Desmet. 2004. Nature conservation requires more than a passion for species. Conservation Biology 18:1674–77. Cox, P. A., T. Elmqvist, E. D. Pierson, and W. E. Rainey. 1991. Flying foxes as strong interactors in south Pacific Island ecosystems: a conservation hypothesis. Conservation Biology 5:448–54.

298 References Craighead, F. C. 1968. The role of the alligator in shaping plant communities and maintaining wildlife in the southern Everglades. Florida Naturalist 41, 2–7, 69–74, 94. Crain, C. M., and M. D. Bertness. 2006. Ecosystem engineering across environmental gradients: implications for conservation and management. BioScience 56:211–18. Creel, S., D. Christianson, S. Liley, and J. A. Winnie Jr. 2007. Predation risk affects reproductive physiology and demography of elk. Science 315:960. Creel, S., and J. A. Winnie. 2005. Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Animal Behaviour 69:1181–89. Creel, S., J. Winnie Jr., B. Maxwell, K. Hamlin, and M. Creel. 2005. Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–97. Crisp, P. N., K. J. M. Dickinson, and G. W. Gibbs. 1998. Does native invertebrate diversity reflect native plant diversity? A case study from New Zealand and implications for conservation. Biological Conservation 83:209–20. Cristancho, S., and J. Vining. 2004. Culturally defined keystone species. Human Ecology Review 11:153–64. Croll, D. A., J. L. Maron, J. A. Estes, E. M. Danner, and G. V. Byrd. 2005. Introduced predators transform subarctic islands from grassland to tundra. Science 307:1959–61. Crooks, J. A. 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–66. Crooks, K. R. 2002. Relative sensitivities of mammalian carnivores to habitat fragmentation. Conservation Biology 16:482–502. Crooks, K. R., and M. E. Soule. 1999. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–66. Croonquist, M. J., and R. P. Brooks. 1991. Use of avian and mammalian guilds as indicators of cumulative impacts in riparian-wetland areas. Environmental Management 15:701–14. Cryanoski, D. 2006. Calls to conserve biodiversity hotspots. Nature 439:774. Csuti, B., S. Polasky, P. H. Williams, R. L. Pressey, J. D. Camm, M. Kershaw, A. R. Kiester, B. Downs, R. Hamilton, M. Huso, and K. Sahr. 1997. A comparison of reserve selection algorithms using data on terrestrial vertebrates in Oregon. Biological Conservation 80:83–97. Cuddington, K. 2007. Ecosystem engineering: utility, contention, and progress. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 69–74. Amsterdam: Elsevier. Cumming, C. H. M. 1983. The decision-making framework with regard to the culling of large mammals in Zimbabwe. In Management of Large Mammals in African Conservation Areas, ed. R.O. Owen-Smith, 173–86. Pretoria: Haum. Curnutt, J., J. Lockwood, H. Luh, P. Nott, and G. Russell. 1994. Hotspots and species diversity. Nature 367:326-327.

References 299 Currie, D. J. 1991. Energy and large-scale patterns of animal- and plant-species richness. American Naturalist 137:27–49. Cury, P. M., L. J. Shannon, J.-P. Roux, G. M. Daskalov, A. Jarre, C. L. Moloney, and D. Pauly. 2005. Trophodynamic indicators for an ecosystem approach to fisheries. ICES Journal of Marine Science 62:430–42. Cushman, S. A., K. S. McKelvey, C. H. Flather, and K. McGarigal. 2008. Do forest community types provide a sufficient basis to evaluate biological diversity? Frontiers in Ecology and the Environment 6:13–17. Cuthbert, R., R. E. Green, S. Ranade, S. Saravanan, D. J. Pain, V. Prakash, and A. A. Cunningham. 2006. Rapid population declines of Egyptian vulture (Neophron percnopterus) and red-headed vulture (Sarcogyps calvus) in India. Animal Conservation 9:349–54. Cuthbert, R., J. Parry-Jones, R. E. Green, and D. J. Pain. 2007. NSAIDs and scavenging birds: potential impacts beyond Asia’s critically endangered vultures. Biology Letters 3:90–93. Dahl, T. E. 2000. Status and Trends of Wetlands in the Conterminous United States 1986 to 1997. Washington, DC: U.S. Department of the Interior, Fish and Wildlife Service. Daily, G. C. 1997. Countryside biogeography and the provision of ecosystem services. In Nature and Human Society: The Quest for a Sustainable World, ed. P. H. Raven, 104–13. Washington, DC: National Research Council, National Academy Press. Daily, G. C., G. Ceballos, J. Pacheco, G. Suzan, and A. Sanchez-Azofeifa. 2003. Countryside biogeography of neotropical mammals: conservation opportunities in agricultural landscapes of Costa Rica. Conservation Biology 17:1814–26. Daily, G. C., P. R. Ehrlich, and N. M. Haddad. 1993. Double keystone bird in a keystone species complex. Proceedings of the National Academy of Sciences 90:592–94. Daily, G. C., P. R. Ehrlich, and G. A. Sanchez-Azofeifa. 2001. Countryside biogeography: use of human-domanated habitats by the avifauna of southern Costa Rica. Ecological Applications 11:1–13. Dale, V. H. and S. C. Beyeler. 2001. Challenges in the development and use of ecological indicators. Ecological Indicators 1:3–10. Dalerum, F., M. J. Somers, K. E. Kunkel, and E. Z. Cameron. 2008. The potential for large carnivores to act as biodiversity surrogates in southern Africa. Biodiversity and Conservation 17:2939–49. Dalsgaard, J., S. S. Wallace, S. Salas, and D. Preikshot. 1998. Mass-balance model reconstruction of the Strait of Georgia: the present, one hundred, and five hundred years ago. UBC Fisheries Centre Research Reports 6:72–91. Danielsen, F., H. Beukema, N. D. Burgess, F. Parish, C. A. Bruhl, P. F. Donald, D. Murdiyarso, B. Phalan, L. Reijnders, M. Struebig, and E. B. Fitzherbert. 2009. Biofuel plantations on forested lands: double jeopardy for biodiversity and climate. Conservation Biology 23:348–58.

300 References Davies, S.P., and S.K. Jackson. 2006. The biological-condition gradient: a descriptive model for interpreting change in aquatic ecosystems. Ecological Applications 16:1251-1266. Davis, A.J., J.D. Holloway, H. Huijbregts, J. Krikken, A.H. Kirk-Spriggs, and S,L. Sutton. 2001. Dung beetles as indicators of change in the forests of northern Borneo. Journal of Applied Ecology 38:593-616. Dayton, P. K. 1972. Toward an understanding of community resilience and the potential effects of enrichment to the benthos of McMurdo Sound, Antarctica. In Proceedings of the Colloquium on Conservation Problems in Antarctica, ed. B. C. Parker, 81–95. Lawrence, KS: Allen Press. de Klerk, H. M., T. M. Crowe, J. Fjeldsa, and N. D. Burgess. 2002. Patterns of species richness and narrow endemism of terrestrial bird species in the Afrotropical region. Journal of Zoology London 256:327–42. de Soyza, A. G., W. G. Whitford, J. E. Herrick, J. W. Van Zee, and K. M. Havstad. 1998. Early warning indicators of desertification: examples of tests in the Chihuahuan Desert. Journal of Arid Environments 39:101–12. Dearborn, D. C., A. D. Anders, and E. N. Flint. 2001. Trends in reproductive success of Hawaiian seabirds: is guild membership a good criterion for choosing indicator species? Biological Conservation 10:97–103. Debinski, D. M., and P. F. Brussard. 1994. Using biodiversity data to assess specieshabitat relationships in Glacier National Park, Montana. Ecological Applications 4:833–43. Delibes, M., S. Cabezas, B. Jiménez, and M. J. Gonzalez. 2009. Animal decisions and conservation: the recolonization of a severely polluted river by the European otter. Animal Conservation 12:400–407. Delibes-Mateos, M., S. M. Redpath, E. Angulo, P. Ferreras, and R. Villafuerte. 2007. Rabbits as a keystone species in southern Europe. Biological Conservation 137:149–56. Didham, R. K., P. H. Hammond, J. H. Lawton, P. Eggleton, and N. E. Stork. 1998. Beetle species responses to tropical forest fragmentation. Ecological Monographs 68:295–323. Dietz, J. M., L. A. Dietz, and E. Y. Nagagata. 1994. The effective use of flagship species for conservation of biodiversity: the example of lion tamarins in Brazil. In Creative conservation: Interactive management of wild and captive animals, ed. P. J. S. Olney, G. M. Mace, and T. C. Feistner, 32–49. London: Chapman and Hall. Dirzo, R., and A. Miranda. 1991. Altered patterns of herbivory and diversity in the forest understory: a case study of the posible consequences of contemporary defaunation. In Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, eds. P. W. Price, T. M. Lewinsohn, G. W. Fernandes, and W. W. Bronson, 273–87. New York, NY: John Wiley & Sons. Dobson, A. P., J. P. Rodriguez, W. M. Roberts, and D. S. Wilcove. 1997. Geographic distribution of endangered species in the United States. Science 275:550–53.

References 301 Doledec, S., B. Statzner, and M. Bournard. 1999. Species traits for future biomonitoring across ecoregions: patterns along a human-impacted river. Freshwater Biology 42:737–58. Donald, P. F. 1998. Changes in the abundance of invertebrates and plants on British farmland. British Wildlife 9:279–89. Downer, C. C. 1996. The mountain tapir, endangered “flagship” species of the high Andes. Oryx 30:45–58. Drechler, M. 2005. Probablistic approaches to scheduling reserve selection. Biological Conservation 122:253–62. Dublin, H. T., A. R. E. Sinclair, and J. MacGladie. 1990. Elephant and fire as causes of multiple stable states in Serengeti-Mara woodlands. Journal of Animal Ecology 59:1147–64. Dudley, N., D. Baldock, R. Nasi, and S. Stolton. 2005. Measuring biodiversity and sustainable management in forests and agricultural landscapes. Philosophiocal Transactions of the Royal Society B 360:457-70 Duelli, P., and M. K. Obrist. 1998. In search of the best correlates for local organismal biodiversity in cultivated areas. Biodiversity and Conservation 7:297–309. DuFrene, M., and P. Legendre 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Applications 67:345– 66. Dulvy, N. K., S. I. Rogers, S. Jennings, V. Stelzenmuller, S. R. Dye, and H. R. Skjoldal. 2008. Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. Journal of Applied Ecology 45:1029– 39. Dumbrell, A. J., E. J. Clark, G. A. Frost, T. E. Randell, J. W. Pitchford, and J. K. Hill. 2008. Changes in species diversity following habitat disturbance are dependent on spatial scale: theoretical and empirical evidence. Journal of Applied Ecology 45:1531–39. Dunk, J. R., W. J. Zielinski, and H. H. Welsh Jr. 2006. Evaluating reserves for species richness and representation in northern California. Diversity and Distributions 12:434–42. Eeley, H. A. C., M. J. Lawes, and B. Reyers. 2001. Priority areas for the conservation of subtropical indigenous forest in southern Africa: a case study from KwaZulu-Natal. Biodiversity and Conservation 10:1221–46. Ehrlich, P. R. 1997. A World of Wounds: Ecologists and the Human Dilemma. Oldenorf/Kuhe, Germany: Ecology Institute. Eken, G., L. Bennun, T. M. Brooks, W. Darwall, L. D. C. Fishpool, M. Foster, D. Knox, P. Langhammer, P. Matiku, E. Radford, P. Salaman, W. Sechrest, M. L. Smith, S. Spector, and A. Tordoff. 2004. Key biodiversity areas as site conservation targets. BioScience 54:1110–18. Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliott, C. R. Ford, D. R. Foster, B. D. Kloeppel, J. D. Knoepp, G. M. Lovett, J. Mohan, D. A. Orwig, N. L. Rodenhouse, W. V. Sobczak, K. A. Stinson, J. K. Stone, C. M. Swan, J. Thompson, B.Von Holle, and J. R. Webster. 2005. Loss of foundation

302 References species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479–86. Elmhagen, B., and S. P. Rushton. 2007. Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecology Letters 10:197–206. Elmqvist, T., C. Folke, M. Nystrom, G. Peterson, J. Bengtsson, B. Walker, and J. Norberg. 2003. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the the Environment 1:488–94. Erasmus, B. F. N., S. Freitag, K. J. Gaston, B. H. Erasmus, and A. S. van Jaarsveld. 1999. Scale and conservation planning in the real world. Proceedings of the Royal Society of London B 266:315–19. Ernest, S. K. M., and J. H. Brown. 2001. Delayed compensation for missing keystone species by colonization. Science 292:101–4. Essington, T. E., A. H. Beaudreau, and J. Wiedenmann. 2006. Fishing through marine food webs. Proceedings of the National Academy of Sciences 103:3171–75. Estes, J. A., and D. O. Duggins. 1995. Sea otters and kelp in Alaska: generality and variation in a community ecological paradigm. Ecological Monographs 65:75– 100. Estes, J. A., and J. F. Palmisano. 1974. Sea otters: their role in structuring nearshore communities. Science185:1058–60. Estes, J. A., M. T. Tinker, T. M. Williams, and D. F. Doak. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473– 76. Estrada, A., P. Cammarano, and R. Coates-Estrada. 2000. Bird species richness in vegetation fences and in strips of residual rain forest vegetation at Los Tuxlas, Mexico. Biodiversity and Conservation 9:1399–416. Estrada, A., R. Coates–Estrada, and D. A. Merritt Jr. 1994. Non flying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico. Ecography 17:229–41. Estrada, A., R. Coates-Estrada, and D. A. Merritt Jr. 1997. Anthropogenic landscape changes and avian diversity at Los Tuxtlas, Mexico. Biodiversity and Conservation 6:19–43. Everest, F. H., D. N. Swanston, C. G. Shaw III, W. P. Smith, K. R. Julin, and S. D. Allen. 1997. Evaluation of the use of scientific information in developing the 1997 Forest Plan for the Tongass National Forest, USDA Forest Service General Technical Report PNW-GTR-415, Portland, OR. Faith, D. P. 1992. Conservation evaluation and phylogenetic diversity. Biological Conservation 61:1–10. Faith, D. P. 2003. Environmental diversity (ED) as surrogate information for species-level biodiversity. Ecography 26:374–79. Faith, D. P., and R. H. Norris. 1989. Correlation of environmental variables with patterns of distribution and abundance of common and rare freshwater macroinvertebrates. Biological Conservation 50:77–98. Faith, D. P., and P. A. Walker. 1996a. Environmental diversity: on the best-possible

References 303 use of surrogate data for assessing the relative biodiversity of sets of areas. Biodiversity and Conservation 5:399–415. Faith, D. P., and P. A. Walker. 1996b. How do indicator groups provide information about the relative biodiversity of different sets of areas? On hotspots, complementarity and pattern-based approaches. Biodiversity Letters 3:18–25. Faith, D. P., P. A. Walker, and C. R. Margules. 2001. Some future prospects for systematic biodiversity planning in Papua New Guinea—and for biodiversity planning in general. Pacific Conservation Biology 6:325–43. Faria, D., M. L. B. Paciencia, M. Dixo, R. R. Laps, and J. Baumgarten. 2007. Ferns, frogs, lizards, birds and bats in forest fragments and shade cacao plantations in two contrasting landscapes in the Atlantic forest, Brazil. Biodiversity and Conservation 16:2335–57. Farina, J. M., J. C. Castilla, and F. P. Ojeda. 2003. The “idiosyncratic” effect of a “sentinel” species on contaminated rocky intertidal communities. Ecological Applications 13:1533–52. Farjon, A., P. Thomas, and N. T. D. Luu. 2004. Conifer conservation in Vietnam: three potential flagship species. Oryx 38:257–265. Favreau, J. M., C. A. Drew, G. R. Hess, M. J. Rubino, F. H. Koch, and K. A. Eschelbach. 2006. Recommendations for assessing the effectiveness of surrogate species approaches. Biodiversity and Conservation 15:3949–69. Fearnside, P. M., and J. Ferraz. 1995. A conservation gap analysis of Brazil’s Amazonian vegetation. Conservation Biology 9:1134–47. Feeley, K. J., and J. W. Terborgh. 2008. Direct versus indirect effects of habitat reduction on the loss of avian species from tropical forest fragments. Animal Conservation 11:353–60. Ferraro, P. J., and S. K. Pattanayak. 2006. Money for nothing? A call for empirical evaluation of biodiversity conservation investments. PLoS 4:482–88. Ferraz, G., G. J. Russell, P. C. Stouffer, R. O. Bierregaard Jr., S. L. Pimm, and T. E. Lovejoy. 2003. Rates of species loss from Amazonian forest fragments. Proceedings of the National Academy of Sciences 100:14069–73. Ferrier, S. 2002. Mapping spatial pattern in biodiversity for regional conservation planning: where to from here? Systematic Biology 51:331–63. Ferrier, S., G. V. N. Powell, K. S. Richardson, G. Manion, J. M. Overton, T. A. Allnut, S. E. Cameron, K. Mantle, N. D. Burgess, D. P. Faith, J. F. Lamoreux, G. Kier, R. J. Hijmans, V. A. Funk, G. A. Cassis, B. L. Fisher, P. Flemons, D. Lees, J. C. Lovett, and R. S. A. R. Van Rompaey. 2004. Mapping more of terrestrial biodiversity for global conservation assessment. BioScience 54:1101–9. Ferrier, S., G. Manion, J. Elith, and K. Richardson. 2007. Using generalized dissimilarity modeling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity and Distributions 13:252–64. Ferrier, S., and G. Watson. 1997. An evaluation of the effectiveness of environmental surrogates and modeling techniques in predicting the distribution of

304 References biological diversity. Environment Australia, Canberra. http://www.deh.gov.au/ biodiversity/publications/technical/surrogates/. Accessed 15 May 2009. Ferris, R., and J. W. Humphrey. 1999. A review of potential biodiversity indicators for application in British forests. Forestry 72:313–28. Ficetola, G. F., R. Sacchi, S. Scali, A. Gentilli, F. De Bernardi, and P. Galeotti. 2007. Vertebrates respond differently to human disturbance: implications for the use of a focal species approach. Acta Oecologia 31:109–18. Fisher, D. O., S. P. Blomberg, and I. P. F. Owens. 2003. Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proceedings of the Royal Society of London B 270:1801–8. Fitzherbert, E. B., M. J. Struebig, A. Morel, F. Danielsen, C. A. Bruhl, P. F. Donald, and B. Phalan. 2008. How will oil palm expansion affect biodiversity? Trends in Ecology and Evolution 23:538–45. Flather, C. H., and C. H. Sieg. 2007. Species rarity: definition, causes, and classification. In Conservation of Rare or Little-Known Species: Biological, Social, and Economic Considerations, eds. M. G. Raphael and R. Molina, 40–66. Washington, DC: Island Press. Flather, C. H., K. R. Wilson, D. J. Dean, and W. C. McComb. 1997. Identifying gaps in conservation networks: of indicators and uncertainty in geographicbased analyses. Ecological Applications 7:531–42. Fleishman, E. R., B. Blair, and D. D. Murphy. 2001. Empirical validation of a method for umbrella species selection. Ecological Applications 11:1489–501. Fleishman, E., B. G. Jonsson, and P. Sjogren-Gulve. 2000b. Focal species modeling for biodiversity conservation. Ecological Bulletins 48:85–99. Fleishman, E., and D. D. Murphy. 2009. A realistic assessment of the indicator potential of butterflies and other charismatic taxonomic groups. Conservation Biology 23:1109–16. Fleishman, E., D. D. Murphy, and P. F. Brussard. 2000a. A new method for selection of umbrella species for conservation planning. Ecological Applications 10:569–79. Fleishman, E., J. R. Thomson, R. Mac Nally, D. D. Murphy, and J. P. Fay. 2005. Using indicator species to predict species richness of multiple taxonomic groups. Conservation Biology 19:1125–37. Fleury, S. A., P. J. Mock, and J. F. O’Leary. 1998. Is the California gnatcatcher a good umbrella species? Western Birds 29:453–67. Fontaine, B., O. Gargominy, and E. Neubert. 2007. Priority sites for conservation of land snails in Gabon: testing the umbrella species concept. Diversity and Distributions 13:725–34. Foose, T. J., and N. van Strien, eds. 1997. Asian Rhinos: Status and Conservation Action Plan (New Edition). IUCN/SSC Asian Rhino Specialist Group. Gland, Switzerland. Fore, L. S., J. R. Karr, and R. W. Wisseman. 1996. Assessing invertebrate responses to human activities: evaluating alternative approaches. Journal of the North American Benthological Society 15:212–31.

References 305 Forest, F., R. Greyner, M. Rouget, T. J. Davies, R. M. Cowling, D. P. Faith, A. Balmford, J. C. Manning, S. Proches, M. van der Bank, G. Reeves, T. A. J. Hedderson, and V. Savolainen. 2007. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–60. Forman, R. T. T., D. Sperling, J. A. Bissonette, A. P. Clevenger, C. D. Cutshall, V. H. Dale, L. Fahrig, R. France, C. R. Goldman, K. Meanue, J. A. Jones, F. J. Swanson, T. Turrentine, and T. C. Winter. 2003. Road Ecology: Science and Solutions. Washington, DC: Island Press. Fox, G. A. 2001. Wildlife as sentinels of human health effects in the Great Lakes–St. Lawrence Basin. Environmental Health Perspectives 109:853–61. Fox, N. J., and L. E. Beckley. 2005. Priority areas for conservation of Western Australian coastal fishes: a comparison of hotspot, biogeographical and complementarity approaches. Biological Conservation 125:399–410. Franco, A. M. A., J. M. Palmeirim, and W. J. Sutherland. 2007. A method for comparing effectiveness of research techniques in conservation and applied ecology. Biological Conservation 134:96–105. Franklin, J. F. 1993. Preserving biodiversity: species, ecosystems, or landscapes? Ecological Applications 3:202–5. Franklin, J. F., K. Cromack, W. Denison, A. McKee, C. Maser, J. Sedell, F. Swanson, and G. Juday. 1981. Ecological characteristics of old-growth Douglas-fir forests. USDA Forest Service General Technical Report PNW-118. Pacific Northwest Forest and Range Experiment Station, Portland, OR. Fraser, S. E. M., A. E. Beresford, J. Peters, J. W. Redhead, A. J. Welch, P. J. Mayhew, and C. Dytham. 2009. Effectiveness of vegetation surrogates for parasitoid wasps in reserve selection. Conservation Biology 23:142–50. Freitag, S., and A. S. van Jaarsveld. 1997. Relative occupancy, endemism, taxonomic distinctiveness and vulnerability: prioritizing regional conservation actions. Biodiversity and Conservation 6:211–32. Freitag, S., and A. S. van Jaarsveld. 1998. Sensitivity of selection procedures for priority conservation areas to survey extent, survey intensity and taxonomic knowledge. Proceedings of the Royal Society of London B 265:1475–82. Fujiwara, M., and H. Caswell. 2001. Demography of the endangered North Atlantic right whale. Nature 414:537–41. Funk, S. M., and J. E. Fa. 2010. Ecoregion prioritization suggests an armoury not a silver bullet for conservation planning. PLoS ONE 5:e8923. Furness, R. W. 1991. The occurrence of burrow-nesting among birds and its influence on soil fertility and stability. Symposium of the Zoological Society of London 63:53–67. Game, E. T., H. S. Grantham, A. J. Hobday, R. L. Pressey, A. T. Lombard, L. E. Beckley, K. Gjerde, R. Bustamante, H. P. Possingham, and A. J. Richardson. 2009. Pelagic protected areas: the missing dimension in ocean conservation. Trends in Ecology and Evolution 24:360–69. Gammon, J. R., W. C. Fatz, and T. P. Simon. 2003. Patterns in water quality and fish assemblages in three central Indiana streams with emphasis on animal feed lot

306 References operations. In Biological Response Signatures: Indicator Patterns Using Aquatic Communities, ed. T. P. Simon, 374–417. Boca Raton, FL: CRC Press. Gardenfors, U. 2001. Classifying threatened species at national versus global levels. Trends in Ecology and Evolution 16:511–16. Gardner, T. A. 2010. Monitoring Forest Biodiversity: Improving Conservation through Ecologically Responsible Management. London: Earthscan. Gardner, T. A., J. Barlow, I. S. Araujo, T. C. Avila-Pires, A. B. Bonaldo, J. E. Costa, M. C. Esposito, L. V. Ferreira, J. Hawes, M. I. M. Hernandez, M. S. Hoormoed, R. N. Leite, N. F. Lo-Nan-Hung, J. R. Malcolm, M. B. Martins, L. A. M. Mestre, R. Miranda-Santos, W. L. Overal, L. Parry, S. L. Peters, M. A. Ribeiro-Junior, M. N. F. da Silva, C. da Silva Motta, and C. A. Peres. 2008a. The cost-effectiveness of biodiversity surveys in tropical forests. Ecology Letters 11:139–50. Gardner, T. A., J. Barlow, R. Chazdon, R. Ewers, C. A. Harvey, C. A. Peres, and N. Sodhi. 2009. Prospects for tropical forest biodiversity in a human-modified world. Ecology Letters 12:561–82. Gardner, T. A., J. Barlow, L. T. W. Parry, and C. A. Peres. 2007a. Predicting the uncertain future of tropical forest species in a data vacuum. Biotropica 39:25–30. Gardner, T. A., I. M. Cote, J. A. Gill, A. Grant, and A. R. Watkinson. 2005. Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long term decline. Ecology 86:174–84. Gardner, T. A., M. I. M. Hernandez, J. S. Barlow, and C. A. Peres. 2008b. Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology 45:883–93. Gardner, T. A, T. Caro, E. Fitzherbert, T. Banda, and P. Lalbhai. 2007c. Conservation value of multiple use areas in East Africa. Conservation Biology 21:1516– 25. Gardner, T. A., M. A. Ribeiro-Junior, J. Barlow, T. C. S. Avila-Pires, M. S. Hoogmoed, and C. A. Peres. 2007b. The value of primary, secondary, and plantation forests for a neotropical herpetofauna. Conservation Biology 21:775–87. Garpe, K. C., S. A. S. Yahya, U. Lindahl, and M. C. Ohman. 2006. Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Marine Ecology Progress Series 315:237–47. Garson, J., A. Aggarwal, and S. Sarkar. 2002. Birds as surrogates for biodiversity: an analysis of a data set from southern Quebec. Journal of Bioscience 27:347–60. Gascon, C., T. E. Lovejoy, R. O. Bierregaard, J. R. Malcolm, P. C. Stouffer, H. Vasconcelos, W. F. Laurance, B. Zimmerman, M. Tocher, and S. Borges. 1999. Matrix habitat and species persistence in tropical forest remnants. Biological Conservation 91:223–29. Gaston, K. J. 1994. Rarity. London: Chapman and Hall, Gaston, K. J. 1996a. Biodiversity: A Biology of Numbers and Difference. Oxford, UK: Blackwell Science.

