Comments on Theoretical Biology, 7: 355±379, 2002 Copyright # 2002 Taylor & Francis 0894-8550/02 $12.00 + .00 DOI: 10.1080/08948550290022385
Beyond Theories of Plant Invasions: Lessons From Natural Landscapes Thomas J. Stohlgren
U.S. Geological Survey, National Institute of Invasive Species Science, Fort Collins Science Center, Fort Collins, Colorado, USA There are a growing number of contrasting theories about plant invasions, but most are only weakly supported by small-scale field experiments, observational studies, and mathematical models. Among the most contentious theories is that species-rich habitats should be less vulnerable to plant invasion than species-poor sites, stemming from earlier theories that competition is a major force in structuring plant communities. Early ecologists such as Charles Darwin (1859) and Charles Elton (1958) suggested that a lack of intense interspecific competition on islands made these low-diversity habitats vulnerable to invasion. Small-scale field experiments have supported and contradicted this theory, as have various mathematical models. In contrast, many large-scale observational studies and detailed vegetation surveys in continental areas often report that species-rich areas are more heavily invaded than species-poor areas, but there are exceptions here as well. In this article, I show how these seemingly contrasting patterns converge once appropriate spatial and temporal scales are considered in complex natural environments. I suggest ways in which small-scale experiments, mathematical models, and largescale observational studies can be improved and better integrated to advance a theoretically based understanding of plant invasions. Keywords: non-native species, habitat vulnerability, issues of scale.
Address correspondence to Thomas J. Stohlgren, USGS Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523-1499, USA. E-mail:
[email protected]
355
356
T. J. Stohlgren
Biological invasions have been suggested as one of the major global environmental changes of our time (Cronk and Fuller 1995; D'Antonio 1996; Mack et al. 2000; Vitousek et al. 1997). Human activities have caused the breakdown of barriers to species dispersal at global scale, and invasions have ramifications at all levels of biological organization from the population and gene levels to the ecosystem and landscape levels (D'Antonio and Vitousek 1992). The economic losses due to invasions are staggering. The estimated costs of impacts of invasive species in the United States exceed $137 billion per year, primarily due to lost agricultural productivity, maintenance costs, and control and eradication costs (Pimentel et al. 2000). The ecological costs are equally disturbing. Over 40% of the species on the Threatened and Endangered Species List are listed due to invasive species (Wilcove et al. 1998). Despite the urgency, magnitude, and escalation of invasive species problems, ecological theories regarding invasions have been contradictory and unhelpful to applied scientists, land management agencies, and the public. Selecting between competing theories of plant invasions may not be easy. It is humbling to note that ecologists do not yet understand causes and patterns of native species richness. The comprehensive review by Palmer (1994; 150 citations) counted 120 plausible hypotheses to explain patterns of species richness. Species invasions from other countries since European settlement) may further test the abilities of scientists to their limits. Constructing general theories of invasions would require consistent observations of native species population dynamics, the population dynamics of invasive species, and the dynamics of the environment that cross several spatial scales and long time periods. One of the most popular and contentious theories is that species-rich, productive, competitive habitats should be less vulnerable to plant invasion than species-poor, low-productivity sites. Early observations by Charles Darwin (1859) and Charles Elton (1958) suggested that lack of intense interspecific competition on islands made these low-diversity habitats vulnerable to invasion. This reasoning led to a long-held paradigm in ecology that competition is a major force in structuring plant communities (MacArthur 1970, 1972; May and MacArthur 1972). Theory suggested that an immigrating native species (or, by extrapolation, an invading nonnative species) would face strong resistance from many interacting species, which monopolize available resources and create a ``stable'' community. However, a smorgasbord of small-scale field experiments, various mathematical models, and large-scale observational studies and quantitative surveys in continental areas have sometimes supported and sometimes contradicted earlier observations (see Levine and D'Antonio 1999 for a review). There appears to be an increasing discontinuity between field observations, theoretical ecologists, and experimental studies of diversity and plant invasions. Too often, small-scale ecological experiments, theoretical models, and local observational studies have been preceded by precious few large-scale observations, or by synthesizing qualitative, site-specific, or
Beyond Theories of Plant Invasions
357
taxon-specific case studies. As a result, the experiments, mathematic models, and observations may have yielded information that is biased, simplistic, and of only local value, as the following examples show.
