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Regional effects as important determinants of local diversity in both marine and terrestrial systems

Howard V. Cornell and Susan P. Harrison

H. V. Cornell (hvcornell@ucdavis.edu) and S. P. Harrison, Dept of Environmental Science and Policy, Univ. of California at Davis, Davis, CA 95616, USA.

Community ecologists have struggled to create unified theories across diverse ecosystems, but it has been difficult to acertain whether marine and terrestrial communities differ in the mechanisms responsible for structure and dynamics. One apparent difference between marine and terrestrial ecology is that the influence of regional processes on local popula-tions and communities is better established in the marine literature. We examine three potential explanations: 1) influen-tial early studies emphasized local interactions in terrestrial communities and regional dispersal in marine communities. 2) regional-scale processes are actually more important in marine than in terrestrial communities. 3) recruitment from a regional species pool is easier to study in marine than terrestrial communities. We conclude that these are interrelated, but that the second and especially the third explanations are more important than the first. We also conclude that in both marine and terrestrial systems, there are ways to improve our understanding of regional influences on local community diversity. In particular, we advocate examining local vs regional diversity relationships at localities within environmentally similar regions that differ in their diversity either because of their sizes or their varying degrees of isola-tion from a species source.

Oikos 122: 288–297, 2013 doi: 10.1111/j.1600-0706.2012.20691.x

© 2012 The Authors. Oikos © 2012 Nordic Society Oikos Subject Editor: Matthew Bracken. Accepted 7 June 2012

Species diversity in ecological communities is widely acknowledged to be governed by a balance between regional processes operating at large spatial scales, such as dispersal from a regional propagule supply, and processes that take place at small spatial scales, such as species interactions (Holyoak et al. 2005, Ricklefs 2007, Harrison and Cornell 2008). In reality, there is a continuum of nested scales, with some processes being strictly local, some nearly local, and some operating at a somewhat larger scales. Moreover, what is defined as local or regional will depend upon the spatial and temporal scale of the study and the goals of the investigator. The definition of scale will also depend upon the ecological characteristics (e.g. dispersal stages) of the organisms themselves which are, in turn, evo-lutionarily shaped by environmental features and processes that determine the patterns and scales of population con-nectivity. Nevertheless, for each defined habitat unit, we can generally identify processes occurring within it that are ‘local’ and processes occurring outside it that are ‘regional’. As a result, the relative importance of local and regional processes can be compared across diverse ecosystems.

The relative roles of regional and local processes have been differently emphasized in marine and terrestrial community ecology. In marine ecology, there is a long tradition of measuring and modeling the influence of regional dispersal on the dynamics of local populations and communities. The ‘supply-side’ perspective, in which local

community composition depends at least as much on the propagule supply as on local interactions, has been well established in the marine literature for decades (Levins and Culver 1971, Levin and Paine 1974, Hastings 1980, Paine and Levin 1981, Lewin 1986, Gaines and Roughgarden 1985, Roughgarden et al. 1985, 1988). In contrast, despite the efforts of some spatially oriented terrestrial ecologists, much of terrestrial community ecology remains firmly centered on local species interactions, as evidenced by a recent review proposing a research agenda with little ref-erence to regional processes (Agrawal et al. 2007). There have been repeated calls for integrating larger scales of space and time into our understanding of terrestrial com-munities (Ricklefs 1987, 2007, Ricklefs and Schluter 1993, Cornell and Lawton 1992, Tilman 1994, Leibold et al. 2004, Harrison and Cornell 2008), and an extreme viewpoint even questions the usefulness of the local com-munity concept (Ricklefs 2008, see Brooker et al. 2009 for a rejoinder). However, many terrestrial community ecologists still remain scarcely aware of these issues, so strongly is the field wedded to its focus on species inter-actions at local spatial scales.

Here we explore this difference in the degree of empha-sis on regional processes in marine versus terrestrial eco-logy from several interrelated perspectives: the history of ideas, the actual importance of regional versus local pro-cesses, and the ease of study of regional influences in marine

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versus terrestrial communities. We also suggest ways to expand the study of regional and local patterns of diversity in both marine and terrestrial systems.