References 307 Gaston, K. J. 1996b. Biodiversity—congruence. Progress in Physical Geography 20:105–12. Gaston, K. J., and T. M. Blackburn. 1995. Mapping biodiversity using surrogates for species richness: macro-scales and New World birds. Proceedings of the Royal Society of London B 262:335–41. Gaston, K. J., and T. M. Blackburn. 1996. The spatial distribution of threatened species: macroscales and New World birds. Proceedings of the Royal Society of London B 263:235–40. Gaston, K. J., S. F. Jackson, A. Nagy, L. Cantu-Salazar, and M. Johnson. 2008. Protected areas in Europe: Principle and Practice. Annals of the New York Academy of Sciences 1134:97–119. Gaston, K. J., and A. S. L. Rodrigues. 2002. Reserve selection in regions with poor biological data. Conservation Biology 17:188–95. Gaston, K. J., and P. H. Williams. 1996. Spatial patterns in taxonomic diversity. In Biodiversity: A Biology of Numbers and Difference, ed. K. J. Gaston, 202–29. Oxford, UK: Blackwell Science. Gehring, T. M., and R. K. Swihart. 2003. Body size, niche breadth, and ecologically scaled responses to habitat fragmentation: mammalian predators in an agricultural landscape. Biological Conservation 109:283–95. Gehrt, S. D., and S. Prange. 2007. Interference competition between coyotes and raccoons: a test of the mesopredator release hypothesis. Behavioral Ecology 18:204–14. Giere, O. 1993. Meiobenthology: The Microscopic Fauna in Aquatic Sediments. Berlin, Germany: Springer-Verlag. Gilbert, L. E. 1980. Food web organization and the conservation of neotropical diversity. In Conservation Biology: An Evolutionary-Ecological Perspective, eds. M. E. Soule and B. A. Wilcox, 11–33. Sutherland, MA: Sinaeur Associates. Gittleman, J. L., S. M. Funk, D. Macdonald, and R. K. Wayne. 2001. Carnivore Conservation. Cambridge, UK: Cambridge University Press. Gjerdrum, C., A. M. J. Vallee, C. Cassidy St. Clair, D. F. Bertram, J. L. Ryder, and G. S. Blackburn. 2003. Tufted puffin reproduction reveals ocean climate variability. Proceedings of the National Academy of Sciences 100:9377–82. Gladstone, W. 2002. The potential value of indicator groups in the selection of marine reserves. Biological Conservation 104:211–20. Gladstone, W. 2007. Requirements for marine protected areas to conserve the biodiversity of rocky reef fishes. Aquatic Conservation: Marine and Freshwater Ecosystems 17:71–87. Gladstone, W., and T. Alexander. 2005. A test of the higher-taxon approach in the identification of candidate sites for marine reserves. Biodiversity and Conservation 14:3151–68. Glynn, P. W. 1993. Coral reef bleaching: ecological perspectives. Coral Reefs 12:1– 17. Grabowski, J. H., and C. H. Peterson. 2007. Restoring oyster reefs to recover

308 References ecosystem services. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 281–98. Amsterdam: Elsevier. Grand, J., J. Buonaccorsi, S. A. Cushman, C. R. Griffin, and M. C. Neel. 2004. A multiscale landscape approach to predicting bird and moth rarity hotspots in a threatened pitch pine-scrub oak community. Conservation Biology 18:1063–77. Grand, J., M. P. Cummings, T. G. Rebelo, T. H. Ricketts, and M. C. Neel. 2007. Biased data reduce efficiency and effectiveness of conservation reserve networks. Ecology Letters 10:364–74. Grantham, H. S., A. Moilanen, K. A. Wilson, R. L. Pressey, T. G. Rebelo, and H. P. Possingham. 2008. Diminishing return on investment for biodiversity data in conservation planning. Conservation Letters 1:190–98. Grantham, H. S., K. A. Wilson, A. Moilanen, T. Rebelo, and H. P. Possingham. 2009. Delaying conservation actions for improved knowledge: how long should we wait? Ecology Letters 12:293–301. Gray, M. A., S. L. Baldauf, P. J. Mayhew, and J. K. Hill. 2007. The response of avian feeding guilds to tropical forest disturbance. Conservation Biology 21:133–41. Greeley, M. S., Jr. 2002. Reproductive indicators of environmental stress in fish. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 321–77. Bethseda, MD: American Fisheries Society. Greenberg, R., P. Bichier, A. C. Angon, and R. Reitsma. 1997b. Bird populations in shade and sun coffee plantations in Central Guatemala. Conservation Biology 11:448–59. Greenberg, R., P. Bichier, and J. Sterling. 1997a. Acacia, cattle and migratory birds in southeastern Mexico. Biological Conservation 80:235–47. Gregory, R. D., A. van Strien, P. Vorisek, A. W. Gmelig Meyling, D. G. Noble, R. P. B. Foppen, and D. W. Gibbons. 2005. Developing indicators for European birds. Philisophical Transactions of the Royal Society of London B 360:269–88. Grelle, C. E. V. 2002. Is higher-taxon analysis an useful surrogate of species richness in studies of neotropical mammal diversity? Biological Conservation 108:101–6. Greyner, R., C. D. L. Orme, S. F. Jackson, G. H. Thomas, R. G. Davies, T. J. Davies, K. E. Jones, V. A. Olson, R. S. Ridgely, P. S. Rasmussen, T.-S. Ding, P. M. Bennett, T. M. Blackburn, K. J. Gaston, J. L. Gittleman, and I. P. F. Owens. 2006. Global distribution and conservation of rare and threatened vertebrates. Nature 444:93–96. Griffin, P. C. 1999. Endangered species diversity “hot spots” in Russia and centers of endemism. Biodiversity and Conservation 8:497–511. Griffiths, R. A., and L. Pavajeau. 2008. Captive breeding, reintroduction, and the conservation of amphibians. Conservation Biology 22:852–61. Groom, M. J., G. K. Meffe, and C. R. Carroll. 2006. Principles of Conservation Biology, 3rd edition. New Malden, MA: Sinaeur Associates. Groves, C. R., D. B. Jensen, L. A. Valutis, K. H. Redford, M. L. Shaffer, J. M. Scott, J. V. Baumgartner, J. V. Higgins, M. W. Beck, and M. G. Andrson. 2002. Planning for biodiversity conservation: putting conservation science into practice. BioScience 52:499–512.

References 309 Grutzner, F., B. Nixon, and R. C. Jones. 2008. Reproductive biology in egg-laying mammals. Sexual Development 2:115–27. Guisan, A., and N. E. Zimmermann. 2000. Predictive habitat distribution models in ecology. Ecological Modeling 135:147–86. Gunnthorsdottir, A. 2001. Physical attractiveness of an animal species as a decision factor for its preservation. Anthrozoos 14:204–16. Gurney, W. S. C., and J. H. Lawton. 1996. The population dynamics of ecosystem engineers. Oikos 76:273–83. Gutierrez, J. L., and C. G. Jones. 2006. Physical ecosystem engineers as agents of biogeochemical heterogeneity. BioScience 56:227–36. Hacker, J. E., G. Colishaw, and P. H. Williams. 1998. Patterns of African primate diversity and their evaluation for the selection of conservation areas. Biological Conservation 84:251–62. Hagan, J. M., and A. A. Whitman. 2006. Biodiversity indicators for sustainable forestry: simplifying complexity. Journal of Forestry (June):203–10. Halaj, J., and D. H. Wise. 2001. Terrestrial trophic cascades: how much do they trickle? American Naturalist 157:262–81. Halffter, G., and L. Arellano. 2002. Response of dung beetle diversity to humaninduced changes in a tropical landscape. Biotropica 34:144–54. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99. Halme, P., M. Monkkonen, J. S. Kotiaho, A.-L. Ylisirnio, and A. Markkanen. 2009. Quantifying the indicator power of an indicator species. Conservation Biology 23:1008–16. Halpern, B. S., K. A. Selkoe, F. Micheli, and C. V. Kappel. 2007. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conservation Biology 21:1301–15. Hamer, K. C., and J. K. Hill. 2000. Scale-dependent effects of habitat disturbance on species richness in tropical forests. Conservation Biology 14:1435–40. Hammond, P. M. 1995. Practical approaches to the estimation of the extent of biodiversity in speciose groups. In Biodiversity: Measurement and Estimation, ed. D. L. Hawksworth, 119–36. London: Royal Society Publications. Handy, R. D., and M. H. Depledge. 1999. Physiological responses: their measurement and use as environmental biomarkers in ecotoxicology. Ecotoxiocology 8:329–49. Hansen, A. J., R. L. Knight, J. M. Marzluff, S. Powell, K. Brown, P. H. Gude, and K. Jones. 2005. Effects of exurban development on biodiversity: patterns, mechanisms, and research needs. Ecological Applications 15:1893–905. Hanski, I. 1982. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–21. Harcourt, A. H. 2000. Coincidence and mismatch of biodiversity hotspots: a global survey of the order, primates. Biological Conservation 93:163–75. Harper, J. L., and D. L. Hawksworth. 1995. Preface. In Biodiversity: Measurement and Estimation, ed. D. L. Hawksworth, 5–12. London: Chapman and Hall.

310 References Harrold, C., and D. C. Reed. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–69. Harvey, C. A., A. Medina, D. M. Sanchez, S. Vilchez, B. Hernandez, J. C. Saenz, J. M. Maes, F. Casanoves, and F. L. Sinclair. 2006. Patterns of animal diversity in different forms of tree cover in agricultural landscapes. Ecological Applications 16:1986–99. Haskell, B. D., B. G. Norton, and R. Constanza. 1992. What is ecosystem health and why should we worry about it? In Ecosystem Health: New Goals for Environmental Management, eds. R. Constanza, B. G. Norton, and B. D. Haskell, 3– 20. Washington, DC: Island Press. Hastings, A., and L. W. Botsford. 2003. Comparing designs of marine reserves for fisheries and for biodiversity. Ecological Applications 13:S65–70. Hastings, A., J. E. Byers, J. A. Crooks, K. Cuddington, C. G. Jones, J. G. Lambrinos, T. S. Talley, and W. G. Wilson. 2007. Ecosystem engineering in space and time. Ecology Letters 10:153–64. Hawes, J., J. Barlow, T. A. Gardner, and C. A. Peres. 2008. The value of forest strips for understorey birds in an Amazonian plantation landscape. Biological Conservation 141:2262–78. Hawes, J., C. da Silva Motta, W. L. Overal, J. Barlow, T. A. Gardner, and C. Peres. 2009. Diversity and composition of Amazonian moths in primary, secondary and plantation forests. Journal of Tropical Ecology 25:281–300. Hayes, T. B. 2004. There is no denying this: defusing the confusion about atrizine. BioScience 54:1138–49. Hayward, M. W., and M. J. Somers, eds. 2009. Reintroduction of Top-order Predators. Oxford, UK: Wiley-Blackwell. Hebblewhite, M., C. A. White, C. G. Nietvelt, J. A. McKenzie, T. E. Hurd, J. M. Fryxell, S. E. Bayley, and P. C. Paquet. 2005. Human activity mediates a trophic cascade caused by wolves. Ecology 86:2135–44. Hecnar, S. J., and R. T. M. M’Closkey. 1997. Patterns of nestednesss and species association in a pond-dwelling amphibian fauna. Oikos 80:371–81. Heino, J., T. Muotka, R. Paavola, and L. Paasivirta. 2003. Among-taxon congruence in biodiversity patterns: can stream insect diversity be predicted using single taxonomic groups? Canadian Journal of Fish and Aquatic Sciences 60:1039– 49. Heino, J., and H. Mykra. 2006. Assessing physical surrogates for biodiversity: do tributary and stream type classifications reflect macroinvertebrate assemblage diversity in running waters? Biological Conservation 129:418–26. Heino, J., R. Paavola, R. Virtanen, and T. Muotka. 2005. Searching for biodiversity indicators in running waters: do bryophytes, macroinvertebrates, and fish show congruent diversity patterns? Biodiversity and Conservation 14:415–28. Heino, J., and J. Soininen. 2007. Are higher taxa adequate surrogates for specieslevel assemblage patterns and richness in stream organisms? Biological Conservation 137:78–89.

References 311 Heithaus, M. R., A. Frid, A. J. Wirsing, and B. Worm 2008. Predicting ecological consequences of marine top predator declines. Trends in Ecology and Evolution 23:202–10. Hellawell, J. M. 1986. Biological Indicator of Freshwater Pollution and Environmental Management. London: Elsevier Applied Science Publishers. Hellou, J., and R. J. Law. 2003. Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. Environmental Pollution 126:407–16. Henke, S. E., and F. C. Bryant. 1999. Effects of coyote removal on the faunal community in western Texas. Journal of Wildlife Management 63:1066–81. Herremans, M. 1995. Effects of woodland modification by African elephant Loxodonta africana on bird diversity in northern Botswana. Ecography 18:440– 54. Herricks, E. E., and Schaeffer, D. J. 1985. Can we optimize biomonitoring? Environmental Management 9:487–92. Hess, G. R., R. A. Bartel, A. K. Leidner, K. M. Rosenfeld, M. J. Rubino, S. B. Snider, and T. H. Ricketts. 2006. Effectiveness of biodiversity indicators varies with extent, grain, and region. Biological Conservation 132:448–57. Hess, G. R., and T. J. King. 2002. Planning open spaces for wildlife I. Selecting focal species using a Delphi survey approach. Landscape and Urban Planning 58:25–40. Hess, G. R., F. H. Koch, M. J. Rubino, K. A. Eschelbach, C. A. Drew, and J. M. Favreau. 2006. Comparing the potential effectiveness of conservation planning approaches in central North Carolina. Biological Conservation 128:358– 68. Heywood, V. H., ed. 1995. Global Biodiversity Assessment. Cambridge, UK: Cambridge University Press. Higgins, M. A., and K. Ruokolainen. 2004. Rapid tropical forest inventory: a comparison of techniques based on inventory data from western Amazonia. Conservation Biology 18:799–811. Hill, C. J. 1996. Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles. Journal of Tropical Ecology 12:449–60. Hill, G. E. 2007. Ivorybill Hunters: The Search for Proof in a Flooded Wilderness. New York: Oxford University Press. Hill, J. K., and K. C. Hamer 2004. Determining impacts of habitat modification on diversity of tropical forest fauna: the importance of spatial scale. Journal of Applied Ecology 41:744–54. Hill, M. O. 1979. TWINSPAN: A Fortran Program for Arranging Multivariate Data in an Ordered Two-way Table by Classification of the Individuals and Attributes. Ithaca, NY: Cornell University Press. Hill, N. M., and P. A. Keddy. 1992. Prediction of rarities from habitat variables: coastal plain plants on Nova Scotia lakeshores. Ecology 73:1852–59. Hilton-Taylor, C., G. M. Mace, D. R. Capper, N. J. Collar, S. N. Stuart, C. J. Bibby,

312 References C. Pollock, and J. B. Thomsen. 2000. Assessment mismatches must be sorted out: they leave species at risk. Nature 404:541. Hilty, J., and A. Merenlender. 2000. Faunal indicator taxa selection for monitoring ecosystem health. Biological Conservation 92:185–97. Hoegh-Guldberg, O. 1999. Climate change, coral bleaching, and the future of the world’s coral reefs. Marine Freshwater Research 50:839–66. Hoegh-Guldberg, O. 2005. Climate change and marine ecosystems. Climate Change and Biodiversity , eds. T. E. Lovejoy and L. Hannah, 256–73. New Haven, CT: Yale University Press. Hoekstra, J. M., T. M. Boucher, T. H. Ricketts, and C. Roberts. 2005. Confronting a biome crisis: global disparities of habitat loss and protection. Ecology Letters 8:23–29. Hof, J. G., and M. Bevers. 1998. Spatial Optimization for Managed Ecosystems. New York: Columbia University Press. Hof, J. G., and L. A. Joyce. 1992. Spatial optimization for wildlife and timber in managed forest ecosystems. Forest Science 38:489–508. Holt, R. D., J. H. Lawton, G. A. Polis, and N. D. Martinez. 1999. Trophic rank and the species-area relationship. Ecology 80:1495–504. Horner-Devine, M. C., G. C. Daily, P. R. Ehrlich, and C. L. Boggs. 2003. Countryside biogeography of tropical butterflies. Conservation Biology 17:168–77. Howard, P. C., P. Viskanic, T. R. B. Davenport, F. W. Kigenyi, M. Baltzer, C. J. Dickinson, J. S. Lwanga, R. A. Matthews, and A. Balmford. 1998. Complementarity and the use of indicator groups for reserve selection in Uganda. Nature 394:472–75. Howe, R. W., R. R. Regal, G. J. Niemi, N. P. Danz, and J. M. Hanowski. 2007. A probability-based indicator of ecological condition. Ecological Indicators 7:793– 806. Hubbell, S. P. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton, NJ: Princeton University Press. Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Guldberg, J. B. C. Jackson, J. Kleypas, J. M. Lough, P. Marshall, M. Nystrom, S. R. Palumbi, J. M. Pandolfi, B. Rosen, and J. Roughgarden. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929–33. Hunsaker, C. T., and D. E. Carpenter, eds. 1990. Environmental monitoring and assessment program: ecological indicators. Office of Research and Development, U.S. Environmental Protection Agency, Research Triangle Park, NC. Hunter, J. E., R. J. Gutierrez, and A. B. Franklin. 1995. Habitat configuration around spotted owl sites in northwestern California. Condor 97:684–93. Hunter, M. 1996. Fundamentals of Conservation Biology. Cambridge, MA: Blackwell Science. Hunter, M. L., and J. P. Gibbs. 2007. Fundamentals of Conservation Biology, 3rd ed. Malden, MA: Blackwell.

References 313 Huntly, N., and R. Inouye. 1988. Pocket gophers in ecosystems: patterns and mechanisms. BioScience 38:786–93. Hurlbert, A. H., and E. P. White. 2005. Disparity between range map- and surveybased analyses of species richness: patterns, processes and implications. Ecology Letters 8:319–27. Hurlbert, S. H. 1997. Functional importance vs kestoneness: reformulating some questions in theoretical biocenology. Australian Journal of Ecology 22:369–82. Hurme, E., M. Monkkonen, A.-L. Sippola, H. Ylinen, and M. Pentinsaari. 2008. Role of the Siberian flying squirrel as an umbrella species for biodiversity in northern boreal forests. Ecological Indicators 8:246–55. Hutto, R. L. 1989. The effect of habitat alteration on migratory land birds in a West Mexican tropical deciduous forest: a conservation perspective. Conservation Biology 3:138–48. Innis, S. A., R. J. Naiman, and S. R. Elliott. 2000. Indicators and assessment methods for measuring the ecological integrity of semi-aquatic terrestrial environment. Hydrobiologia 422/423:111–30. IPCC 2007. Climate Change 2007: The Physical Sciences Basis. The Contribution of the Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press. IUCN 2003. IUCN Red List of Threatened Species. Gland, Switzerland: IUCN. IUCN 2008. Guidelines for Using the IUCN Red List Categories and Criteria: Version 7.0., Gland, Switzerland, and Cambridge, UK: Species Survival Commission, International Union of the Conservation of Nature and Natural Resources. Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner, and R. R. Warner. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–38. Jaffre, T., P. Bouchet, and J.-M. Veillon. 1998. Threatened plants of New Caledonia: is the system of protected areas adequate? Biodiversity and Conservation 7:109–35. Jain, K. E., I. K. Birtwell, and A. P. Farrell. 1998. Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Canadian Journal of Zoology 76:1488–96. James, A., K. Gaston, and A. Balmford. 2001. Can we afford to conserve biodiversity? BioScience 51:43–52. Jamil, K. 2001. Bioindicators and Biomarkers of Environmental Pollution and Risk Asessment. Enfield, NH: Science Publishers, Inc. Jenkins, J., J. D. Aber, and C. D. Canham. 1999. Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests. Canadian Journal of Forest Research 29:630–45. Jennings, S. 2005. Indicators to support an ecosystem approach to fisheries. Fish and Fisheries 8:212–32.

314 References Jennings, S., and N. K. Dulvy. 2005. Reference points and reference directions for size-based indicators of community structure. ICES Journal of Marine Science 62:397–404. Johnsingh, A. J. T., and J. Joshua. 1994. Conserving Rajaji and Corbett National Parks—the elephant as a flagship species. Oryx 28:135–140. Johnson, R. K., T. Widerholm, and D. M. Rosenberg. 1993. Freshwater biomonitoring using individual organisms, populations, and species assemblages of benthic macroinvertebrates. In Freshwater Biomonitoring and Benthic Macroinvertebrates, eds. D. M. Rosenberg and V. H. Resh, 40–158. New York: Chapman and Hall. Jones, C. G., and J. L. Gutierrez. 2007. On the purpose, meaning, and usage of the physical ecosystem engineering concept. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 3–24. Amsterdam: Elsevier. Jones, C. G., J. H. Lawton, and M. Shachak. 1994. Organisms as ecosystem engineers. Oikos 69:373–86. Jones, C. G., J. H. Lawton, and M. Shachak. 1997. Positive and negative effects of organisms as ecosystem engineers. Ecology 78:1946–57. Jones, G. P., M. I. McCormick, M. Srinivasan, J. V. Eagle. 2004. Coral decline threatens fish biodiversity in marine reserves. Proceedings of the National Academy of Sciences 101:8251–53. Jones, M. E., A. Cockburn, R. Hamede, C. Hawkins, H. Hesterman, S. Lachish, D. Mann, H. McCallum, and D. Pemberton. 2008. Life-history change in disease-ravaged Tasmanian devil populations. Proceedings of the National Academy of Sciences 105:10023–27. Jonzen, N., A. Linden, T. Ergon, E. Knudsen, J. O. Vik, D. Rubolini, D. Piacentini, C. Brinch, F. Spina, L. Karlsson, M. Stervander, A. Andersson, J. Waldenstrom, A. Lehikoinen, E. Edvardsen, R. Solvang, and N. C. Stenseth. 2006. Rapid advance of spring arrival dates in long-distance migratory birds. Science 312:1959–61. Jorgensen, S. E., F.-Lu. Xu, F. Salas, and J. C. Marques. 2005. Application of indicators for the assessment of ecosystem health. In Handbook of Ecological Indicators for Assessment of Ecosystem Health, eds. S. E. Jorgensen, R. Constanza, and F.-L. Xu, 5–66. Boca Raton, FL: CRC Press. Jouquet, P., J. Dauber, J. Lagerlof, P. Lavelle, and M. Lepage. 2006. Soil invertebrates as ecosystem engineers: intended and accidental effects on soil land feedback loops. Applied Soil Ecology 32:153–64. Justus, J., and S. Sarkar. 2002. The principle of complimentarity in the design of reserve networks to conserve biodiversity: a preliminary history. Journal of Biosciences 27:421–435. Juutinen, A., and M. Monkkonen. 2004. Testing alternative indicators for biodiversity conservation in old-growth boreal forests: ecology and economics. Ecological Economics 50:35–48.

