trials within a season were completed for all species, except for Gafrarium dispar and Mya arenaria. ...... plankton fraction in two species (T. piratica and T. sp.) ...
BIVALVE TRAITS AND DISTRIBUTIONS TO EXPLORE SPECIES DIVERSITY AT TROPICAL AND TEMPERATE TIDAL FLATS
The research reported in this thesis was carried out as an Ubbo Emmius bursaal for the Marine Biology department of the University of Groningen. The research was performed at the Department of Marine Ecology of the Royal Netherlands Institute for Sea Research, the Department of Environment and Conservation in Broome (Australia), Broome Bird Observatory, TAFE Aquaculture Centre and WA Fisheries, Broome. Financial support came from the Ubbo Emmius fund and the Department of Environment and Conservation in Perth (Australia). Cover design: Brode Compton Printed by: PrintPartners Ipskamp
RIJKSUNIVERSITEIT GRONINGEN
Bivalve traits and distributions to explore species diversity at tropical and temperate tidal flats
Proefschrift
ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr F. Zwarts, in het openbaar te verdedigen op vrijdag 24 oktober 2008 om 16.15 uur
door
Tanya Joan Compton geboren op 28 juni 1977 te Johannesburg, Zuid Afrika
Promotores:
Prof. dr. W. J. Wolff Prof. dr. T. Piersma
Beoordelingscommissie:
Prof. dr. G. J. Vermeij Prof. dr. C. H. R. Heip Prof. dr. H. Olff
ISBN: 978-90-367-3523-0
“Flesh and blood is the stuff of life. Stripping it away leaves skeletons – names, distributions, and abundances – that are so devoid of biological meaning that the patterns and explanations fail to capture the very phenomena that motivated the interest of biologists in the first place” Geerat Vermeij (2004)
To my family
Contents Chapter 1
General introduction
9
Chapter 2
Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates
29
Chapter 3
Overlap in the feeding morphology of bivalves from a species-rich and a species-poor intertidal flat: using gill-palp ratios for comparative analyses of mollusc assemblages
47
Chapter 4
Carbon isotope signatures reveal that diet is related to the relative sizes of the gills and palps in bivalves
61
Chapter 5
Selection of sediment habitat by three bivalve species across six European tidal flat systems
81
Chapter 6
Distributional overlap rather than habitat differentiation characterizes co-occurrence of bivalves in intertidal soft sediment systems
101
Chapter 7
Discussion
123
Summary
141
Definitions
153
Appendices Appendix 1 Appendix 2 Appendix 3
155 159 165
Acknowledgements
171
Introduction
Chapter 1. General introduction Species diversity is well-known for its peak in the tropics. Recognising that global diversity is the result of a multitude of factors, there is still much potential to discover emergent patterns because new methods and approaches can examine diversity in threedimensional space and time (see books by Lomolino & Heaney 2004, Lomolino et al. 2006b). In addition, there has previously been a tendency to focus on species diversity in one dimension (latitude) using a single parameter (species richness, Gaston 2000). Two examples of approaches that are improving our description and understanding of diversity are macrophysiology and trait approaches. Macrophysiology describes how physiological traits are distributed in space (Chown et al. 2004). Morphological traits have been used to explore selection pressures between assemblages of differing diversity (Vermeij 1978, Ricklefs & Miles 1994, Roy et al. 2004, Vermeij 2004, McGill et al. 2006). In stark contrast to the ubiquity of sedimentary systems (Snelgrove 1999), little is known about the patterns of species diversity and the possible processes that maintain increased richness within these systems. In this thesis, I examine how bivalve species in tidal flat systems are adapted to different climates and how species coexist when diversity is inflated using: (1) physiology and morphological traits and (2) species distributions. Based on the hypothesis that the physiological cost of living is lower, and that there is increased ecological opportunities and resource limitation between species in the tropics relative to temperate regions, it might be expected that tropical species are more differentiated in their morphology and habitat occupation than temperate species (Dobzhansky 1950, Vermeij 2005). Indeed there is evidence from terrestrial systems that suggests species from diverse systems display a large degree of functional differentiation (Ricklefs & Miles 1994) and coexist within habitats of increased heterogeneity (MacArthur 1972, Murdoch et al. 1972, Williams et al. 2002). To examine whether this hypothesis holds for tidal flat systems, we compared the thermal tolerance ranges of bivalves from tropical and temperate tidal flats and the composition of the feeding morphology of bivalves from a tropical and temperate tidal flat system. To explore how species coexist within their sedimentary environment, the distributions of species were compared across both tropical and temperate systems.
9
Chapter 1
Box 1. Some hypotheses for the latitudinal diversity gradient (for references see reviews by Pianka 1966, Lomolino et al. 2006a, Mittelbach et al. 2008) The Mid-domain effect: the random placement of geographic ranges between two hard boundaries results in high species richness. Neutral theory of diversity: assuming species are equivalent, random extinctions and random speciation may favour higher species richness in the tropics. Time for diversification is greater in the tropics. Diversification rates are greater in the tropics. Lower extinction rates in the tropics. Tropical environments tend to be more stable over short and long time periods, such that species are less subject to extinctions and are more capable of specialization. Glacial expansions and climatic fluxes of the Pleistocene caused extinctions of high latitude species and the subsequent interglacial period has been insufficient to re-establish these species. Less seasonality in the tropics enables species to become more specialized. Tropical regions have tended to occur in tropical latitudes for longer periods of time allowing more species to accumulate in the tropics over time. Tropical environments are more benign and can be inhabited by more species. More solar energy is available in the tropics to support higher productivity in the tropics. Higher temperatures in the tropics promote higher metabolic rates and shorter generation times leading to faster speciation rates. Tropical areas cover a larger area than temperate areas. Increased environmental complexity in the tropics enables more species to coexist. Natural selection in temperate regions is controlled by the physical environment, whereas biological competition is more important in the tropics. Greater production leads to greater diversity, everything else being equal. Tropical species tend to be more specialised, and therefore more species can be packed into the tropics. Populations with higher growth rates in the tropics provide more opportunities for ecological specialization.
1.1 Biological diversity A peak in species diversity at tropical latitudes, relative to temperate and polar latitudes, has intrigued scientists from the dawn of ecology (von Humboldt 1805, Darwin 1860). Recent analyses have proven that a peak in species diversity at tropical latitudes, with tapering diversity towards cooler latitudes, is a general phenomena that occurs in most taxonomic
10
Introduction
groups (Hillebrand 2004). In addition, it appears that species diversity gradients have steepened over time (Crame 2004). Consequently, more than 25 hypotheses aim to describe causality for this global phenomenon (reviews by Pianka 1966, Rohde 1992, Gaston 2000, Turner & Hawkins 2004, Mittelbach et al. 2008, see Box 1). Some of these hypotheses include chance, historical perturbation, environmental stability, habitat heterogeneity, productivity and species interactions. Even when recognising that historical factors have played a substantial role in shaping diversity gradients (Gaston 2000, Crame 2002, Jablonski et al. 2006), a primary cause for the latitudinal diversity gradient is not evident (Pianka 1966, Rohde 1992, Rosenzweig 1995, Hillebrand 2004). Instead, the latitudinal gradient in diversity most likely reflects a number of correlated factors that play roles of varying importance across space and time (Gaston 2000, Chown et al. 2004). Latitudinal gradients of species richness are one-dimensional patterns, whereas in reality species are spread across a three dimensional globe (Hawkins & Diniz 2004). Spatial patterns in diversity thus vary across other spatial dimensions. For example, echinoderm and decapod diversity vary with both latitude and longitude in the coastal waters of South Australia (O'Hara & Poore 2000). In the Atlantic Ocean, species diversity peaks at bathyl depths (1000 - 1500 m) and tapers off towards the continental shelf and slope (~ 0 - 1000 m) and the deep abyss (> 4000 m, Rex 1981, Rex et al. 2005). Additional anomalies to the latitudinal diversity gradient occur in tectonically active or topographically complex regions that harbour ‘hotspots’ of diversity; probably the result of geographic barriers that have formed and shifted frequently (Vermeij 2005). An example of a diversity ‘hotspot’ region is the Indo-west Pacific, which appears to be a centre of origination and accumulation for many species (Briggs 1992, 2004, 2005, 2007). Recognising that species diversity is spread across the globe in multiple dimensions, with a peak in the tropics, a rejuvenation of old and new approaches is currently leading to insights on how species diversity is distributed and the processes that could drive it (Lomolino & Heaney 2004, Lomolino et al. 2006b). 1.2 Approaches to exploring global diversity ‘Macroecology’ has discovered emergent patterns in the distributions of organisms and has also shed light on possible mechanistic processes (Brown 1995, Gaston & Blackburn 2000, Lomolino et al. 2006b). One macroecological pattern that has been linked to species diversity across latitudes is known as ‘Rapoport’s Rule’. Rapoport observed that the geographic range sizes of temperate species tend to cover larger areas and span a wider range of latitudes than tropical species (Rapoport 1982). This observation was reinforced by an analysis of Stevens (1989), who introduced a logical possible mechanism underlying this pattern – the climate variability hypothesis, which stems from earlier ideas by Dobzhansky (1950) and Janzen (1967). Stevens (1989) argued that geographical range sizes were greater
11
Chapter 1
in temperate species because they can tolerate greater climatic variability; this would enable them to occur across a wider range of latitudes. In contrast, tropical species are expected to be restricted in the habitats where they can survive because they are adapted to a stable climate regime (Stevens 1989). Rapoport’s rule, however, shows many exceptions and is thus not actually a ‘rule’ (Gaston et al. 1998), e.g. the geographical range sizes of molluscs in the Pacific Ocean vary independently of each other (Roy et al. 1994). Despite evidence that geographic range sizes do not follow a general rule, the climate variability hypothesis is still considered a process that can affect the range size of species (Gaston et al. 1998). ‘Macrophysiology’, the comparison of physiological traits at large spatial scales, has been stimulated by emergent patterns revealed through macroecology (Chown et al. 2004). For example, the climate variability effect appears to be supported by the thermal tolerance ranges of insect species which are larger at northern latitudes and narrower towards the equator (Addo-Bediako et al. 2000). The variation in growth rates of species across latitudinal clines is also a macrophysiological pattern (Dittman 1997). In bivalves, growth rates are faster at higher/warmer latitudes than colder latitudes (Dittman 1997). An explanation for this pattern, the temperature compensation hypothesis proposes that individuals from colder temperature regimes compensate for temperature associated slowing of physiological functions by being more active than individuals at warmer temperatures (Lonsdale & Levinton 1985). In support of this hypothesis, a common garden experiment revealed that the cilia on the feeding organs of cold climate oysters were more active than oysters from warmer climates; and that cilia movement across latitude has a genetic basis (Dittman 1997). It appears that large-scale comparative physiology can contribute considerable understanding to both physiology and ecology (Chown et al. 2002). However, an enlargement of current databases is required, as there is a lack of comparable data at large spatial scales and information about the extent to which variance is partitioned when controlling for phylogenetic relatedness (Harvey & Pagel 1991, Chown et al. 2002, Osovitz & Hofmann 2007). Similar to macroecology and macrophysiology, the functional trait approach is interested in explaining the abundances and distributions of species (McGill et al. 2006). The functional trait approach differs from macroecology in that it advocates the examination of numerous functional traits and also species’ abundance and trait distributions across environmental gradients (McGill et al. 2006). The goal of the functional trait approach is to explore how the fundamental niche is determined by physiological and morphological traits and consequently how organismal traits and the fundamental niche are related to the realised niche (McGill et al. 2006). A functional trait is defined as an attribute of an organisms’ morphology or physiology that affects fitness indirectly via growth, reproduction and survival (Violle et al. 2007). A trait based approach in combination with an understanding of where species occur in relation to environmental gradients may provide new perspectives to
12
Introduction
species diversity; especially because most spatial and temporal patterns of diversity are currently based solely on the unit of species richness (Roy et al. 2004). Morphological traits are useful tools for detecting different selection pressures at species-rich and species-poor systems (Vermeij 1978). For example, gastropod shell armour is more elaborate in species-rich tropical than in species-poor temperate rocky intertidal environments. This relationship infers a gradient of protection against predation towards the species-rich tropics (Vermeij 1978, Vermeij & Currey 1980). Although most diversity measures are likely to correlate with species richness, e.g. genetic diversity, in some cases the relationship between species richness and the traits of species can be complex and non-linear (Foote 1997, Roy & Foote 1997). For example, in the diversity hotspot region of the tropical Indo-west Pacific, the shell shapes of strombid gastropod species vary greatly, but the correlation between shell shape and species richness is not linear. Instead, morphological diversity in the most species-rich systems is no higher than in systems with half the number of species, suggesting that species-poor systems can still harbour a great variety of morphological trait diversity (Roy et al. 2001). Morphological traits have also been used to examine differences between species-rich and species-poor systems (see review by Ricklefs & Miles 1994). From basic principles, morphological traits of species in species-rich systems, relative to species-poor systems, could be expected to display either (a) increased morphological trait variety, i.e. a greater occupied morphospace, and trait differences between species, (b) minimized trait differences between species within a larger or similar occupied morphospace as temperate species or (c) have similar traits, i.e. show morphological overlap, in an occupied morphospace similar to temperate species (MacArthur 1972, Ricklefs & Miles 1994), see Figure 1. A number of studies on birds, bats, lizards and fishes show that morphological traits differ from each other and display a greater variety in species-rich than species-poor systems (Ricklefs & Miles 1994). For example, tropical night-flying moths had a greater variety of dissimilar morphological traits than temperate moths (Ricklefs & O'Rourke 1975). Recent evidence from the feeding morphology of tropical reef fishes and strombid gastropods show that morphological overlap can also occur in species-rich systems (Roy et al. 2001, Bellwood et al. 2006). Morphological overlap might suggest that species within the same environment are functionally equivalent and are able to exploit the same resources (Bellwood et al. 2006). This is contrary to the idea that differences in morphology reflect character displacement via competition for resources (MacArthur 1972, Ricklefs & Miles 1994). In summary, morphological traits of species may be useful and powerful tools that can be used in multiple ways to enlarge the descriptive database of diversity. A clear advantage of using metrics that reflect selection pressures is that the traits do the talking. This is especially important in situations where the measurement of direct biological interactions is difficult (Vermeij 2004).