History of ideas in terrestrial and marine ecology

As community ecology moved in the 1940s–1960s from a descriptive to a more theoretical science, emphasis shifted from the historical origins of species diversity to mainten-ance of species diversity in small localities. The central con-cepts were species niches, interactions, competition, and coexistence, which were modeled using the approach pioneered by Lotka and Volterra (Schoener 1986, Ricklefs 1987, Cornell 1999). Robert MacArthur, a terrestrial ecologist who worked mainly with bird communities, was enormously influential in the development of this shift (MacArthur 1965, 1969, 1972, MacArthur and Levins 1967, May and MacArthur 1972). In a classic paper addressing patterns of species diversity, MacArthur (1965) proposed two alternative explanations for why some areas might support more species than others: ‘If the areas being compared are not saturated with species, an historical answer involving rates of speciation and length of time available will be appropriate; if the areas are saturated with species then the answer must be expressed in terms of the size of the niche space …. and the limiting similarity of co-existing

species…’. These alternatives hinge on whether competi-tion limits the number of coexisting species in a particu-lar area. MacArthur believed that local dynamics happened so quickly relative to regional dynamics that communi-ties would quickly become ecologically saturated with species due to the filling of niche space. Thus, historical/ biogeographic processes such as speciation and extinc-tion rates, although they might explain regional diver-sity, could be ignored when explaining local diversity (MacArthur 1965). In this scenario, if regional diversity increases through time, it causes beta or between-habitat diversity to increase (MacArthur 1969, see also Fig. 1a). In the alternative scenario, communities do not become saturated and historical processes can determine diversity at both regional and local scales (Fig. 1b).

MacArthur’s persuasive reasoning and the coherent beauty of his theoretical framework (reviewed by Schoener 1989) made the focus on local ecological processes a default belief for many terrestrial community ecologists, more of an underlying assumption than a hypothesis to be tested. This assumption still persisted after later models predicted that there was no general limit to the similarity of over-lapping niches and thus no limit to the number of locally coexisting species, even under conditions of environmental variability (May and MacArthur 1972, Turelli 1978, Abrams 1983, see also Cornell 1999, Rosenzweig and Ziv 1999).

Figure 1. Two alternative explanations for why some areas might support more species than others. In (a) niche space sets limits on local diversity. Regional diversity increases through evolutionary time, but local diversity becomes saturated and beta (between-habitat) diversity increases. In (b) niche space does not fill and regional diversity determines local diversity. Local diversity increases steadily through time with increase in regional diversity. Beta diversity increases, but more slowly, and only because of increases in regional diversity, upon which it partially depends.

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Nonetheless, the theory of island biogeography (MacArthur and Wilson 1967) showed that MacArthur also had an appreciation of large-scale influences on local diversity, an apparent contradiction that Schoener (1983) termed ‘MacArthur’s paradox’. The subsequent 1970s–1980s explosion of studies testing island biogeography theory in islands and terrestrial habitat fragments (reviewed by Shafer 1990) provided excellent evidence for regional effects on the local diversity of insular terrestrial systems. Later, regional effects inconsistent with MacArthurian satura-tion were found in analyses of diversity at multiple scales (Cornell 1985, Shurin and Srivastava 2005, Harrison and Cornell 2008). Better integration of large and small scales in both space and time was urged in an influential edited volume on community ecology (Ricklefs and Schluter 1993). More recently, neutral theory (Hubbell 2001) attempted to direct terrestrial ecologists to an emphasis on regional species pools, and the recent development of meta-community theory has led to a new framework for con-sidering the interplay between regional and local processes in communities at the mesoscale (Leibold et al. 2004).

Modern marine community ecology also began with an emphasis on local interactions as the primary explanation for differences in species diversity. Classical experimental ecology originated in marine systems with the pathbreak-ing work of Connell (1961), Paine (1966) and Underwood et al. (1983) and continues to be used in these systems today. This experimental work definitively showed that competition and predation could have dramatic effects on the number of species coexisting in the same community. However, there were often conflicts among the results of the same experiments conducted in different places and at different times (Connell 1985, Gaines and Roughgarden 1985, Roughgarden et al. 1988). In reaction to these inconsistencies, marine ecologists began to focus on larger-scale processes, and this shift in emphasis had a powerful effect on the development of marine community theory.