References 315 Juutinen, A., M. Monkkonen, and A.-L. Sippola. 2006. Cost-efficiency of decaying wood as a surrogate for overall species richness in boreal forests. Conservation Biology 20:74–84. Karban, R., and I. T. Baldwin. 1997. Induced Responses to Herbivory. Chicago: University of Chicago Press. Kareiva, P., and M. Marvier. 2003. Conserving biodiversity coldspots. American Scientist 91:344–51. Karr, J. R. 1981. Assessment of biotic integrity using fish communities. Fisheries 6:21–27. Karr, J. R. 1991. Biological integrity: a long-neglected aspect of water resource management. Ecological Applications 1:66–84. Karr, J. R. 1999. Defining and measuring river health. Freshwater Biology 41:221– 34. Karr, J. R., and D. R. Dudley. 1981. Ecological perspectives on water quality goals. Environmental Management 5:55–68. Karr, J. R., K. D. Fausch, P. L. Angermeier, P. R. Yant, and I. J. Schlosser. 1986. Assessing the Biological Integrity in Running Waters: A Method and Its Rationale. Special Publication 5. Champaign, IL: Illinois Natural History Survey. Kati, V., P. Devillers, M. Dufrene, A. Legakis, D. Voukou, and P. Lebrun. 2004a. Hotspots, complementarity or representativeness? Designing optimal smallscale reserves for biodiversity conservation. Biological Conservation 120:471–80. Kati, V., P. Devillers, M. Dufrene, A. Legakis, D. Vokou, and P. Lebrun. 2004b. Testing the value of six taxonomic groups as biodiversity indicators at a local scale. Conservation Biology 18:667–75. Kautz, R. S., and J. A. Cox. 2001. Strategic habitats for biodiversity conservation in Florida. Conservation Biology 15:55–77. Keesing, F. 1998. Impacts of ungulates on the demography and diversity of small mammals in central Kenya. Oecologia 116:381–89. Keitt, T. H., O. N. Bjornstad, P. M. Dixon, and S. Citron-Pousty. 2002. Accounting for spatial pattern when modeling organism-environment interactions. Ecography 25:616–25. Kelly, J. R. and M. A. Harwell. 1990. Indicators of ecosystem recovery. Environmental Management 14:527–45. Kennard, M. J., A. H. Arthington, B. J. Pusey, and B. D. Harch. 2005. Are alien fish a reliable indicator of river health? Freshwater Biology 50:174–93. Kennedy, A. D., and C. A. Jacoby. 1999. Biological indicators of marine environmental health: meiofauna—a neglected benthic community? Environmental Monitoring and Assessment 54:47–68. Kerans, B. L., and J. R. Karr. 1994. A benthic index of biotic integrity (B–IBI) for rivers of the Tennessee Valley. Ecological Applications 4:768–85. Kerbes, R. H., P. M. Kotanen, and R. L. Jefferies. 1990. Destruction of wetland habitats by lesser snow geese: a keystone species on the west coast of Hudson Bay. Journal of Applied Ecology 27:242–58.

316 References Kerley, G. I. H., M. Landman, L. Kruger, N. Owen-Smith, D. Balfour, W. F. de Boer, A. Gaylard, K. Lindsay, and R. Slotow. 2001. Effects of elephants on ecosystems and biodiversity. In Elephant Management: A Scientific Assessment for South Africa, eds. R. J. Scholes and K. G. Mennell, 146–205. Johannesburg: Wits University Press. Kerr, J. T. 1997. Species richness, endemism, and the choice of areas for conservation. Conservation Biology 11:1094–1100. Kerr, J. T., and L. Packer. 1997. Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature 385:252–54. Kerr, J. T., A. Sugar, and L. Packer. 2000. Indicator taxa, rapid biodiversity assessment, and nestedness in an endangered ecosystem. Conservation Biology 14:1726–34. Kershaw, M., G. M. Mace, and P. H. Williams. 1995. Threatened staus, rarity, and diversity as alternative selection measures for protected areas—a test using Afrotropical antelopes. Conservation Biology 9:324–34. Kessler, M., S. Abrahamczyk, M. Bos, D. Buchori, D. Dwi Putra, S. R. Gradstein, P. Hohn, J. Kluge, F. Orend, R. Pitopang, S. Saleh, C. H. Schulze, S. G. Sporn, I. Steffan-Dewenter, S. S. Tjitrosoedirdjo, and T. Tscharntke. 2009. Alpha and Beta diversity of plants and animals along a tropical land-use gradient. Ecological Applications 19:2142–56. Kilgour, B. W., and D. R. Barton. 1999. Associations between stream fish and benthos across environmental gradients in southern Ontario, Canada. Freshwater Biology 41:553–66. King, M. C., and K. F. Beazley. 2005. Selecting focal species for marine protected area network planning in the Scotia-Fundy region of Atlantic Canada. Aquatic conservation: Marine and Freshwater Ecosystems 15:367–85. Kintsch, J. A., and D. L. Urban. 2002. Focal species, community representation, and physical proxies as conservation strategies: a case study in the Amphibolite mountains, North Carolina, U.S.A. Conservation Biology 16:936–47. Kirkpatrick, J. B. 1983. An iterative method for establishing priorities for the selection of nature reserves: an example from Tasmania. Biological Conservation 25:127–34. Klein, A.-M., I. Steffan-Dewenter, D. Buchori, and T. Tscharntke. 2002. Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees and wasps. Conservation Biology 16:1003–14. Knight, R. L., R. M. Cowling, and B. M. Campbell. 2006. An operational model for implementing conservation action. 2006. Conservation Biology 20:408–19. Knight, R. L., G. N. Wallace, and W. E. Riebsame. 1995. Ranching the view: subdivisions versus agriculture. Conservation Biology 9:459–61. Koh, L.P. 2007. Impacts of land use change on South-east Asian forest butterflies: a review. Journal of Applied Ecology 44:703–13. Kolkwitz, R., and M. Marsson. 1908. Okologie der pflanzlichen Saprobien. Berlin Dt. Bot. Ger. 26:505–19.

References 317 Kontoleon, A., and T. Swanson. 2003. The willingness to pay for property rights for the giant panda: can a charismatic species be an instrument for nature conservation? Land Economics 79:483–99. Kotze, D. J., and M. J. Samways. 1999. Support for the multi-taxa approach in biodiversity assessment, as shown by epigaeic in an Afromontane forest archipelago. Journal of Insect Conservation 3:125–43. Kremen, C. 1992. Assessing the indicator properties of species assemblages for natural areas monitoring. Ecological Applications 2:203–16. Kremen, C. 1994. Biological inventory using target taxa: a case study of butterflies of Madagascar. Ecological Applications 4:407–22. Kruger, O. 2005. The role of ecotourism in conservation: panacea or Pandora’s box? Biodiversity and Conservation 14:579–600. Kushlan, J. A. 1974. Observations on the role of the American alligator (Alligator mississippiensis) in the southern Florida wetlands. Copiea 31:993–96. Laidre, K. L., I. Stirling, L. F. Lowry, O. Wiig, M. P. Heide-Jorgensen, and S. H. Fergusen. 2008. Quantifying the sensitivity of arctic marine mammals to climate-induced habitat change. Ecological Applications 18:S97–125. Laland, K. N., F. J. Odling-Smee, and M. W. Feldman. 1999. Evolutionary consequences of niche construction and their implications for ecology. Proceedings of the National Academy of Sciences 96:10242–47. Lam, P. K. S., and J. S. Gray. 2003. The use of biomarkers in environmental monitoring programmes. Marine Pollution Bulletin 46:182–86. Lambeck, R. J. 1997. Focal species: a multi-species umbrella for nature conservation. Conservation Biology 11:849–57. Lambeck, R. J. 1999. Landscape planning for biodiversity conservation in agricultural regions: a case study from the wheatbelt of Western Australia. Biodiversity technical paper 2. Canberra: Environment Australia. Lambeck, R. J. 2002. Focal species and restoration ecology: response to Lindenmayer et al. Conservation Biology 16:549–51. Lamoreux, J. F., J. C. Morrison, T. H. Ricketts, D. M. Olson, E. Dinerstein, M. W. McKnight, and H. H. Shugart. 2006. Global tests of biodiversity concordance and the importance of endemism. Nature 440:212–14 Landres, P. B. 1992. Ecological indicators: panacea or liability? In Ecological Indicators, vols 1 & 2, eds. D. H. McKenzie, D. E. Hyatt, and V. J. McDonald, 1295– 318. New York: Elsevier Science Publications. Landres, P. B., J. Verner, and J. W. Thomas. 1988. Ecological uses of vertebrate indicator species: a critique. Conservation Biology 2:316–27. Lapin, M., and B. V. Barnes. 1995. Using the landscape ecosystem approach to assess species and ecosystem diversity. Conservation Biology 9:1148–58. Larsen, F. W., J. Bladt, and C. Rahbek. 2007. Improving the performance of indicator groups for the identification of important areas for species conservation. Conservation Biology 21:731–40. Larsen, F. W., J. Bladt, and C. Rahbek. 2009. Indicator taxa revisited: useful for conservation planning? Diversity and Distributions 15:70–79.

318 References Larsen, F. W., and C. Rahbek. 2003. Influence of scale on conservation priority setting—a test on African mammals. Biodiversity and Conservation 12:599–614. Launer, A. E., and D. D. Murphy. 1994. Umbrella species and the conservation of habitat fragments: a case of a threatened butterfly and a vanishing grassland ecosystem. Biological Conservation 69:143–53. Laurance, W. F., S. G. Laurance, L. V. Ferreira, J. M. Rankin-de Merona, C. Gascon, and T. E. Lovejoy. 1997. Biomass collapse in Amazonian forest fragments. Science 278:1117–18. Laurance, W. F., T. E. Lovejoy, H. L. Vasconcelos, E. M. Bruna, R. K. Didham, P. C. Stouffer, C. Gascon, R. O. Bierregaard, S. G. Laurance, and E. Sampaio. 2002. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology 16:605–18. Laurance, W. F., and C. A. Peres eds. 2006. Emerging Threats to Tropical Forests. Chicago: University of Chicago Press. Laurance, W. F., and D. C. Useche. 2009. Environmental synergisms and extinctions of tropical species. Conservation Biology 23:1427–37. Lavelle, P., S. Barot, M. Blouin, T. Decaens, J. J. Jiminez, and P. Jouquet. 2007. Earthworms as key actors in self-organizing soil systems. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 77–106. Amsterdam: Elsevier. Lawler, J. J., D. White, J. C. Sifneos, and L. L. Master. 2003. Rare species and the use of indicator groups for conservation planning. Conservation Biology 17:875–82. Laws, R. M. 1970. Elephants as agents of habitat and landscape change in East Africa. Oikos 21:1–15. Lawton, J. H., D. E. Bignell, B. Bolton, G. F. Bloemers, P. Eggleton, P. M. Hammond, M. Hodda, R. D. Holt, T. B. Larsen, N. A. Mawdsley, N. E. Stork, D. S. Srivastava, and A. D. Watt. 1998. Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature 391:72–76. Le Corre, M. 2008. Cats, rats and seabirds. Nature 451:134–35. Leader-Williams, N., and H. T. Dublin. 2000. Charismatic megafauna as “flagship” species. In Has the Panda Had Its Day? Future Priorities for the Conservation of Mammal Diversity, eds. A. Entwistle and N. Dunstone, 53–81. Cambridge, UK: Cambridge University Press. Leech, T. J., A. M. Gormley, and P. J. Seddon. 2008. Estimating the minimum viable population size of kaka (Nestor meridionalis), a potential surrogate species in New Zealand lowland forest. Biological Conservation 141:681–91. Lehmkuhl, J. F., and M. G. Raphael. 1993. Habitat pattern around northern spotted owl locations on the Olympic Peninsula, Washington. Journal of Wildlife Management 57:302–14. Lenihan, H. S., and C. H. Peterson. 1998. How habitat degredation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecological Applications 8:128–40.

References 319 Lennon, J. J., P. Koleff, J. J. D. Greenwood, and K.J. Gaston. 2004. Contribution of rarity and commonness to patterns of species richness. Ecology Letters 7:81–87. Lenth, B. A., R. L. Knight, and W. C. Gilbert. 2006. Conservation value of clustered housing developments. Conservation Biology 20:1445–56. Leu, M., S. E. Hanser, and S. T. Knick. 2008. The human footprint in the west: a large-scale analysis of anthropogenic impacts. Ecological Applications 18:1119– 39. Levin, L. L., and P. K. Dayton. 2009. Ecological theory and continental margins: where shallow meets deep. Trends in Ecology and Evolution 24:606–17. Levin, S. A. 1992. The problem of pattern and scale in ecology. Ecology 73:1943– 67. Lewis, S. N. W. 1997. Birds as indicators of biodiversity: a study of avifaunal diversity and composition in two contrasting land-use types in the Eastern Transvaal Lowveld, South Africa. MSc dissertation, University of East Anglia, Norwich, UK. Linde, A. R., S. Sanchez-Galan, J. I. Izquierdo, P. Arribas, E. Maranon, and E. Garcia-Vasquez. 1998. Brown trout as biomonitor of heavy metal pollution: effect of age on the reliability of the assessment. Ecotoxicology and Environmental Safety 40:120–25. Lindenmayer, D., and M. A. Burgman. 2005. Practical Conservation Biology. Collingwood, Australia: CSIRO Publishing. Lindenmayer, D. B., and J. Fischer. 2003. Sound science or social hook—a response to Brooker’s application of the focal species approach. Landscape and Urban Planning 62:149–58. Lindenmayer, D. B., A. D. Manning, P. L. Smith, H. P. Possingham, F. Fischer, I. Oliver, and M. A. McCarthy. 2002. The focal-species approach and landscape restoration: a critique. Conservation Biology 16:338–45. Lindenmayer, D. B., C. R. Margules, and D. B. Botkin. 2000. Indicators of biodiversity for ecologically sustainable forest management. Conservation Biology 14:941–50. Lindsey, P. A., R. Alexnder, J. T. du Toit, and M. G. L. Mills. 2005. The cost efficiency of wild dog conservation in South Africa. Conservation Biology 19:1205– 14. Linnell, J. D. C., J. E. Swenson, and R. Andersen. 2000. Conservation of biodiversity in Scandinavian boreal forests: large carnivores as flagships, umbrellas, indicators, or keystones. Biodiversity and Conservation 9:857–68. Lips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier, and J. P. Collins. 2006. Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community. Proceedings of the National Academy of Sciences 103:3165–70. Little, E. E. 2002. Behavioral measures of environmental stressors. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 431–72. Bethseda, MD: American Fisheries Society.

320 References Living Landscapes Bulletin 2. September 2001. The landscape species approach—a tool for site-based conservation. New York: Wildlife Conservation Society. Living Landscapes Bulletin 3. May 2002. The role of landscape species in site-based conservation. New York: Wildlife Conservation Society. Lo-Man-Hung, N. F., T. A. Gardner, M. A. Ribeiro-Junior, J. Barlow, and A. B. Bonaldo. 2008. The value of primary, secondary and plantation forests for neotropical epigeic arachnids. Journal of Arachnology 36:394–401. Loh, L. P., P. Levang, and J. Ghazoul. 2009. Designer landscapes for sustainable biofuels. Trends in Ecology and Evolution 24:431–38. Lohse, D. P. 1993. The importance of secondary substratum in a rocky intertidal community. Journal of Experimental Marine Biology and Ecology 166:1–17. Loiselle, B. A., C. A. Howell, C. H. Graham, J. M. Goerck, T. Brooks, K. G. Smith, and P. H. Williams. 2003. Avoiding pitfalls of using species distribution models in conservation planning. Conservation Biology 17:1591–600. Lombard, A. T. 1995. The problems with multi-species conservation: do hotspots, ideal reserves and existing reserves coincide? South African Journal of Zoology 30:145–63. Lombard, A. T., R. M. Cowling, R. L. Pressey, and P. J. Mustart. 1997. Reserve selection in a species-rich and fragmented landscape on the Agulhas Plain, South Africa. Conservation Biology 11:1101–16. Lombard, A. T., R. M. Cowling, R. L. Pressey, and A. G. Rebelo. 2003. Effectiveness of land classes as surrogates for species in conservation planning for the Cape Floristic Region. Biological Conservation 112:45–62. Longino, J. T., J. Coddington, and R. K. Cowell. 2002. The ant fauna of a tropical rainforest: estimating species richness three different ways. Ecology 83:689– 702. Loomis, J. B., and D. S. White. 1996. Economic benefits of rare and endangered species: summary and meta-analysis. Ecological Economics 18:197–206. Lorimer, J. 2007. Nonhuman charisma. Environment and Planning D: Society and Space 25:911–32. Lotze, H. K., and B. Worm. 2009. Historical baselines for large marine animals. Trends in Ecology and Evolution 24:254–62. Lovell, S., M. Hamer, R. Slotow, and D. Herbert. 2007. Assessment of congruency across invertebrate taxa and taxonomic levels to identify potential surrogates. Biological Conservation 139:113–25. Loya, Y., K. Sakai, K. Yamazato, Y. Nakano, H. Sambali, and R. van Woesik. 2001. Coral bleaching: the winners and losers. Ecology Letters 4:122–31. Luck, G. W. 2007. A review of the relationships between human population density and biodiversity. Biological Reviews 82:607–45. Luck, G. W., and G. C. Daily. 2003. Tropical countryside bird assemblages: richness, composition, and foraging differ by landscape context. Ecological Applications 13:235–47. Luebke, R. W., P. V. Hodson, M. Faisal, P. S. Ross, K. A. Grasman, and J. Zelikoff.

References 321 1997. Aquatic pollution-induced immunotoxicity in wildlife species. Fundamental and Applied Toxicology 37:1–15. Lund, M. P., and C. Rahbek. 2002. Cross-taxon congruence in complementarity and conservation of temperate biodiversity. Animal Conservation 5:163–71. Lydy, M. J., P. M. Stewart, and T. P. Simon. 2003. Relationships between fish assemblages and organochloride insecticides in sediment and fish tissue in south central Kansas. In Biological Response Signatures: Indicator Patterns Using Aquatic Communities, ed. T. P. Simon, 313–323. Boca Raton, FL: CRC Press. Mace, G. M., J. L. Gittleman, and A. Purvis. 2003. Preserving the tree of life. Science 300:1707–9. Mace, G. M., H. P. Possingham, and N. Leader-Williams. 2006. Prioritizing choices in conservation. In Key Topics in Conservation Biology, eds. D. Macdonald and K. Service, 17–34. Oxford, UK: Blackwell. Machiote, M., L. C. Branch, and D. Villarreal. 2004. Burrowing owls and burrowing animals: are ecosystem engineers interchangeable as facilitators? Oikos 106:527–35. Mackey, B. G., H. A. Nix, J. A. Stein, and S. E. Cork. 1989. Assessing the representativeness of the wet tropics of Queensland World Heritage Property. Biological Conservation 50:279–303. Maclaurin, J., and K. Sterelny. 2008. What Is Biodiversity? Chicago: University of Chicago Press. MacNally, R., A. F. Bennett, G. W. Brown, L. F. Lumsden, A.Yen, S. Hinkley, P. Lillywhite, and D. Ward. 2002. How well do ecosystem-based planning units represent different components of biodiversity? Ecological Applications 12:900– 912. Maddock, A., and G. A. Benn. 2000. Identification of conservation-worthy areas in Northern Zululand, South Africa. Conservation Biology 14:155–66. Maes, D., D. Bauwens, L. de Bruyn, A. Anselin, G. Vermeersch, W. de Landuyt, G. de Knijf, and M. Gilbert. 2005. Species richness coincidence: conservation strategies based on predictive modeling. Biodiversity and Conservation 14:1345–64. Maes, D., and H. van Dyck. 2005. Habitat quality and biodiversity indicator performances of a threatened butterfly versus a multispecies group for wet heathlands in Belgium. Biological Conservation 123:177–87. Maestas, J. D., R. L. Knight, and W. C. Gilgert. 2001. Biodiversity and land-use change in the American Mountain West. Geographical Review 91:509–24. Maestas, J. D., R. L. Knight, and W. C. Gilgert. 2003. Biodiversity across a rural land-use gradient. Conservation Biology 17:1425–34. Magurran, A. E. 2004. Measuring Biological Diversity. Malden, MA: Blackwell. Malm, O., M. B. Castro, W. R. Bastos, F. J. P. Branches, J. R. D. Guimaraes, C. E. Zuffo, and W. C. Pfeiffer. 1995. An assessment of Hg pollution in different goldmining areas, Amazon Brazil. The Science of the Total Environment 175:127–40.

322 References Mandelik, Y., T. Dayan, V. Chikatunov, and V. Kravchenko. 2007. Reliability of a higher-taxon approach to richness, rarity, and composition assessments at the local scale. Conservation Biology 21:1506–15. Manley, P. N., W. J. Zielinski, M. D. Schlesinger, and S. R. Mori. 2004. Evaluation of a multiple-species approach to monitoring species at the ecoregional scale. Ecological Applications 14:296–310. Manne, L. L., and P. H. Williams. 2003. Building indicator groups based on species characteristics can improve conservation planning. Animal Conservation 6:291–97. Marcot, B. G., and C. H. Flather. 2007. Species-level strategies for conserving rare or little-known species. In Conservation of Rare or Little-Known Species: Biological, Social, and Economic Considerations, eds. M. G. Raphael and R. Molina, 125–64. Washington, DC: Island Press. Margules, C. R., A. O. Nicholls, and R. L. Pressey. 1988. Selecting networks of reserves to maximize biological diversity. Biological Conservation 43:63–70. Margules, C. R., A. O. Nicholls, and M. B. Usher 1994. Apparent species turnover, probability of extinction and the selection of nature reserves: a case study of the Ingleborough Limestone pavements. Conservation Biology 8:398–409. Margules, C. R., and R. L. Pressey. 2000. Systematic conservation planning. Nature 405:243–53. Margules, C., and S. Darkar. 2007. Systematic Conservation Planning. Cambridge, UK: Cambridge University Press. Marques, J. C., F. Salas, J. M. Patricio, and M. A. Pardal. 2005. Application of ecological indicators to assess environmental quality in coastal zones and transitional waters: two case studies. In Handbook of Ecological Indicators for Asessment of Ecosystem Health, eds. S. E. Jorgensen, R. Constanza, and F.-L. Xu, 67–104. Boca Raton, FL: CRC Press. Martikainen, P., L. Kaila, and Y. Haila. 1998. Threatened beetles in white-backed woodpecker habitats. Conservation Biology 12:293–301. Master, L. L. 1991. Assessing threats and setting conservastion priorities. Conservation Biology 5:559–63. Mayfield, M. M., and G. C. Daily. 2005. Countryside biogeography of neotropical herbaceous and shrubby plants. Ecological Applications 15:423–39. McDonald-Madden, E., M. Bode, E. T. Game, H. Grantham, and H. P. Possingham. 2009. The need for speed: informed land acquisitions for conservation in a dynamic property market. Ecology Letters 11:1169–77. McGeoch, M. A. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73:181–201. McGeoch, M. A. 2007. Insects and bioindication: theory and progress. In Insect Conservation Biology, eds. A. J. A. Stewart, T. R. New, and O. T. Lewis, 144–74. London: The Royal Entomological Society. McGeoch, M. A., and S. L. Chown. 1998. Scaling up the value of bioindicators. Trends in Ecology and Evolution 13:46–47.