13
Chapter 1
Figure 1. From basic principles, morphological traits of species in species-rich systems, relative to species-poor systems, could be expected to display either (a) increased morphological trait variety, i.e. a greater occupied morphospace, and trait differences between species, (b)
minimized trait
differences between species within a larger or similar occupied morphospace as temperate species or (c) have similar traits, i.e. show morphological overlap, in an occupied morphospace similar to temperate species.
The distribution of species and species’ traits across environmental gradients can provide an understanding of how assemblages, that differ in diversity, are composed and their relative selection pressures (McGill et al. 2006). Comparing assemblages at local scales can often yield more insights into processes that drive diversity compared to global or regional scales (Gaston 2000). A challenge to understanding various local processes is the comparison of assemblages with differing abundances in space and time, different histories (Underwood & Petraitis 1993) and differing climatic and environmental settings. One approach for comparing diversity across latitudes has been to run controlled experiments at different latitudes (Pennings & Silliman 2005). Another approach is to compare the spatial distributions of species at different geographic localities to look for generalities in community composition or habitat use (MacArthur 1972, Pianka 1973, Warwick & Ruswahyuni 1987, Piersma et al. 1993b, Thrush et al. 2005). The benefit of using a multiple
14
Introduction
system approach is that theories considered general from single systems can often be reversed when processes at larger scales become evident, e.g. the intensity of local interactions can be affected by larval inputs into a population (Connolly & Roughgarden 1998). 1.3 Using species’ traits and distributions to examine bivalve diversity in tropical and temperate tidal flats In stark contrast to the wide distribution of sedimentary systems in the deep-sea and along coastal margins there is a lack of description and understanding of the processes that could maintain diversity in these systems (Snelgrove 1998, Rex et al. 2005). This is most prominently the case in coastal systems from the tropics where there appears to be a peak in diversity, however, as there are only few studies this pattern might not even be realistic (see (Alongi 1990, Piersma et al. 1993b, Attrill et al. 2001). Also see Box 2 for an introduction to studying marine sedimentary systems. In an on-going approach to explore temperate and tropical tidal flats, there has been extensive research carried out in the Wadden Sea, Roebuck Bay and Banc d’Arguin and other places for the last fifteen years by T. Piersma and his group. These sites have been identified on the basis of their role as shorebird stop-over sites (e.g. Piersma 2007), but are also of importance for their high macrobenthic diversity (Piersma et al. 1993b, Rogers et al. 2005, Bocher et al. 2007, Honkoop et al. 2007). Recognizing that tropical systems need much more attention globally, and that it would be ideal to have more systems in this study, we explore tropical and temperate diversity of tidal flats using a variety of approaches to determine if we can find emergent patterns that might be suggestive of processes that maintain diversity. Based on the hypothesis that there is a lower physiological cost of living in the tropics, increased ecological opportunities and resource limitation between species, it might be expected that tropical species are more differentiated in their morphology and their habitat occupation relative to temperate species (Dobzhansky 1950, Vermeij 2005). To examine whether this hypothesis might hold for tidal flat systems, we compared the thermal tolerance ranges of bivalves from tropical and temperate tidal flats to determine whether species have narrower physiological tolerance ranges in the tropics. The feeding organs of bivalves from a tropical and temperate tidal flat system were also compared to identify whether functional differentiation was greater in the tropics. Finally, to explore how species coexist within their local sedimentary environment, the distributions of species, with respect to sediment, were compared across both tropical and temperate systems.
15
Chapter 1
Box 2. Examining species diversity in sedimentary systems The marine realm encompasses a wide variety of environments from the lightless, high pressure and low temperature deep-sea to shallow coastal systems that vary in shape, size and form (Snelgrove 1999). In stark contrast to the ubiquity of deep-sea and coastal sedimentary systems, little is known about sedimentary systems and the organisms that live within them! The gap in knowledge about sedimentary systems can be attributed to logistical and sampling effort constraints (Snelgrove 1999), as well as the difficulty of sampling and experimentally manipulating benthic organisms that occur within a hidden three-dimensional matrix that collapses upon sampling. Despite the drawbacks, it can be argued that sedimentary systems are important for understanding global diversity; theoretically and for conservation. Sedimentary systems have already provided insights to biodiversity theory through the deep-sea species diversity gradients across latitude and depth (see review by Rex et al. (2005), which differ to terrestrial diversity gradients because they are characterised by low and constant temperatures, virtually no light (light does not penetrate to depths > 100 m) and no in-situ primary production (Rex et al. 2005). Understanding deep-sea gradients might thus hold the promise to discovering the common underlying causes of these global patterns (Rex et al. 2005). Coastal sedimentary systems should provide promising avenues to explore diversity because they can be easily compared across the globe; if comparable sampling regimes are followed and abiotic variables are measured. In addition, it is of value to understand these systems because coastal systems provide ecosystem services to terrestrial, freshwater and ocean systems via nutrient cycling and production, the regulation of nutrient fluxes and the transport of water, particles and organisms (Levin et al. 2001). In addition, they are nursery areas for many oceanic species, e.g. larval fishes (Jackson & Jones 1999, Morrison et al. 2002). Intrinsic to the services provided by coastal sediment ecosystems are the functional roles carried out by benthic organisms, e.g. organisms (1) maintain sediment stability by bioturbation, (2) break down organic matter and (3) remove organic particles from the water column via suspension feeding (Levin et al. 2001). Notably, shifts or losses of benthic organisms with key functional roles in coastal sediment systems can have cascading effects on coastal, terrestrial, freshwater and oceanic ecosystems (Levin et al. 2001). For example, the introduction of invasive species, habitat alteration and overfishing have all been noted as capable of changing the structure and function of coastal sedimentary systems (Levin et al. 2001, Kennish 2002, van Gils et al. 2006). Marine tidal flat systems are coastal wetlands that form when mud is deposited by rivers, sea and oceans. Extensive tidal flat areas (>1 km wide at low tide) can be found in sheltered areas such as bays, lagoons and estuaries (Robertson 1994, Bakker & Piersma 2005). Sediments are comprised of fine muddy particles, because low wave-energy conditions do not remove the fine grades of sediment in tidal flat systems (Robertson 1994, Bakker & Piersma 2005). Within some marine tidal flat systems, bivalves and gastropods are known to constitute a large proportion of the total biomass (Wolff 1983, Reise 1985, Piersma et al. 1993a), maintain water quality (Ward & Shumway 2004) and form an important part of the food chain for a variety of consumers (Wolff 1983), including migratory shorebirds (Zwarts & Blomert 1992).
16
Introduction
1.4 Bivalve traits at a species-rich (tropical Roebuck Bay) and a species-poor (temperate Dutch Wadden Sea) system Species diversity and species’ geographic range sizes are expected to be determined in-part by geographic climate variability (Stevens 1989). Diversity is expected to be limited in temperate regions because variable climates that characterise temperate regions should require a greater amount of physiological flexibility for an organism to survive relative to constant climates (Dobzhansky 1950). Consequently, it is speculated that physiological flexibility should come at a cost that limits adaptation and speciation (Dobzhansky 1950). A recent book (Spicer & Gaston 1999) that followed a journal review (Gaston et al. 1998) demonstrate that support for the climate variability effect is scant (Vernberg & Tashian 1959, Brattstrom 1968, Brett 1970, Snyder & Weathers 1975, Addo-Bediako et al. 2000). The reason for the lack of support for the climate variability hypothesis, especially in the marine environment, is that few studies have examined the lower lethal thermal limits of organisms (Spicer & Gaston 1999). Thus the climate variability effect should be compared across a number of species and habitat types, controlling for phylogeny, before it can be considered a general phenomenon. One such environment where the climate variability effect should be examined is marine tidal flat systems. Marine tidal flats might not display a strong climate variability effect, because the organisms should be relatively protected from temperature variation, emersion and wind desiccation by sediments and the associated interstitial water. To investigate if climate variability has an effect on the physiological flexibility of the bivalves in Roebuck Bay and the Wadden Sea we compared their thermal tolerance ranges with the local temperature variation in the sediment (Chapter 2). Due to the lower physiological cost of living in the tropics, increased ecological opportunities, e.g. greater habitat space, and resource limitation between multiple species, it might be expected that tropical species show greater adaptation and diversification to biotic pressures like competition and predation (Dobzhansky 1950, Vermeij 2005). In diverse systems, competition between species should lead to an increased division of labour, specialization and functional differentiation (Vermeij 2005). Indeed, evidence suggests that functional differentiation in terms of morphological variety is greater in species-rich than species-poor systems; and appears to be associated with resource acquisition (Ricklefs & Miles 1994). Alternatively, new evidence suggests that morphological similarity in diverse systems is also possible (Roy et al. 2001, Bellwood et al. 2006). To examine whether morphological variety was greater in a tropical than a temperate system, we compared the feeding morphology of bivalve species at the species-rich Roebuck Bay and the species-poor Dutch Wadden Sea (Chapter 3).
17
Chapter 1
Contrary to initial proposals that bivalve feeding organs indiscriminately select food from the overlying water column or sediment (see review by Ward and Shumway, 2004), bivalve feeding morphology can be considered a finely-tuned functional trait because bivalve feeding organs: (1) select food particles based on their quality (Levinton et al. 1996, Ward et al. 1997, Ward & Shumway 2004), (2) adjust to changing food circumstances, i.e. turbidity and silt conditions (Theisen 1982, Essink 1991, Payne et al. 1995, Barille et al. 2000, Honkoop et al. 2003, Drent et al. 2004), and (3) are reflective of feeding mode, i.e. relatively larger gills indicate more suspension feeding and relatively larger palps indicate more deposit feeding (Beesley et al. 1998). In addition, the feeding organs of bivalves are similar in form across most species, making them a perfect ruler for comparison between species; when organ sizes are adjusted for relative size (log gill-to-palp mass ratio). To ascertain whether bivalve feeding morphology has a direct relationship to bivalve diet, we correlated bivalve feeding morphology with the assimilated carbon stable isotope composition, at a single point in time, in Roebuck Bay (Chapter 4). 1.5 Habitat use in bivalves across multiple tidal flat systems In the second part of this thesis, I compare the spatial distributions of species across multiple tidal flat systems to explore how species might coexist in diverse systems. Initially, I examine the distributions of European bivalve species for patterns that might reflect habitat selection. Habitat selection should suggest that organisms are finely tuned to their habitat type and thus need greater habitat diversity in tropical systems to coexist (Simpson 1949, Dobzhansky 1950, Pianka 1966, MacArthur & Levins 1967). To examine whether habitat heterogeneity was greater in tropical systems we explored species richness in relation to the diversity of the sedimentary habitat. In this study, all systems were sampled with the same sampling design and at similar spatial scales; a necessary prerequisite for local system comparisons (Underwood & Petraitis 1993). The beauty of using tidal flat systems for local system comparisons is that they can be sampled in a consistent manner with a sediment corer. In addition, the environmental variable intrinsic to these systems, sediment, is considered a measure of available habitat for benthic species (Sanders 1958, Gray 1974, Wolff 1983) because it reflects a number of processes that occur in these systems, e.g. hydrodynamics are associated with food supply (Snelgrove & Butman 1994, Thrush et al. 2005). In addition, sediment can easily be compared between systems using a common metric, e.g. median grain size or percentage of silt (Levinton 2001). Within single coastal sediment systems, it has commonly been observed that species distributions are correlated with sediment (Sanders 1958, Gray 1974, Whitlatch 1980, Ysebaert et al. 2002, Thrush et al. 2003, Ellis et al. 2006). However, few studies have investigated the degree to which these patterns are repeatable across systems. Repeatable
18
Introduction