Marine community theory placed a central emphasis on the regional propagule supply, beginning with Levin and Paine’s (1974) influential model that incorporated disturbance, patchiness, and a regional propagule pool linking patches together into what would now be termed

a metacommunity. Each local community on a patch was viewed as being bathed in a species pool from the surround-ing region (Fig. 2a), a powerful metaphor for the influ-ence of dispersal and recruitment processes on local species assemblages. This propagule bath model was later success-fully tested in the intertidal zone (Paine and Levin 1981). Subsequently, the term ‘supply-side ecology’ (Lewin 1986) was coined to describe models emphasizing the impact of pre-recruitment propagule supply on population dynamics (Roughgarden et al. 1985, 1988).

Although supply-side ecology models at first empha-sized population dynamics, their relevance to the structure of intertidal, fish, and benthic communities was quickly grasped. Propagule supply was proposed to be at least as important to communities as post-recruitment species interactions (Gaines and Roughgarden 1985), and this continues to be a central concept in marine ecology (Caley et al. 1996, Hughes et al. 2000, Sousa et al. 2007, Menge et al. 2009). Supply-side models have even been applied to mangrove forests, which may be regarded as marine systems in terms of their propagule dispersal (Sousa et al. 2007).

Marine ecologists have also made considerable progress in understanding the nature of the regional species pool and the causes of patterns in regional diversity. Using a combination of modeling and data, marine ecologists have analyzed the roles of speciation, dispersal, and extinc-tion in creating large-scale gradients in species diversity and composition (Connolly et al. 2003, Jablonski et al. 2006, Renema et al. 2008, Buzas and Culver 2009). Terrestrial ecologists have made some progress in this area (Latham and Ricklefs 1993, Ricklefs et al. 2006, Mittelbach et al. 2007), but the role of local ecological processes in generating such gradients is often still empha-sized (Willig et al. 2003, Mittelbach et al. 2007, see Currie et al. 2004 for counterevidence).

However, as previously mentioned, terrestrial ecolo-gists have been theorizing about regional-scale influences at least since MacArthur and Wilson (1967). We conclude, therefore, that regional and local processes have been foun-dational in both marine and terrestrial ecology. Thus, even though the marine-terrestrial difference in emphasis has existed for a long time, it is unlikely to be due to the history

Figure 2. Scenarios for propagule supply in marine and terrestrial systems. (a) In marine systems, habitats are immersed in a homogeneous surrounding medium containing propagules of many species with few dispersal barriers, many of which pass through the fitness filter and are able to recruit to the habitat. (b) In terrestrial systems, topography and environmental heterogeneity erect larger dispersal and fitness barriers to arriving propagules and ‘seed banks’ confound arriving propagules with those already present in the habitat.

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environment are likely to be much larger both with respect to the geographic area from which they draw and the number of species. As a consequence, the sampling density and duration necessary to characterize the regional pool may be greater in marine environments. However, if enough panels are deployed over a sufficiently large timespan, accurate measures of the species pool are pos-sible with reasonable effort, with the possible exception of rare species from distant sources; at the same time, valuable data on replicate local communities are obtained (Witman et al. 2004, Freestone and Osman 2011). Because of pos-sible preemption of later settlers by earlier ones, it is critical that some panels be devoted exclusively to the evaluation of the pool. Clean panels need to be immersed at regu-lar intervals to make sure that settlement opportunities are always available and to detect seasonal variation in propagule availability. In a recent example, Canning-Clode et al. (2009) studied hard substrate communities at differ-ent successional stages across four biogeographic regions using replicated settlement panels. Regional richness was estimated from species accumulation curves across panels exclusively devoted to the evaluation of regional richness at the depth and time of the deployment. The study showed that the relationship of local richness to regional richness strengthened through time, even though most panels used to assess local richness exhibited 100% cover shortly after immersion, suggestive of saturation.