References 323 McGeoch, M. A., B. J. van Rensburg, and A. Botes. 2002. The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. Journal of Applied Ecology 39:661–72. McKenzie, D. J., E. Garofalo, M. J. Winter, S. Ceradini, F. Verweij, N. Day, R. Hayes, R. van der Oost, P. J. Butler, J. K. Chipman, and E. W. Taylor. 2007. Complex physiological traits as biomarkers of the sub-lethal toxicological effects of pollutant exposure in fishes. Philosophical Transactions of the Royal Society 362:2043–59. McKinney, M. L. 1999. High rates of extinction and threat in poorly studied taxa. Conservation Biology 13:1273–81. McKinney, M. L. 2002. Urbanization, biodiversity, and conservation. BioScience 52:883–90. McKnight, M. W., P. S. White, R. I. McDonald, J. F. Lamoreux, W. Sechrest, R. Ridgely, and S. N. Stuart. 2007. Putting beta-diversity on the map: broadscale congruence and coincidence in the extremes. PLoS Biology 5:2424–32. McLaren, B. E., and R. O. Peterson. 1994. Wolves, moose and tree rings on Isle Royale. Science 266:1555–58. McNeill, S. E. 1994. The selection and design of marine protected areas: Australia as a case study. Biodiversity and Conservation 3:586–605. Medellin, R. A., M. Equihua, and M. A. Amin. 2000. Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conservation Biology 14:1666–75. Meffe, G. K., and C. R. Carroll. 1997. Principles of Conservation Biology. Sunderland, MA: Sinauer Associates. Meijaard, E., and V. Nijman. 2003. Primate hotspots on Borneo: predictive value for general biodiversity and the effects of taxonomy. Conservation Biology 17:725–32. Meir, E., S. Andelman, and H. P. Possingham. 2004. Does conservation planning matter in a dynamic and uncertain world? Ecology Letters 7:615–22. Menge, B. A., E. L. Berlow, C. A. Blanchette, S. A. Navarette, and S. B. Yamada. 1994. The keystone species concept: variation in interaction strength in a rocky intertidal habitat. Ecological Monographs 64:249–86. Metrick, A., and M. L. Weitzman. 1996. Patterns of behavior in endangered species preservation. Land Economics 72:1–16. Meuser, E., H. W. Harshaw, and A. O. Mooers. 2009. Public preference for endemism over other conservation-related species attributes. Conservation Biology 23:1041–46. Micheli, F., B. J. Halpern, L. W. Botsford, and R. R. Warner. 2004. Trajectories and correlates of community change in no-take marine reserves. Ecological Applications 14:1709–23. Mikusinski, G., M. Gromadzki, and P. Chylarecki. 2001. Woodpeckers as indicators of forest bird diversity. Conservation Biology 15:208–17. Miller, B., R. Reading, J. Hoogland, T. Clark, G. Ceballos, R. List, S. Forrest,

324 References L. Hanebury, P. Manzano, J. Pacheco, and D. Uresk. 2000. The role of prairie dogs as a keystone species: response to Stapp. Conservation Biology 14:318– 21. Miller, B., R. Reading, J. Strittholt, C. Carroll, R. Noss, M. Soule, O. Sanchez, J. Terborgh, D. Brightsmith, T. Cheeseman, and D. Foreman. 1999. Using focal species in the design of nature reserve networks. Wild Earth 1998/00:81–92. Mills, L. S., M. E. Soule, and D. F. Doak. 1993. The keystone-species concept in ecology and conservation. BioScience 43:219–24. Millsap, B. A., J. A. Gore, D. E. Runde, and S. I. Cerulean. 1990. Setting priorities for conservation of fish and wildlife species in Florida. Wildlife Monographs 111:1–57. Mittermeier, R. A. 1986. Primate conservation priorities in the neotropical region. In Primates: The Road to Self-Sustaining Populations, ed. K. Benirschke, 221–40. New York: Springer-Verlag. Mittermeier, R. A., N. Myers, P. R. Gil, and C. G. Mittermeier 1999. Hotspots: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. Monterrey, Mexico: Cemex, Conservation International, and Agrupacion Sierra Madre. Mittermeier, R. A., N. Myers, J. B. Thomsen, G. A. B. da Fonseca, and S. Olivieri.1998. Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conservation Biology 12:516–20. Mittermeier, R.A., P.R. Gil, M. Hoffmann, J. Pilgrim, T. Brooks, C.G. Mittermeier, J. Lamoreux, and C.A.B. da Fonseca. 2004. Hotspots Revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. Monterrey, Mexico, Cemex, Conservation International, Agrupacion Sierra Madre, University of Virginia. Montgomery, C. A. 2002. Ranking the benefits of biodiversity: an exploration of relative values. Journal of Environmental Management 65:313–26. Moore, J., A. Balmford, T. Allnutt, and N. Burgess. 2004. Integrating costs into conservation planning across Africa. Biological Conservation 117:343–50. Moore, S. E., and H. P. Huntingdon. 2008. Arctic marine mammals and climate change: impacts and resilience. Ecological Applications 18:suppl. S157–65. Moore, J. L., A. Balmford, T. Brooks, N. D. Burgess, L. A. Hansen, C. Rahbek, and P. H. Williams. 2003. Performance of sub-Saharan vertebrates and indicator groups for identifying priority areas for conservation. Conservation Biology 17:207–18. Moritz, C., K. S. Richardson, S. Ferrier, G. B. Monteith, J. Stanisic, S. E. Williams, and T. Whiffin. 2001. Biogeographical concordance and efficiency of taxon indicators for establishing conservation priority in a tropical rainforest biota. Proceedings of the Royal Society of London B 268:1875–81. Moyle, P. B., and T. Light. 1996. Biological invasions of freshwater: empirical rules and assembly theory. Biological Conservation 78:149–61. Mumby, P. J., K. Broad, D. R. Brumbaugh, C. P. Dahlgren, A. R. Harbone, A. Hastings, K. E. Holmes, C. V. Kappel, F. Micheli, and J. N. Sanchirico. 2008.

References 325 Coral reef habitats as surrogates of species, ecological functions, and ecosystem services. Conservation Biology 22:941–51. Munday, P. L. 2004. Habitat loss, resource specialization, and extinction on coral reefs. Global Change Biology 10:1642–47. Munoz, J. 2007. Biodiversity conservation including uncharismatic species. Biodiversity and Conservation 16:2233–35. Muotka, T., R. Paavola, A. Haapala, M. Novikmec, and P. Laasonen. 2002. Longterm recovery of stream habitat structure and benthic invertebrate communities from in-stream restoration. Biological Conservation 105:243–53. Murawski, S. A. 2000. Definitions of overfishing from an ecosystem perspective. ICES Journal of Marine Science 57:649–58. Murphy, D. D., and B. A. Wilcox. 1986. Butterfly diversity in natural habitat fragments: a test of the validity of vertebrate-based management. In Wildlife 2000: Modeling Habitat Relations of Terrestrial Vertebrates, eds. J. Verner, M. L. Morrison, and C. J. Ralph, 287–92. Madison, WI: University of Wisconsin Press. Murray-Smith, C., N. A. Brummitt, A. T. Oliveira-Filho, S. Bachman, E. Moat, E. M. Nic Lughadha, and E. J. Lucas. 2009. Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conservation Biology 23:151–63. Myers, M. S., and J. W. Fournie. 2002. Histopathological biomarkers as integrators of anthropogenic and environmental stressors. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 221–87. Bethseda, MD: American Fisheries Society. Myers, N., R. A. Mittermeier, C. G. Millermeier, G. A. B. da Fonseca, and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853–58. Naidoo, R., A, Balmford, P. J. Ferraro, S. Polasky, T. H. Ricketts, and M. Rouget. 2006. Integrating economic costs into conservation planning. Trends in Ecology and Evolution 21:681–87. Naiman, R. J., J. M. Melillo, and J. E. Hobbie. 1986. Ecosystem alteration of boreal forest streams by beaver (Castor canadensis). Ecology 67:1254–69. Najera, A., and J. A. Simonetti. 2010. Enhancing avifauna in commercial plantations. Conservation Biology 24:319–24. Negi, H. R., and M. Gadgil. 2002. Cross-taxon surrogacy of biodiversity in the Indian Garhwal Himalaya. Biological Conservation 105:143–55. Neumann, R. P. 1998. Imposing Wilderness: Struggles over Livelihood and Nature Preservation in Africa. Berkeley, CA: University of California Press. New, T. R. 1995. Introduction to Invertebrate Conservation Biology. Oxford, UK: Oxford University Press. Newman, M. C., and W. H. Clements. 2008. Ecotoxicology: A Comprehensive Treatment. Boca Raton, FL: CRC Press. Newman, S. C., A. Chmura, K. Converse, A. M. Kilpatrick, N. Patel, E. Lammers, and P. Daszak. 2007. Aquatic bird disease and mortality as an indicator of changing ecosystem health. Marine Ecology Progress Series 352:299–309. Newmark, W. D. 1987. A land-bridge island perspective on mammalian extinctions in western North American parks. Nature 325:430–32.

326 References Nichols, E., T. Larsen, S. Spector, A. L. Davis, F. Escobar, M. Favila, K. Vulinec, the Scarabaeinae Research Network. 2007. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological Conservation 137:1–19. Nicholson, M. D., and S. Jennings. 2004. Testing candidate indicators to support ecosystem-based management: the power of monitoring surveys to detect temporal trends in fish community metrics. ICES Journal of Marine Sciences 61:35– 42. Niemela, J., and B. Baur. 1998. Threatened species in a vanishing habitat: plants and invertebrates in calcareous grasslands in the Swiss Jura mountains. Biodiversity and Conservation 7:1407–16. Niemi, G. J., J. M. Hanowski, A. R. Lima, T. Nicholls, and N. Weiland. 1997. A critical analysis on the use of indicator species in management. Journal of Wildlife Management 61:1240–52. Nilsson, S. G., U. Arup, R. Baranowski, and S. Ekman. 1995. Tree-dependent lichens and beetles as indicators in conservation forests. Conservation Biology 9:1208–15. Nippress, D. A., A. N. Andersen, A. J. Pik, R. Bramble, P. Wilson, and A. J. Beattie. 2008. The influence of spatial scale on the congruence of classifications circumscribing morphological units of biodiversity. Diversity and Distributions 14:917–24. Noble, I. R., and R. Dirzo. 1997. Forests as human-dominated ecosystems. Science 277:522–25. Noon, B. R., and K. S. McKelvey. 1996. Management of the spotted owl: a case history in conservation biology. Annual Review of Ecology and Systematics 27:135– 62. Norden, B., and T. Appelqvist. 2001. Conceptual problems of ecological continuity and its bioindicators. Biodiversity and Conservation 10:779–91. Norden, B., H. Paltto, F. Gotmark, and K. Wallin. 2007. Indicators of biodiversity, what do they indicate? Lessons for conservation of cryptograms in oak-rich forest. Biological Conservation 135:369–79. Norton, B. G. 1991. Ecosystem health and sustainable resource management. In Ecological Economics: The Science and Management of Sustainability, ed. R. Constanza, 102–17. New York: Columbia University Press. Noss, R. F. 1987. From plant communities to landscapes in conservation inventories: a look at The Nature Conservancy. Biological Conservation 41:11–37. Noss, R. F. 1990. Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology 4:355–64. Noss, R. F. 1999. Assessing and monitoring forest biodiversity: a suggested framework and indicators. Forest Ecology and Management 115:135–46. Noss, R. F. 2004. Some suggestions for keeping national wildlife refuges healthy and whole. Natural Resources Journal 44:1093–111. Noss, R. F., C. Carroll, K. Vance-Borland, and G. Wuerthner. 2002. A multicriteria

References 327 assessment of the irreplaceability and vulnerability of sites in the Greater Yellowstone Ecosystem. Conservation Biology 16:895–908. Noss, R. F., H. B. Quigley, M. G. Hornocker, T. Merrill, and P. C. Paquet. 1996. Conservation biology and carnivore conservation in the Rocky Mountains. Conservation Biology 10:949–63. Novotny, V., and Y. Basset. 2000. Ecological characteristics of rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89:564–72. Nupp, T. E., and R. K. Swihart. 2000. Landscape-level correlates of small-mammal assemblages in forest fragments of farmland. Journal of Mammalogy 81:512– 26. Oaks, J. L., M. Gilbert, M. Z. Virani, R. T. Watson, C. U. Meteyer, B. A. Rideout, H. L. Shivaprasad, S. Ahmed, M. J. I. Chaudhry, M. Arshad, S. Mahmood, A. Ali, and A. A. Khan. 2004. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427:630–33. O’Brien, D. J., J. B. Kaneene, and R. H. Poppenga. 1993. The use of mammals as sentinels for human exposure to toxic contaminants in the environment. Environmental Health Perspectives 99:351–68. O’Connor, T. P. 1998. Mussel watch results from 1986 to 1996. Marine Pollution Bulletin 37:14–19. O’Dea, N., M. B. Araujo, and R. J. Whittaker. 2006. How well do Important Bird Areas represent species and minimize conservation conflict in the tropical Andes? Diversity and Distributions 12:205–16. Odell, E. A., and R. L. Knight. 2001. Songbird and medium-sized mammal communities associated with exurban development in Pitkin County, Colorado. Conservation Biology 15:1143–50. Office of Technology Assessment (OTA). 1987. Technologies to maintain biological diversity. Washington, DC: U.S. Government Printing Office. Oliver, I., and A. J. Beattie. 1996a. Designing a cost-effective invertebrate survey: a test of methods for rapid assessment of biodiversity. Ecological Applications 6:594–607. Oliver, I., and A. J. Beattie. 1996b. Invertebrate morphospecies as surrogates for species: a case study. Conservation Biology 10:99–109. Oliver, I., A. Holmes, J. M. Dangerfield, M. Gillings, A. J. Pik, D. R. Britton, M. Holley, M. E. Montgomery, M. Raison, V. Logan, R. L. Pressey, and A. J. Beattie. 2004. Land systems as surrogates for biodiversity in conservation planning. Ecological Applications 14:485–503. Olson, D. M., and E. Dinerstein. 1998. The Global 200: a representation approach to conserving the earth’s most biologically valuable ecoregions. Conservation Biology 12:502–15. Olson, D. M., E. Dinerstein, E. D. Wikramanayake, N. D. Burgess, G. V. N. Powell, E. C. Underwood, J. A. D’Amico, I. Itoua, H. E. Strand, J. C. Morrison, C. J. Loucks, T. F. Allnutt, T. H. Ricketts, Y. Kura, J. F. Lamoreux, W. W. Wettengel,

328 References P. Hedao, and K. R. Kassem. 2001. Terrestrial ecoregions of the world: a new map of life on earth. BioScience 51:933–38. O’Neill, S. J., T. J. Osborn, M. Hulme, I. Lorenzoni, and A. R. Watkinson. 2008. Using expert knowledge to assess uncertainties in future polar bear populations under climate change. Journal of Applied Ecology 45:1649–59. Oren, Y., A. Perevolotsky, S. Brand, and M. Shachak. 2007. Livestock and engineering network in the Israels Negev: implications for ecosystem management. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 323–42. Amsterdam: Elsevier. Orme, C. D. L., R. G. Davies, M. Burgess, F. Eigenbrod, N. Pickup, V. A. Olson, A. J. Webster, T.-S. Ding, P. C. Rasmussen, R. S. Ridgely, A. J. Stattersfield, P. M. Bennett, T. M. Blackburn, K. J. Gaston, and I. P. F. Owens. 2005. Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–19. Ostrowski, S., E. Bedin, D. M. Lenain, and A. H. Abuzinada. 1998. Ten years of Arabian oryx conservation breeding in Saudia Arabia—achievements and regional perspectives. Oryx 32:209–22. Ovadia, O. 2003. Ranking hotspots of varying sizes: a lesson from the nonlinerality of the species-area relationship. Conservation Biology 17:1440–41. Ozaki, K., M. Isono, T. Kawahara, S. Iida, T. Kudo, and K. Fukuyama. 2006. A mechanistic approach to evaluation of umbrella species as conservation surrogates. Conservation Biology 20:1507–15. Pace, M. L., J. J. Cole, S. R. Carpenter, and J. F. Kitchell. 1999. Trophic cascades in diverse ecosystems. Trends in Ecology and Evolution 14:483–88. Padoa-Schioppa, E., M. Baietto, R. Massa, and L. Bottoni. 2006. Bird communities as bioindicators: the focal species concept in agricultural landscapes. Ecological Indicators 6:83–93. Paillet, Y., L. Berges, J. Hjalten, P. Odor, C. Avon, M. Bernhardt-Romermann, R.-J. Bijlsma, L. de Bruyn, M. Fuhr, U. Grandin, R. Kanka, L. Lundin, S. Luque, T. Magura, S. Matesanz, I. Meszaros, M.-T. Sebastia, W. Schmidt, T. Sandovar, B. Tothmeresz, A. Uotila, F. Valladares, K. Vellak, and R. Virtanen. 2010. Biodiversity differences between managed and unmanaged forests: meta-analysis of species richness in Europe. Conservation Biology 24:101–12. Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100:65–75. Paine, R. T. 1969. A note on trophic complexity and community stability. American Naturalist 103:91–93. Pakkala, T., J. Pellikka, and H. Linden. 2003. Capercaillie Tetrao urogallus—a good candidate for an umbrella species in taiga forests. Wildlife Biology 9:309–16. Palomares, F., and T. M. Caro. 1999. Interspecific killing among mammalian carnivores. American Naturalist 153:492–508. Palomares, F., P. Gaona, P. Ferraras, and M. Delibes. 1995. Positive effects on game species of top predators by controlling smaller predator populations: an example with lynx, mongooses, and rabbits. Conservation Biology 9:295–305.

References 329 Panwar, H. S. 1982. What to do when you’ve succeeded: Project Tiger, ten years later. In National Parks, Conservation and Development: The Role of Protected Areas in Sustaining Society, ed. A. Jeffrey, 183–89. Washington, DC: Smithsonian Institute Press. Panzer, R., and M. W. Schwartz. 1998. Effectiveness of vegetation-based approach to insect conservation. Conservation Biology 12:693–702. Pardini, R., G. M. Accacio, R. R. Laps, E. Mariano, M. L. B. Paciencia, M. Dixo, J. Baumgarten, and D. Faria. 2009. The challenge of maintaining biodiversity in the Atlantic forest: a multi-taxa conservation assessment of an agro-forestry mosaic in southern Bahia. Biological Conservation 142:1178–90. Part, T. and B. Soderstrom. 1999. Conservation value of semi-natural pastures in Sweden: contrasting botanical and avian measures. Conservation Biology 13:755–65. Paszkowski, C. A., and W. M. Tonn. 2000. Community concordance between fish and aquatic birds of lakes in northern Alberta: the relative importance of environmental and biotic factors. Freshwater Biology 43:421–37. Patterson, B. D. 1984. Mammalian extinction and biogeography in the southern Rocky Mountains. In Extinctions, ed. M. H. Nitecki, 247–93. Chicago: University of Chicago Press. Patton, D. R. 1987. Is the use of “management indicator species” feasible? Western Journal of Applied Forestry 2:33–34. Pauly, D., V. Christensen, J. Dalsgaard, R. Froese, and F. Torres Jr. 1998. Fishing down marine food webs. Science 279:860–63. Pawar, S.P., A.C. Birand, M.F. Ahmed, S. Sengupta, and T.R.S. Raman. 2007. Conservation biogeography in north-east India: hierarchical analysis of cross-taxon distributional congruence. Diversity and Distributions 13:53–65. ———. 2006. Conservation biogeography in north-east India: hierarchical analysis of cross-taxon distributional congruence. Diversity and Distributions 13:53–65. Pearman, P. B., and D. Weber. 2007. Common species determine richness patterns in biodiversity indicator taxa. Biological Conservation 138:109–19. Pearsall, W. H. 1957. Report on an ecological survey of the Serengeti National Park, Tanganyika. Oryx 4:71–136. Pearson, D. L. 1995. Selecting indicator taxa for the quantitative assessment of biodiversity. In Biodiversity: Measurement and estimation, ed. D. L. Hawksworth, 75–79. London: Royal Society Publications. Pearson, D. L., and F. Cassola. 1992. World-wide species richness patterns of tiger beetles (Coleoptera Cicindelidae) indicator taxon for biodiversity and conservation studies. Conservation Biology 6:376–91. Pellew, R. A. 1983. The impacts of elephant, giraffe and fire upon the Acacia tortolis woodlands of the Serengeti. African Journal of Ecology 21:41–74. Peres, C. A., and F. Michalski. 2006. Synergistic effects of habitat disturbance and hunting in Amazonian forest vertebrates. In Emerging Threats to Tropical Forests, eds. W. F. Laurance and C. A. Peres, 105–27. Chicago: University of Chicago Press.

330 References Perhans, K., C. Kindstrand, M. Boman, L. B. Djupstrom, L. Gustafsson, L. Mattsson, L. M. Schroeder, J. Weslien, and S. Wikberg. 2008. Conservation goals and the relative importance of costs and benefits in reserve selection. Conservation Biology 22:1331–39. Perry, A. L., P. J. Low, J. R. Ellis, and J. D. Reynolds. 2005. Climate change and distribution shifts in marine fishes. Science 308:1912–15. Petit, L. J., and D. R. Petit. 2003. Evaluating the importance of human-modified lands for neotropical bird conservation. Conservation Biology 17:687–94. Phillips, D. J. H., and D. A. Segar. 1986. Use of bio-monitors in monitoring conservative contaminants: programme design imperatives. Marine Pollution Bulletin 17:10–17. Philpott, S. M., W. J. Arendt, I. Armbrecht, P. Bichier, T. V. Dietsch, C. Gordon, R. Greenberg, I. Perfecto, R. Reynoso-Santos, L. Soto-Pinto, C. Tejeda-Cruz, G. Williams-Linera, J. Valenzuela, and J. M. Zolotoff. 2008. Biodiversity loss in Latin American coffee landscapes: review of the evidence on ants, birds, and trees. Conservation Biology 22:1093–105. Pik, A. J., I. Oliver, and A. J. Beattie. 1999. Taxonomic sufficiency in ecological studies of terrestrial invertebrates. Australian Journal of Ecology 24:555–62. Pimental, D., U. Stachow, D.A. Takacs, H.W. Brubaker, A.R. Dumas, J.J. Meaney, J.A.S. O’Neill, D.E. Onsi, and D.B. Corzilius. 1992. Conserving biological diversityin agricultural/forestry systems: most biological diversity exists in human-managed ecosystems. BioScience 42:354–362. Pimm, S. L. 1991. The Balance of Nature? Ecological Issues in the Conservation of Species and Communities. Chicago: University of Chicago Press. Pimm, S. L., G. J. Russell, J. L. Gittleman, and T. M. Brooks. 1995. The future of biodiversity. Science 269:347–50. Pineda, E., C. Moreno, F. Escobar, and G. Halffter. 2005. Frog, bat, and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Conservation Biology 19:400–410. Pinel-Alloul, B., G. Methot, L. Lapierre, and A. Willsie. 1996. Macroinvertebrate community as a biological indicator of ecological and toxicological factors in Lake Saint-Francois (Quebec). 1996. Environmental Pollution 91:65–87. Pinto, M. P., J. A. F. Diniz-Filho, L. M. Bini, D. Blamires, and T. F. L. V. B. Rangel. 2008. Biodiversity surrogate groups and conservation priority areas: birds of the Brazilian Cerrado. Diversity and Distributions 14:78–86. Pintor, L. M., and D. A. Soluk. 2006. Evaluating the non-consumptive, positive effects of a predator in the persistence of an endangered species. Biological Conservation 130:584–91. Pitkanen, M., and J. Tiainen. 2001. Biodiversity of Agricultural Landscapes in Finland. Birdlife Conservation Series (No. 3). Helsinki, Finland: Birdlife. Poiani, K. A., M. D. Merrill, and K. A. Chapman. 2001. Identifying conservationpriority areas in a fragmented Minnessota landscape based on the umbrella species concept and selection of large patches of natural vegetation. Conservation Biology 15:513–22.