distributions with respect to sediment across tidal flat systems could reflect active habitat selection on the part of the benthic species. Species might preferentially settle and/or survive on specific sediment types because sediment type can have direct and/or indirect fitness consequences. Consistent with the expectation that species select their habitat, benthic bivalve species are known to be capable of actively or passively dispersing after settlement. In juvenile bivalves, active dispersal is facilitated by byssus-drifting in the water column (Baggerman 1953, Butman 1987, Beukema & de Vlas 1989, Armonies 1992, Cummings et al. 1993, Armonies 1994a, b, Cummings et al. 1995, Norkko et al. 2001). In this study we compared the juvenile and adult distributions of three common bivalve species (Macoma balthica, Cerastoderma edule and Scrobicularia plana) across six northwest European tidal flat systems, German Wadden Sea, The Wash, Dutch Wadden Sea, Mont Saint-Michel Bay, Marennes-Oléron Bay and Aiguillon Bay (Chapter 5). At the scale of global diversity, it has been proposed that the heterogeneity of a habitat may be important for the coexistence of species in diverse systems (Simpson 1949, Dobzhansky 1950, Pianka 1966, MacArthur & Levins 1967). Many studies show support for the habitat heterogeneity hypothesis, but they tend to be biased towards vertebrates and habitats under anthropogenic influence (Tews et al. 2004). Evidence from invertebrate species and other environments are necessary to examine the generality of this hypothesis (Tews et al. 2004). Although marine soft sediment environments are often considered to be vast and homogenous (Hewitt et al. 2005), in reality sedimentary systems are complex environments which are known to be associated with diversity. For example, shell debris (Hewitt et al. 2005) and seagrass beds (Orth et al. 1984, Edgar et al. 1994, Sheridan 1997, Boström et al. 2006, Honkoop et al. 2007) are associated with increased species richness. In addition, richness appears to be highest where particle size diversity is greatest; alpha diversity (Gray 1981, Whitlatch 1981, Etter & Grassle 1992). We thus explored whether the sediment heterogeneity of a system correlates with local species diversity of a system at systems from across the globe. In addition, we investigated whether local richness was correlated with increased particle size diversity (Chapter 6). References Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc Royal Soc B 267:739-745 Alongi DM (1990) The ecology of tropical soft-bottom benthic ecosystems. Oceanogr Mar Biol Ann Rev 28:381 - 496 Armonies W (1992) Migratory rhythms of drifting juvenile molluscs in tidal waters of the Wadden Sea. Mar Ecol Prog Ser 83:197-206
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Chapter 1
Armonies W (1994a) Drifting meiobenthic and macrobenthic invertebrates on tidal flats in Konigshafen - A review. Helgolander Meeresun 48:299-320 Armonies W (1994b) Turnover of postlarval bivalves in sediments of tidal flats in Konigshafen: a review. Helgolander Meeresun 48:291-297 Attrill MJ, Stafford R, Rowden AA (2001) Latitudinal diversity patterns in estuarine tidal flats: indications of a global cline. Ecography 24:318-324 Baggerman B (1953) Spatfall and transport of Cardium edule L. L Arch Néerl Zool 10:315342 Bakker J, Piersma T (2005) Restoration of intertidal flats and tidal salt marshes. In: van Andel J, Aronson J (eds) Restoration Ecology, the New Frontier. Blackwell Science Ltd: p 174-192 Barille L, Haure J, Cognie B, Leroy A (2000) Variation in pallial organs and eulatero-frontal cirri in response to high particulate matter concentrations in the oyster Crassostrea gigas. Can J Fish Aquat Sci 57:837-843 Beesley PL, Ross GJB, Wells A (1998) Mollusca: The Southern Synthesis, Part B. CSIRO publishing, Melbourne Bellwood DR, Wainwright PC, Fulton CJ, Hoey AS (2006) Functional versatility supports coral reef biodiversity. Proc R Soc B 273:101-107 Beukema JJ, de Vlas J (1989) Tidal-current transport of thread-drifting postlarval juveniles of the bivalve Macoma balthica from the Wadden Sea to the North Sea. Mar Ecol Prog Ser 52:193-200 Bocher P, Piersma T, Dekinga A, Kraan C, Yates MG, Guyot T, Folmer EO, Radenac G (2007) Site- and species-specific distribution patterns of molluscs at five intertidal soft-sediment areas in northwest Europe during a single winter. Mar Biol 151:577594 Boström C, Jackson EL, Simenstad CA (2006) Seagrass landscapes and their effects on associated fauna: A review. Estuar Coast Shelf Sci 68:383-403 Brattstrom BH (1968) Thermal acclimation in anuran amphibians as a function of latitude and altitude. Comp Biochem Phys 24:93-111 Brett JR (1970) Fish: functional approaches. In: Kinne O (ed) Marine Ecology, Vol 1, Environmental Factors, Part 1, Chapter 3: Temperature. Wiley-Interscience, Chichester, p 515-616 Briggs JC (1992) The marine East-Indies - Center of origin. Glob Ecol Biogeogr Lett 2:149156 Briggs JC (2004) A Marine Centre of Origin: Reality and Conservation. In: Lomolino MV, Heaney LR (eds) Frontiers in Biogeography: New directions in the Geography of Nature. Sinauer Associates, Sunderland
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Introduction
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Thrush SF, Hewitt JE, Herman PMJ, Ysebaert T (2005) Multi-scale analysis of speciesenvironment relationships. Mar Ecol Prog Ser 302:13-26 Thrush SF, Hewitt JE, Norkko A, Nicholls PE, Funnell GA, Ellis JI (2003) Habitat change in estuaries: predicting broad-scale responses of intertidal macrofauna to sediment mud content. Mar Ecol Prog Ser 263:101-112 Turner JRG, Hawkins BA (2004) The global diversity gradient. In: Lomolino MV, Heaney LR (eds) Frontiers in Biogeography: New Directions in the Geography of Nature. Sinauer Associates Inc., Sunderland Underwood AJ, Petraitis PS (1993) Structure of intertidal assemblages in different locations: how can local processes be compared? In: Ricklefs RE, Schluter D (eds) Species Diversity in Ecological Communities: Historical and Geographical Perspectives. The University of Chicago Press, London van Gils JA, Piersma T, Dekinga A, Spaans B, Kraan C (2006) Shellfish dredging pushes a flexible avian top predator out of a marine protected area. PLOS Biology 4:2399-2404 Vermeij GJ (1978) Biogeography and Adaptation: Patterns of marine life. Harvard University Press, Cambridge MA Vermeij GJ (2004) Island life: A view from the sea. In: Lomolino MV, Heaney LR (eds) Frontiers in Biogeography: New Directions in the Geography of Nature. Sinauer Associates Inc., Sunderland, Massachusetts Vermeij GJ (2005) From phenomenology to first principles: toward a theory of diversity. Proc Cal Acad Sci 56:12 - 23 Vermeij GJ, Currey JD (1980) Geographical variation in the strength of thaidid snail shells. Biol Bull 158:383-389 Vernberg FJ, Tashian RE (1959) Studies on the physiological variation between tropical and temperate fiddler crabs of the genus Uca .1. Thermal death limits. Ecology 40:589593 Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882-892 von Humboldt A (1805) Essai sur la geographie des plantes accompagne d'un tableau physique des regions equinoxiales, fonde sur des mesures executees, depuis le dixieme degre de latitude boreale jusqu'au dixieme degre de latitude australe, pendant les annees 1799, 1800, 1801, 1802 et 1803. Levrault Schoell, Paris Ward JE, Levinton JS, Shumway SE, Cucci T (1997) Site of particle selection in a bivalve mollusc. Nature 390:131-132 Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83-130 Warwick RM, Ruswahyuni (1987) Comparative study of the structure of some tropical and temperate marine soft-bottom macrobenthic communities. Mar Biol 95:641-649
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Whitlatch RB (1980) Patterns of resource utilization and coexistence in marine intertidal deposit feeding communities. J Mar Res 38:743-765 Whitlatch RB (1981) Animal-sediment relationships in intertidal marine benthic habitats: some determinants of deposit-feeding species diversity. J Exp Mar Biol Ecol 53:31 45 Williams SE, Marsh H, Winter J (2002) Spatial scale, species diversity, and habitat structure: Small mammals in Australian tropical rain forest. Ecology 83:1317-1329 Wolff WJ (1983) Ecology of the Wadden Sea. A.A. Balkema, Rotterdam Ysebaert T, Meire P, Herman PMJ, Verbeek H (2002) Macrobenthic species response surfaces along estuarine gradients: prediction by logistic regression. Mar Ecol Prog Ser 225:79-95 Zwarts L, Blomert A-M (1992) Why knot Calidris canutus take medium-sized Macoma balthica when six prey species are available. Mar Ecol Prog Ser 83:113-128
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Climate variability effect in intertidal bivalves
Chapter 2. Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates Tanya J. Compton, Micha J.A. Rijkenberg, Jan Drent, Theunis Piersma Journal of Experimental Marine Biology and Ecology 352 (2007) 200–211 !
Abstract The climate variability hypothesis proposes that in variable temperate climates poikilothermic animals have wide thermal tolerance windows, whereas in constant tropical climates they have small thermal tolerance windows. In this study we quantified and compared the upper and lower lethal thermal tolerance limits of numerous bivalve species from a tropical (Roebuck Bay, north western Australia) and a temperate (Wadden Sea, north western Europe) tidal flat. Species from tropical Roebuck Bay had higher upper and lower lethal thermal limits than species from the temperate Wadden Sea, and Wadden Sea species showed an ability to survive freezing temperatures. The increased freezing resistance of the Wadden Sea species resulted in thermal tolerance windows that were on average 7°C greater than the Roebuck Bay species. Furthermore, at a local-scale, the upper lethal thermal limits of the Wadden Sea species were positively related to submersion time and thus to encountered temperature variation, but this was not the case for the Roebuck Bay species. A review of previous studies, at a global scale, showed that upper lethal thermal limits of tropical species are closer to maximum habitat temperatures than the upper lethal thermal limits of temperate species, suggesting that temperate species are better adapted to temperature variation. In this study, we show for the first time, at both local and global scales, that the lethal thermal limits of bivalves support the climate variability effect in the marine environment. 1. Introduction The greater magnitude of temperature variation at temperate latitudes is expected to select for wider physiological tolerance windows in poikilothermic animals, whereas the smaller magnitude of temperature variation at tropical latitudes is expected to lead to narrower tolerance windows (Dobzhansky 1950, Stevens 1989). The relationship between climate variation and thermal tolerance windows has been termed the climate variability hypothesis (Stevens 1989). It has far-reaching implications for geographical range sizes and species richness patterns (Gaston et al. 1998).
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Direct evidence for the climate variability hypothesis in the marine environment is scarce (Gaston et al. 1998, Spicer & Gaston 1999). The reason for a lack of support for the climate variability hypothesis, especially in the marine environment, is that few studies have examined the lower lethal thermal limits of organisms (Spicer & Gaston 1999). Thus, the effects of thermal acclimation on both heat and cold tolerance have seldomly been reported in multiple species adapted to different thermal habitats (Pörtner et al. 2006, Osovitz & Hofmann 2007). A large scale approach of examining physiological traits, macrophysiology (Chown et al. 2004), has proven promising in insects, and is expected to be an important for understanding species’ distributions in the marine environment (Osovitz & Hofmann 2007). For example, a meta-analysis of the thermal limits of insects has shown that the lower rather than the upper lethal thermal limits of insects are correlated with latitude (Addo-Bediako et al. 2000, Sinclair et al. 2003). Based on available knowledge, tolerance windows in marine organisms as estimated by lethal and critical thermal limits have displayed a relationship with climate regime. Note that lethal thermal limits can be used as indirect relevant correlates to examine biogeographical limits (Pörtner 2002). Fishes and bivalves from the Antarctic are known to have narrow thermal tolerance windows relative to temperate fishes with broad thermal tolerance windows that reflect the higher variation in their environmental temperatures (Somero & de Vries 1967, Brett 1970, Peck & Conway 2000, Peck et al. 2002). An adaptation to climate regime has also been shown in the upper lethal thermal limits of crabs and bivalves, as tropical species displayed higher upper lethal thermal limits than temperate species (Vernberg & Tashian 1959, Stillman & Somero 2000). In addition, where lower lethal thermal limits have been estimated in crabs it appears that tropical species have higher lower lethal thermal limits than temperate species (Vernberg & Tashian 1959). Interestingly, an examination of the upper thermal limits of porcelain crabs (Genus Petrolisthes) along the Pacific coast indicated that temperate species have a larger safety buffer in their upper thermal limits than temperate species (Stillman & Somero 2000, Stillman 2002). To investigate whether congeneric bivalve species from intertidal sedimentary habitats display evidence of a climate variability effect, we measured lethal thermal limits of 18 bivalve species from a tropical (Roebuck Bay, North West Australia) and a temperate tidal flat (Wadden Sea, The Netherlands) in relation to the local climate regime at each location. Thermal tolerance windows were compared between bivalves from both locations to test for a climate variability effect. Seasonal acclimatisation was examined to observe whether differences between locations would be greater than seasonal differences. The upper lethal thermal limits were related to the local habitat to examine relationships with submergence time. To examine whether at a global scale bivalves display a relationship between their upper lethal thermal limits and habitat temperature we obtained additional values from the literature and examined this correlation.