Parenthetically, the ‘greater ease of study’ argument may apply to paleontological as well as modern studies of marine community assembly. Many marine invertebrate taxa have left excellent fossil records because of their calcareous skeletons – which are the indirect result of their plank-tonic propagules and dispersal abilities – and because of the shallow depositional environments they inhabit. This has made it possible to explore the historical development of regional faunas and their dispersal into local assemblages to a degree that is almost inconceivable for terrestrial taxa (Roy et al. 2001, Jablonski et al. 2006).

In terrestrial environments, dispersal is lower for many species (Kinlan and Gaines 2003), generally does not follow predictable patterns such as ocean currents, and is often impeded by geographic barriers that prevent many species from immigrating to suitable localities (May 1994). Some marine species may show more limited dispersal than estimated by Kinlan and Gaines (Puebla et al. 2009, Pinsky et al. 2010), but most show at minimum a higher potential for long-distance dispersal relative to most terrestrial species (Roughgarden et al. 1988, Palumbi 1992, Mora and Sale 2002). Slow and inconsistent dispersalin terrestrial environments makes it difficult or impossible to estimate regional propagule supplies directly. Instead, the most frequent approach to estimating regional species pools is by using the total diversity of a collection of local sites. Almost by definition, this requires that the localities are highly environmentally similar both within and among regions and that all species can disperse among the local sites. It is then relatively easy to define which species are likely to prosper in that particular habitat type. However, terrestrial regions are often topographically and environ-mentally heterogeneous, with considerable habitat special-ization and endemism (Fig. 2b; Cornell and Lawton 1992).

of ideas per se. Other factors must be responsible, and we suggest that it is because regional-level approaches have generally been more successful at explaining local commu-nity structure in marine than terrestrial studies.

Ease of study of regional processes in marine and terrestrial systems

One of the greatest challenges in studying regional effects on local communities is the requirement that the regional species pool be defined and measured. The regional pool is sometimes defined as the list of all species present in a region that are capable of dispersing to a focal local-ity (reviewed by Zobel 1997). The local environmental conditions then filter out those species that are not capable of persisting at that locality. An alternative defi-nition is that the species pool includes those species that can both disperse to and potentially persist at a locality based upon the locality’s abiotic environmental conditions (Zobel 1997, Karlson et al. 2004). We prefer the second definition, believing that it is not very useful to include species specialized to other habitats in the pool for the habitat of interest. We apply the terms ‘propagule bath’ for marine systems and ‘propagule rain’ for terrestrial systems to the total arrivals at a locality (Fig. 2).

Marine environments differ from terrestrial ones in ways that may make the species pool easier to define. They tend to be more environmentally homogeneous at scales that are relevant to definitions of the species pool, and are often well-mixed with few barriers to dispersal for many marine species (May 1994, Palumbi 1994, Jablonski and Roy 2003, Dawson and Hamner 2008). The gener-ally larger geographic ranges of marine species and the lower incidence of endemism in marine biogeographic regions (Paulay and Meyer 2002, Shanks and Eckert 2005, Kinlan et al. 2005) lend support to this idea. This does not mean that marine systems are totally homogeneous, however. Although they may be more so than terrestrial systems, they are far from well-mixed in all cases and dispersal can be much more localized than previously thought (Jones et al. 1999, Puebla et al. 2009, Pinsky et al. 2010). If marine species pools are indeed more spa-tially homogeneous in space than terrestrial species pools, this may increase the ease (i.e. number and distribution of samples) and accuracy of characterizing regional species pools in marine systems.

Another difference between marine and terrestrial envi-ronments is that ‘banks’ of dormant propagules, although they do occur (Worm et al. 1999, Edwards 2000), are less common in marine than in terrestrial systems, mak-ing diversity easier to estimate at both regional and local scales (Fig. 2a). Marine benthic communities occupy-ing hard substrates are perhaps the easiest environment in which to study regional effects on local richness (Witman et al. 2004). Many sessile species with pelagic larvae occupy these habitats. Substrates can be experimentally cleared and recolonization can be monitored, or artificial settlement panels mimicking natural hard substrate can be dipped into the propagule bath and colonization observed. Because of the long-distance dispersal poten-tial of many marine species, regional pools in the marine

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because lower propagule mortality means that fewer propagules are needed for successful establishment. These requirements, coupled with environmental heterogeneity, barriers to dispersal, and habitat specialization, may make dispersal potential lower relative to marine envi-ronments (May 1994, Kinlan and Gaines 2003, but see Dawson and Hamner 2008). Because of these differences, propagule production, behavior, and mortality, settlement cues, and recruitment processes may play a greater role in structuring marine than terrestrial communities (Gaines and Roughgarden 1985, Hughes et al. 2000, but see Caro et al. 2010).