References 331 Poiani, K. A. B. D. Richter, M. G. Anderson, and H. E. Richter. 2000. Biodiversity conservation at multiple scales: functional sites, landscapes, and networks. BioScience 50:133–46. Polasky, S., E. Nelson, J. Camm, B. Csuti, P. Fackler, E. Lonsdorf, C. Montgomery, D. White, J. Arthur, B. Garber-Yonts, R. Haight, J. Kagan, A. Starfield, and C. Tobalske. 2008. Where to put things? Spatial land management to sustain biodiversity and economic returns. Biological Conservation 141:1505–24. Polasky, S., J. D. Camm, and B. Garber-Yonts. 2001. Selecting biological reserves cost-effectively: an application to terrestrial vertebrate conservation in Oregon. Land Economics 77:68–78. Polis, G. A., and D. R. Strong. 1996. Food web complexity and community dynamics. American Naturalist 147:813–46. Possingham, H., I. Ball, and S. Andelman. 2000. Mathematical models for identifying representative reserve networks. In Quantitative Methods for Conservation Biology, eds. S. Ferson and M. Burgman, 291–306. New York: Springer-Verlag. Pounds, J. A., M. R. Bustamante, L. A. Coloma, J. A. Consuegra, M. P. Fogden, P. N. Foster, E. La Marca, K. L. Masters, A. Merino-Viteri, R. Puschendorf, S. R. Ron, G. A. Sanchez-Azofeifa, C. J. Still, and B. E. Young. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–67. Power, M. 2002. Assessing fish population responses to stress. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 379–421. Bethseda, MD: American Fisheries Society. Power, M. E., D. Tilman, J. A. Estes, B. A. Menge, W. J. Bond, L. Scott Mils, G. Daily, J. C. Castilla, J. Lubchenco, and R. T. Paine. 1996. Challenges in the quest for keystones. BioScience 46:609–20. Prance, G. T. 1995. A comparison of the efficacy of higher taxa and species numbers in the assessment of the biodiversity in the neotropics. In Biodiversity: Measurement and Estimation, ed. D. L. Hawksworth, 89–99. London: Royal Society Publications. Prange, S., and S. D. Gehrt. 2007. Response of skunks to a simulated increase in coyote activity. Journal of Mammalogy 88:1040–49. Prendergast, J. R., and B. C. Eversham. 1997. Species richness covariance in higher taxa: empirical tests of the biodiversity indicator concept. Ecography 20:210– 16. Prendergast, J. R., R. M. Quinn, J. H. Lawton, B. C. Eversham, and D. W. Gibbons. 1993. Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365:335–37. Prendrini, L., L. Theron, K. van der Merwe, N. Owen-Smith. 1996. Abundance and guild structure of grasshoppers (Orthoptera: Acridiodea) in communally grazed and protected savanna. South African Journal of Zoology 31:120–29. Pressey, R. L. 1994. Ad hoc reservations: forward or backward steps in developing representative reserve systems? Conservation Biology 8:662–68.

332 References Pressey, R. L. 2004. Conservation planning and biodiversity: assembling the best data for the job. Conservation Biology 18:1677–81. Pressey, R. L., T. C. Hagar, K. M. Ryan, J. Schwarz, S. Wall, S. Ferrier, and P. M. Creaser. 2000. Using abiotic data for conservation assessments over extensive regions: quantitative methods applied across New South Wales, Australia. Biological Conservation 96:55–82. Pressey, R. L., C. J. Humphries, C. R. Margules, R. I. Vane-Wright, and P. H. Williams. 1993. Beyond opportunism: key principles for systematic reserve selection. Trends in Ecology and Evolution 8:124–28. Pressey, R. L., and V. S. Logan. 1995. Reserve coverage and requirements in relation to partitioning and generalization of land classes: analyses for western New South Wales. Conservation Biology 9:1506–17. Pressey, R. L., and A. O. Nicholls. 1989. Efficiency in conservation evaluation: scoring vs. iterative procedures. Biological Conservation 50:199–218. Pressey, R. L., H. P. Possingham, V. S. Logan, J. R. Day, and P. H. Williams. 1999. Effects of data characteristics on the results of reserve selection algorithms. Journal of Biogeography 26:179–91. Pressey, R. L., and K. H. Taffs. 2001. Sampling of land types by protected areas: three measures of effectiveness applied to western New South Wales. Biological Conservation 101:105–17. Prevey, J. S., M. J. Germino, N. J. Huntly, and R. S. Inouye. 2010. Exotic plants increase and native plants decrease with loss of foundation species in sagebrush steppe. Plant Ecology 207:39–51. Prugh, L. R., C. J. Stoner, C. W. Epps, W. T. Bean, A. S. Laliberte, and J. S. Brashares. 2009. The rise of the mesopredator. BioScience 59:779–91. Purtauf, T., J. Dauber, and V. Wolters. 2005. The response of carabids to landscape simplification differs between trophic groups. Oecologia 142:458–64. Purvis, A. J., L. Gittlemam, G. Cowlishaw, and G. M. Mace. 2000. Predicting extinction risk in declining species. Proceedings of the Royal Society of London B 267:1947–52. Qian, H., and R. E. Ricklefs. 2008. Global concordance in diversity patterns of vascular plants and terrestrial vertebrates. Ecology Letters 11:547–53. Quinn, J. L., and Y. Kokorev. 2002. Trading-off risks from predators and from aggressive hosts. Behavioral Ecology and Sociobiology 51:455–60. Quirijns, F. J., J. J. Poos, and A. D. Rijnsdorp. 2008. Standardizing commercial CPUE data in monitoring stock dynamics: accpunting for targeting behaviour in mixed fisheries. Fisheries Research 89:1–8. Rabinowitz, A. 1986. Jaguar. New York: Random House. Rabinowitz, D., S. Cairns, and T. Dillon. 1986. Seven forms of raity and their frequency in the flora of the British Isles. In Conservation Biology: The Science of Scarcity and Diversity, ed. M. E. Soule, 182–204. Sunderland, MA: Sinauer Assoc. Racey, G. D., and D. L. Euler. 1982. Small mammal and habitat response to shore-

References 333 line cottage development in central Ontario. Canadian Journal of Zoology 60:865–80. Rachowicz, L. J., J. M. Hero, R. A. Alford, J. W. Taylor, J. A. T. Morgan, V. T. Vredenburg, J. P. Collins, and C. J. Briggs. 2005. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology 19:1441–48. Raffa, K. F., and A. A. Berryman. 1987. Interacting selective pressures in coniferbark beetle systems: a basis for reciprocal adaptations? American Naturalist 129:234–62. Rahbek, C. 1995. The elevational gradient of species richness: a uniform pattern? Ecography 18:200–205. Rahbek, C. 2005. The role of spatial scale and the perception of large-scale speciesrichness patterns. Ecology Letters 8:224–39. Rahbek, C., and G. R. Graves. 2000. Detection of macro-ecological patterns in South American hummingbirds is affected by spatial scale. Proceedings of the Royal Society London B 267:2259–65. Rahbek, C., and G. R. Graves. 2001. Multiscale assessment of patterns of avian species richness. Proceedings of the National Academy of Sciences 98:4534–39. Randall, D. J., and SC. Brauner. 1991. Effects of environmental factors on exercise in fish. Journal of Experimental Biology 160:113–26. Ranius, T. 2002. Osmoderma eremita as an indicator of species richness of beetles in tree hollows. Biodiversity and Conservation 11:931–41. Rapport, D. J. 1989. What constitutes ecosystem health? Perspectives in Biology and Medicine 33:120–32. Rapport, D. J., C. Gaudet, J. R. Karr, J. S. Baron, C. Bohlen, W. Jackson, B. Jones, R. J. Naiman, B. Norton, and M. M. Pollock. 1998. Evaluating landscape health: integrating societal goals and biophysical processes. Journal of Environmental Management 53:1–15. Ratcliffe, F. N., K. Myers, B. V. Fennessy, and J. H. Calaby. 1952. Myxomatosis in Australia: a step towards the biological control of the rabbit. Nature 170:1– 13. Ray, J. C., K. H. Redford, R. S. Steneck, and J. Berger. 2005. Large Carnivores and the Conservation of Biodiversity.Washington, DC: Island Press. Rayner, M. J., M. E. Hauber, M. J. Imber, R. K. Stamp, and M. N. Clout. 2007. Spatial heterogeneity of mesopredator release within an oceanic island system. Proceedings of the National Academy of Sciences 104:20862–65. Rebelo, A. G., and W. R. Siegfried. 1990. Protection of Fynbos vegetation: ideal and real-world options. Biological Conservation 54:15–31. Rebelo, A. G., and W. R. Siegfried. 1992. Where should nature reserves be located in the Cape Floristic Region, South Africa? Models for the spatial configuration of a reserve network aimed at maximizing the protection of floral diversity. Conservation Biology 6:243–52. Redford, K. H. 1992. The empty forest. BioScience 42:412–22.

334 References Reed, K. E., and J. G. Fleagle. 1995. Geographic and climatic control of primate diversity. Proccedings of the National Academy of Sciences. 92:7874–76. Regan, H. M., M. Colyvan, and M. A. Burgman 2002. A taxonomy and treatment of uncertainty for ecology and conservation biology. Ecological Applications 12:618–28. Regier, H. 1990. Workshop issue paper: indicators and assessment of the state of fisheries. Environmental Monitoring and Asessment 15:289–94 Reichman, O. J., J. H. Benedix, and T. R. Seastedt. 1993. Distinct animal-generated edge effects in a tallgrass prairie community. Ecology 74:1281–85. Reichman, O. J., and E. W. Seabloom. 2002. The role of pocket gophers as subterranean ecosystem engineers. Trends in Ecology and Evolution 17:44–49. Reid, W. V. 1998. Biodiversity hotspots. Trends in Ecology and Evolution 13:275– 280. Reunanen, P., M. Monkkonen, and A. Nikula. 2000. Managing boreal forest landscapes for flying squirrels. Conservation Biology 14:218–26. Rey Benayas, J. M., and E. de la Montana. 2003. Identifying areas of high-value vertebrate diversity for strengthening conservation. Biological Conservation 114:357–70. Reyers, B., A. S. van Jaarsveld, and M. Kruger. 2000. Complementarity as a biodiversity indicator strategy. Proceedings of the Royal Society of London B 267:505– 13. Rice, C. D., and M. R. Arkoosh. 2002. Immunological indicators of environmental stress and disease susceptibility in fishes. In Biological Indicators of Aquatic Ecosystem Stress, ed. S. M. Adams, 187–220. Bethseda, MD: American Fisheries Society. Rice, J. 2003. Environmental health indicators. Ocean & Coastal Management 46:235–59. Rice, J. A. 1990. Bioenergetics modeling approaches to evaluation of stress in fishes. American Fisheries Society Symposium 8:90–92. Rice, J. C. 2000. Evaluating fishery impacts using metrics of community structure. ICES Journal of Marine Science 57:682–88. Rice, J. C., and M.-J. Rochet. 2005. A framework for selecting a suite of indicators for fisheries management. ICES Journal of Marine Science 62:516–27. Richardson, D., and W. J. Bond. 1991. Determinants of plant distribution: evidence from pine invasions. American Naturalist 137:639–68. Richardson, D. M., P. Pysek, M. Rejmanek, M. G. Barbour, F. D. Panetta, and C. J. West. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6:93–107. Ricketts, T. H. 2001. Aligning conservation goals: are patterns of species richness and endemism concordant at regional scales? Animal Biodiversity and Conservation 24:91–99. Ricketts, T. H., G. C. Daily, and P. R. Ehrlich. 2002. Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales. Biological Conservation 103:361–70.

References 335 Ricketts, T. H., G. C. Daily, P. R. Ehrlich, J. P. Fay. 2001. Countryside biogeography of moths in a fragmented landscape: biodiversity in native and agricultural habitats. Conservation Biology 15:378–88. Ricketts, T. H., E. Dinerstein, D. M. Olson, and C. Loucks. 1999. Who’s where in North America? BioScience 49:369–81. Riley, S. P. D., R. M. Sauvajot, T. K. Fuller, E. C. York, D. A. Kamradt, C. Bromley, and R. K. Wayne. 2003. Effects of urbanization and habitat fragmentation of bobcats and coyotes in southern California. Conservation Biology 17:566–76. Ripple, W. J., and R. L. Beschta. 2004. Wolves and the ecology of fear: can predation risk structure ecosystems? BioScience 54:755–66. Ripple, W. J., and R. L. Beschta. 2006. Linking a cougar decline, trophic cascade, and catastrophic regime shift in Zion National Park. Biological Conservation 133:397–408. Ripple, W. J., and R. L. Beschta. 2007. Restoring Yellowstone’s aspen with wolves. Biological Conservation 138:514–19. Ripple, W. J., and E. J. Larsen. 2000. Historic aspen recruitment, elk, and wolves in northern Yellowstone National Park. Biological Conservation 95:361–70. Ripple, W. J., E. J. Larsen, R. A. Renkin, and D. W. Smith. 2001. Trophic cascades among wolves, elk and aspen on Yellowstone National Parks’s northern range. Biological Conservation 102:227–34. Ripple, W. J., P. D. Lattin, K. T. Hershey, F. F. Wagner, and E. C. Meslow. 1996. Landscape patterns around northern spotted owl nest sites in southwestern Oregon. Journal of Wildlife Management 61:151–58. Ritchie, E. G., and C. N. Johnson. 2009. Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters 12:982–98. Roberge, J.-M., and P. Angelstam. 2004. Usefulness of the umbrella species concept as a conservation tool. Conservation Biology 18:76–85. Roberge, J.-M., and P. Angelstam 2006. Indicator species among resident forest birds—a cross-regional evaluation in northern Europe. Biological Conservation 130:134–47. Roberge, J.-M., G. Mikusinski, and S. Svensson. 2008. The white-backed woodpecker: umbrella species for forest conservation planning? Biodiversity and Conservation 17:2479–94. Roberts, C. 2005. Marine protected areas and biodiversity conservation. In Marine Conservation Biology: The Science of Maintaining the Sea’s Biodiversity, eds. E. A. Norse, and L. B. Crowder, 265–79. Washington DC: Island Press. Roberts, C. M., S. Andelman, G. Branch, R. H. Bustamante, J. C. Castilla, J. Dugan, B. S. Halpern, K. D. Laferty, H. Leslie, J. Lubchenco, D. McArdle, H. P. Possingham, M. Rucklelshaus, and R. R. Warner. 2003. Ecological criteria for evaluating candidate sites for marine reserves. Ecological Applications 13:S199– 214. Robinson, R. A., and W. J. Sutherland, 2002. Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology 39:157–76. Rodrigues, A. S. L., H. R. Akcakaya, S. J. Andelman, M. I. Bakarr, L. Boitani, T. M.

336 References Brooks, J. S. Chanson, L. D. C. Fishpool, G. A. B. da Fonseca, K. J. Gaston, M. Hoffmann. P. A. Marquet, J. D. Pilgrim, R. L. Pressey, J. Schipper, W. Sechrest, S. N. Stuart, L. G. Underhill, R. W. Waller, M. E. J. Watts, and X. Yan. 2004b. Global gap analysis: priority regions for expanding the global protected-area network. BioScience 54:1092–100. Rodrigues, A. S. L., S. J. Andelman, M. I. Bakarr, L. Boitani, T. M. Brooks, R. M. Cowling, L. D. C. Fishpool, G. A. B. da Fonseca, K. J. Gaston, M. Hoffmann. J. S. Long, P. A. Marquet, J. D. Pilgrim, R. L. Pressey, J. Schipper, W. Sechrest, S. N. Stuart, L. G. Underhill, R. W. Waller, M. E. J. Watts, and X. Yan. 2004a. Effectiveness of the global protected area network in representing species diversity. Nature 428:640–42. Rodrigues, A. S. L., and T. M. Brooks. 2007. Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Annual Review of Ecology, Evolution and Systematics 38:713–37. Rodrigues, A. S. L., and K. J. Gaston. 2002. Rarity and conservation planning across geopolitical units. Conservation Biology 16:674–82. Rodrigues, A. S. L., K. J. Gaston, and R. D. Gregory. 2000a. Using presenceabsence data to establish reserve selection procedures that are robust to temporal species turnover. Proceedings of the Royal Society B 267:897–902. Rodrigues, A. S. L., R. D. Gregory, and K. J. Gaston. 2000b. Robustness of reserve selection procedures under temporal species turnover. Proceedings of the Royal Society of London B 267:49–55. Rodrigues, A. S. L., J. D. Pilgrim, J. F. Lamoreux, M. Hoffmann, and T. M. Brooks. 2006. The value of the IUCN Red List for conservation. Trends in Ecology and Evolution 21:71–76. Rodrigues, A. S. L., R. Tratt, B. D. Wheeler, and K. J. Gaston. 1999. The performance of existing networks of conservation areas in representing biodiversity. Proceedings of the Royal Society of London B 266:1453–60. Rodriguez, J. P., D. L. Pearson, and R. Barrera. 1998. A test for the adequacy of bioindicator taxa: are tiger beetles (Coleoptera: Cicindelidae) appropriate indicators for monitoring the degradation of tropical forests in Venezuela? Biological Conservation 83:69–76. Roff, J. C., and S. M. J. Evans. 2002. Frameworks for marine conservation—nonhierarchical approaches and distinctive habitats. Aquatic Conservation: Marine and Freshwater Ecosystems 12:635–48. Rogers, C. M., and M. J. Caro. 1998. Song sparrows, top carnivores, and nest predation: a test of the mesopredator release hypothesis. Oecologia 116:227–33. Rohlf, D. J. 1991. Six biological reasons why the endangered species act doesn’t work and what to do about it. Conservation Biology 5:273–82. Rohr, J. R., A. M. Schotthoefer, T. R. Raffel, H. J. Carrick, N. Halstead, J. T. Hoverman, C. M. Johnson, L. B. Johnson, C. Lieske, M. D. Piwoni, P. K. Schoff, and V. R. Beasely. 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235–39.

References 337 Rolstad, J., I. Gjerde, V. S. Gundersen, and M. Saetersdal. 2002. Use of indicator species to assess forest continuity: a critique. Conservation Biology 16:253–57. Rondinini, C., S. Stuart, and L. Boitani. 2005. Habitat suitability models and the shortfall in conservation planning for African vertebrates. Conservation Biology 19:1488–97. Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rozenzweig, and J. A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57–60. Root, T. L., and S. H. Schneider. 2002. Climate change: overview and implications for wildlife. In Wildlife Responses to Climate Change: North American Case Studies, eds. S. H. Schneider and T. L. Root, 1–56. Washington, DC: Island Press. Rosenberg, D. M., and V. H. Resh, eds. 1993. Freshwater Biomonitoring and Benthic Macroinvertebrates. New York: Chapman & Hall. Roth, T., and D. Weber. 2008. Top predators as indicators for species richness? Prey species are just as useful. Journal of Applied Ecology 45:987–91. Rothley, K. D., C. N. Berger, C. Gonzalez, E. M. Webster, and D. I. Rubenstein. 2004. Combining strategies to select reserves in fragmented landscapes. Conservation Biology 18:1121–31. Rowland, M. M., M. J. Wisdom, L. H. Suring, and C. W. Meinke. 2006. Greater sage-grouse as an umbrella species for sagebrush-associated vertebrates. Biological Conservation 129:323–35. Roy, A. H., A. D. Rosemond, D. S. Leigh, M. J. Paul, and J. B. Wallace. 2003. Habitat-specific responses of stream insects to land cover disturbance: biological consequences and monitoring implications. Journal of North American Benthological Society 22:292–307. RSPB. 2007. Conservation Science 2007 in the RSPB. London: Royal Society for the Protection of Birds Reports. Rubino, M. J., and G. R. Hess. 2002. Planning open spaces for wildlife 2: modeling and verifying focal species habitat. Landscape and Urban Planning 64:89–104. Rubinoff, D. 2001. Evaluating the California gnatcatcher as an umbrella species for conservation of southern California coastal sage scrub. Conservation Biology 15:1374–83. Russ, G. R., and A. C. Alcala. 1996. Marine reserves: rates and patterns of recovery and decline of large predatory fish. Ecological Applications 6:947–61. Ryti, R. T. 1992. Effect of the focal taxon on the selection of nature reserves. Ecological Applications 2:404–10. Saetersdal, M., I. Gjerde, and H. H. Blom. 2005. Indicator species and the problem of spatial inconsistency in nestedness patterns. Biological Conservation 122:305–16. Saetersdal, M., J. M. Line, and H. J. B. Birks. 1993. How to maximize biological diversity in nature reserve selection: vascular plants and breeding birds in deciduous woodlands, western Norway. Biological Conservation 66:131–38. Safalsky, N., R. Margoulis, K. H. Redford, and J. G. Robinson. 2002. Improving

the practice of conservation: a conceptual framework and research agenda for conservation science. Conservation Biology 16:1469–79. Samways, M. J. 1994. Insect Conservation Biology. London: Chapman and Hall. Sanderson, E. W., M Jaiteh, M. A. Levy, K. H. Redford, A. V. Wannebo, and G. Woolmer. 2002c. The human footprint and the last of the wild. BioScience 52:891–904. Sanderson, E. W., K. H. Redford, C.-L. B. Chetkiewicz, R. A. Medellin, A. R. Rabinowitz, J. G. Robinson, and A. B. Taber. 2002b. Planning to save a species: the jaguar as a model. Conservation Biology 16:58–72. Sanderson, E. W., K. H. Redford, A. Vedder, P. B. Coppolillo, and S. E. Ward. 2002a. A conceptual model for conservation planning based on landscape species requirements. Landscape and Urban Planning 58:41–56. Sandin, S. A., J. E. Smith, E. E. DeMartini, E. A. Dinsdale, S. D. Donner, A. M. Friedlander, T. Konotchick, M. Malay, J. E. Maragos, D. Obura, O. Pantos, G. Pauly, M. Ritchie, F. Rohwer, R. E. Schroeder, S. Walsh, J. B. C. Jackson, N. Knowlton, and E. Sala. 2008. Baselines and degradation of coral reefs in the Northern Line Islands. PLoS ONE 3:e1548. Sarkar, S., R. L. Pressey, D. P. Faith, C. R. Margules, T. Fuller, D. M. Stoms, A. Moffett, K. A. Wilson, K. J. Williams, P. H. Williams, and S. Andelman. 2006. Biodiversity conservation planning tools: present status and challenges for the future. Annual Reviews of Environment and Resources 31:123–59. Sauberer, N., K. P. Zulka, M. Abensperg-Traun, H.-M. Berg, G. Bieringer, N. Milasowszky, D. Moser, C. Plutzar, M. Pollheimer, C. Storch, R. Trostl, H. Zechmeister, G. Grabherr. 2004. Surrogate taxa for biodiversity in agricultural landscapes of eastern Austria. Biological Conservation 117:181–90. Schaeffer, D. J., E. E. Herricks, and H. W. Kerster. 1988. Ecosystem health: 1. Measuring ecosystem health. Environmental Management 12:445–55. Scheffler, P.Y. 2005. Dung beetle (Coleoptera: Scarabaeidae) diversity and community structure across three disturbance regimes in eastern Amazonia. Journal of Tropical Ecology 21:9–19. Schmitz, O. J., P. A. Hamback, and A. Beckerman. 2000. Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. American Naturalist 155:141–53. Schneider, D. C. 1994. Quantitative Ecology: Spatial and Temporal Scaling. San Diego, CA: Academic Press. Schulze, C. H., M. Waltert, P. J. A. Hessler, R. Pitopang, Shahabuddin, D. Veddeler, M. Muhlenberg, S. R. Gradstein, C. Leuschner, I. Steffan-Dewenter, and T. Tscharntke. 2004. Biodiversity indicator groups of tropical land-use systems: comparing plants, birds, and insects. Ecological Applications 14:1321–33. Scott, J. M., F. Davis, B. Csuti, R. Noss, B. Butterfield, C. Groves, H. Anderson, S. Caicco, F. D’Erchia, T. C. Edwards Jr., J. Ullman, and R. G. Wright. 1993.

References 339 Scott, J. M., F. W. Davis, R. G. McGhie, R. G. Wright, C. Groves, and J. Estes. 2001. Nature reserves: do they capture the full range of America’s biological diversity? Ecological Applications 11:99–1007. Sebastiao, H., and C. E. V. Grelle. 2009. Taxon surrogates among Amazonian mammals: can total species richness be predicted by single orders? Ecological indicators 9:160–66. Seddon, P. J., and T. Leech. 2008. Conservation short cut, or long and winding road? A critique of umbrella species criteria. Oryx 42:240–45. Seed, R. 1996. Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shores. Journal of Marine Biology Association 76:203–10. Sekercioglu, C. H., P. R. Ehrlich, G. C. Daily, D. Aygen, and R. F. Sandi. 2002. Disappearance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences 99:263–67. Sekercioglu, C. H., S. R. Loarie, F. O. Brenes, P. R. Ehrlich, and G. C. Daily. 2007. Persistence of forest birds in the Costa Rican agricultural countryside. Conservation Biology 21:482–94. Sepkoski, J. J., Jr. 1992. Phylogenetic and ecological patterns in Phanerozoic history of marine biodiversity. In Systematics, Ecology, and the Biodiversity Crisis, ed. N. Eldridge, 77–100. New York: Columbia University Press. Sergio, F., J. Blas, M. Forero, N. Fernandez, J. A. Donazar, and F. Hiraldo. 2005b. Preservation of wide-ranging top predators by site-protection: black and red kites in Donana National Park. Biological Conservation 125:11–21. Sergio, F., T. Caro, D. Brown, B. Clucas, J. Hunter, J. Ketchum, K. McHugh, and F. Hiraldo. 2008. Top predators as conservation tools: ecological rationale, assumptions and efficacy. Annual Review of Evolution, Ecology and Systematics 39:1–19. Sergio, F., L. Marchesi, and P. Pedrini. 2004. Integrating individual habitat choices and regional distribution of a biodiversity indicator and top predator. Journal of Biogeogaphy 31:619–28. Sergio, F., I. Newton, and L. Marchesi. 2005a. Top predators and biodiversity. Nature 436:192. Sergio, F., I. Newton, L. Marchesi, and P. Pedrini. 2006. Ecologically justified charisma: preservation of top predators delivers biodiversity conservation. Journal of Applied Ecology 43:1049–55. Sergio, F., P. Pedrini, and L. Marchesi. 2003. Reconciling the dichotomy between single species and ecosystem conservation: black kites (Milvus migrans) and eutrophication in pre-Alpine lakes. Biological Conservation 110:101–11. Shackelton, C. M. 2000. Comparison of plant diversity in protected and communal lands in the Bushbuckridge lowveld savanna, South Africa. Biological Conservation 94:273–85. Shaffer, M. L. 1992. Keeping the Grizzly Bear in the American West: A Strategy for Real Recovery. Washington, DC: Wilderness Society.