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Climate variability effect in intertidal bivalves
2. Materials and methods 2.1. Local temperature variation Annual climate regimes of the Roebuck Bay, North Western Australia (17°S and 122°E) and the Wadden Sea, The Netherlands (53°N and 5°E) tidal flats were recorded using Stowaway Tidbit™ loggers (hourly readings, buried 5 cm deep into the sediment) for periods of 6 to 12 months over a four year period (2002 to 2006). We averaged daily measurements to show seasonal trends in temperature, including yearly maxima and minima. The annual temperature range at each location was determined by subtracting the upper from the lower quartile value for each year. 2.2. Collection of bivalve species The species sampled in this experiment represent all the numerically important species (Piersma et al. 2001, Pearson et al. 2003). At both locations most species were sampled at the tidal flat and one species was collected from a hard substrate (Mytilus edulis in Wadden Sea and Barbatia pistachia in Roebuck Bay). In The Netherlands one species was collected in the subtidal North Sea, Spisula subtruncata (although this species does appear in the intertidal occasionally, T.P. pers obs.). Overall, the thermal limits of eleven species in Roebuck Bay, and seven species in the Wadden Sea were determined. Bivalve species were collected directly before placement into the experiment, and thus the field temperature at the time of collection is regarded as the acclimatization temperature for each trial. All collection and handling of animals was completed according to the legal requirements of each country. 2.3 Experimental trials The tested range of temperatures was 0 - 45°C for the bivalves from Roebuck Bay and -10 to 40°C for bivalves from the Wadden Sea; in both cases treatments were separated by 5°C intervals. All lethal thermal tolerance ranges were determined in the local sea-water. Each experiment tested only one species at a time. Each species’ experiment was terminated at 24 hours, and at the end of the experiment a gaping response indicated death; i.e. the lack of adductor muscle contractions (Ansell et al. 1980a). In aquatic organisms, lethal limits are determined in the time-frame when survival is passive and time-limited at high temperatures, i.e. at the end-point of survival. During passive survival blood oxygen levels are minimal and life is supported by anaerobic metabolism, heat shock proteins and an antioxidative defence (Pörtner & Knust 2007). Seasonal variation in the upper lethal thermal limits was examined for six of the 11 species in Roebuck Bay and five of the seven species in the Wadden Sea. Replicate species’ trials within a season were completed for all species, except for Gafrarium dispar and Mya arenaria. In Roebuck Bay the winter species trials ran from July to August (2003), and the
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summer species trials ran in November (2003). In the Wadden Sea the winter trials ran from February to March (2003), and the spring species trials ran in May (2003). In Roebuck Bay, the lower lethal thermal limits of all species were determined in November 2003. In the Wadden Sea species the lower temperatures from 20°C to -5°C were examined in May 2003, and as no species died, we tested another level of freezing tolerance (-10°C) in June 2004. Freezing tolerance limits were tested in spring due to logistical reasons. Replicate (n=2) temperature treatment basins were used for both the warm (20- 45 °C) and cool (15 – 0 °C) temperature treatments. Within each basin salt water filled aquaria (n=3-6, size: 11.5 x 18 x 18 cm, WS salinity 28‰, RB salinity 35‰) held the experimental species at the desired temperature. Temperatures above 20°C were maintained in basins with aquarium heaters (Tetra™ (20°C, 25°C), Reptistat™ (35°C, 40°C) and Schlego™ heaters (40°C, 45°C)). In Roebuck Bay, temperatures below 20°C were maintained in basins that were held in air-conditioned rooms (20°C, 15°C), Engel™ refrigerator units (10°C, 5°C) and ice (0°C). For the Wadden Sea species, cool temperature basins were maintained in a climate room (15°C), a temperature controlled water bath using anti-freeze (MGW Lauda K2R) (10°C, 5°C) , basins with ice (0°C) and a temperature controlled cabinet (Weiss Enet Model HETK 3057.S, The Netherlands) (-5°C, -10°C). In the temperature treatment of -5 °C, aquaria filled with sea water were placed directly into the refrigerator unit. Temperature readings were taken every four hours. As temperatures varied by 1- 2°C, the average temperature from each basin, during an experimental trial, was used in the final analysis. 2.4 Phylogenetic analysis Related species can share similar adaptations such that species can no longer be regarded as independent samples (Felsenstein 1985). To establish whether such effects of evolutionary history should be of concern, we examined whether the lethal thermal limits at both sites were related to phylogeny. In this study the phylogenetic topology of the bivalve species was drawn from Giribet and Wheeler (see Fig. 11, p 296, in Giribet & Wheeler 2002) and family descriptions from Beesley et al. (1998). To examine whether the bivalve thermal limits were phylogenetically constrained (Harvey & Pagel 1991), a test for serial independence was run (Abouheif 1999, Reeve & Abouheif 2003). In each simulation the relationship between lethal thermal limits and phylogeny was non-significant: upper lethal thermal limits P = 0.48, lower lethal thermal limits P = 0.36, lethal thermal range P = 0.38. Therefore, as the lethal thermal limits were not significantly correlated with phylogeny, traditional statistical analyses can be safely applied (Abouheif 1999, Ackerly & Reich 1999). 2.5 Tidal height and upper thermal limits Submergence time was calculated from the two spatial mapping databases available for each location (see Pepping et al. 1999, Piersma et al. 2001). Based on the positive
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Climate variability effect in intertidal bivalves
occurrence of species in the spatial mapping database we calculated an average submergence time (hours) for each species. The average submergence time was then converted into a percentage (12.42 h is a full tidal cycle). Average submergence time (%) was estimated for all species, except for the two hard substrate species. 2.6 Statistical analyses As mortality is a sigmoid function of temperature, a logit linear regression was used to separately estimate the upper and lower thermal limit of each species trial (day n=2, season n=2), and each replicate within a trial (basin n=2). The coefficients of the logit linear regression were used to calculate the temperature at which half of the sample population died within 24 h. All lethal thermal limit values are presented as a mean and standard error in the results. Upper lethal thermal limits were tested separately for each species using a two-way ANOVA to examine differences between season and replicate species’ trials. In species where season was not tested, a one-way ANOVA was used to examine differences between replicate species’ trials. A summary of these statistical results are presented in Table 1. To determine whether the upper and lower lethal thermal limits are correlated, we ran a Pearson correlation. The lethal thermal tolerance windows (upper – lower thermal limits) of all the species were calculated and tested for a difference between the two locations in a one-way ANOVA. All statistical analyses were performed in the statistical package Systat® version 11. 3. Results The temperature data demonstrated that the tidal flat temperatures at Roebuck Bay showed less annual variation (5.64 ± 2.05°C, mean ± SD of difference between upper and lower quartile) than the Wadden Sea (9.74 ± 2.11°C, mean ± SD of difference between upper and lower quartile) (Fig. 1). The Roebuck Bay tidal flat also attained higher maximum (32.51 ± 0.17°C, mean ± SE) and minimum (18.82 ± 0.75°C, mean ± SE) average daily temperatures relative to the Wadden Sea tidal flat (22 ± 1.14°C maximum and 1.89 ± 0.59°C minimum, mean ± SE).
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Figure 1. Annual and daily temperature variation at a tropical and temperate tidal flat. The dots represent the average daily temperature at each location. The black line represents Roebuck Bay (RB) and the grey line represents the Wadden Sea (WS). June temperatures are winter in Roebuck Bay and summer in the Wadden Sea. The boxplots show the annual temperature range. A boxplot shows 50% of the measured values, with the whiskers representing the outliers. The line in the middle of the boxplot represents the median value.
The average lethal thermal tolerance windows of the Roebuck Bay bivalve species were significantly narrower (F1,56 = 42.29, P x > 110 "m) and (3) 60 "m (110 "m> x > 60 "m) that were deployed behind a slow moving boat adjacent to the flats. The plankton was concentrated onto a Whatmann glass-fiber filter (GF/C) with a vacuum pump, and the filters frozen for storage. At low tide, a brown-green sheen progressively developed across the exposed mud flats, presumed to be diatoms moving to the surface as the tide receded. A two stage process was used to isolate the diatoms. Initially, where the browngreen colour was most strongly developed, the top few mm of material was carefully scraped and concentrated into a container for return to the laboratory. In the laboratory, the sediment was kept moist and covered by GF/C filters with glass cover slips placed on top of the filter. A light gradient was then used to attract the diatoms through the filter and onto the cover slips. The diatoms on the cover-slip were then dried and scraped into a tin-foil crucible. This process was repeated until sufficient mass was collected for isotopic determination (n = 1). Preparation and measurement of source material was done using the same methods as the tissue stable isotope analysis, except that the source material was weighed to ~5.5 mg to allow for lower carbon content.
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2.5. Analysis Isotopic mass balance equations were used to estimate the range of possible food sources contributing to the diet of each bivalve species using the Isosource model (Phillips, 2001; Phillips and Gregg, 2003). To estimate the predicted diet values of the bivalves, fractionation values of 1 ‰ !C13 and 3.4 ‰ !N15 were subtracted from the isotopic signatures of the bivalves prior to analysis. These fractionation values have been determined previously in two bivalve species (Yokoyama et al. 2005) and other organisms (Minagawa and Wada 1984, Rau et al. 1983). In the Isosource model, the diet of each species was calculated from the average isotopic food source values: plankton (60 -110 "m, 110 - 250 "m and > 250 "m), diatoms and mangrove material (i.e. POM and mangrove leaf material). Macroalgae were excluded from the model as they are rare on this tidal flat. To test whether nitrogen isotope signatures differed between feeding modes a one-way ANOVA was used. Finally, a linear regression was used to examine whether there was a significant correlation between the log gill-to-palp mass ratio and the !13C ratios of the bivalves. 3. Results At Roebuck Bay, the bivalve species were clearly differentiated into three groups based on their carbon isotope signatures (Fig. 2, Table 2). In contrast, the nitrogen isotope signatures (!15N) did not differ between the suspension (from 6.33 to 7.50 ‰) and deposit feeding modes (F1,34 = 0.075, P = 0.79, from 6.6 to 7.2 ‰, Table 2). At this site, the suspension feeders had relatively depleted carbon isotope signatures in the range of -16.2 to 17.0 ‰, and the deposit feeders had more enriched carbon isotope signatures with values in the range of -12.3 to -13.7 ‰. Notably, each species had a distinct carbon isotope signature (Fig. 2). In a single case, the lucinid bivalve (D. irpex) showed a depleted carbon isotope value of !13C -23.1 ‰, as well as a depleted nitrogen isotope value of !15N -0.9 ‰ (Fig. 2, Table 2). The Isosource model calculated the food source contributions to all bivalve species (Table 3), except for the lucinid bivalve D. irpex. Notably, the model predicted that the suspension and deposit feeding bivalves were consuming very different proportions of available food sources in this system. Specifically, all suspension feeding species consumed a large proportion of mangrove material (average POM = 24.6 % and average leaf = 24 %). Only in two suspension feeders (B. pistachia and A. squamosa) was oceanic plankton, in combination with mangrove material, an important dietary component. In the deposit feeding species, benthic diatoms were the most important diet component (average diatoms = 31 %).
68
Relationship between diet and size of the gills and palps
Figure 2. Carbon (!13C) and nitrogen (!15N) isotope signatures (with standard error bars) of the nine bivalve species and their potential food sources (mangrove leaf, mangrove particulate organic matter (POM) diatoms, and plankton (60, 110 and 250 "m). Note that the species names are abbreviated in the figure (Suspension feeders: Asq – A. squamosa, Gtum – G. tumidium, Pber – P. berryi, Agr – A. granosa, Bpis – B. pistachia and Deposit feeders: Tsp – T. spec A, Tcap – T.capsoides, Tpir – T. piratica, Lucinid bivalve – D. irpex). Macroalgae was rare on the tidal flat. The predicted diets, based on trophic fractionation steps of 1 ‰ for C13 and 3.5 ‰ for N15, of the suspension and deposit feeding bivalves are also indicated. Note that the size fractions of the oceanic plankton are abbreviated in the figure: 250 "m (> 250 "m), 100 "m (< 250 "m > 110 "m) and 60 "m (250 "m) Plankton (< 250 >110 "m) Plankton (60 "m) Diatoms
70
!13C -25.92
SE 0.68
!15N 0.93
SE 0.65
n 3
-27.49 -26.43 -24.91 -23.72 -11.04 -13.81
0.40 0.21 0.16 0.37 0.86 0.69
2.39 2.18 1.30 1.38 4.40 4.74
0.44 1.20 0.25 0.03 0.18 0.29
3 3 3 3 3 3
-19.35
0.10
7.31
0.16
4
-13.00
1.01
5.54
0.06
3
-5.51 -6.74
0.11
5.52 1.58
0.56
6 1
Relationship between diet and size of the gills and palps
The second most important dietary component for the deposit feeders was the smallest plankton fraction in two species (T. piratica and T. sp.) or mangrove particulate organic matter in a single species (T. capsoides). In this system, the carbon isotope signatures of bivalve species differed both between the suspension and deposit feeders and within each feeding mode (Fig. 3). Notably, in parallel with the clear differentiation of carbon isotope signatures, the log gill-to-palp mass ratios of the bivalves formed a gradient from suspension to deposit feeding (Fig. 3). This resulted in a significant correlation between the log gill-to-palp mass ratio and the carbon isotope signatures (R2 = 0.85, F1, 34 = 203, P < 0.01, Fig. 3). Table 4. Mean contributions (% followed by the range in brackets) of the oceanic and tidal flat food sources to the diet of each bivalve species. Values were calculated using the IsoSource mixing model by Phillips and Gregg (2003) using an increment of 1 % and a tolerance of 0.1 per mil. The size fractions of the oceanic plankton are abbreviated in the table: 250 "m (> 250 "m), 100 "m (< 250 "m > 110 "m) and 60 "m (|z|)
#
-60.04
21.1
-2.85
15 species) (Roy et al. 2001). This suggests that there is a limit to the total amount of morphospace that can be occupied, or in other words a limit to morphological differentiation. In this thesis, it appears that morphological overlap is akin to diet overlap in the species-rich system of Roebuck Bay (Chapters 3 and 4). So far, morphological overlap has only been observed in marine environments (Roy et al. 2001, Bellwood et al. 2006). Perhaps this hints at important differences in the ecological processes that maintain diversity in marine and terrestrial systems. 1.5 Thoughts on morphospace occupation Comparisons across more systems are needed to confirm whether the morphological overlap observed in Roebuck Bay is general for other tidal flat systems. To tease apart the degree to which morphological overlap is determined by food acquisition (shared diet) relative to shared ancestry (phylogeny) it could be interesting to relate morphospace occupation to both stable isotope signatures and phylogenetic information. See Latiolais et al. (2006) for a study where gastropod shell morphology has been linked to phylogeny.