In the past decade, marine ecologists have pulled back from the ‘propagule bath’ hypothesis, as there has been increasing emphasis on retention of larvae at small spa-tial scales (Puebla et al. 2009, Pinsky et al. 2010, Morgan et al. 2009, 2011). Moreover, as mentioned previously, many marine organisms have adaptations for limiting their dispersal (Neilson and Perry 1990, Stobutzki and Bellwood 1997, Jones et al. 1999, Puebla et al. 2009) Nevertheless, dispersal distributions in marine environ-ment probably have heavier tails than those in the terrestrial realm (May 1994, Kinlan and Gaines 2003), which may explain why theory developed from the study of marine systems emphasized the propagule supply and theory developed from terrestrial systems emphasized local interac-tions and deemphasized regional processes.

How can the regional species pool be ‘manipulated’ to test its effects on local richness?

Much of the inspiration for the idea that regional effects can influence local species richness thorough dispersal originated with the theory of island biogeography (MacArthur and Wilson 1967). According to this theory, the number of species on an island or continent increases with area and decreases with isolation from a source pool due to a shifting balance between extinction and colonization rates. These relationships between species numbers and area or isolation suggest ways to ‘manipulate’ (in a comparative observational sense) the regional spe-cies pool to test for its effects on local richness. One the one hand, regional areas of different size are likely to sup-port different numbers of species which can colonize the communities embedded within these regions. The local richness of these communities can then be observed for its response to increases in the source pool as regions become larger. On the other hand, regional areas may be isolated to different degrees from a larger species pool which pro-vides the original source of species for each of these areas. More isolated areas are likely to have smaller source pools and again the responses of local richness in the embed-ded local communities can be observed. These methods of course assume that the regions are as environmentally similar as possible, that all of the species in each region can disperse to each locality, and that the niche space is the same in each locality across regions.

The first type of manipulation is exemplified by a terrestrial study employing cynipid gall wasps that spe-cialize on oak species indigenous to the Pacific Slope of California (Cornell 1985). Gall wasps (Family: Cynipidae)

Species may also differ in their habitat breadths, affinities, and dispersal abilities. The result may be an inaccurate estimate of the pool of species capable of arriving and sur-viving at any given site (Srivastava 1999). On the other hand, if the species pool estimate is based only on the species occupying particular localities at a particular time, it will often be too small, especially when some species are present as dormant propagules such as seed banks in plant communities (Philippi 1993).

Relative importance of regional processes in marine and terrestrial systems

Another possibility we consider is that dispersal from the regional species pool is actually more significant in marine than in terrestrial communities. Propagules in the marine realm are borne by seawater whereas the terrestrial realm is surrounded by atmospheric air and the physical character-istics of these two media are very different. The relatively high density and viscosity of seawater allow particles to remain suspended for relatively long periods without set-tling, which permits planktonic life stages (eggs, larvae, adults) to be relatively common (Strathmann 1990, Paulay and Meyer 2002, Dawson and Hamner 2008, Vermeij and Grosberg 2010). In contrast, the low density and viscosity of the atmosphere prevents suspension for long periods of time and planktonic life stages, with a few exceptions, are relatively less common (Strathmann 1990, Dawson and Hamner 2008).