340 References Shapcott, A., M. Rakotoarinivo, R. J. Smith, G. Lysakova, M. F. Fay, and J. Dransfield. 2007. Can we bring Madagascar’s critically endangered palms back from the brink? Genetics, ecology and conservation of the critically endangered palm Beccariophoenix madagarascensis. Botanical Journal of the Linnean Society 154:589–608. Shi, H., A. Singh, S. Kant, Z. Zhu and E. Waller. 2005. Integrating habitat status, human population pressure, and protection status into biodiversity conservation priority setting. Conservation Biology 19:1273–85. Shin, Y.-J., M.-J. Rocet, S. Jennings, J. G. Field, and H. Gislason. 2005. Using sizebased indicators to evaluate the ecosystem effects of fishing. ICES Journal of Marine Science 62:384–96. Shurin, J. B., E. T. Borer, E. W. Seabloom, K. Anderson, C. A. Blanchette, B. Broitman, S. D. Cooper, and B. S. Halpern. 2002. A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters 5:785–91. Simberloff, D. 1998. Flagships, umbrellas and keystones: is single-species management passé in the landscape era? Biological Conservation 83:247–57. Simila, M., J. Kouki, M. Monkkonen, A.-L. Sippola, and E. Huhta. 2006. Covariation and indicators of species diversity: Can richness of forest-dwelling species be predicted in northern boreal forests? Ecological Indicators 6:686– 700. Simon, T. P., ed. 2003. Biological Response Signatures: Indicator Patterns Using Aquatic Communities. Boca Raton, FL: CRC Press. Simon, T. P., and J. A. Exl. 2003. Effects of silviculture of biotic integrity for benthic macroinvertebrate and fish assemblages in northeastern Minnesota’s northern lakes and forest ecoregion (USA). In Biological Response Signatures: Indicator Patterns Using Aquatic Communities, ed. T. P. Simon, 325–46. Boca Raton, FL: CRC Press. Siriwardena, G. M., D. K. Stevens, G. Q. A. Anderson, J. A. Vickery, N. A. Calbrade, and S. Dodd. 2007. The effect of supplementary winter seed food on breeding populations of farmland birds: evidence from two large-scale experiments. Journal of Applied Ecology 44:920–32. Sisk, T. D., A. E. Launer, K. R. Switky, and P. R. Ehrlich. 1994. Identifying extinction threats. BioScience 44:592–604. Slik, J. W. F., C. S. Bernard, F. C. Breman, M. Van Beek, A. Salim, and D. Sheil. 2008. Wood density as a conservation tool: quantification of disturbance and identification of conservation-priority areas in tropical forests. Conservation Biology 22:1299–308. Slocum, R. 2004. Polar bears and energy-efficient lightbulbs: strategies to bring climate change home. Environment and Planning D 22:413–38. Smart, R., M. J. Whiting, and W. Twine. 2005. Lizards and landscapes: integrating field surveys and interviews to assess the impact of human disturbance on lizard assemblages and selected reptiles in a savanna in South Africa. Biological Conservation 122:23–31.

References 341 Smith, D. W., R. O. Peterson, and D. B. Houston. 2003. Yellowstone after wolves. BioScience 53:330–40. Smith, G. A., and M. V. Lomolino. 2004. Black-tailed prairie dogs and the structure of avian communities on the shortgrass plains. Oecologia 138:592–602. Smith, G. F., T. Gittings, M. Wilson, L. French, A. Oxbrough, S. O’Donoghue, J. O’Halloran, D. L. Kelly, F. J. G. Mitchell, T. Kelly, S. Iremonger, A.-M. McKee, and P. Giller. 2008. Identifying practical indicators of biodiversity for stand-level management of plantation forests. Biodiversity and Conservation 17:991–1015. Smith, W. P., S. M. Gende, and J. V. Nichols. 2005. The northern flying squirrel as an indicator species of temperate rain forest: test of an hypothesis. Ecological Applications 15:689–700. Snyder, C. D., J. A. Young, D. P. Lemarie, and D. R. Smith. 2002. Influence of eastern hemlock (Tsuga canadensis) forests on aquatic invertebrate assemblages in headwater streams. Canadian Journal of Fish and Aquatic Science 59:262– 75. Sodhi, N. S., B. W. Brook, and C. J. A. Bradshaw. 2007. Tropical Conservation Biology. Malden, MA: Blackwell Publishing. Sotherton, N. W., and M. J. Self. 2000. Changes in plant and arthropod diversity on lowland farmland: an overview. In Ecology and Conservation of Lowland Farmland Birds, eds. N. J. Aebischer, A. D. Evans, P. V. Grice and J. A. Vickery, 26– 35. Tring, UK: British Ornithologists Union. Soule, M. E. 1985. Biodiversity indicators in California: taking nature’s temperature. California Agriculture 49:40–44. Soule, M. E., D. T. Bolger, A. C. Alberts, R. Sauvajot, J. Wright, M. Sorice, and S. Hill. 1988. Reconstructed dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conservation Biology 2:75–92. Soule, M. E., J. A. Estes, B. Miller, and D. L. Honnold. 2005. Strongly interacting species: conservation policy, management, and ethics. BioScience 55:168–76. Soule, M. E., B. A. Wilcox, and C. Holtby. 1979. Benign neglect: a model of faunal collapse in the game reserves of East Africa. Biological Conservation 15:259–72. Sovada, M. A., A. B. Sargeant, and J. W. Grier. 1995. Differential effects of coyotes and red foxes on duck nest success. Journal of Wildlife Management 59:1–9. Sparling, D. W., G. M. Fellers, and L. L. McConnell. 2001. Pesticides and amphibian population declines in California. Environmental Toxicology and Chemistry 20:1591–95. Spellerberg, I. F. 1991. Monitoring Ecological Change. Cambridge: Cambridge University Press. Springer, A. M., G. V. Byrd, and S. J. Iverson. 2007. Hot oceanography: planktivorous seabirds reveal ecosystem responses to warming of the Bering Sea. Marine Ecology Progress Series 352:289–97. Springer, A. M., J. A. Estes, G. B. van Vilet, T. M. Williams, D. F. Doak, E. M. Danner, K. A. Forney, and B. Pfister. 2003. Sequential megafaunal collapse in the

342 References north Pacific ocean: an ongoing legacy of industrial whaling? Proceedings of the National Academy of Sciences 100:12223–28. Stahl, R. G., Jr. 1997. Can mammalian and non-mammalian “sentinel species” data be used to evaluate the human health implications of environmental contaminants? Human Ecological Risk Assessment 3:329–35. Stattersfield, A. M., M. J. Crosby, A. J. Long, and D. C. Wege. 1998. Endemic Bird Areas of the World: Priorities for Biodiversity Conservation. Cambridge, UK: Birdlife International. Steedman, R. J. 1988. Modification and assessment of an index of biotic integrity to quantify stream quality in southern Ontario. Canadian Journal of Fisheries and Aquatic Sciences 45:492–501. Steffan-Dewenter, I. 2003. Importance of habitat area and landscape context for species richness of bees and wasps in fragmented orchard meadows. Conservation Biology 17:1036–44. Steffan-Dewenter, I., U. Munzenberg, C. Burger, C. Thies, and T. Tscharntke. 2002. Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–32. Stegemann, J. J., K. W. Rento, B. R. Woodin, Y.-S. Zhang, and R. F. Addison. 2002. Molecular responses to environmental contamination: enzyme and protein systems as indicators of chemical exposure and effect. In Biomarkers: Biochemical, Physiological and Histological Markers of Anthropogenic Stress, eds. R. J. Hugget, R. A. Kimerly, M. Mehrle, and H. L. Bergman, 235–65. Chelsea, MI: Lewis Publishers. Steneck, R. S., and E. Sala. 2005. Large marine carnivores: trophic cascades and top-down controls in coastal ecosystems past and present. In Large Carnivores and the Conservation of Biodiversity, eds. J. C. Ray, K. H. Redford, R. S. Steneck, and J. Berger, 110–37. Washington, DC: Island Press. Stevens, C. E., C. A. Paszkowski, and A. L. Foote. 2007. Beaver (Castor canadensis) as a surrogate species for conserving anuran amphibians on boreal streams in Alberta, Canada. Biological Conservation 134:1–13. Stevens, G. C. 1992. The elevational gradient in altitudinal range: an extension of Rapoport’s latitudinal rule to altitude. American Naturalist 140:893–911. Stevens, T., and R. M. Connolly. 2004. Testing the utility of abiotic surrogates for marine habitat mapping at scales relevant to management. Biological Conservation 119:351–62. Stoddard, J. L., D. P. Larsen, C. P. Hawkins, R. K. Johnson, and R. H. Norris. 2006. Setting expectations for the ecological condition of streams: the concept of reference condition. Ecological Applications 16:1267–76. Stoner, C., T. Caro, S. Mduma, C. Mlingwa, G. Sabuni, and M. Borner. 2007. Assessment of effectiveness of protection strategies in Tanzania based on a decade of survey data for large herbivores. Conservation Biology 21:635–46. Stoner, C., T. Caro, S. Mduma, C. Mlingwa, G. Sabuni, M. Borner, and C. Schel-

References 343 ten. 2006. Changes in large herbivore populations across large areas of Tanzania. African Journal of Ecology 45:202–15. Stouffer, P. C., and R. O. Bierregaard Jr. 1995a. Use of Amazonian forest fragments by understorey insectivorous birds. Ecology 76:2429–45. Stouffer, P. C., and R. O. Bierregaard Jr. 1995b. Effects of forest fragmentation on understorey hummingbirds in Amazonian Brazil. Conservation Biology 9:1085– 94. Stouffer, P. C., R. O. Bierregaard Jr., C. Strong, and T. E. Lovejoy. 2006. Long-term landscape change and bird abundance in Amazonian rainforest fragments. Conservation Biology 20:1212–23. Stouffer, P. C., C. Strong, and L. N. Naka. 2009. Twenty years of understorey bird extinctions from Amazonian rain forest fragments: consistent trends and landscape-mediated dynamics. Diversity and Distributions 15:88–97. Stratford, J. A., and P. C. Stouffer. 1999. Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conservation Biology 13:1416–23. Stribling, J. M., J. C. Cornwell, and O. A. Glahn. 2007. Microtopography in tidal marshes: ecosystem engineering by vegetation? Estuaries and Coasts 30:1007– 15. Strong, D. R. 1992. Are trophic casdcades all wet? The redundant differentiation in trophic architecture of high diversity ecosystems. Ecology 73:747–54. Su, J., D. M. Debinski, M. E. Jakubauskas, and K. Kindscher. 2004. Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conservation Biology 18:167–73. Summerville, K. S., L. M. Ritter, and T. O. Crist. 2004. Forest moth taxa as indicators of lepidopteran richness and habitat disturbance: a preliminary assessment. Biological Conservation 116:9–18. Suter, W., R. F. Graf., and R. Hess. 2002. Capercaille (Tetrao urogallus) and avian biodiversity: testing the umbrella-species concept. Conservation Biology 16:778– 88. Sutherland, W. J., A. S. Pullin, P. M. Dolman, and T. M. Knight. 2004. The need for evidence-based conservation. Trends in Ecology and Evolution 19:305–8. Svancara, L. K., R. Brannon, J. M. Scott, C. R. Groves, R. F. Noss, and R. L. Pressey. 2005. Policy-driven versus evidence-based conservation: a review of political targets and biological needs. BioScience 55:989–95. Swan, G. V. Naidoo, R. Cuthbert, R. E. Green, D. J. Pain, D. Swarup, V. Prakash, M. Taggart, L. Bekker, D. Das, J. Diekmann, M. Diekmann, E. Killian, A. Meharg, R. C. Patra, M. Saini, and K. Wolter. 2006. Removing the threat of diclofenac to critically endangered Asian vultures. PloS Biology 4:395–402. Swengel, S. R., and A. B. Swengel. 1999. Correlations in abundance of grassland songbirds and prairie butterflies. Biological Conservation 90:1–11. Talley, T. S., and J. A. Crooks. 2007. Habitat conversion associated with bioeroding

344 References marine isopods. In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 185–202. Amsterdam: Elsevier. Tanner, J. E., T. P. Hughes, and J. H. Connell. 1994. Species coexistence, keystone species, and succession: a sensitivity analysis. Ecology 75:2204–19. Taper, M. L., K. Bohning-Gaese, and J. H. Brown. 1995. Individualistic responses of bird species to environmental change. Oecologia 101:478–86. Tardif, B., and J.-L. DesGranges. 1998. Correspondence between bird and plant hotspots of the St. Lawrence River and influence of scale on their location. Biological Conservation 84:53–63. Tear, T. H., P. Kareiva, P. L. Angermeier, P. Comer, B., Czech, R. Kautz, L. Landon, D. Mehlman, K. Murphy, M. Ruckelshaus, J. M. Scott, and G. Wilhere. 2005. How much is enough? The recurrent problem of setting measurable objectives in conservation. BioScience 55:835–49. Terborgh, J. 1986. Keystone plant resources in the tropical forest. In Conservation Biology: the Science of Scarcity and Diversity, ed. M. E. Soule, 330–44. Sunderland, MA: Sinaeuer Associates. Terborgh, J., F. A. Estes, P. Paquet, K. Ralls, D. Boyd-Heger, B. J. Miller, and R. F. Noss. 1999. The role of top carnivores in regulating terrestrial ecosystems. In Continental Conservation: Scientific Foundations of Regional Reserve Networks, eds. M. E. Soule and J. Terborgh, 39–64. Washington, DC: Island Press. Terborgh, J., K. Feeley, M. Silman, P. Nunez, and B. Balukjian. 2006. Vegetation dynamics of predator-free land-bridge islands. Journal of Applied Ecology 94:253–63. Terborgh, J., L. Lopez, P. Nunez, M. Rao, G. Shahabuddin, G. Orijuela, M. Riveros, R. Ascanio, G. H. Adler, T. D. Lambert, and L. Balbas. 2001. Ecological meltdown in predator-free forest fragments. Science 294:1923–26. Terborgh, J., G. Nunez-Iturri, N. C. A. Pitma, F. H. Cornejo Valverde, P. Alvarez, V. Swamy, E. G. Pringle, and C. E. T. Paine. 2008. Tree recruitment in an empty forest. Ecology 89:1757–68. Terborgh, J., and B. Winter. 1983. A method for siting parks and reserves with special reference to Colombia and Ecuador. Biological Conservation 27:45–58. Tews, J., U. Brose, V. Grimm, K. Tielborger, M. C. Wichmann, M. Schwager, and F. Jeltsch. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31:79– 92. Thayer, C. W. 1979. Biological bulldozers and the evolution of marine benthic communities. Science 203:458–61. Thomas, G. H. 2008. Phylogenetic distributions of British birds of conservation concern. Proceedings of the Royal Society of London B 275:2077–83. Thomas, J. A. 2005. Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philosophical Transactions of the Royal Society B 360:339–57. Thomas, J. A., M. G. Telfer, D. B. Roy, C. D. Preston, J. J. D. Greenwood, J. Asher,

References 345 R. Fox, R. T. Clarke, and J. H. Lawton. 2004. Comparative losses of British butterflies, birds, and plants and the global extinction crisis. Science 303:1879– 81. Thomson, J. R., E. Fleishman, R. M. MacNally, and D. S. Dobkin. 2005. Influence of the temporal resolution of data on the success of indicator species models of species richness across multiple taxonomic groups. Biological Conservation 124:503–18. Thorne, J. H., D. Cameron, and J. F. Quinn. 2006. A conservation design for the central coast of California and the evaluation of mountain lion as an umbrella species. Natural Areas Journal 26:137–48. Tingley, M. W., D. A. Orwig, R. Field, and G. Motzkin. 2002. Avian response to removal of a forest dominant: consequences of hemlock woolly adelgid infestations. Journal of Biogeography 29:1505–16. Tisdell, C., H. S. Nantha, and C. Wilson. 2007. Endangerment and likeability of wildlife species: how important are they for payments proposed for conservation? Ecological Economics 60:627–33. Tognelli, M. F. 2005. Assessing the utility of indicator groups for the conservation of South American terrestrial mammals. Biological Conservation 121:409–17. Tognelli, M. F., P. I. Ramirez de Arellano, and P. A. Marquet. 2008. How well do the existing and proposed reserve networks represent vertebrate species in Chile? Diversity and Distributions 14:148–58. Tompkins, D. M., A. P. Dobson, P. Arneberg, M. E. Begon, I. M. Cattadori, J. V. Greenman, J. A. P. Heesterbeek, P. J. Hudson, D. Newborn, A. Pugliese, A. P. Rizzoli, R. Rosa, F. Rosso, and K. Wilson. 2001. Parasites and host population dynamics. In The Ecology of Wildlife Diseases, eds. P. A. Hudson, A. Rizzoli, B. T. Grenfell, H. Heesterbeck, and A. P. Dobson, 45–62. Oxford, UK: Oxford University Press. Torres, M. A., M. P. Barros, S. C. G. Campos, E. Pinto, S. Rajamani, R. T. Sayre, and P. Colepicolo. 2008. Ecotoxicology and Environmental Safety 71:1–15. Towns, D. R., G. R. Parrish, C. L. Tyrrell, G. T. Ussher, A. Cree, D. G. Newman, A. H. Whitaker, and I. Westbrooke. 2006. Responses of tuatara (Sphenodon punctatus) to removal of introduced Pacific rats from islands. Conservation Biology 21:1021–31. Trakhtenbrot, A., and R. Kadmon. 2005. Environmental cluster analysis as a tool for selecting complementary networks of conservation sites. Ecological Applications 15:335–45. Trenkel, V. M., and M.-J. Rochet. 2003. Performance of indicators derived from abundance estimates for detecting the impact of fishing on a fish community. Canadian Journal of Fisheries and Aquatic Sciences 60:67–85. Troumbis, A. Y., and P. G. Dimitrakopoulos. 1998. Geographic coincidence of diversity threatspots for three taxa and conservation planning in Greece. Biological Conservation 84:1–6. Tscharntke, T., A. Gathmann, and I. Steffan-Dewenter. 1998. Bioindication using

346 References trap-nesting bees and wasps and their natural enemies: community structure and interactions. Journal of Applied Ecology 35:708–19. Tscharntke, T., C. H. Sekercioglu, T. V. Dietsch, N. S. Sodhi, P. Hoehn, and J. M. Tylianakis. 2008. Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89:944–51. Tuomisto, H., K. Ruokolainen, R. Kalliola, A. Linna, W. Danjoy, and Z. Rodriguez. 1995. Dissecting Amazonian biodiversity. Science 269:63–66. Turner, W. R., and D. S. Wilcove. 2006. Adaptive decision rules for acquisition of nature reserve. Conservation Biology 20:527–37. Turpie, J. K., L. E. Beckley, and S. M. Katua. 2000. Biogeography and the selection of priority areas for conservation of South African coastal fishes. Biological Conservation 92:59–72. Tushabe, H., J. Kalema, A. Byaruhanga, J. Asasira, P. Ssegawa, A. Balmford, T. Davenport, J. Fjeldsa, I. Friis, D. Pain, D. Pomeroy, P. Williams, and C. Williams. 2006. A nationwide assessment of the biodiversity value of Uganda’s Important Bird Area network. Conservation Biology 20:85–99. Uehara-Prado, M., J. D. Fernandes, A. D. Bello, G. Machado, A. J. Santos, F. Z. Vaz-de-Mello, and A. V. L. Freitas. 2009. Selecting terrestrial arthropods as indicators of small-scale disturbance: a first approach in Brazilian Atlantic forest. Biological Conservation 142:1220–28. Ueno, D., M. Watanabe, A. Subramanian, H. Tanaka, G. Fillman, P. K. S. Lam, G. J. Zheng, M. Muchtar, H. Razak, M. Prudente, K.-H. Chung, and S. Tanabe. 2005. Global pollution monitoring of polychlorinated dibenzo-p-dioxins (PCDDs), furans (PCDFs) and coplanar polychlorinated biphenyls (coplanar PCBs) using skipjack tuna as bioindicator. Environmental Pollution 136:303– 13. UNEP/DEWA 2001. The Mesopotamian Marshlands: Demise of an Ecosystem. Early warning and Assessment. Technical Report No. TR.01-3. Nairobi, Kenya: UNEP. USDA Forest Service. 1984. Wildlife, fish, and sensitive plant habitat management. Title 2600. Amendment No. 48. Washington, DC: USDA Forest Service. USDA Forest Service. 2005. Cleveland National Forest Land Management Plan, September. USDA Forest Service, Pacific Southwest. USDA, Forest Service, U.S. Fish and Wildlife Service, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, National Park Service, Bureau of Land Management, and Environmental Protection Agency. 1993. Forest ecosystem management: an ecological, economic, and social assessment: report of the Forest Ecosystem Management Assessment Team. Portland, OR. U.S. Department of Interior. 1992. Final Draft Recovery Plan for the Northern Spotted Owl, vol. 2. Portland, OR: U.S. Fish and Wildlife Service.. Usher, M. B. 1986. Wildlife conservation evaluation: attributes, criteria and values. In Wildlife Conserrvation Evaluation, ed. M. B. Usher, 3–44. London: Chapman & Hall.

References 347 van der Schalie, W. H., H. S. Gardner, J. A. Bantle, C. T. De Rosa, R. A. Finch, J. S. Reif, R. H. Reuter, L. C. Bakker, J. Burger, L. C. Folmar, and W. S. Stokes. 1999. Animals as sentinels of human health hazards of environmental chemicals. Environmental Health Perspectives 107:309–15. van Houtan, K. S., S. L. Pimm, T. O. Bierregaard Jr., T. E. Lovejoy, and P. C. Stouffer. 2006. Local extinctions in flocking birds in Amazonian forest fragments. Evolutionary Ecology Research 8:129–48. van Jaarsveld, A. S., S. Freitag, S. L. Chown, C. Muller, S. Koch, H. Kull, C. Bellamy, M. Kruger, S. Endrody-Younga, M. W. Mansell, and C. H. Scholtz. 1998. Biodiversity assessments and conservation strategies. Science 279:2106– 8. van Langevelde, F., A. Schotman, F. Claasen, and G. Sparenburg. 2000. Competing land use in the reserve site selection problem. Landscape Ecology 15:243–56. van der Oost, R., J. Beyer, and N. P. E. Vermeulen. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13:57–149. van Strien, A. J., O. Knol, L. van Duuren, B. ten Cate, and R. Leewis. 2004. Natuurcompendium 2004. Natuur in ciifers, Milieu- en Natuurolanbureau en CBS 2004. http://www.natuurcompendium.nl. accessed 15 May 2009. Vanderlaan, A. S. M., and C. T. Taggart. 2009. Efficacy of a voluntary area to be avoided to reduce risk of lethal vessel strikes to endangered whales. Conservation Biology 23:1467–74. Vandermeulen, H. 1998. The development of marine indicators for coastal zone management. Ocean and Coastal Management 39:63–71. Vane-Wright, R. I., C. J. Humphries, and P. H. Williams. 1991. What to protect?— Systematics and the agony of choice. Biological Conservation 55:235–54. Vellend, M., P. L. Lilley, and B. M. Starzomski. 2008. Using subsets of species in biodiversity surveys. Journal of Applied Ecology 45:161–69. Verissimo, D., I. Fraser, J. Groombridge, R. Bristol, and D. C. MacMillan. 2009. Birds as tourism flagship species: a case study of tropical islands. Animal Conservation 12:549–88. Vessby, K., B. Soderstrom, A. Glimskar, and B. Svensson. 2002. Species-richness correlations of six different taxa in Swedish seminatural grasslands. Conservation Biology 16:430–39. Vickery, J. A., A. D. Evans, P. Grice, R. Brand-Hardy, and N. A. Aebischer. 2004. Ecology and conservation of lowland farmland birds II: the road to recovery. Ibis 146 (suppl 2):1–258. Villasenor, J. L., G. Ibarra-Manriquez, J. A. Meave, and E. Ortiz. 2005. Higher taxa as surrogates of plant biodiversity in a megadiverse country. Conservation Biology 19:232–38. Virolainen, K. M., P. Ahlroth, E. Hyvarinen, E. Korkeamaki, J. Mattila, J. Paivinen, T. Rintala, T. Suomi, and J. Suhonen. 2000. Hot spots, indicatopr taxa, complementarity and optimal networks of taiga. Proceedings of the Royal Society of London B 267:1143–47.