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The direct correlation between the gill-to-palp mass ratio and carbon isotope signatures appears to suggest that stable isotope signatures will be an important parameter for understanding how food resources are partitioned between species. However, as only a subset of species were examined (n =6), this correlation should be verified for the entire Roebuck Bay assemblage, and other bivalve assemblages, to determine whether it is general. To explore how species might coexist within Roebuck Bay, gill-to-palp mass ratios and carbon isotope signatures could also be measured across environmental space to determine whether there is a spatial component to food acquisition that alleviates competition for food resources. As an aside, the isotope signatures from Roebuck Bay currently suggest that most bivalves are consuming a diet that partly constitutes mangrove detritus. This could suggest that mangroves are important for ecosystem functioning in Roebuck Bay. In this study, the feeding organs of bivalves (the log gill-to-palp ratio) are shown to be a useful functional trait for comparing bivalve assemblages and diet relationships. Other work has also shown that the log gill-to-palp ratio is a useful trait for comparing a single species across space and time (Theisen 1982, Essink 1991, Payne et al. 1995a, Payne et al. 1995b, Barille et al. 2000, Honkoop et al. 2003, Drent et al. 2004). The knowledge that the log gillto-palp mass ratio is a trait that reflects the feeding environment of bivalves opens up many avenues for future research. For example, comparisons of bivalve morphology along other environmental axes (e.g. latitude, depth, primary productivity) may be useful in understanding how species coexist in sedimentary systems. 2. Distributional approach 2.1 Habitat selection Habitat selection would suggest that tropical species require more habitat heterogeneity to coexist. To examine whether habitat selection is occurring in tidal flat systems we compared the distributions of three bivalve species at six European tidal flat systems. We assumed that if a species has a similar sediment preference across systems, it must be selecting its habitat. Sediment grain size is a measure of the mediated effects that are likely to affect habitat suitability (see Chapter 5 and Snelgrove & Butman 1994, Thrush et al. 2005). Support for a habitat selection process is found in all three species. Specifically, the distributions of adult and juvenile C. edule did not differ and occurred in sandy sediment types. Adult and juvenile S. plana also did not differ and preferred muddy sediments. In C. edule and S. plana it is not clear whether habitat selection is active via byssal migration or whether there is another habitat selection process that leads to similar distributions between adults and juveniles. The distributions of juvenile M. balthica differed to the adults at three of the six studied systems. The observation that the juvenile distributions differed relative to the
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adults fits with expectation, as it is known that juvenile M. balthica actively migrate to higher and often muddier tidal flat areas to avoid predation (Beukema & de Vlas 1989, Beukema 1993, Bouma et al. 2001a, Bouma et al. 2001b, Beukema & Dekker 2003), and also that migration strategies differ in timing between systems (Bouma et al. 2001a, Bouma et al. 2001b). We thus infer that the observed distributional differences between adult and juvenile M. balthica indicate active habitat selection. This study suggests that habitat selection occurs widely in bivalve species from coastal sedimentary systems. As sediment is only a proxy for habitat selection, the factors affecting habitat selection should be investigated further. Habitat selection is probably a means for juveniles to select habitats that have an optimum combination of: (1) low predation pressure, (2) high food concentrations, (3) low competition and/or (4) favourable abiotic factors for survival. In addition, experiments across multiple systems should explore whether habitat selection processes are similar between systems or reflect different factors that lead to the same patterns. 2.2 Habitat heterogeneity Species diversity is expected to be correlated with habitat heterogeneity (Simpson 1949, Dobzhansky 1950, Pianka 1966, MacArthur & Wilson 1967). Greater habitat heterogeneity could either provide more niche space for species and/or enable greater coexistence. To examine whether species richness is related to sediment heterogeneity, the species richness of a local system was correlated with local sediment heterogeneity. In addition, to explore how species diversity is distributed within a local system, alpha diversity was examined with respect to sediment particle size. To examine this hypothesis we compared three tropical tidal flat systems and six temperate tidal flat systems. Surprisingly, across the three tropical and six temperate systems of this study, species richness and sediment heterogeneity were not correlated. Nevertheless, two systems with the lowest species richness (Aiguillon Bay and Eighty-mile Beach) also had the smallest range of sediment heterogeneity. At Aiguillon Bay, the low bivalve diversity may be a result of poor living conditions in structurally homogenous fine clays and muds (Gray 1981, Thrush et al. 2003). At the tropical Eighty-Mile Beach, the low bivalve diversity and sediment heterogeneity may be due to its unprotected position towards the open ocean (Piersma et al. 2005), suggesting a physically harsh environment (Gray 1981). Instead of habitat differentiation, bivalve species showed distributional overlap within a local system, i.e. alpha diversity was highest towards fine-grained sediments. This observation is in agreement with other studies from sedimentary systems (Biernbaum 1979, Whitlatch 1981, Etter & Grassle 1992). Distributional overlap might suggest that species are facilitating their own coexistence via positive interactions and feedback loops (Etter & Grassle 1992, Meysman et al. 2006). Positive interactions have been observed widely in
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benthic communities, especially where individual species or functional groups are capable of modifying habitat structure and nutrient dynamics (Bertness & Leonard 1997, Thrush & Dayton 2002, Lohrer et al. 2004, Solan et al. 2004, Hewitt et al. 2005, Coco et al. 2006, Thrush et al. 2008). In the systems from this study positive interactions could be due to (1) the bivalve species facilitating their own coexistence or (2) the habitat of the bivalve species being reworked by another functional group resulting in positive feedbacks for the bivalves. Although negative interactions have been observed previously in tidal flat systems (Rhoads & Young 1970, Black & Peterson 1988, Ólafsson et al. 1994), it has been noted that positive interactions are often detected at large spatial scales because they reflect processes that interact across scales (Bruno & Bertness 2001, Bruno et al. 2003, Thrush et al. 2008). 2.3 Thoughts on the habitat heterogeneity hypothesis and tidal flat systems The hypothesis that habitat heterogeneity of a total system is correlated to species diversity is not supported by this analysis. However, there are still other ways that this hypothesis could be explored. For example, a combination of environmental (tidal height, current speed), structural (shell debris) and biological (mangroves, seagrasses) variables could act together to create greater habitat heterogeneity in tropical than temperate systems. This would need to be explored further before we could reject the habitat heterogeneity hypothesis. It has been proposed by Hewitt et al. (2007) that to understand emergent patterns scientists should nest manipulative field studies within a correlative framework. In this context, the significant correlations between alpha diversity and sediment observed in the systems of this study should be explored further using an experimental approach and additional correlation analyses. Perhaps the emergent pattern of alpha diversity and sediment particle size reflects different processes that act across the systems (mediated effects sensu Thrush et al. 2005). For example, different benthic species may have key functional roles that need to be filled in tidal flat systems for optimal diversity and ecosystem functioning. 3. Synthesis In this thesis, I explore the hypothesis that a lower physiological cost of living in the tropics, in combination with increased ecological opportunities and resource limitation, leads to greater differentiation of tropical species relative to temperate species (Dobzhansky 1950, Vermeij 2005). I find support for the proposition that tropical species are adapted to a narrower range of climatic variability, suggesting they might have a lower physiological cost of living relative to temperate species (Dobzhansky 1950). However, morphological overlap is observed in the tropical bivalve assemblage, instead of functional differentiation. In addition, species richness within a system is concentrated towards fine-grained sediment
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types, suggesting species share a large degree of distributional overlap. The observation of morphological and distributional overlap in the tidal flat of Roebuck Bay appears to be at odds with the expectation of greater species differentiation in diverse systems. In the context of local tidal flat diversity either these results suggest that functional differentiation is not important for diversity or that we have not measured the ‘right’ trait and distributional axes to find functional differentiation. The latter possibility is a general problem in ecology and raises the question of whether we might throw the ‘baby away with the bathwater’ if we firstly do not attempt to understand what overlap means for species coexistence; especially as here parameters that influence bivalve fitness are measured (the feeding organs and sediment). Another possibility may be that functional differentiation is important in some systems but not all. For example, organisms on the rocky intertidal are known to be subject to intense competition for food and space (Connell 1961a, b), whereas in sedimentary systems exploitative competition is arguably not as important because there is relatively more food and space available (Peterson & Beal 1989, Peterson 1991). If functional differentiation is dependent on the system, it suggests that it is not a general theory that can be used to explain differences in diversity. Interestingly, the hypothesis that ‘niche breadths’ are narrower in the tropics was also found to be subject to exception (Vazquez & Stevens 2004). This raises a general conundrum, similar to that raised for community ecology (Lawton 1999), of whether diversity theories are contingent and whether there are any general ‘laws’. Although, the ultimate causes of diversity may be difficult to elucidate – it can be argued that our understanding of diversity is a ‘bellwether of our understanding of ecological systems’ (Ricklefs 2004). Before the 1960s diversity theory was dominated by ideas from community ecology that emphasized interactions between coexisting species and the physical environment as factors that constrain species richness (see review by Ricklefs 2004). Since the 1960s ecologists accepted that communities are connected and that individuals move between patches, e.g. metapopulations (Hanski & Gilpin 1997) and supply-side ecology (Roughgarden et al. 1987). But the different spatial and time scales of diversity have only recently started to receive attention (see review by Ricklefs 2004). Diversity of a local assemblage thus reflects the influence of historical, regional and local factors (see Fig. 1).
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Figure 1. A flow diagram depicting how historical, regional and local factors are all related to diversity. Historical factors reflect the ‘deep time history’ effects on diversity. Regional diversity reflects the unique geological and other attributes that describe a region. Historical and regional events should influence the total pool of species available. Across a region environmental gradients can be expected to affect diversity, e.g. sharp temperature discontinuities may act as a barrier to dispersal. Within a region, the movement of larvae between systems, via e.g. oceanographic currents, should result in either an increase or decrease in local diversity. Regional diversity can also be enhanced by the diversity of a local system. Some local systems will hold more species than others, e.g. systems with increased productivity, habitat diversity etc. Within a local system diversity, diversity will be facilitated by, e.g. positive interactions between species.
Recognising this ecologists are faced with the problem of having to reconcile the disparate scales of diversity (Ricklefs 2004). In this thesis we miss a large part of the picture, as we do not have a clue about species diversity in the other tidal flats of the Indo-Pacific. These results thus provide a useful first step, but to really understand the causes of high diversity in Roebuck Bay we need to consider exploring other tidal flats in the Indo-Pacific. For example, it is known that the Indo-Pacific region is a hotspot of diversity (Briggs 1992, 1999b, a, 2000, 2004, 2005), and that many species in Roebuck Bay are rare (both infrequent and also low in abundance) and known to occur in adjacent Indo-Pacific sites (Kastoro et al. 1989). The high level of rarity in Roebuck Bay might suggest that it is a system receiving larvae from other
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systems in the Indo-Pacific. In the context of morphological overlap, a high turnover of species in Roebuck Bay might suggest that species are not in direct competition and thus do not need to become functionally differentiated to coexist. Recognising that regional and historical factors are important for diversity makes the job of an ecologist difficult, as there is no single hypothesis that can explain diversity. Instead, latitudinal patterns of diversity will probably remain a popular way to explain diversity because of the relative ease with which diversity can be explored and explained. However, this will continue to drive the ‘flurry’ of ideas that try to explain diversity (Ricklefs 2004)! In reality, we should integrate information about diversity using the new tools and approaches that are available (see books by Lomolino & Heaney 2004, Lomolino et al. 2006). The goal should be to develop hypotheses for diversity that are more amenable to direct measurement and lead to generalisations that are more solidly grounded in the processes that produce them (Ricklefs 2004). In the context of tidal flat systems, this means there is a lot of work to be done, especially as many systems are unstudied. The role of larval dispersal and the role of local habitats in harbouring diversity would be important first steps in understanding diversity of tidal flats. Investigation of tidal flat diversity can be considered a priority, as tidal flat systems are under immense pressure from anthropogenic factors like urbanisation (high sedimentation, pollutant and nutrient loads) and fisheries (Europe and Asia). References Aarset AV (1982) Freezing tolerance in intertidal invertebrates (a review). Comp Biochem Phys 73A:571-580 Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc Royal Soc B 267:739-745 Barille L, Haure J, Cognie B, Leroy A (2000) Variation in pallial organs and eulatero-frontal cirri in response to high particulate matter concentrations in the oyster Crassostrea gigas. Can J Fish Aquat Sci 57:837-843 Beesley PL, Ross GJB, Wells A (1998) Mollusca: The Southern Synthesis, Part B. CSIRO publishing, Melbourne Bellwood DR, Wainwright PC, Fulton CJ, Hoey AS (2006) Functional versatility supports coral reef biodiversity. Proc R Soc B 273:101-107 Bertness MD, Leonard GH (1997) The role of positive interactions in communities: Lessons from intertidal habitats. Ecology 78:1976-1989 Beukema JJ (1993) Successive changes in distribution patterns as an adaptive strategy in the bivalve Macoma balthica (L.) in the Wadden Sea. Helgolander Meeresun 47:287-304
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Schoener TW (1971) Large-billed insectivorous birds - precipitous diversity gradient. Condor 73:154-160 Schum M (1984) Phenetic structure and species richness in north and central American bat faunas. Ecology 65:1315-1324 Simpson EH (1949) Measurement of diversity. Nature 163:688 Smartt RA (1978) Comparison of ecological and morphological overlap in a Peromyscus community. Ecology 59:216-220 Snelgrove PVR, Butman CA (1994) Animal sediment relationships revisited - cause versus effect. Oceanogr Mar Biol Annu Rev 32:111-177 Snyder GK, Weathers WW (1975) Temperature adaptations in amphibians. Am Nat 109:93101 Solan M, Cardinale B, Downing A, Englehardt K, Ruesink L, Srivastava D (2004) Extinction and ecosystem function in the marine benthos. Science 306:1177 - 1180 Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: Optima, limits, and costs of living. Int Comp Biol 42:780-789 Stevens GC (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am Nat 133:240-256 Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of Eastern Pacific Porcelain crabs, Genus Petrolisthes: Influences of latitude, vertical zonation, acclimation and phylogeny. Physiol biochem zool 73:200-208 Theisen BF (1982) Variation in size of gills, labial palps, and adductor muscle in Mytilus edulis L. (Bivalvia) from Danish waters. Ophelia 21:49-63 Thompson JK, Nichols FH (1988) Food availability controls seasonal cycle of growth in Macoma balthica (L.) in San Francisco Bay, California. J Exp Mar Biol Ecol 116:4361 Thrush S, Coco F, Hewitt JE (2008) Complex positive connections between functional groups are revealed by neural network analysis of ecological time series. Am Nat 171:669 - 677 Thrush SF, Dayton PK (2002) Disturbance to marine benthic habitats by trawling and dredging: Implications for marine biodiversity. Ann Rev Ecol Syst 33:449-473 Thrush SF, Hewitt JE, Herman PMJ, Ysebaert T (2005) Multi-scale analysis of speciesenvironment relationships. Mar Ecol Prog Ser 302:13-26 Thrush SF, Hewitt JE, Norkko A, Nicholls PE, Funnell GA, Ellis JI (2003) Habitat change in estuaries: predicting broad-scale responses of intertidal macrofauna to sediment mud content. Mar Ecol Prog Ser 263:101-112 Vazquez DP, Stevens RD (2004) The latitudinal gradient in niche breadth: Concepts and evidence. Am Nat 164:E1-E19