These differences in life history have clear conse-quences for dispersal potential. Propagules suspended in a viscous medium with few dispersal barriers can ride cur-rents relatively long distances from birth to settlement (Strathmann 1990, Kinlan and Gaines 2003). Indeed, planktonic development and length of pelagic period often correlate with dispersal ability and geographic range (Paulay and Meyer 2002). Moreover, because disper-sal agents are rare or non-existent and mortality risks are high, tens of thousands of propagules are often produced to guarantee that a few will settle and survive. These strat-egies do not mean that dispersal distance is always easily predictable. Recent theoretical work has indicated that dispersal patterns are often unpredictable due to the stochastic/chaotic nature of oceanographic currents (Siegel et al. 2008, Berkley et al. 2010, Bode et al. 2011). More-over, dispersal potential is not the only regional factor influ-encing community diversity and species composition. But all else being equal, greater dispersal distances should gen-erally correlate with greater impact of the regional species pool on the structure and dynamics of local populations and communities.

Propagule dispersal in terrestrial environments is some-times passive (‘aerial plankton’), but often requires active movement, because of the low density of the atmospheric medium and (in some cases) because directed dispersal is an effective adaptation to deal with environmental hetero-geneiety. Active movement may be limited by the avail-ability of energy either to disperse or to build structures to attract dispersal agents (Paulay and Meyer 2002). Thus, active dispersal may result in lower propagule production because of high energetic costs and (if dispersal is directed)

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each region (Bellwood et al. 2005), but isolation from the Indonesian diversity hotspot due to distance (Karlson and Cornell 1998) and westward-flowing currents (Connolly et al. 2003) also play an important role. Five regions (large, widely spaced island groups) with different diversities were sampled along the gradient, at three local scales, (10 m transects 100–2 m apart, sites 103–4 m apart on 15 islands and islands 104–6 m apart within each region). Slopes of the regressions of log-LSR on log-RSR were linear or nearly linear, suggesting that local coral assemblages are again open to enrichment from the regional species pool (Fig. 4). No clear limit on local richness was apparent even in the species-rich region around Indonesia. Estimates

lay eggs on oak plant parts and the hatched larvae secrete chemicals into the plant tissues which induce them to form galls around the developing insect. Gall wasps are highly specialized to the oaks and most are specialized to just a few oak species. Each oak species is thus a distinct ‘region’ for its gall wasp fauna. The California oaks vary widely in their distributional ranges, and those that are more broadly distributed support more gall wasp species, that is, they have larger regional species richness (RSR; Fig. 3a). RSR, in turn, predicts the local species richness (LSR) of gall wasps on local populations of different oak species (Fig. 3b). The effect of regional area on local richness by means of increasing regional richness has been termed the ‘echo pattern’ of large scale species–area relationships, and it can be shown theoretically that this ‘echo pattern’ pre-dicts linear LSR–RSR relationships (Rosenzweig and Ziv 1999). Indeed, several other early studies used this method and most found strong LSR–RSR relationships (Srivastava 1999).

Varying the regional area can be a useful technique for manipulating the species pool, but care must be taken that the pool is not disproportionately overestimated in larger regions relative to smaller regions. Such overestimates are possible because greater environmental heterogeneity and larger dispersal distances in larger regions may reduce the size of the actual pool to those species occupying smaller areas surrounding the locality of interest. Such disproportionate overestimates may lead to spurious satu-rating LSR–RSR relationships unless regional area is stan-dardized in some way (Srivastava 1999).

The second type of manipulation varies the isolation of regional areas from a species source region and thus the species pools for their embedded communities. It is exem-plified by a marine study employing coral species assem-blages associated with reef environments (Karlson et al. 2004, Cornell et al. 2008). Coral reefs comprise some of the richest species assemblages in marine environments and thus represent an excellent system for strong tests of LSR– RSR relationship. The study was carried out over a longitu-dinal gradient across part of the Indo-Pacific biogeographic region spanning from Indonesia in the east to French Polynesia to the west. Coral species richness peaks at over 600 species around the Indonesian archipelago and tapers off to about 130 in French Polynesia (Karlson et al. 2004). The eastward decline in richness is partially explained by declining area of shallow water habitat within

Figure 4. Regression of local species richness on regional species richness of west–central Pacific coral species plotted at three local spatial scales.

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Figure 3. (a) Regression of cynipid gall wasp species richness on the geographic range of California oak species. (b) regression of local species richness on regional species richness for cynpid gall wasps on California oaks.