348 References Virolainen, K. M., K. Nattinen, J. Suhonen, and M. Kuitunen. 2001. Selecting herb-rich forest networks to protect different measures of biodiversity. Ecological Applications 11:411–20. Vitousek, P. M. 1990. Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13. Vogel, W. O. 1989. Response of deer to density and distribution of housing in Montana. Wildlife Society Bulletin 17:406–13. Wallis de Vries, M. F. 1995. Large herbivores and the design of large-scale nature reserves in western Europe. Conservation Biology 9:25–33. Walpole, M. J., and N. Leader-Williams. 2002. Tourism and flagship species in conservation. Biodiversity and Conservation 11:543–47. Walters, C. J. 2003. Folly and fantasy in the analysis of spatial catch-rate data. Canadian Journal of Fisheries and Aquatic Sciences 60:1433–36. Walters, D. M., D. S. Leigh, and A. B. Bearden. 2003. Urbanization, sedimentation, and the homogenization of fish assemblages in the Etowah River Basin. Hydrobiologia 494:5–10. Ward, P. I., N. Mosberger, C. Kistler, and O. Fischer. 1998. The relationship between popularity and body size in zoo animals. Conservation Biology 12:1408– 11. Ward, T. J., and C. A. Jacoby. 1992. A strategy for assessment and management of marine ecosystems: baseline and monitoring studies in Jervis Bay, a temperate Australian embayment. Marine Pollution Bulletin 25:163–71. Ward, T. J., M. A. Vanderklift, A. O. Nicholls, and R. A. Kenchington. 1999. Selecting marine reserves using habitats and species assemblages as surrogates for biological diversity. Ecological Applications 9:691–98. Warman, L. D., D. M. Forsyth, A. R. E. Sinclair, K. Freemark, H. D. Moore, T. W. Barrett, R. L. Pressey, and D. White. 2004. Species distributions, surrogacy, and important conservation regions in Canada. Ecology Letters 7:374–79. Warwick, R. M., and K. R. Clarke. 1994. Relearning the ABC: taxonomic changes and abundance/biomass relationships in distributed benthic communities. Marine Biology 118:739–44. Warwick, R. M., T. H. Pearson, and Ruswahyuni. 1987. Detection of pollution effects on marine macrobenthos: further evaluation of the species abundance/ biomass method. Marine Biology 95:193–200. Watson, J., D. Freudenberger, and D. Paull. 2001. An assessment of the focalspecies approach for conserving birds in variegated landscapes in southeastern Australia. Conservation Biology 15:1364–73. Weaver, J. C. 1995. Indicator species and scale of observation. Conservation Biology 9:939–42. Weibull, A.-C., J. Bengtsson, and E. Nohlgren. 2000. Diversity of butterflies in the agricultural landscape: the role of farming system and landscape heterogeneity. Ecography 23:743–50. Weibull, A.-C., O. Ostman, and A. Granqvist. 2003. Species richness in agroecosys-

References 349 tems: the effect of landscape, habitat, and farm management. Biodiversity and Conservation 12:1335–55. Weilgart, L. S. 2007. The impacts of anthropogenic ocean noise on cetaceans and implications for management. Canadian Journal of Zoology 85:1091–116. Welcomme, R. L., K. O. Winemiller, and I. G. Cowx. 2006. Fish environmental guilds as a tool for assessment of ecological condition of rivers. River Research and Applications 22:377–96. Wenger, S. J. 2008. Use of surrogates to predict the stressor response of imperiled species. Conservation Biology 22:1564–71. Weseloh, D. V., K. D. Holmes, P. J. Ewins, D. Best, T. Kubiak, and M. C. Sheildcastle. 2002. Herring gulls and great black-backed gulls as indicators of contaminants in bald eagles in Lake Ontario, Canada. Environmental Toxicology and Chemistry 21:1015–25. Wessels, K. J., S. Freitag, and A. S. van Jaarsveld. 1999. The use of land facets as biodiversity surrogates during reserve selection at a local scale. Biological Conservation 89:21–38. Wessels, D. C. J., and L.-A. Wessels. 1991. Erosion of biogenically weathered Clarens sandstone by lichenophagius barworm larvae (Lepidotera; Psychidae). Lichenology 23:283–91. Western, D. 1989. Africa’s elephants and rhinos: flagships in crisis. Trends in Ecology and Evolution 2:343–46. Whelan, R.J. 2002. Managing fire regimes for conservation and property protection: an Australian response. Conservation Biology 16:1659–1661. Wheeler, N., and R. Sederoff. 2009. The role of genomics in the potential restoration of the American chestnut. Tree Genetics and Genomics 5:181–87. White, P. C. L., A. C. Bennett, and E. J. V. Hayes. 2001. The use of willingness-topay approaches in mammal conservation. Mammal Review 31:151–67. Whittaker, R.H. 1960. Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 30:279–338. Wiens, J. A., T. O. Crist, R. H. Day, S. M. Murphy, and G. D. Hayward. 1996. Effects of the Exxon Valdez oil spill on marine bird communities in Prince William Sound, Alaska. Ecological Applications 6:828–41. Wiens, J. A., G. D. Howard, R. S. Holthausen, and M. J. Wisdom. 2008. Using surrogate species and groups for conservation planning and management. BioScience 58:241–52. Wilcove, D. 1993. Getting ahead of the extinction curve. Ecological Applications 3:218–20. Wilcove, D. S. 1994. Turning conservation goals into tangible results: the case of the spotted owl and old-growth forests. In Large-scale Ecology and Conservation Biology, eds. P. J. Edwards, R. M. May, and N. R. Web, 313–29. Oxford, UK: Blackwell Scientific. Wilcox, B. A. 1984. In situ conservation of genetic resources: determinants of minimum area requirements. In National Parks, Conservation, and Development:

350 References Proceedings of the World Congress on National Parks, eds. J. A. McNeely, and K. R. Miller, 18–30. Washington, DC: Smithsonian Institution Press. Wilkinson, C. 2002. Status of Coral Reefs of the World. Townsville, Queensland: Australian Institute of Marine Science. Williams, H. H., and K. Mackenzie. 2003. Marine parasites as pollution indicators: an update. Parasitology 126:S27–41. Williams, P., D. Gibbons, C. Margules, A. Rebelo, C. Humphries, and R. Pressey. 1996. A comparison of richness hotspots, rarity hotspots, and complementary areas for conserving diversity of British birds. Conservation Biology 10:155– 74. Williams, P. H. 1999. WORLDMAP 4 Windows: Software and Help Document 4.19. London. http://www.nhm.ac.uk/science/projects/worldmap/. 15 May 2009. Williams, P. H., N. D. Burgess, and C. Rahbek. 2000a. Flagship species, ecological complementarity and conserving the diversity of mammals and birds in sub-Saharan Africa. Animal Conservation 3:249–60. Williams, P. H., N. Burgess, and C. Rahbek. 2000b. Assessing large “flagship” for representing the diversity of sub-Saharan mammals. In Has the Panda Had Its Day? Future Priorities for the Conservation of Mammal Diversity, eds. A. Entwistle and N. Dunstone, 85–99. Cambridge, UK: Cambridge University Press. Williams, P., D. Faith, L. Manne, W. Sechrest, and C. Preston. 2006. Complementarity analysis: mapping the performance of surrogates for biodiversity. Biological Conservation 128:253–64. Williams, P. H., and K. J. Gaston. 1994. Measuring more of biodiversity: can higher-taxon richness predict wholesale species richness? Biological Conservation 67:211–17. Williams, P. H., C. J. Humprhies, and K. J. Gaston. 1994. Centres of seed-plant diversity: the family way. Proceedings of the Royal Society of London B 256:67–70. Williams, T. M., J. A. Estes, D. F. Doak, and A. M. Springer. 2004. Killer appetities: assessing the role of predators in ecological communities. Ecology 85:3373–84. Wilmers, C. C., R. L. Crabtree, D. W. Smith, K. M. Murphy, and W. M. Getz. 2003. Trophic facilitation by introduced top predators: grey wolf subsidies to scavengers in Yellowstone National Park. Journal of Animal Ecology 72:909–16. Wilmers, C. C., and W. M. Getz. 2005. Gray wolves as climate change buffers in Yellowstone. PLoS Biology 3:571–76. Wilson, E. O. 1987. The little things that run the world (the importance and conservation of invertebrates). Conservation Biology 1:344–46. Wilson, E. O. 1992. The Diversity of Life. Cambridge, MA: Harvard University Press. Wilson, K., R. L. Pressey, A. Newton, M. Burgman, H. Possingham, and C. Weston. 2005. Measuring and incorporating vulnerability into conservation planning. Environmental Management 35:527–43. Wilson, K. A., M. F. McBride, M. Bode, and H. P. Possingham. 2006. Prioritizing global conservation efforts. Nature 440:337–40.

References 351 Wilson, K. A., E. C. Underwood, S. A. Morrison, K. R. Klausmeyer, W. W. Murdoch, B. Reyers, G. Wardell-Johnson, P. A. Marquet, P. W. Rundel, M. F. McBride, R. L. Pressey, M. Bode, J. M. Hoekstra, S. Andelman, M. Looker, C. Rondinini, P. Karieva, M. R. Shaw, and H. P. Possingham. 2007. Conserving biodiversity efficiently: what to do, where, and when. PLoS Biology 5:1850–61. Wilson, K. A., M. I. Westphal, H. P. Possingham, and J. Elith. 2004. Sensitivity of conservation planning to different approaches to using predicted species distribution data. Biological Conservation 122:99–112. Wilson, S. K., N. A. J. Graham, M. S. Pratchett, G. P. Jones, and N. V. C. Polunin. 2006. Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biology 12:2220–34. Wilson, W. G. 2007. A new spirit and concept for ecosystem engineering? In Ecosystem Engineers: Plants to Protists, eds. K. Cuddington, J. E. Byers, W. G. Wilson, and A. Hastings, 47–68. Amsterdam: Elsevier. Witman, J. D., and P. K. Dayton. 2001. Rocky subtidal communities. In Marine Community Ecology, eds. M. D. Bertness, S. D. Gaines, and M. E. Hay, 339–66. Sunderland, MA: Sinauer Associates. Wolda, H. 1987. Altitude, habitat and tropical insect diversity. Biological Journal of the Linnean Society 30:313–23. Wolters, V., J. Bengtsson, and A. S. Zaitsev. 2006. Relationship among the species richness of different taxa. Ecology 87:1886–95. Woodroffe, R., and J. R. Ginsberg. 1998. Edge effects and the extinction of populations inside protected areas. Science 280:2126–28. Woodroffe, R., S. Thirgood, and A. Rabinowitz. 2005. People and Wildlife: Conflict or Coexistence? Cambridge, UK: Cambridge University Press. World Wildlife Fund and World Conservation Union. 1994. Europe, Africa, South West Asia and the Middle East. Vol. 1 of Centres of Plant Diversity: A Guide and Strategy for Their Conservation. Cambridge, UK: World Conservation Union Publications. World Wildlife Fund and World Conservation Union. 1995. Asia, Australasia and the Pacific. Vol. 2 of Centres of Plant Diversity: A Guide and Strategy for Their Conservation. Cambridge, UK: World Conservation Union Publications. World Wildlife Fund and World Conservation Union. 1997. The Americas. Vol. 3 of Centres of plant diversity: A Guide and Strategy for Their Conservation. Cambridge, UK: World Conservation Union Publications. Worm, B., H. K. Loetze, and R. A. Myers. 2003. Predator diversity hotspots in the blue ocean. Proceedings of the National Academy of Sciences 100:9884–88. Wright, D. H., B. D. Patterson, G. M. Mikkelson, A. Cutler, and W. Atmar. 1998. A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20. Wright, J. P., A. S. Flecker, and C. G. Jones. 2003. Local vs landscape controls on plant species richness in beaver meadows. Ecology 84:3162–73. Wright, J. P., and C. G. Jones. 2006. The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56:203–9.

352 References Wright, J. P., C. G. Jones, and A. S. Flecker. 2002. An ecosystem engineer, the beaver, increases species richness at the landscape scale. Oecologia 132:96–101. Wright, S. J., and H. C. Duber. 2001. Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm Attalea butyraceae, with implications for tropical tree diversity. Biotropica 33:583–95. Wright, S. J., M. E. Gompper, and B. DeLeon. 1994. Are large predators keystone species in neotropical forests? The evidence from Barro Colorado Island. Oikos 71:279–94. Wright, S. J., A. Hernandez, and R. Condit. 2007. The bushmeat harvest alters seedling banks by favoring lianas, large seeds, and seeds dispersed by bats, birds, and wind. Biotropica 39:363–71. Wright, S. J., and H. C. Muller-Landau. 2006. The future of tropical forest species. Biotropica 38:207–301. Wright, S. J., H. Zeballos, I. Dominguez, M. M. Gallardo, M. C. Moreno, and R. Ibanez. 2000. Poachers alter mammal abundance, seed dispersal, and seed predation in a neotropical forest. Conservation Biology 14:227–39. Xu, H., J. Wu, Y. Liu, H. Ding, M. Zhang, Y. Wu, Q. Xi, and L. Wang. 2008. Biodiversity congruence and conservation strategies: a national test. BioScience 58:632–39. Yamaura, Y., T. Amano, T. Koizumi, Y. Mitsuda, H. Taki, and K. Okabe. 2009. Does land-use change affect biodiversity dynamics at a macroecological scale? A case study of birds over the past 20 years in Japan. Animal Conservation 12:110–19. Zacharias, M. A., and J. C. Roff. 2001. Use of focal species in marine conservation and management: a review and critique. Aquatic Conservation: Marine and Freshwater Ecosystems 11:59–76.

In one of the first studies of umbrella species, the number of large sympatric mammals and birds was surveyed in an area used by a small population of black rhinoceros living in Namibia. (Drawing by Sheila Girling.)

scientific names of species mentioned in the text

Plants Port Orford cedar Redwood Bald cypress Balsam fir White fir Fraser fir Whitebark pine Coulter pine Scotch pine Bigcone Douglas fir Douglas fir Eastern hemlock Oil palm Cheatgrass Cordgrass Black needle rush Water hyacinth Corn Ceiba or kapok tree Cottonwood Aspen American chestnut Blue oak Engelmann oak California black oak Valley oak Yellow poplar Blackwood

Chamaecyparis lawsoniana Sequoia sempervirens Taxodium distichum Abies balsamea Abies concolor Abies fraseri Pinus albicaulis Pinus coulteri Pinus sylvestris Pseudotsuga macrocarpa Pseudotsuga menziesii Tsuga canadensis Elaeis guineensis Bromus tectorum Spartina anglica Juncus gerardi Eichhornia crassipes Zea mays Ceiba pentandra Populus angustifolia, P. trichocarpa Populus tremula, P. tremuloides Castanea dentate Quercus douglasii Quercus engelmannii Quercus kelloggii Quercus lobata Liriodendron tulipifera Acacia melanoxylon 355

356 Scientific Names of Species Mentioned in the Text

Acacia Coca Jarrah

Acacia pennatula Erythroxylum coca Eucalyptus marginata

Invertebrates Deep-sea corals

Paragorgia arborea, Primnoa resedaeformis, Lophelia pertusa Littorina littorea Mytilus californianus Mytilus edulis Crassostrea virginica Mya arenaria Placopecten magellanicus Paraponera clavata Adelges tsugae Danaus plexippus Mitella polymerus Balanus cariosus Meganyctiphanes norvegica Jasus lalandii Avicularia avicularia Calacarus flagelliseta Pistaster ochraceus

European periwinkle California blue mussel Mussel Oyster Soft shell clam Sea scallop Bullet ant Woolly adelgid Monarch butterfly Goose-necked barnacle Acorn barnacle Krill Rock lobster Tarantula Eriophyis mite Starfish

Fish Porbeagle shark Silky shark Dusky shark Whitetip shark Spiny dogfish shark Barndoor shark Freshwater stingray Arapaima Atlantic herring American shad

Lamna nasus Carcharhinus falciformis Carcharhinus obscurus Carcharhinus longimanus Squalus acanthias Raja laevis Potamotrygon humerosa Arapaima gigas Clupea harengus Alosa sapidissima

Scientific Names of Species Mentioned in the Text 357

Goldfish European carp Striped shiner Squawfish Amber darter Bronze darter Arctic grayling/Cutthroat trout Brown trout Atlantic salmon Pacific salmon/steelhead Cusk Atlantic cod Haddock Pollock Eastern gambusia Swordtail Platy Northern wolffish Atlantic wolffish Spotted wolffish Northern sand lance Skipjack tuna Atlantic halibut Winter flounder

Carassius auratus Cyprinus carpio Luxilus chrysocephalus Ptychocheilus lucius Percina antesella Percina palmaris Thymallus arcticus Salmo trutta Salmo salar Onchorhynchus mykiss Brosme brosme Gadus morhua Melanogrammus aeglefinus Pollachius virens Gambusia holbrooki Xiphophorus helleri Xiphophorus maculates Anarhichas denticulatus Anarhichas lupus Anarhichas minor Ammodytes dubius Kastuwonus pelamis Hippoglossus hippoglossus Pseudopleuronectes americanus

Amphibians Western toad Arroyo toad African clawed toad Boreal chorus frog Leopard frog Wood frog

Bufo boreas Bufo californicus Xenopus laveis Pseudacris maculata Rana pipiens Rana sylvatica

Reptiles Blanding’s turtle Eastern box turtle

Emydoidea blandingi Terrapene carolina


Giant river turtle Loggerhead turtle Leatherback turtle Tuatara Common iguana Anaconda American alligator Black caiman Salt-water or estuarine crocodile

Podocnemis expansa Caretta caretta Dermochelys coriacea Sphenodon punctatus Iguana iguana Eunectes murinus Alligator mississippiensis Melanosuchus niger Crocodylus porosus

Mammals Duck-billed platypus Virginia opossum Tasmanian devil Large hairy armadillo Nine-banded armadillo Giant anteater Pemba flying fox Gland-tailed free-tailed bat Golden-headed lion tamarin Golden-rumped or black lion tamarin Golden lion tamarin Howler monkey, red howler monkey Central American spider monkey Black spider monkey Capuchin monkey Angolan black and white colobus Gorilla Bonobo Chimpanzee Coyote Wolf Domestic dog Gray fox Red fox Domestic cat Eurasian or European lynx Bobcat

Ornithorhynchus anatinus Didelphis virginianus Sarcophilus harrisii Chaetophractus villosus Dasypus novemcinctus Myrmecophaga tridactyla Pteropus voeltzkowi Chaerephon bemmeleni Leontopithecus chrysomelas Leontopithecus chrysopygus Leontopithecus rosalia Alouatta seniculus Ateles geoffroyi Ateles paniscus Cebus olivaceus Colobus angolensis Gorilla gorilla Pan paniscus Pan troglodytes Canis latrans Canis lupus Canis familiaris Urocyon cineroargenteus Vulpes vulpes Felis catus Lynx lynx Lynx rufus


Mountain lion, Cougar, Florida panther Lion Jaguar Leopard Tiger Sea otter European otter Giant river otter Striped skunk Spotted skunk Wolverine Long-tailed weasel American badger Walrus Northern fur seal Steller’s sea lion Bearded seal Harp seal Ringed seal Hooded seal Harbor seal Monk seal Raccoon Giant panda Spectacled bear European brown bear, brown bear, grizzly bear Polar bear Bowhead whale North Atlantic right whale Blue whale Fin whale Humpback whale Gray whale Killer whale Beluga Narwhal Harbor porpoise Northern bottlenose whale West Indian manatee

Felis concolor Panthera leo Panthera onca Panthera pardus Panthera tigris Edhydra lutris Lutra lutra Pteronura brasiliensis Mephitis mephitis Splilogale gracilis Gulo gulo Mustela frenata Taxidea taxus Odobenus rosmarus Callorhinus ursinus Eumetopias jubatus Erignathus barbatus Pagophilus groenlandicus Phoca hispida Cystophora cristata Phoca vitulina Monachus sp. Procyon lotor Ailuropoda melanoleuca Tremarctos ornatus Ursus arctos Ursus maritimus Baleana mysticetus Eubalaena glacialis Balaenoptera musculus Balaenoptera physalus Megaptera novaeangliae Eschrichtius robustus Orcinus orca Delphinapterus leucas Monodon monoceros Phocoena phocoena Hyperoodon ampullatus Trichechus manatus


Asian elephant African elephant Mountain zebra South American Tapir Baird’s tapir Mountain tapir White rhinoceros Black rhinoceros Javan rhinoceros White-lipped peccary Vicuña Giraffe Elk Moose Mule deer White-tailed deer Reindeer, caribou Pronghorn Greater kudu African buffalo Bighorn sheep Domestic sheep Gemsbok Arabian oryx Gunnison’s prairie dog Black-tailed prairie dog Gray squirrel Fox squirrel Eastern chipmunk Red squirrel Northern flying squirrel Southern flying squirrel Siberian flying squirrel American beaver Botta’s pocket gopher Banner-tailed kangaroo rat Red-backed vole Somali pygmy gerbil Tinfield’s rock rat Pacific or Polynesian rat

Elephas maximus Loxodonta africana Equus zebra Tapirus terrestris Tapirus bairdii Tapirus pinchaque Ceratotherium simum Diceros bicornis Rhinoceros sondaicus Tayassu pecari Vicugna vicugna Giraffa camelopardalis Cervus elaphus Alces alces Odocoileus hemionus Odocoileus virginianus Rangifer tarandus Antilocapra americana Tragelaphus strepsiceros Syncerus caffer Ovis canadensis Ovis domesticus Oryx gazella Oryx leucoryx Cynomys gunnisoni Cynomys ludovicianus Sciurus carolinensis Sciurus niger Tamias striatus Tamiasciurus hudsonicus Glaucomys sabrinus Glaucomys volans Pteromys volans Castor canadensis Thomomys bottae Dipodomys spectabilis Clethrionomys gapperi Microdillus peeli Aethomys stannarius Rattus exulans


Bushy-tailed woodrat Dusky-footed woodrat Deer mouse Indian crested or desert porcupine Plains viscacha Agouti European rabbit

Neotoma cinerea Neotoma fuscipes Peromyscus maniculatus Hystrix indica Lagostomus maximus Dasyprocta leporine Oryctolagus cuniculus

Birds Ostrich Black-footed albatross Laysan albatross Cook’s petrel Balearic shearwater Red-tailed tropicbird Red-footed booby Double-crested cormorant Brown pelican Snow goose Greater flamingo Lesser flamingo Andean condor Red kite Black kite Bald eagle Marabou stork Egyptian vulture White-rumped vulture Long-billed vulture Slender-billed vulture Red-headed vulture Northern harrier Northern goshawk Eurasian sparrowhawk Broad-winged hawk Common buzzard Harpy eagle Lesser kestrel

Struthio camelus Diomedea nigripes Diomedea immutabilis Pterodroma cookii Puffinus mauretanicus Phaethon rubricauda Sula sula Phalacrocorax auritus Pelecanus occidentalis Anser caerulescens Phoenicopterus ruber Phoenicopterus minor Vultur gryphus Milvus milvus Milvus migrans Haliaeetus leucophalus Leptoptilus crumeniferus Neophron percnopterus Gyps bengalensis Gyps indicus Gyps tenuirostris Sarcogyps calvus Circus cyaneus Accipter gentilis Accipter nisus Buteo platypterus Buteo buteo Harpia harpyja Falco naumanni


Eurasian kestrel Peregrine falcon Baillon’s crake Whooping crane Grey crowned crane Common snipe Red-necked phalarope Herring gull Caspian tern Common-white tern Roseate tern Black noddy Razorbill Atlantic puffin Tufted puffin Least auklet Dodo Kaka Crimson rosella Barn owl European scops owl Eurasian eagle owl Tawny owl Spotted owl Barred owl Eurasian pigmy owl Burrowing owl Tengmalm’s or boreal owl Long-eared owl Red-cockaded woodpecker Three-toed woodpecker Pileated woodpecker Ivory-billed woodpecker Yellow-bellied flycatcher Red wattlebird Hooded robin Eastern yellow robin Florida scrub jay Black-billed magpie American crow