CONTRASTING THEORIES AND STUDY LIMITATIONS All studies are constrained by cost, time, and the need to simplify overly complex phenomena for easier study. These constraints manifest themselves in reductionist approaches to invasion ecology. It may be informative to evaluate common design considerations and trade-offs in various types of research to better understand why broad generalizations and theories have been slow to develop.
Small-Scale Experiments Several small-scale experiments have been used to derive general theories about the role of plant competition in the invasion process by experimentally manipulating plant species richness and diversity. Artificially structured ``communities'' (read 3m 3 m or 1 m 1 m plots) with 1 to 24 species per plot have shown negative relationships between species richness and invasibility (Knops et al. 1997; Tilman 1999; Tilman et al. 1996). Microcosm studies with up to 17 species have shown similar results, with species-poor treatments being more successfully invaded than the species-rich microcosms (Burke & Grime 1996). In direct contrast, two small-scale experiments in California found that more diverse plots were more heavily invaded than lowdiversity plots (Levine 2000; Robinson et al. 1995). One 7-year study from seed plantings found that species identity (e.g., the effect of an uncommon highly productive species) could have greater impact than species richness on the ``invasion'' of other species, though native plant immigration into plots was studied (Crawley et al. 1999). There are many reasons for the contradictory results of small-scale diversity-invasion experiments. Designing realistic and general experiments of plant invasions is particularly difficult. Experiments often attempt to assess processes of competition, resource availability, and plant establishment, growth, and reproduction between native and nonnative (or invasive and less-invasive) species. To precisely evaluate specific processes at very local scales (the plant neighborhood), small plots are typically used, often less than 3 m2 (Crawley et al. 1995; Tilman et al. 1996) and sometimes very much smaller (0.032 m2; Levine 2000). Often, the number of plant species used in experiments is usually quite small relative to the number of species in the regional species pool (Table 1). The sizes and ages of the selected species are often minimized in experiments, just as habitat heterogeneity, intensity of environmental gradients, and level of disturbances are minimized.
358
T. J. Stohlgren
TABLE 1 General attributes of typical invasion experiments relative to conditions in natural landscapes Typical experiments Number of species evaluated
Size of species evaluated
Environmental gradients
Atypically low richness in small plots or pots (e.g., < 6 species= 1-m2 plot on average, and usually less than 25 species) Often all plants grown from seed; typically short-lived grasses and herbaceous species tested, long-lived larger trees and shrubs are not considered (several hidden treatment effects, see Huston 1997) Usually contained in one field or site, and thus one vegetation type and biome with limited environmental gradients considered; extrapolation to other sites is limited
Types of species selected
Often a matter of convenienceÐe.g., available seed, mixes of local native and nonnative species
Level of protection from disturbance
Protected environments: free of large grazers, small rodent activity, fire, insect outbreaks, and other disturbances
Typical natural landscapes Higher density of species per 1-m2 plot is very common, regional species pool may be >1000 species in most natural settings Much higher potential for long-lived perennial and large-biomass species in the greater species pool, greater mixes of various longevities and sizes in the regional pool Wide range of soil characteristics (texture, chemistry), microclimate, hydrology, etc.; usually, multiple gradients in several horizontal and vertical directions Greater range of native to nonnative species ratios in preinvaded and postinvaded habitats from a local to regional seed pool Wide range of disturbances from large grazers, small rodent activity, fire, insect outbreaks, and other catastrophes (Continued)
Beyond Theories of Plant Invasions
359
TABLE 1 (Continued) Typical experiments Spatial scale of processes operating
Only neighborhood-scale such as competition with very local neighboring plants, usually grown from seed
Temporal scale considered
Usually short term (