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Vermeij GJ (1978) Biogeography and Adaptation: Patterns of marine life. Harvard University Press, Cambridge MA Vermeij GJ (2005) From phenomenology to first principles: toward a theory of diversity. Proc Cal Acad Sci 56:12-23 Vermeij GJ, Currey JD (1980) Geographical variation in the strength of Thaidid snail shells. Biol Bull 158:383-389 Vernberg FJ, Tashian RE (1959) Studies on the physiological variation between tropical and temperate fiddler crabs of the genus Uca .1. Thermal death limits. Ecology 40:589593 Whitlatch RB (1981) Animal-sediment relationships in intertidal marine benthic habitats: some determinants of deposit-feeding species diversity. J Exp Mar Biol Ecol 53:31 45 Wiens JA, Rotenberry JT (1980) Patterns of morphology and ecology in grassland and shrubsteppe bird populations. Ecol Monograph 50:287-308 Wiens JA, Rotenberry JT (1981) Morphological size ratios and competition in ecological communities. Am Nat 117:592-599 Winemiller KO (1991) Ecomorphological diversification in lowland fresh-water fish assemblages from 5 biotic regions. Ecol Monograph 61:343-365
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Summary 1. Global biodiversity The peak of species diversity in tropical areas has mystified temperate European scientists since the exploration of the new world lead to the discovery of so many new species. The latitudinal gradient in diversity has since become a hot topic of discussion with debate about its generality and the processes that maintain it. Nowadays, more than 25 hypotheses have been dreamed up to explain the latitudinal gradients in biodiversity. In the last decade, the use of the word latitude has started to loose ground, as latitude per se is quite a weak representation of many correlated variables, e.g. local deep time history and climate. In addition, new multi-dimensional approaches and techniques are describing emergent patterns that are changing how we perceive species diversity. New approaches have been stimulated in part by the advent of powerful computers and the internet (enabling the growth of on-line diversity databases, OBIS and GBIF, and genetic databases, see books by Lomolino & Heaney 2004, Lomolino et al. 2006). Species diversity has predominantly been explored using a single parameter – species richness. But species richness is limited in what it can tell us about adaptation. Instead, species traits are more useful for identifying how a species is adapted to life in a diverse environment. A well-known example of the traits ‘doing the talking’ is gastropod shells. In tropical gastropods, shell thickness is generally thicker than in temperate species, and is correlated with higher predation rates (Vermeij 1978). In summary, a combination of approaches has stimulated a boom in scientific exploration of species diversity! However, on the other side of the coin, much elementary descriptive and comparative work needs to be done, especially in tropical systems that have received little scientific attention, e.g. marine tidal flats. 2. Marine tidal flat systems need our attention! In stark contrast to the wide distribution of sedimentary systems in the deep-sea and along coastal margins, there is a lack of description and understanding of the processes that maintain diversity in these systems (Snelgrove 1998, Rex et al. 2005). In an on-going approach to explore tropical tidal flats, there has been extensive research carried out in both Roebuck Bay and the Banc d’ Arguin for the last fifteen years by T. Piersma and his group. These sites have been identified on the basis of their role as shorebird stop-over sites, but are also of importance for their high macrobenthic species diversity. Recognizing that tropical tidal flat systems need much more attention globally, and that it would be ideal to have more systems in this study, we explored tropical and temperate bivalve diversity to determine if we can find emergent patterns that might be suggestive of processes that maintain bivalve
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diversity. Marine bivalves are often considered a model organism for examining diversity because they are an important component of virtually all habitats and they have an extensive fossil record. In marine tidal flat systems, bivalves often constitute a large proportion of the total biomass and perform important ecosystem functions, e.g. being a crucial link in food chains or maintaining water quality. A variety of different approaches for exploring tidal flat diversity should provide insights to how species are adapted and coexist in systems of differing diversity. I hope this thesis will act as a baseline for future trait and distribution comparisons across large spatial scales in tidal flat systems. 3. Cost of living lower in the tropics? Based on the hypothesis that in the tropics there is a lower physiological cost of living, increased ecological opportunities and resource limitation between species, it might be expected that tropical species are more differentiated in their morphology and their habitat differentiation than temperate species (Dobzhansky 1950, Vermeij 2005). To examine whether this could have merit to understand species diversity in tidal flat systems, I used a trait and a distributional approach to explore adaptation and coexistence between species. 3.1 Trait approach: (1) The thermal tolerance ranges of bivalves from tropical and temperate tidal flats to determine whether species have narrower physiological tolerance ranges in the tropics suggesting that tropical species have lower physiological costs and have more the capability of diversifying along other niche axes. (2) The feeding organs of bivalves from a tropical and temperate tidal flat system to identify whether functional differentiation was greater in the tropics. Feeding organs were also examined in relation to stable isotope signatures of diet. 3.2 Distributional approach: (3) Habitat selection in European species. Habitat selection would suggest that tropical species would require more habitat heterogeneity to coexist in diverse systems. (4) Habitat differentiation of bivalve species within local assemblages across three tropical and six temperate tidal flat systems. 4. Traits: The cost of living indeed appears to be cheaper in the tropics Consistent with the climate variability hypothesis, we found narrower thermal tolerance ranges at the tropical system than in the temperate system. In addition, we observed that tropical species appear to be living closer to their maximum field temperatures than
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temperate species, suggesting that they do not have a large safety buffer to deal with temperature variation. Bivalves, perhaps not surprisingly, are adapted to local temperature variation! This is consistent with the notion that diversity might be limited in temperate regions because variable climates require a greater amount of physiological flexibility to survive relative, ultimately limiting adaptation and speciation (Dobzhansky 1950). 5. Traits: Tropical bivalves are NOT functionally differentiated The feeding organs, the gills and palps, of bivalves showed a large degree of morphological overlap in the tropical system of Roebuck Bay relative to the temperate Dutch Wadden Sea. A direct correlation between the feeding organs of the bivalves and their diet signature, as determined by carbon isotopes, also support the proposition that morphological overlap is synonymous with diet overlap. It thus appears that competition for food may not be important for functional differentiation in this diverse system. This is in disagreement with the notion that competition between species should lead to an increased division of labour, specialization and functional differentiation, in diverse systems (Vermeij 2005). Morphological overlap has previously been observed in other marine systems, fishes and gastropod shells. From these studies, it has been suggested that there may be a limit to morphological diversity (Roy et al. 2001) and that tropical species may coexist by being versatile in their feeding behaviour (Bellwood et al. 2006), which perhaps alleviates any morphological or physiological limits reached to functional differentiation. As an aside, it has also been observed that morphological diversity is not always directly correlated with species richness (Roy et al. 2001), suggesting that morphological diversity also reflects phylogenetic diversity. 6. Distributions: Habitat selection The adult and juvenile distributions of three European bivalve species showed support for a habitat selection process across six tidal flats. The juveniles and adults of Cerastoderma edule and Scrobicularia plana showed similar distributions. In Macoma balthica juveniles and adults showed habitat separation, consistent with the migration strategy of the juveniles of this species to settle as spatfall at higher tidal levels to avoid epibenthic predation, and later to migrate down shore to benefit from improved food conditions (Beukema 1993). In further support of a habitat selection process, the adult bivalves showed repeatable distributions across systems, i.e. C. edule preferred sandy sediments, whereas M. balthica and S. plana preferred muddy sediments. Preferential selection for specific sediment types was observed across systems, suggesting that specific sediment types might be associated with increased fitness and/or survival. As sediment is only a proxy for habitat, the factors affecting
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habitat selection should be investigated further. Habitat selection is probably a means for juveniles to select habitats that have an optimal combination of: (1) low predation pressure, (2) high food concentrations, (3) low competition and/or (4) favourable abiotic factors for survival. 7. Distributions: Habitat heterogeneity Instead of habitat differentiation, bivalve species showed a large degree of distributional overlap within a local system, i.e. species richness per sample point (alpha diversity) was greatest towards fine-grained sediments. Distributional overlap might suggest that there are physical or biological factors that lead to coexistence rather than habitat differentiation. For example, fine-grained sediments may be a favourable habitat for most bivalve species, e.g. due to higher food concentrations (Levinton 1987) or increased habitat space and food levels that are created by sediment reworking and positive feedback loops (Etter & Grassle 1992, Meysman et al. 2006). Distributional overlap is contrary to the expectation that species coexistence in diverse systems should be facilitated by greater habitat diversity and differentiation between species in environmental space. 8. Synthesis – What do these results mean for the understanding of tidal flat diversity? The results in this thesis support the notion that tropical species are adapted to a narrower range of climate variation than temperate species, suggesting that species have a wider capability to diversify than temperate species. However, the results in this thesis are not consistent with the proposition that tropical species are more differentiated than temperate species. Instead, the tropical bivalve assemblage of Roebuck Bay shows morphological overlap and all systems show a large degree of distributional overlap, with respect to the sediment gradient at each system. The results in this thesis could suggest that: - functional differentiation is not important for bivalve diversity in the tidal flat of Roebuck Bay, - other morphological and/or environmental factors than the feeding organs of bivalves or sediment particle size are more important for maintaining coexistence between species in tropical systems, - an alternative hypothesis could be posed for increased local diversity of tidal flat systems: for example: Positive interactions between species and positive feedback loops enable coexistence in diverse tidal flat systems, i.e. that ‘biodiversity begets biodiversity’ and that conditions for this to build up have been found especially in tropical intertidal areas.
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More work should be done to understand these diverse coastal tidal flat systems, especially as many of these systems are under threat from urbanisation (increased sedimentation, nutrient and other chemical loads) and overfishing (worldwide, but especially in Asia and Europe).
Samenvatting 1. Biodiversiteit Sinds de ontdekking van zoveel nieuwe soorten tijdens de exploratie van de nieuwe wereld heeft de hoge tropische soorten diversiteit de europese wetenschappers voor raadsels gesteld. Deze gradiënt in diversiteit die gerelateerd is aan de breedtegraad is sindsdien het onderwerp geworden van verhitte discussies. Hierbij staan meer specifiek de algemene regel waarbij de gradiënt aan soorten diversiteit aan de breedtegraad wordt gerelateerd en de processen die deze gradiënt in stand houden ter discussie. Tot nog toe zijn meer dan 25 mogelijke veronderstellingen geopperd om dit fenomeen te verklaren. In de laatste 10 jaar begint het relateren van dit fenomeen aan de breedtegraad zelf aan grond te verliezen omdat de breedtegraad slechts een representatie is van vele aan de breedtegraad gecorreleerde variabelen, zoals bijvoorbeeld de natuurlijke historie en klimaat. Verder verschaffen nieuwe technieken en een benadering van het fenomeen vanuit meerdere dimensies ons met nieuwe ideeen over hoe we over soorten diversiteit denken. Nieuwe benaderingen zijn voornamleijk gestimuleerd door de opkomst van internet en steeds krachtiger computers en hiermee de groei in het aantal databases zoals OBIS en GBIF zie voor meer informatie hierover de boeken van Lomolino & Heaney (2004) en Lomolino et al. (2006). Tot nog toe heeft het onderzoek naar de diversiteit in soorten zich voornamelijk bediend van slechts een enkele parameter, namelijk soorten rijkdom. Echter het aanpassings vermogen van soorten kan ons meer vertellen over het ontstaan van de diversiteit in soorten dan de parameter “soorten rijkdom” zelf. Om het aanpassings vermogen van soorten aan het leven in een divers milieu te onderzoeken zijn eigenshappen specifiek voor dat soort beter bruikbaar. De schelpen van gastropoden zijn een bekend voorbeeld van zo’n eigenschap die ons iets zou kunnen vertellen over diversiteit. De dikte van de schelp in tropische gastropoden zijn vaak dikker dan die van gastropoden die in een meer gematigd klimaat leven en deze dikte is afhankelijk van de kans dat een gastropod door een roofdier wordt gegeten (Vermij 1978). Alles samengevat, een combinatie van benaderingen heeft het wetenschappelijk onderzoek naar de diversiteit in soorten in een stroom versnelling gebracht. Alhoewel niet moet worden vergeten dat het beschrijvende en vergelijkende werk dat aan de basis van veel onderzoek staat uiterst belangrijk is. Het beschrijvende en vergelijkende werk is vooral belangrijk voor tropische systemen die nog weinig wetenschappelijke belangstelling hebben gehad zoals bijvoorbeeld de getijde systemen.
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2. Getijde systemen hebben onze aandacht nodig! Alhoewel sedimentatie systemen wijd zijn verspreid, van de diepzee tot aan de getijde systemen in de kust gebieden, is er toch nog weinig bekend over de processen die een rol spelen in het behouden van de diversiteit aan soorten in zulke systemen (Snelgrove 1998, Rex et al. 2005). Echter, gedurende de laatste 15 jaar is er door T. Piersma en zijn groep uitgebreid onderzoek gedaan naar tropische sedimentatie systemen in Roebuck Bay en Banc d’ Arguin. Het zijn specifiek deze systemen die veel aandacht krijgen vanwege hun rol in de migratie van kust vogels en vanwege de hoge diversiteit aan macrobentische soorten. Wetend dat we meer kennis moet hebben over tropische sedimentatie systemen wereldwijd hebben wij ons toegelegd op het onderzoek van de diversiteit van schelpdieren in zowel tropsiche als gematigde sedimentatie gebieden om te zien of we patronen kunnen relateren aan processen die invloed hebben op de diversiteit van deze schelpdieren. Zout water schelpdieren worden over het algemeen als een goed model gezien om onderzoek naar diversiteit te verrichten, niet alleen omdat ze wijd verspreid voorkomen maar ook omdat er door de grote hoeveelheid fosiel materiaal veel kennis is over het verleden van schelpdieren. Schelpdieren vormen in veel sedimentatie system een belangrijke deel van de totale hoeveelheid biomassa en spelen een belangrijke rol in het functioneren van ecosystemen, bijvoorbeeld als een onderdeel van de voedselketen maar ook in het behouden van een goede kwaliteit water. Verschillende benaderingen van het onderzoek naar diversiteit in sedimentatie systemen met uiteenlopende aantallen aan soorten moet ons inzicht geven in hoe soorten zich aanpassen en naast elkaar kunnen voortbestaan. Ik hoop dat dit proefschrift als een basis kan dienen voor toekomstig onderzoek dat gebruik maakt van gegevens over de kenmerken en ruimtelijke verspreiding van soorten over meerdere sedimentatie systemen. 3. Is het energetische gemakkelijker om in de tropen te leven? Gebaseerd op de hypothesen dat (i) het energetisch gemakkelijker is om in de tropen te leven, (ii) er meer ecologische mogelijkheden zijn in de tropen en (iii) er over het algemeen een limitatie is aan voedsel, wordt in het algemeen verwacht dat er in de tropen meer soorten zijn die verschillen in hun morfologie en in de specifieke omgeving waarin ze leven dan in een gematigde omgeving (Dobzhansky 1950, Vermeij 2005). Om te onderzoeken of deze hypothesen gebruikt kunnen worden in het onderzoek naar de soorten diversiteit in sedimentaire systemen heb ik gebruik gemaakt van een methode gebaseerd op soort specifieke eigenschappen en de verspreiding van soorten om onderzoek te doen aan soort aanpassing en hoe verschillende soorten in een sedimentair systeem samen kunnen leven.