Falco tinnunculus Falco peregrinus Porzana pusilla Grus americana Balearica regulorum Gallinago gallinago Phalaropus lobatus Larus argentatus Sterna caspia Gygis alba Sterna dougallii Anous minutus Alca torda Fratercula arctica Fratercula cirrhata Aethia pusilla Raphus cucullatus Nestor meridionalis Platycercus elegans Tyto alba Otus scops Bubo bubo Strix aluco Strix occidentalis Strix varia Glaucidium passerium Athene cunicularia Aegolius funereus Asio otus Picoides borealis Picoides tridactylus Dryocopus pileatus Camperphilus principalis Empidonax flaviventris Anthochaera carunculata Melanodryas cucullata Eopsaltria australis Aphelocoma coerulescens Pica hudsonia Corvus brachyrhyncos


Raven African black-headed oriole Least Bell’s vireo European blackbird American robin European starling Red-breasted flycatcher Marsh tit Willow tit Coal tit Crested tit Great tit Blue tit House sparrow Lemon-breasted seedeater Black and white warbler Ovenbird Corn bunting Brewer’s sparrow Spotted towhee

Corvus corax Oriolus larvatus Vireo bellii Turdus merula Turdus migratorius Sturnus vulgaris Fidecula parva Parus palustris Parus montanus Parus ater Parus cristatus Parus major Parus caerulus Passer domesticus Serinus citrinipectus Mniotilta varia Seiurus aurocapillus Miliaria calandra Spizella breweri Pipilo maculates

The American beaver modifies its environment by cutting trees and damming watercourses. This ecosystem engineer formerly lived at much higher population densities than today and must have had a great impact on the terrestrial landscape of North America. (Drawing by Sheila Girling.)

index

Accumulators, 167 Africa, see also South Africa. complimentarity and, 46–47 keystone species and, 130 rarity and, 52 scale and, 11 species richness and, 33, 52 threatened species and, 52 umbrella species and, 106–107 African wild dog, 124 Albertine rift, 56 Algae, biodiversity and, 90 environmental indicator species as, 170, 171 Alpha diversity. 3, 13. See also Species richness. Amphibians, biodiversity and, 20, 21, 32, 33, 34, 35, 39, 40, 31–42, 43, 47, 49, 50, 52, 63, 65, 72, 74, 76, 81 cross-taxon-response indicator species as, 225–226 decline in, 235–236 ecological-disturbance indicator species as, 199, 201, 206–208 environmental indicator species as, 158, 173, 177–178 flagship species and, 254 umbrella species and, 113 Andes, 247, 272 Angiosperms, 38 Antlions, 78, 81, 86 Ants, see also Hymenoptera. biodiversity and, 68, 71, 74 ecological-disturbance indicator species as, 200–201

Angola, 120 Aquatic plants, biodiversity and, 62–64, 76 environmental indicator species as, 178 Argentina, 74 Arroyo toad, 232–233 Atlantic forest, 39, 56 Atrizine, 173 Australia, 238 endemic species and, 72, 82 environmental surrogates and, 92– 93 focal species and, 17–19, 102 iconic species and, 258 keystone species and, 130 rarity and, 52, 76–77 taxon subsets and, 68 Austria, 63, 76, 81 Background species, 109 definition 16, 27 Baselines, 166–167, 172 Bats, biodiversity and, 57, 81 cross-taxon-response indicator species as, 225–226 ecological-disturbance indicator species as, 196, 200 flagship species and, 254 Bear, brown, 246 grizzly, 21, 95, 107–108, 253 polar, 183, 258, 259 Beaver, American, 94 ecosystem engineer as, 144, 146– 148 365

366 Index Beccariophoenix madagascarensis, 258 Bees, 206–208, 226. See also Hymenoptera. Beetles 30, 68, 101, 286. See also Dung beetles. biodiversity and, 33, 34, 35, 69, 71, 74, 78, 81, 84, 86 cross-taxon-response indicator species as, 227 ecological-disturbance indicator species as, 199, 201–203 umbrella species and, 104, 106 Behavior, 238–239 Belgium, 63, 102 Belize, 250, 253–254 Berger-Parker index, 164 Beta diversity. 3, 13, 83. See also Species richness. cross-taxon congruency in, 34 Bioaccumulators 162, 184 Biodiversity, 3–8. See also Species indicators of biodiversity. definition, 3 distribution of, 271–274 Bioindicator species, 161. See also Environmental indicators. Biological diversity. See Biodiversity. Biological Dynamics of Forest Fragmentation, 197–203 Biological indicators. See Environmental indicators. Biological integrity, 160–161 Biomarkers, 173 Birdlife International, 31, 52 Birds, biodiversity and, 21, 32, 33, 54, 35, 38, 39, 40, 41–42, 43–44, 47, 49, 50, 52, 53, 56, 62–64, 65, 66, 72, 73, 74, 76, 80, 81, 86 cross-taxon-response indicator species as, 225, 229–231, 240 decline in, 235–236 ecological-disturbance indicator species as, 199–201, 204–205, 206– 207, 209–210, 214 endangered species act and, 260 environmental indicator species as, 170, 173, 177–178, 182–183

flagship species and, 253, 254 intraguild-response indicator species as, 228–229 latent risk of extinction and, 238 umbrella species and, 101, 105, 110– 113 Bobcat, 94 Bobwhite, northern, 94 Bolivia, 74, 122 Borneo, 63 Bray-Curtis similarity index, 171 Brazil, 197–203, 206–208, 249, 280– 282 Britain, 69, 83–84, 85 congruency in, 62–64, 69–70, 76–77 Bryophytes, biodiversity and, 63, 74 Burma, 39 Butterfly Alcon blue, 102–104 Bay checkerspot, 105–106 biodiversity and, 33, 34, 35, 51, 62– 64, 66, 70, 71, 73, 76, 78, 80, 81, 86 cross-taxon-response indicator species as, 223–224 ecological-disturbance indicator species as, 199, 200, 206–207, 214 flagship species and, 253, 255 Monarch, 60 umbrella species and, 105–106 Buzzard, common, 111–113 Buzzwords. See Conservation buzzwords Cameroon 52, 56, 219–222 Canada. See also North America. cross-taxon-response indicator species and, 240, 241 engineering species and, 148 flagship species and, 246 focal species and, 19–21 keystone species and, 130 multi-surrogacy and, 268–270 rarity and, 78 species richness and, 33, 63, 78 threatened species and, 73 Cape floristic region, 56

Index 367 Capercaillie, 101, 110–111 Caribbean, 39, 56 Caribou, 120 Carnivores, flagship species and, 246, 250, 254– 255, 256–257 latent risk of extinction and, 237 mesopredators, 132–134 multi-surrogacy and, 268–270 reintroductions, 136–138, 224–225 response to fragmentation, 224–225 umbrella species and, 107–108 Charismatic species. See Flagship species. Cheetah, 107, 247 Chile, 78, 79, 88 China, 56, 250 endemic species and, 72, 74–75, 78 species richness and, 63, 65, 74–75 threatened species and, 75–78 Classic umbrella species, 99, 264–265 criteria for, 116–117 cross-taxon-response indicator species and, 218 mammals and, 106–107 Climate change, coral reefs and, 181 fish assemblages and, 181 marine ecosystems and, 181–184, 236–237 Coca, 250 Coffee, 204–205, 225–226 Colobus, black and white, 246 Coldspots, 63 Columbia, 39 Community similarity, 65–66 Comoros, 56 Complementarity, 45–49, 53, 79–86 definition, 45, 79 flexibility and, 79 irreplaceability and, 79 scale and, 11 Compliance indicators, 162–163 Concordance. See Congruency. Congo, 122 Congruency, surrogacy curve and, 47–49 Congruency at a large scale

endemic species, 39–42 rarity, 42 species richness, 32–35 threatened species, 43–45 Congruency at a small scale, endemic species, 72, 74–76, 78–79 rarity, 73, 76–78 species richness, 74–79 threatened species, 73, 78–79 Conservation buzzwords, xv, 2–3, 184–185 Conservation International, 31, 272 Conservation proxy. See Conservation shortcuts. Conservation shortcuts, xv, 1–3, 15–16 Corals, 268–269 biodiversity and, 90 environmental indicator species as, 181–183 Core species, 153 Corn, 251 Cost evaluation, anthropogenic change, measurement of, 280–282 biodiversity inventories, 273–274 reserve selection, 274–277 species monitoring of, 279 Costa Rica, 204–205 Cougar, 253, 270 Countryside biogeography, 203–205, 208 Coyote, 132–134 Crane, crowned, 247 Cross-taxon-response indicator species, 266, 268 confusion over terminology, 24–25, 217–218 definition, 24–25, 190 problems with, 239–242 Crustaceans, 43 Darter, 239 Defenders of Wildlife, 247 Delphi approach, 19–24, 94 Democratic Republic of Congo, 52 Denmark, 81 Diagnostic indicators, 162–163 Diatoms, 69

368 Index Dodo, 259 Dominant species. See Foundation species. Dragonflies, biodiversity and, 62–64, 76 umbrella species and, 101 Duck-billed platypus, 258 Dung beetles, 196–197, 206–208, 214, 225–226 Early warning indicators. See Sentinel species. Early warnings. See Sentinel species. Eastern Arc mountains, 39, 56, 272 Ecological baselines. See Baselines Ecological engineering species. See Ecosystem engineers. Ecological indicator species. See Crosstaxon-response indicator species. Ecological integrity, 160 Ecological meltdown, 134–136 Ecological-disturbance indicator species, 266, 268 confusion over terminology, 26, 161, 190 criteria for, 190–195 definition, 24–25, 189 management umbrella species and, 100 research effort and, 16 single species, 194–196 species-groups, 196–197 Ecosystem engineers, 130, 143–153, 278 advantages of, 153 confusion over terminology, 22 definition, 143 keystone species and, 144 management and, 154–155 marine ecosystems in, 150 mechanisms of operation, 144–146 problems with, 151–153 Ecosystem health, definition, 159, 184 measurement, 161–167 Ecuador, 39, 74, 120 Edge effects, 200–201

Elephant, African, 150, 255–256 Asian, 249 Elk, 95 Endangered species, act, 43, 105, 260 definition, 5–7 flagship species and, 251 Endemic bird areas, 39 Endemic species birds, 29–40, 58 congruency, 39–42, 72, 83 definition, 4, 39, 72 documentation of, 8 species richness and, 50–52, 74–76, 83 threatened species and, 50–51, 78 Endemism. See Endemic species. Engineering species. See Ecosystem engineers. Englemann oak, 232–233 Environmental baselines. See Baselines. Environmental indicator species, 266, 268 definition, 24–25 research effort and, 16 Environmental health. See Ecosystem health. Environmental indicators, 162–167, 184 Environmental surrogates, 15, 36–37, 90–95, 274 complementarity and, 83 Environmental variables, 91–92, 274 anthropogenic change and, 278– 279 biodiversity inventories and, 271– 273 reserve design and, 277–278 Ethiopia, 56 Eucalyptus, 206–208 Europe, 228, 229–231 Evaluation species, 232 Exploiter species, 164 Extinct species, 5–7 Exurban development, 209–210

Index 369 Families. See Higher taxa. Fauna and Flora Preservation Society, 247 Featured species, 231 Finland, 69, 93 Fish, biodiversity and, 43–44, 49, 63, 69, 72, 74, 90–91 environmental indicator species as, 170, 172, 177–180, 181 Fisher, 108 Flagship species, 27, 267–268. See also Flagship umbrella species. alternatives to, 281–282 characteristics of , 245–246, 251, 257–258 confusion over terminology, 22, 26 definition, 245 ecosystem engineers and, 153, 156 keystone species and, 143, 156 landscape species and, 124 research effort and, 16 umbrella species and, 247 Flagship umbrella species, examples of, 247–248 tests of, 251–257 utility of, 260 Flying fox, 250 Focal species, 17–21, 264–265 confusion over definition, 21–22 definition of Lambeck, 17–18, 102 landscape species and, 121 umbrella species and, 116, 277– 278 Foundation species, 153–155, 264, 266, 278 definition, 153 management and, 154–155 research effort and, 16 France, 254 Fragmentation, 132–134, 197–203, 224–225, 228–229, 239 Freshwater pollution, 171–174 Frogs, biodiversity and, 72 flagship species and, 254 latent risk of extinction and, 238

Fungi, biodiversity and, 69–70, 76, 84–85 umbrella species and, 104 Galliformes, 110–111 Gamma diversity, 2, 83. See also Species richness. Gastropods, 74, 108 Genera. See Higher taxa Ghats, Western, 39, 56 Gnatcatcher, California, 102 Goshawk, 111–113, 253 Governments, 247–248 Greece, 73–74, 78, 81 Greenpeace, 246 Guatemala, 204 Guinea, 56 Guyana, 250 Habitat evaluation procedures, 232 Hawk, broad winged, 94 Hemlock, eastern, 154 Higher taxa, 37–38, 58, 66–71, 84– 86 Himalayas, 56, 68, 69 Hotspots, biodiversity of, 31, 276–277 species richness of, 34, 52, 62–64, 76–77 endemic species of, 39–41 rarity of, 42, 76–77 Hymenoptera, 224–225 Hummingbirds, 101 ecological-disturbance indicator species as, 199 Iconic species, 258–259, 267–268 Important bird areas, 88 Index of biological integrity, 164– 166 India, 247 Indicator species, confusion over terminology, 22– 26 definition, 24–25 Indonesia 39, 56, 209, 249, 272 IndVal, 191–192, 281

370 Index Insects, biodiversity and, 43, 49, 82 cross-taxon-response indicator species as, 223–224 flagship species as, 246 Intraguild predation. See Mesopredator release. Intraguild-response indicator species, 228–229 Invasive species, 138–139, 152 Inventory abbreviation, 66–67 Invertebrates, biodiversity and, 63, 69, 90–91, 93 environmental indicator species as, 172, 177–178, 200, 206–209 umbrella species and, 105–106 Israel, 69 Italy 21, 104, 111, 253 IUCN criteria, 5–7, 73, 74 Jaguar, iv, 124, 201, 250, 253–254 Japan, 253 Kaka, 113 Kenya, 39, 56, 246 Kestrel, 111–113, 279 Key biodiversity areas, 57–58 Keystone species, 264–265, 278 advantages of, 142–143 confusion over terminology, 22 context dependency, 139–142 definition of, 130, 142 examples of, 127–132 introductions and, 136–138 management and, 154–155 problems with, 139–142 research effort and, 16 Kite, 111–113 Landscape species, 120–124, 264–265, 278 criteria for, 120–122 definition, 120 monitoring and, 122–123 Latent risk of extinction, 237–238 Leafhoppers, biodiversity and, 71

ecological-disturbance indicator species as, 200 Leopard, 270 Lichens, 62–64, 68, 76 Liverworts, biodiversity and, 68 umbrella species and, 104 Local umbrella species, 99–100, 264– 265 birds and, 108–114 criteria for, 116–117 cross-taxon-response indicator species and, 218 land snails and, 107 mammals and, 107–108 Lynx, 95, 21, 108 Madagascar, 31, 39, 52, 56, 258, 272 Malaysia, 209 Mammals, biodiversity and, 21, 32, 33, 34, 35, 38, 39, 40, 41–42, 43, 46, 47, 49, 51, 52, 53, 65, 72, 74, 76, 80, 81, 86 ecological-disturbance indicator species as, 199, 200–201, 204–205, 210 endangered species act and, 260 environmental indicator species as, 183–184 flagship species and, 253, 254 umbrella species and, 105 Management areas, 211–212, 227– 228 Management indicator species, 230– 234, 266, 268 cross-taxon-response indicator species and, 232 definition, 231 ecological-disturbance indicator species and, 232 management umbrella species and, 100, 232 problems with, 233–234 Management umbrella species, 100, 113, 264–265 criteria for, 116–117

Index 371 Marine pollution, 169–171 indices of, 171 Matrix between fragments, 201 Mauritius, 56 Measurement, detection probability, 212–213 higher taxa, 37, 69–70 surrogate species, 23–26 threatened taxa, 43–45 Mesopredator release, 132–134 Mexico, 68, 136, 196, 204 Mollusks, biodiversity and, 43–44, 69, 90 environmental indicator species as, 163, 170 flagship species and, 254 umbrella species and, 113 Morphospecies, 71–72 Moss, 68 Moths, biodiversity and, 69, 71, 73, 80, 81, 84 cross-taxon-response indicator species as, 223–224 ecological-disturbance indicator species as, 204–205, 206–207 Mussels, xiv, 120, 127, 154, 170 Mythical animals, 259 Namibia, 254 Natural Resources Defense Council, 246 Nestedness, 81, 105, 224–225, 240– 241 New Britain, 90 New Caledonia, 87 New Guinea, 31, 56, 62 New Zealand, 56, 138–139, 195–196, 223 NGOs, 246–248, 281 Nicaragua, 204 Norway, 82, 246 North America. See also Canada, United States of America. engineering species and, 146–149, 152 higher taxa, 69

reintroductions, 136–138 species richness and, 33–35 threatened species and, 43–44, 49, 51–52 Nuthatch, 102 Oil palm, 188, 208–209 Orca. See Whale, killer Orthopterans, 74 Oryx, Arabian, 247 Otter, European, 254 Ovenbird, 94 Owl, barred, 22, 94 eagle, 111–113, 253 long-eared, 111–113, 253 pygmy, 98, 111–113, 253 scops, 111–113, 253 spotted, 113, 195, 251–253 tawny, 111–113, 253 Tengmalm’s, 111–113, 253 Panama, 136, 204 Panda, giant, 247, 251 Parasites, 170 Parids. See Tits. Peccary, white-lipped, 253–254 Peru, 66–67 Philippines, 39, 56 Pig, 250 Pisaster, 127–129, 139 Plantations, 206–209 Plants. See Vascular plants. See also Aquatic plants, Woody plants. Pocket gopher, 148 Poland, 109 Pollution, 169. See also Freshwater pollution, Marine pollution Population, monitoring, 210–211, 213–214, 229–230, 240 persistence, 83–84 Portfolios. See Complementarity. Portugal, 69, 85, 279 Prairie dog, 148–149 Primates biodiversity and, 52, 63, 65

372 Index Primates (continued) ecological-disturbance indicator species as, 201 flagship species and, 255–256 latent risk of extinction and, 237 Protected areas, biodiversity and, 53–56 coverage, 86–88 endemism and, 56 marine 89–90, 179–180, 268–270 size, 57 Proxy. See Conservation shortcuts. Rainforests, 197–209, 262 Rapid Assessment Team, 213 Rarity, congruency, 42, 73 definition, 4, 73 documentation of, 8 measurement of, 4, 81–82 species richness and, 52, 76–78 threatened species and, 52, 79 Recovery species, 231 Red-listed species, 103–104, 237 Reintroductions, 136–138 Reptiles, biodiversity and, 20, 21, 32, 34, 35, 39, 41–42, 49, 50, 63, 65, 72, 74, 76, 81 ecological-disturbance indicator species as, 206–208 umbrella species and, 105 Reserve selection, 26 research effort and, 16 umbrella species and, 101 uncertainty and, 275 socioeconomics and, 274–277 Restoration, 241 Resilience, 160–161 Resistance, 161 Reunion, 56 Rhinoceros, black, 106–107, 254, 354 River flow regime, 174–176 River modification, 174–177 Robin, 18–19 Rodents, 65 Ryuku Islands, 56

Sage grouse, 111 Salamanders, 113 Sao Tome, 56 Scale, 2, 42 cross-taxon-response indicator species and, 241 extent, 11–13, 79 grain, 11–13, 79 importance of, 9–13 Scandinavia, 63 Sea otter, 126, 128–129, 154, 156 Sensitive species, 231 Sentinel species, 167–169, 184, 235, 266, 268 definition, 168 criteria for, 168–169 Seychelles, 56 Shannon-Weiner index, 164 Shopping basket approach, 79, 96 Shortcuts. See Conservation shortcuts. Shrike, loggerhead, 94 Simpson index, 164 Snails, 34, 35, 72, 82 Snakes, 33, 47, 52 Snipe, common, 216 South Africa, 56, 81, 96, 227–228 endemism and, 72 rarity and, 73, 78 species richness and, 63, 78, 85– 86 South America, 42, 238 complementarity and, 46–47 Spain, 63, 76, 79, 224 Sparrowhawk, 111–113 Species acculumlation curve, 49 Species indicators of biodiversity, 264– 265 confusion over terminology, 26 definitions, 24–25 research effort and, 16 umbrella species and, 101 Species richness, congruency, 32–35, 45–47, 66–67, 79–82 definition, 3 documentation of, 8 endemism and, 50–52, 74–76

Index 373 rarity and, 52, 76–78 threatened species and, 50–55, 78 Spider monkey, 253–254 Spiders biodiversity and, 69, 71, 74, 85 ecological-disturbance indicator species as, 207 Squirrel, 219 flying, 17, 102, 108, 223 Sri Lanka, 39, 56, 85 Strongly interacting species. See Keystone species. Substitute species, 238–239, 266, 268 definition, 238 Sulawesi, 219–222 Sundaland, 39 Surrogacy curve, 47–49 Surrogate species, 1–3 assessment of success, 270–271 confusion over terminology, 22–27 definition, xv, 1–2, 16 examination of, 32 multi-surrogacy, 268–270 taxonomy of, 15–16, 263–268 use in conservation planning, 15, 283 Surrogate taxa. See Surrogate species. Sweden, 76, 78, 104, 106, 134, 224– 225, 250 Switzerland, 63, 110, 111 Systematic conservation planning, 13– 15, 283 effectiveness, 86–88 efficiency, 86–88 Target species, 16 Tamarins, 246, 249 Tanzania, 39, 88, 211–212, 228, 250 Tapir, Baird’s, 253–254 mountain, 247 Tasmanian devil, 259 Taxonomic distinctiveness, 8–9 Termites, 120 biodiversity and, 81, 86 Thailand, 56

Threatened species, congruency, 43–45, 73–74, 82 definition, 4, 5–7, 73 documentation of, 8 endemism and, 50–51, 74, 78 proxy for, 11 rarity and, 52, 79 species richness and, 50–53, 78 Tiger, 247 Tits, 111–113 Tortoises, 72 Trees. See also Woody plants. biodiversity and, 34, 35 ceiba, 250 ecological-disturbance indicator species as, 200 flagship species and, 253 management indicator species and, 233–234 umbrella species and, 112 Transformer species, 152 Trophic cascades, 130–132, 253 Tuatara, 195–196 Turtle, Blanding’s, 19 eastern box, 94 TWINSPAN, 190–191 Ungulates, 106–107, 255 Uganda, 63, 80 Umbrella index, 113–116 Umbrella species. 26–27. See also Classic umbrella species, Flagship umbrella species, Local umbrella species, Management umbrella species. birds, 108–116 butterflies, 113–116 confusion over definition, 22 definition, 100–101 habitat specialists, 118–119 indicators of biodiversity and, 101 invertebrates, 105–106 mammals, 106–108 multi-species, 102–104, 116 plants, 103–105 problems with, 117–119

374 Index Umbrella species (continued) research effort and, 16 top predators and, 113, 118–119 United States of America. See also North America. congruency at a small scale, 82–83 cross-taxon-response indicator species, 224–225, 241 ecological-disturbance indicator species, 209–210 endangered species, 43–44 engineering species, 147–148 environmental surrogates, 95 flagship species, 251–253, 254–255 keystone species, 127–129 management indicator species, 232– 233 reserve selection, 274–275 sampling methods and, 212–213 substitute species, 239 umbrella species, 105–106, 107– 108, 111, 118–119 Vascular plants, biodiversity and, 32, 35, 37, 39, 40, 44, 49, 63, 65, 66, 68, 69, 71, 72, 73, 74, 78, 81, 82, 84, 90–91 cross-taxon-response indicator species as, 241 ecological-disturbance indicator species as, 214 umbrella species and, 105 Venezuela, 74, 134–136, 225–226. Vertebrates, See also taxonomic names. biodiversity and, 63, 72, 82, 88, 95

cross-taxon-response indicator species as, 219–223 ecological-disturbance indicator species as, 209 Vicuna, 122 Vietnam, 56 Viverrids, 238 Vulnerability. See Vulnerable species. Vulnerable species, 4, 5–7 Vultures, 235–236 Whale, 246 killer, 128–129 North Atlantic right, 211, 268–269 Wholeness, 161 Wildlife Conservation Society, 120, 272 Willingness-to-pay, 251–252 Wolf, xvii, 21, 95, 253 reintroductions, 136–138 Wolverine, 21, 95, 108 Woodpecker, 109–110 green, 109 ivory-billed, 258 lesser spotted, 109 middle spotted, 109 pileated, 94 Woody plants, biodiversity and, 68, 80, 85 umbrella species and, 104 World Wildlife Fund, 247 ecoregions, 31, 32, 41–42, 58, 272 Zoos, 245, 247–248