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scale definitions is to examine the consistency of the rela-tionship across different spatial scales (Hillebrand and Blenckner 2002, Shurin and Srivastava 2005, Harrison and Cornell 2008). Such an approach increases the power to detect curvilinear patterns, which are often missed when the local scale is too large relative to the regional scale (Shurin and Srivastava 2005). Cornell et al. (2008) evalu-ated the LSR–RSR relationship at three spatial scales in the coral study described above and found the linear rela-tionship was robust to differences in the size of the local-ity (see also Freestone and Harrison 2006). Regional pools can also be assessed at multiple scales if data are hierarchi-cally structured. Although multiple assessments at different scales could be time-consuming and impractical in many situations, they offer a powerful way to identify relevant scales for assessing the LSR–RSR relationship.

The LSR–RSR relationship may also be distorted by statistical artifacts, most notably lack of independence and spatial autocorrelation (Srivastava 1999, Harrison and Cornell 2008). For example, linear LSR–RSR relationships at very large local scales may occur because large locali-ties subsume multiple habitats, substantial beta diversity and therefore a large proportion of regional diversity, pro-ducing autocorrelation at the two scales (Huston 1999, Loreau 2000, Hillebrand and Blenckner 2002). Also, sim-ple mathematical considerations demand that RSR must always be greater than LSR, constraining LSR–RSR regressions to a wedge-shaped operational space (Szava- Kovats et al. 2012).

There are several possible ways of dealing with such autocorrelation. It can be avoided when truly independent datasets are available to measure local and regional richness (Srivastava 1999), and ⁄ or by choosing scales for sampling local richness that are small enough to minimize inter-nal environmental heterogeneity (Harrison and Cornell 2008). When abundance data are available, autocorrela-tion can also be mitigated by comparing observed LSR– RSR relationships to null models generated by randomly sampling individuals from the regional pool (Belmaker and Jetz 2012). Problems deriving from the wedge-shaped operational space of the LSR–RSR relationship can be remedied by log-ratio transformation of LSR and RSR, coupled with a null model based solely on the presence of a statistically significant regression slope (Szava-Kovats et al. 2012). This method also can accurately measure curvature in the LSR–RSR relationship independent of the local and regional spatial scale, and thus may mitigate some of the autocorrelation deriving from large LSR/RSR ratios (Szata-Kovats et al. 2012). Finally, quasi-binomial generalized linear models (GLMs) can be used to model the probability of local species occurrence given their regional presence (Belmaker and Jetz 2012). Like log-ratio transfor-mation, the GLM method both mitigates the wedge-shaped operational space problem and provides a formal statistical means to estimate curvature (Belmaker and Jetz 2012).

Discussion

We have presented three hypotheses as to why regional effects on local communities may be a more firmly established

of local richness in this region indicated that as many as 40 coral species might coexist in an area subtended by a 10-m line transect (Cornell et al. 2008).

As far as we are aware, this is the only study to use varying degrees of isolation from a larger source pool to manipulate the size of regional species pools to test the LSR–RSR relationship. Marine systems may offer better opportunities to use this method than terrestrial systems because they are relatively more homogeneous and limits to dispersal potential are likely to derive mainly from dis-tance from a source, current speed, and current direction. Such limits may be simpler to identify than those due to the complicated topography and habitat heterogeneity characteristic of terrestrial systems. Moreover, the ubiquity of planktonic life stages and passive dispersal over longer distances suggests that dispersal abilities, although spe-cies might vary in larval stage lengths and survival rates, are likely to be more similar than in terrestrial systems. The variety of dispersal modes in terrestrial systems (wind, frugivory, phoresy, adult movement) may result in more variable dispersal potential that is more difficult to manip-ulate. The Indo-Pacific biogeographic region is a good example. Species diversity for both corals and fishes peaks near the Indonesian archipelago and declines east-ward toward Africa and westward toward South America (Connolly et al. 2003). Many fish and coral species disperse via planktonic larvae. Distance from Indonesia and pre-vailing current direction are likely to play important roles for both groups (Karlson and Cornell 1998, Connolly et al. 2003). Many other shallow-water marine taxa also show similar diversity gradients in this region (Renema et al. 2008).