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3.1 Soort specifieke eigenschappen werden onderzocht: (1) De temperatuur gradient waarin twee kleppigen kunnen leven werd zowel voor tropsiche als gematigde twee kleppigen onderzocht. Het idee is dat als tropische soorten een kleinere tolerantie begrenzing voor temperatuur hebben dan hebben ze minder energie nodig om zich fysiologisch aan extreme temperaturen aan te passen. Deze energie kunnen ze dan dus gebruiken om zich op andere vlakken aan hun omgeving aan te passen. (2) De voedings organen van zowel tropsiche als gematigde twee kleppigen werden onderzocht om te zien of er functionele verschillen waren en of de diversiteit in deze functionele verschillen groter was in een tropische omgeving. Ook werd het verband tussen deze voedings organen en het dieet van de twee kleppigen onderzocht door de concentraties aan stabiele koolstof en stikstof isotopen in de voedings organen te relateren aan de concentraties die in het dieet gevonden werden. 3..2 De verspreiding van soorten (3) Habitat selectie in Europese soorten. Indien twee kleppigen inderdaad hun habitat selecteren dan zou men verwachten dat het habitat van tropische soorten meer divers zou moeten zijn dan het habitat van gematigde soorten. Dit omdat de tropische habitats veel meer soorten moeten herbergen dan de gematigde habitats. (4) Een vergelijking van de verspreiding van soorten over verschillende habitats tussen drie tropische en zes gematigde getijde systemen. 4. Soort specifieke eigenschappen: de energetische kosten lijken inderdaad lager te zijn in een tropische omgeving De temperatuur gradient waarin tropische twee kleppigen kunnen leven is inderdaad kleiner dan voor de soorten in gematigde systemen. Verder ontdekten we dat tropische soorten veel dichter bij hun maximum temperatuur leven dan de gematigde soorten. Dit betekent dat ze geen grote buffer hebben om variatie in temperatuur naar boven toe te kunnen overleven. Het is misschien geen verassing dat uit deze resultaten blijkt dat twee kleppigen zich sterk hebben aangepast aan het lokale klimaat waarin zij leven. Het betekent ook dat de diversiteit in twee kleppigen in gematigde gebieden kleiner is omdat de gematigde soorten meer energie moeten steken in hun fysiologische flexibiliteit om zich aan de grote variatie in het gematigde klimaat aan te passen. Deze hogere energetische kosten voorkomt dat twee kleppigen in gematigde gebieden energie kunne steken in een hogere mate van specialisatie en verdere aanpassing aan hun leef omgeving (Dobzhansky 1950).
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5. Soort specifieke eigenschappen: de voedings organen van tropische twee kleppigen zijn functioneel niet verschillend van elkaar De voedings organen van twee kleppigen, de gills en de palps, in het tropische Roebuck Bay laten een grote mate van morfologische overeenkomst zien in vergelijking met de voedings organen van de twee kleppigen in de gematigde Nederlandse Wadden Zee. Een directe correlatie tussen de morfologie van de voedings organen en het dieet van de twee kleppigen, zoals we aan hebben getoond met stabiele koolstof isotopen, laat zien dat het dieet van de twee kleppigen direct gekoppeld is aan de morfologie van de voedings organen. Dit betekent dat de competitie voor voedsel waarschijnlijk geen belangrijke drijfveer vormt voor de functionele differentiatie van de voedsel organen in de twee kleppigen van Roebuck Bay. Deze waarneming komt niet overeen met het idee dat competitie tussen soorten zou leiden tot een toename in het scheiden van arbeid, specialisatie en functionele differentiatie in een omgeving die rijk is aan verschillende soorten (Vermeij 2005). Morfologische overeenkomst tussen verschillende soorten is eerder waargenomen in het marine milieu, zowel bij vissen als bij gastropoden. Deze studies suggereerden dat er een limiet is aan de mate waaraan soorten morfologisch kunnen verschillen (Roy et al. 2001) en dat een groot aantal tropische soorten samen kunnen leven door variatie in hun gedrag met betrekking tot het verkrijgen van voedsel (Bellwood et al. 2006), waardoor grensen in het aanpassings vermogen betreffende hun morfologie en fysiologie geen onoverkomelijk probleem vormt. Verder is het al eerder opgemerkt dat diversiteit in morfologie niet altijd correleerd met soorten rijkdom (Roy et al. 2001), wat suggereert dat diversiteit in morfologie niet alleen wordt veroorzaakt door omgevings factoren maar dat er ook een zeker fylogenetische invloed is. 6. De verspreiding van soorten: de keuze van een leef omgeving De verspreiding van de volwassenen en de onvolwassenen van drie soorten twee kleppigen over zes verschillende getijde gebieden laat zien dat twee kleppigen hun leef gebied selecteren. De volwassen en onvolwassen Cerastoderma edule en Scrobicularia plana vertonen dezelfde verspreiding. De volwassen en onvolwassen Macoma balthica vertonen een verschillende verspreiding. Dit verschil in verspreiding hadden we verwacht aangezien de onvolwassen M. balthica zich in hoger gelegen getijde gebieden vestigen om predatie te voorkomen. In een later stadium migreert M. balthica dan naar lager gelegen getijde gebieden om gebruik te kunnen maken van de betere voedsel condities (Beukema 1993). Wat verder het idee ondersteunt dat de twee kleppigen hun leef omgeving selecteren is de gelijke distributie van de volwassen twee kleppigen in elk onderzocht getijde gebied. Zo was het duidelijk dat C. edule een voorkeur heeft voor een zanderige omgeving terwijl M. balthica en S. plana duidelijk een voorkeur hebben voor een meer modderige omgeving. Het selecteren
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van zekere typen sediment door de verschillende soorten twee kleppigen in alle onderzochte getijden gebieden suggereert dat twee kleppigen aangepast zijn aan een specifieke leef omgeving en daar beter overleven. Aangezien sediment slechts een aanwijzing is voor hoe zo’n habitat er inderdaad uit ziet is het noodzakelijk dat andere factoren die correleren aan sediment en van belang zijn voor twee kleppigen onderzocht worden. Het selecteren van een bepaalde leef omgeving is voor de onvolwassen twee kleppigen van groot belang omdat ze zo een optimale keuze kunnen maken waarbij ze verschillende factoren zoals: (1) een lage predatie, (2) veel voedsel, (3) weinig concurrentie, (4) andere abiotische factoren die voor overleving van belang zijn, af kunnen wegen. 7. Verspreiding: de verscheidenheid van een habitat In plaats van dat verschillende soorten twee kleppigen in verschillende habitats leven blijkt het dat er een grote mate van overeenkomst is in de habitat waarin de verschillende soorten leven binnen een getijde systeem, met andere woorden de soorten rijkdom per monster punt (alpha diversiteit) was het grootste in de fijne sedimenten. De overeenkomst in de verspreiding van twee kleppigen suggereert dat de nadelen van het samenleven met andere soorten onderdoen voor de voordelen van zekere fysische en biologische factoren. Bijvoorbeeld, fijne sedimenten kunnen een uitstekende habitat vormen voor de meeste twee kleppigen doordat er bijvoorbeeld meer voedsel gevonden kan worden (Levinton 1987) of doordat er meer verschillende habitats zijn doordat organismen het sediment bewerken (Etter & Grassle 1992, Meysman et al. 2006). Over het algemeen is een overeenkomst in de verspreiding van soorten onverwacht aangezien het idée is dat een habitat met een grotere verscheidenheid aan leef omgevingen meer verschillende soorten kan herbergen. 8. Synthese – Wat betekenen deze resultaten voor ons begrip van de soorten diversiteit van een getijde systeem? De resultaten beschreven in dit proefschrift laat zien dat tropische soorten inderdaad zijn aangepast aan een kleinere klimaat variabiliteit dan de gematigde soorten. Dit suggereert dat de tropische soorten meer energie kunnen steken in specialisatie resulterend in een hogere soorten diversiteit dan gevonden wordt in gematigde gebieden. Echter, de resultaten in dit proefschrift komen niet overeen met dit idee. In plaats daarvan zien we dat de verschillende soorten twee kleppigen in Roebuck Bay een sterke overeenkomst in hun morfologie vertonen. Daarnaast zien we, wanneer je verschillende getijde systemen vergelijkt, dat twee kleppigen zich op eenzelfde manier over verschillende sedimenten verspreiden. De resultaten van dit proefschrift sugereren dan ook dat:
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- functionele diverentiatie is niet belangrijk voor de diversiteit van twee kleppigen in Roebuck Bay - andere morfologische en/of omgevings factoren dan de voedings organen van de twee kleppigen en de deeltjes grootte van het sediment zijn belangrijk om verschillende soorten samen te laten leven in tropische systemen - een alternative hypothese om een verhoogde locale diversiteit aan soorten te verklaren kan bijvoorbeeld zijn dat positieve interacties tussen soorten en positieve terug koppeling er voor zorgen dat vele verschillende soorten samen kunnen leven in getijde systemen, in andere woorden “biodiversiteit veroorzaakt biodiversiteit” en dat tropische getijde systemen daar een ideale locatie voor zijn. Er moet meer werk verricht worden om de ecologie in al deze diverse kust gebieden te kunnen begrijpen en het is zaak om daarmee haast te maken aangezien veel van deze gebieden bedreigt worden door verstedelijking (resulterened in verhoogde sedimentatie snelheid en een toename in voedingsstoffen en ander chemicalien) en overbevissing (specifiek in Azie en Europa). References/Referenties Bellwood DR, Wainwright PC, Fulton CJ, Hoey AS (2006) Functional versatility supports coral reef biodiversity. Proc R Soc B 273:101-107 Beukema JJ (1993) Successive changes in distribution patterns as an adaptive strategy in the bivalve Macoma balthica (L.) in the Wadden Sea. Helgolander Meeresun 47:287-304 Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:209-221 Etter RJ, Grassle JF (1992) Patterns of species diversity in the deep-sea as a function of sediment particle size diversity. Nature 360:576-578 Gray JS (1981) The ecology of marine sediments: An introduction to the structure and function of benthic communities, Cambridge University Press, Cambridge Levinton JS (1987) Ecology of deposit-feeding animals in marine sediments. Quart Rev Biol 62:235 - 259 Lomolino MV, Heaney LR (2004) Frontiers of Biogeography: New Directions in the Geography of Nature, Sinauer Associates Inc., Sunderland Lomolino MV, Riddle BR, Brown JH (2006) Biogeography, Third Edition. Sinauer Associates, Inc., Sunderland, Massachusetts Meysman FJR, Middelburg JJ, Heip CHR (2006) Bioturbation: a fresh look at Darwin's last idea. Trends Ecol Evol 21:688-695 Rex MA, Crame AJ, Stuart CT, Clark AG (2005) Large-scale biogeographic patterns in marine mollusks: a confluence of history and productivity? Ecology 86:2288-2297
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Roy K, Balch DP, Hellberg ME (2001) Spatial patterns of morphological diversity across the Indo-Pacific: analyses using strombid gastropods. Proc R Soc Lond B 268:2503-2508 Snelgrove PVR (1998) The biodiversity of macrofaunal organisms in marine sediments. Biodivers Conserv 7:1123-1132 Vermeij GJ (1978) Biogeography and Adaptation: Patterns of marine life, Harvard University Press, Cambridge MA Vermeij GJ (2005) From phenomenology to first principles: toward a theory of diversity. Proc Cal Acad Sci 56:12 - 23
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Definitions Diversity - diversity is the term used to define the diversity of life. It can be used to refer to any of several levels of biological organization from genes to ecosystems (Gaston 2000). Functional trait – morphological or physiological traits that impact fitness indirectly via their effects on growth, reproduction and survival (Violle et al. 2007). Fundamental niche – The physiological tolerance range of an organism to abiotic factors. Or in other words the total range where a species can occur, if biotic interactions were not at play (Hutchinson 1957). Habitat - a description of a physical place, at a particular scale of space and time, where an organism either actually or potentially lives (Kearney 2006). Macroecology - a multi-scale approach to investigate the assembly and structure of biotas (Brown et al. 1995, Gaston & Blackburn 2000). Macrophysiology - the comparison of physiological attributes at large spatial scales (Chown et al. 2004). Niche - a multidimensional space whose axes comprise the conditions and resources that limit an organism’s survival and reproduction (Hutchinson 1957). Occupied morphospace – a species can occupy a part of total morphospace, and an assemblage of species gives a measure of occupied morphospace. Realised niche – The sites where an organism occurs due to its ability to withstand abiotic and biotic factors (Hutchinson 1957). The realized niche should typically be smaller than the fundamental niche. Total morphospace – an n-dimensional hypervolume where the axes are morphological variables, e.g. feeding apparatus of fishes and bivalves. Trait – In its simplest definition, a trait is a surrogate of organismal performance, and this meaning of the term has been used by evolutionists for a long time (Violle et al. 2007).
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References Brown JH, Mehlman DW, Stevens GC (1995) Spatial variation in abundance. Ecology 76:2028-2043 Chown SL, Gaston KJ, Robinson D (2004) Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Funct Ecol 18:159-167 Gaston KJ (2000) Global patterns of biodiversity. Nature 405:220-227 Gaston KJ, Blackburn TM (2000) Pattern and Process in Macroecology. Blackwell Science, Oxford Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Symposium Quantitative Biology 22:415–427 Kearney M (2006) Habitat, environment and niche: what are we modelling? Oikos 115:186191 Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882-892
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Appendix 1 (Chapter 2, Climate variability effect in intertidal bivalves )
Appendices
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Appendix 1 (Chapter 2, Climate variability effect in intertidal bivalves )
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Appendix 1 (Chapter 2, Climate variability effect in intertidal bivalves )
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Appendix 1 (Chapter 2, Climate variability effect in intertidal bivalves )
References Ansell AD, Barnett PRO, Bodoy A, Masse H (1980a) Upper temperature tolerances of some European molluscs. 1. Tellina fabula and T. tenuis. Mar Biol 58:33-39 Ansell AD, Barnett PRO, Bodoy A, Masse H (1980b) Upper temperature tolerances of some European molluscs. 2. Donax Vittatus, D. Semistriatus and D.Trunculus. Mar Biol 58:41-46 Ansell AD, Barnett PRO, Bodoy A, Masse H (1981) Upper temperature tolerances of some European Molluscs. 3. Cardium glaucum, C. tuberculatum and C. edule. Mar Biol 65:177-183 Ansell AD, McLachlan A (1980) Upper temperature tolerances of three molluscs from South African sandy beaches. J Exp Mar Biol Ecol 48:243-251 Davenport J, Davenport J (2005) Effects of shore height, wave exposure and geographical distance on thermal niche width of intertidal fauna. Mar Ecol Prog Ser 292:41-50 Hicks DW, Tunnell JWJ, McMahon RF (2001) Population dynamics of the nonindigenous brown mussel Perna perna in the Gulf of Mexico compared to other world-wide populations. Mar Ecol Prog Ser 211:181-192 Kennedy VS, Mihursky JA (1971) Upper temperature tolerances of some estuarine bivalves. Chesap Sci 12:193-204 Masse H, Parache A (1984) Evolution de la tolerance thermique de Mytilus galloprovincialis Lamarck en fonction des temperatures saisonnieres; comparaison de la sensibilite thermique d' individus provenant de population differentes. Haliotis 14:111-118 Tyler-Walters H, Davenport J (1990) The relationship between the distribution of genetically distinct inbread lines and upper lethal temperature in Lasaea rubra. J Mar Biol Ass U K 70:557-570 Urban HJ (1994) Upper temperature tolerance of ten bivalve species off Peru and Chile related to El-Nino. Mar Ecol Prog Ser 107:139-145
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 2 (Chapter 5, Bivalve diversity and sediment relationships)
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Appendix 3 (Chapter 6, Distributional overlap in bivalves)
Appendix 3. Maps showing the grid program at each system Benthic and sediment sampling points are shown as circles, where the sediment sample points are indicated as larger circles. Median grain size values are shown in categories (Wentworth Scale). Darker colours are muddy sample points whereas lighter colours are sandier.