Species pools can also vary among regions with similar environments for reasons other than regional size and isola-tion. Historical ‘accidents’ can also play a role. For example, temperate forest tree diversity is lower in Europe than in North America because of geography and higher extinc-tion in the latter half of the Tertiary in Europe (Latham and Ricklefs 1993) and mangrove diversity is lower in New vs Old World estuaries because of lower rates of lineage origi-nation (Ricklefs et al. 2006). Such effects can also provide opportunities to test regional effects on local richness.

Several approaches have been used to overcome the problems inherent in observational studies of regional and local richness. One is to carefully define the species pool to include only those species known to occur in environ-ments similar to those occupied by the local assemblage. Another solution is to incorporate environmental cova-riates of LSR and RSR directly into the analysis. Both approaches were used in a recent study exploring LSR–RSR relationships in the Californian flora (Harrison et al. 2006). Source pools were defined as only those species occupying the same soil type and elevational belt as the focal localities, and covariates including climate, soils, geologic age, and disturbance were considered. They found that the LSR– RSR relationship was strong and consistent after account-ing for correlated environmental variation at both local and regional scales.

The strength and form of the LSR–RSR relationship may depend on arbitrary definitions of local and regional spatial scales (Loreau 2000). One way to avoid arbitrary

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aspect of marine than terrestrial ecology: history of ideas, relative importance, and ease of study. While all three have some merit, we believe that terrestrial ecologists have been aware of and interested in regional effects on local communities for just as long as marine ecologists, so that the difference is not simply a matter of academic cultures. We believe the three explanations are probably linked; that is, because dispersal occurs more regularly and pre-dictably in marine systems, leading to readily observable effects on local communities, dispersal effects are easier to perceive and study, and therefore propagule supply has had a larger impact on the development of community theory in marine systems. In terrestrial systems, in con-trast, the role of regional dynamics is considerably harder to detect due to heterogeneous environments and slower and unpredictable dispersal dynamics. Nonetheless, island biogeographic studies, local–regional richness analyses, and micro- and mesocosm studies have demonstrated the importance of regional influences in terrestrial systems. We believe, in short, that regional processes are equally impor-tant in terrestrial communities but that they are necessar-ily studied in different and often less direct ways than in marine communities.

We have restricted our discussion to observational approaches, which in the past have suffered a number of statistical pitfalls including lack of independence and spatial autocorrelation in the data. There are now effective methods for avoiding these pitfalls (Harrison and Cornell 2008, Belmaker and Jetz 2012, Szava-Kovats et al. 2012) which need to be implemented in future studies compar-ing species richness at different spatial scales. In addi-tion, the various filters on local occupancy such as species sorting, environmental conditions, dispersal limitation and species interactions need to be identified and con-trasted using multi-predictor models (Harrison et al. 2006, Belmaker and Jetz 2012). It is also clear that observational studies should be complemented where possible by experi-mental approaches such as altering the size of the species pool and observing its effects on the richness and composi-tion of the local community. Such experiments have been repeatedly carried out in terrestrial and aquatic systems (Harrison and Cornell 2008), but less commonly in marine systems. In fact, studies of LSR–RSR relationships are generally much less common in marine systems (Cornell et al. 2008). This is unfortunate given the considerable opportunities marine systems offer for advancing our understanding of multiscale processes affecting species diversity. We conclude with the hope that marine ecologists will seize these opportunities and continue to contribute to our understanding of this important topic.

Acknowledgements – Many thanks are due to Josh Idjadi and Randi Rotjan for organizing the symposium ‘Surf and Turf: establishing new paradigms by integrating theory and forging partnerships between marine and terrestrial ecology’ for the 94th ESA Annual Meeting in 2009 where this paper was delivered. We also thank Matthew Bracken, Josh Idjadi, Randi Rotjan, Diane Srivastava and Jon Witman for heplful and perceptive comments on earlier versions of this paper. This work was funded by the College of Agricultural and Environmental Sciences, University of California, Davis.

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