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Appendix 3 (Chapter 6, Distributional overlap in bivalves)
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Appendix 3 (Chapter 6, Distributional overlap in bivalves)
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Appendix 3 (Chapter 6, Distributional overlap in bivalves)
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Appendix 3 (Chapter 6, Distributional overlap in bivalves)
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Acknowledgements
Acknowledgements For the ‘scream team’ Lewis Carroll (from Through the Looking-Glass and What Alice Found There, 1872)
The Walrus and the Carpenter Were walking close at hand; They wept like anything to see Such quantities of sand: "If this were only cleared away," They said, "it would be grand!" "If seven maids with seven mops Swept it for half a year. Do you suppose," the Walrus said, "That they could get it clear?" "I doubt it," said the Carpenter, And shed a bitter tear. "O Oysters, come and walk with us!" The Walrus did beseech. "A pleasant walk, a pleasant talk, Along the briny beach: We cannot do with more than four, To give a hand to each." The eldest Oyster looked at him, But never a word he said: The eldest Oyster winked his eye, And shook his heavy head-Meaning to say he did not choose To leave the oyster-bed.
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But four young Oysters hurried up, All eager for the treat: Their coats were brushed, their faces washed, Their shoes were clean and neat-And this was odd, because, you know, They hadn't any feet. Four other Oysters followed them, And yet another four; And thick and fast they came at last, And more, and more, and more-All hopping through the frothy waves, And scrambling to the shore. The Walrus and the Carpenter Walked on a mile or so, And then they rested on a rock Conveniently low: And all the little Oysters stood And waited in a row. "The time has come," the Walrus said, "To talk of many things: Of shoes--and ships--and sealing-wax-Of cabbages--and kings-And why the sea is boiling hot-And whether pigs have wings." "But wait a bit," the Oysters cried, "Before we have our chat; For some of us are out of breath, And all of us are fat!" "No hurry!" said the Carpenter. They thanked him much for that.
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"A loaf of bread," the Walrus said, "Is what we chiefly need: Pepper and vinegar besides Are very good indeed-Now if you're ready, Oysters dear, We can begin to feed." "But not on us!" the Oysters cried, Turning a little blue. "After such kindness, that would be A dismal thing to do!" "The night is fine," the Walrus said. "Do you admire the view? "It was so kind of you to come! And you are very nice!" The Carpenter said nothing but "Cut us another slice: I wish you were not quite so deaf-I've had to ask you twice!" "It seems a shame," the Walrus said, "To play them such a trick, After we've brought them out so far, And made them trot so quick!" The Carpenter said nothing but "The butter's spread too thick!" "I weep for you," the Walrus said: "I deeply sympathize." With sobs and tears he sorted out Those of the largest size, Holding his pocket-handkerchief Before his streaming eyes.
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"O Oysters," said the Carpenter, "You've had a pleasant run! Shall we be trotting home again?' But answer came there none-And this was scarcely odd, because They'd eaten every one.
Institutional thanks: This project would not have been possible without support from the University of Groningen, the Netherlands Institute for Sea Research, the Department of Environment and Conservation, Broome Bird Observatory, the Broome TAFE Aquaculture Centre and WA Fisheries Facility in Broome. In the Netherlands, I would especially like to thank my colleagues and the administration and technical department at the Netherlands Institute for Sea Research for their support during the years of my thesis. Some people I would especially like to thank are: Joke Mulder, Irene Wernand, Marlies Bruining, Wim Pool and Rob Dekker. From the University of Groningen I would like to thank Gezien van Roon for being available to help me with administrative questions etc. In Australia, I would like to thank the Department of Environment and Conservation in Perth and Broome for logistical support. I would especially like to thank some individuals who have been especially helpful: Joanne Smith, Brent Johnson, Alan Clarke, Jim Cocking, Mike Lapwood, Tim Willing (no longer with DEC) and Mike Kingsley. In Broome, I would like to thank Broome Bird Observatory for its support of this project. In addition, the TAFE aquaculture facility and their staff in Broome have been important for the work conducted in Broome. I would especially like to thank Tony Salisbury and Anthony Aris for their support. Within the TAFE aquaculture centre we were allowed to use the Western Australian fisheries facility. This was also a fantastic resource. I would especially like to acknowledge Justin Bellenger for his patience and understanding when we shared this facility with him. Promotors: I would like to thank Wim for his support in getting this project funded and for his continuous support during the years of my PhD. Thank you also for your quick responses to my questions and your critical eye when looking over my manuscripts.
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Thank you Theunis for giving me the opportunity to take on this project, and for opening my eyes to curiosity and fundamental driven scientific exploration. At a personal level thank you for being supportive during all the ups and downs that this journey has brought. I am really grateful to you for all those hours that I am sure you have spent outside of work hours to read my work and respond in the punctual time, which you always do! You have always been available for my questions and stressful moments, I remember phone calls from Broome to Gaast, and that you (and Petra) have been always available to give support and advice. I am grateful that you accepted me as part of the ‘birdwing’ and gave me the opportunity to develop during these last years. Supervisors: Thank you Grant for your commitment and belief in this project and me. Grant you have been a pillar of support during the stressful periods in Broome and have always put in a large effort to help make the fieldwork successful. You have been a great listener and a great advisor and have always been available for me. Thank you! I would like to acknowledge Jan Drent as a supervisor (although officially he is not). Jan has been involved from start to end in this project. He helped me develop ideas and experiments that are now papers in this thesis (thermal tolerance and gill-palp). He has also been the person I have often gone to for experimental, logistical and theoretical advice and discussions. Jan I have always enjoyed our discussions and am grateful that you were available to help me. I would like to acknowledge the passion that Theunis, Petra and Grant share and have put towards an otherwise unstudied tidal flat. They are a unique team whose energies have attracted a number of ornithological and benthic scientists to this area and will continue to do so in the future. They all put their own personal time towards the study of the science of Roebuck Bay. I hope that in the near future all the hard efforts of Theunis and Grant will lead to Roebuck Bay (and Eighty-mile beach) being recognized as being just as unique in ecological significance as an area like the Great Barrier Reef. Colleagues: I would like to thank my colleagues at NIOZ for many cosy coffee/tea times, stimulating and lively discussions and their support during my thesis. Colleagues include: Piet van den Hout, Joana Cardoso, Oscar Bos, Pieternella Luttikhuizen, Jutta Leyrer, Luisa Mendes, Wim Boer, Jeroen Reneerkens, Pieter Honkoop, Rob Dekker, Dennis Waasdorp, Kees Camphuysen, Bernard Spaans, Anne Dekinga, Henrike Andresen,
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Matthijs van der Geest, Pim Edelaar, Jan van Gils, Maarten Brugge, Maaike de Heij, Wim Boer, Pim Edelaar, Sebastian Holmes. I would like to make personal thanks to: Jaap van der Meer for contribution of ideas and his lessons in R and statistics, which have led me to the next step in my scientific career…. Wouter Vahl for getting me involved from my starting time at NIOZ. Over the years I have been grateful for your support and friendship. You made my time at NIOZ good fun, as well as stimulating. I really enjoyed all our wide-ranging discussions and of course miss them. Tineke Troost for literally being my ‘troost’! Thanks Tineke for your confidence building and support. I have enjoyed working with you as you can make complex problems resolve into simple ones and you have an artful way of describing statistics and programming. Thanks!!! Francois Vezina for his enthusiasm and lots of fun discussions! I miss hearing about summit metabolic rates! Isabelle Smallegange for her help and support, as well as fun times, during the last years. Casper Kraan for sharing the office with me for a couple of years and also for all those database questions. Marc Lavaleye for teaching me about the worms and small critters in the mud at Broome. Also for helping with the identification of samples brought back from Broome! Especially for sharing his amazing knowledge and enthusiasm of benthic critters! Petra de Goeij for her help in the field, positive energy and love for Broome, which always reminds me how cool all the little things are even after looking at them for hours on end. Annette van Koutrick for the sediment analysis and teaching of my students at NIOZ. Internationally, I would like to acknowledge Pierrick Bocher for allowing me to work with the French data, Sabine Dittmann, and Andrew Storey from Australia. I would also like to thank Bob Hickey for his help in producing tidal heights of Roebuck Bay and Eighty Mile Beach. Also Shirley Slack-Smith, Loisette Marsh and Richard Willan for their help in identifying species in Roebuck Bay.
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Students: Thanks to the ‘scream team’ for all those long hours worked and fun times shared in 2003. Renske de Jonge for her positive spirit, lots of laughs, hard work, enthusiasm and ideas Kirsten Krans for her hard work, energy, lots of laughs and lively personality Roos Kentie for her hard work, enthusiasm and grounded personality Heleen Sombroek for all those cages! To being committed to the project when things were personally tough. Heleen you have amazing skills with people and a natural ability to deal with tough tropical conditions. Thanks to Konrad Gorski for doing the ‘locomotion’ too many hours of benthos work! Also for being so motivated and interested during his project period. I would also like to thank: Marisela Meegdes Chiel Abma Anton Schrijver for their help during this project. Volunteers: Thank you to all the volunteers who have helped out with fieldwork during this project. E.g. Australian Conservation Volunteers (2002), Humera Rind, Ayano Nakayama, David Barlow, Melinda Gunson, Helen MacArthur, Mavis Russell, Phil Joy, Jamie Wallis, Jack Terra, Hans van Haren, Loes Gerringa, Anne-Claire Baudoux, Judith Lavoie, Rosalie, Felix, Geno and many others. I would also like to thank my brother Brode for his help and support in the field during 2003. Of course Micha Rijkenberg has been a volunteer for much work too! I would like to make a special thank you to Grant Morton for his help on this project. He found the ‘Mud Tellina’ on one of our first field trips and was always around with a smile and lots of energy when we were feeling exhausted. Grant often drove the hovercraft for us and was helping out on his days off. Thanks Grant!! Family: My parents Thanks mom and dad for your faith and support for me during these years. You initiated the motivation to study biology, starting with our visit to Hluhluwe National park and dads work at the Uni. of Natal (which I thought was cool cause dad could wear yellow sunshine suits!). Mom also signed me up for a course at Durban Oceanarium and got me involved at Jo’burg zoo. All these little steps started my dream to become a scientist. However, times were not so
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easy after our big migration, and a lot of family support had to get me to university and beyond. I now appreciate how difficult it was for you to take such a big step to immigrate to Australia. Thank you for all your love and support! Brode Thanks to my little brother for fun times shared and his love and support over the years! Including help in the field in Broome and also help with the cover of this thesis. Micha Rijkenberg Thank you, for being my best friend and the person who stands by me through all the ups and downs. Also for being more than just a chemist – but also a good biologist who has been involved in my fieldwork, experiments, theoretical discussions and most importantly in getting papers ready for publication! In a good way, you are continuously pushing me to the end of my limits. You are incredibly supportive, and have most recently showed that by following me to the other side of the world. I guess the road with adventures won’t stop here … so I thank you ahead for everything! Han Rijkenberg To my Hannie thank you for your love and support. Since we met you took me in and accepted me as part of the family. You have brought me lots of laughs during the time of my PhD, as well as moral support and lots of listening! Family Rijkenberg Thanks to the family Rijkenberg (Jaap, Carla, Ivar, Joerie, Patrique and Tante Gre) for their support during the last years. Special thanks to people who sowed the seeds for me to come this far: Especially my maths teacher at high school (David Grover, Chatswood High School, Sydney) who would invest his free-time in after school classes and for his motivating lectures where he would actively walk up and down the room emphasizing that maths is exciting. To the Sydney scientists for their support in the years prior to the Netherlands: Iain Suthers, Tom Trnski, Jeff Leis, Kevin Rowling, Shirley Scott Friends: Netherlands Thank you guys for all the fun times on Texel! Especially my room mates: Anne-Claire Baudoux, Joana Cardoso and Ben Abbas
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And my second family: Francois, Judith, Felix and Rosalie Other people I would like to thank are: Sebastian Holmes, Nicola Miller and Ismael Mayo-Enriquez for taking care of me in the early days on Texel. Wouter Vahl and Maaike de Heij Isabelle Smallegange Helene Agogue Pascal Hollart Oscar Bos Jack Terra Jutta Leyrer Janneke and John Boelhouwers Broome Stefan Jordanoff for a fun house stay during my fieldwork in 2004. And ‘grasshopper’ Kirsten for a great time in Broome. Other people I would like to thank include: Tim Willing Inka Veltheim, Megan Underwood and Emma Bayly-Stark Adrian Boyle Chris Hassell and Andrea Spencer Sydney I would like to thank my mates in Sydney for their support from a distance: Peta Oliver, Steph Ngeow, Sara Maleki, Julia Ashfield, Rebecca Jones, Vanessa Caldwell, Vernita Brown, Yvette Poshoglian, Marnie Little, Kirsty Collard, Jon Rez POEM BY RENSKE DE JONGE Sinterklaas December 2003 There was a girl from Amsterdam Who wasn’t fussed about killing a clam She chose a nice spot in the tropen To cut heaps of bivalves open
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