Arrington D.A.1, 2 Winemiller K.O.1
1 Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, USA
2 Department of Biological Sciences, University of Alabama, Tuscaloosa, USA
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Key Words: beta diversity, colonization, community assembly, fishes, flood pulse, gamma diversity, spatiotemporal heterogeneity, Venezuela |
ABSTRACT
Historical and zoogeographic factors appear to explain the origin of Neotropical freshwater fish diversity, but proximate factors maintaining such remarkable levels of regional diversity, particularly in large floodplain rivers, remains unknown. Floodplain rivers are characterized by high levels of landscape and temporal heterogeneity. The littoral zone is composed of a mosaic of habitat templets upon which local communities are assembled and represents a highly dynamic component of the landscape due to seasonal water level fluctuations associated with the annual flood pulse. Results presented indicate littoral species are forced to continually disperse across the landscape in association with a moving land-water interface and lend support to an implicit theoretical trade off between colonization and competition ability among fishes of tropical floodplain rivers. The continual disassembly and reassembly (due to dispersal) of local communities across a spatially heterogeneous landscape should result in low extinction rates (i.e. at the regional level) and could theoretically maintain a nearly infinite regional species pool. Consequently, we suggest that the flood pulse paradigm should be expanded to include a potential mechanistic understanding of maintenance of high levels of beta and gamma diversity in floodplain rivers. Interactions among seasonal hydrology, variability in habitat structural complexity and landscape heterogeneity appear to maintain high aquatic species richness in these lowland rivers. It follows that alteration of seasonal water level fluctuation (e.g. damming) and habitat heterogeneity (e.g. channelization) should have substantial and negative consequences on the maintenance of regional biodiversity pools in floodplain rivers.
INTRODUCTION
Tropical floodplain rivers are home to the largest fraction of freshwater fish biodiversity (Dudgeon 2000; Lundberg 2001) and as such should be a focal point of global conservation efforts. Recently, conservationists have focused their efforts on species conservation through identification and conservation of hotspots (i.e. areas with high levels of endemism) (Meyers et al. 2000). Unfortunately, tropical rivers and associated fish faunas are absent from this conservation initiative (Meyers et al. 2000; Brooks et al. 2002). Not only have rivers been undervalued in conservation efforts, but also ecological understanding of community and assemblage dynamics in lowland rivers lags behind other fields of study (e.g. limnology in temperate lakes). We suggest that better conceptual understanding of these systems will lead to more effective conservation and restoration practices.
Recent studies have made great headway in understanding large-scale patterns of freshwater fish diversity. In an insightful review of the source of South American freshwater fish fauna richness, Lundberg (2001) identified area and latitudinal gradient as suitable explanations for large-scale maintenance of neotropical riverine freshwater fish diversity, but suggested that a historic-zoogeographic perspective is needed to understand the genesis of this diversity. Lundberg presented evidence that river basins were repeatedly transformed during periodic geological upheavals and changes in basin boundaries and inter-basin connections resulted in sympatric speciation opportunities. Lundberg reasoned that low baseline extinction rates resulted in the present-day richness of neotropical freshwater fish species.
Although historical and zoogeographic factors may explain the origin of neotropical freshwater fish diversity, there is little understanding of proximate factors (sensu Resetarits and Bernardo 2001) maintaining this remarkable diversity across the landscape at regional and local scales, particularly in large floodplain rivers. Fish assemblages in European and North American temperate forested lakes are structured by a series of nested filters operating first at regional and subsequently at local scales (Tonn 1990; Tonn et al. 1990). Stream fish assemblages in the same two regions (Europe and North America) also exhibited hierarchical structure with regional zoogeography and local habitat templets structuring local fish assemblages (Matthews 1998; Lamouroux, Poff and Angermeier 2002). Characterization of the relationship between regional and local fauna richness has been identified as a useful metric to evaluate the degree that species interactions regulate local community dynamics (Cornell and Lawton 1992; Hugueny and Cornell 2000). Cornell and Lawton (1992) stated that unsaturated assemblages are ubiquitous in nature and as a consequence regional richness is free of local constraints, although this logic has been seriously challenged (Shurin et al. 2000). Cornell and Lawton (1992) speculated that the regional species pool regulates local richness, which should be a function of landscape heterogeneity and evolutionary diversification. Empirical data have revealed that contemporary energy availability and habitat heterogeneity successfully predict the current global distribution of riverine fish diversity (Guégan, Lek and Oberdorff 1998). Furthermore, fish assemblages in Africa, North America and Western Europe may be either unsaturated i.e. non-interactive (Tonn et al. 1990; Hugueny and Paugy 1995; Griffiths 1997; Oberdorff et al. 1998) or saturated i.e. interactive (Tonn et al. 1990; Angermeier and Winston 1998). In their comparative study, Tonn et al. (1990) demonstrated that North American assemblages exhibited an asymptotic relationship between local and regional richness (i.e. interactive local assemblages), whereas European assemblages did not (i.e. non-interactive local assemblages). Similar to temperate lakes, North American stream fish assemblages (i.e. Virginia) also showed local community saturation (Angermeier and Winston 1998). The likelihood that neotropical fish assemblages are saturated seems high, because regional diversity in these settings is remarkably high (Jepsen 1997; Arrington and Winemiller 2003) yet alpha diversity is not substantially greater than similar North American samples (Matthews 1998), that have much lower regional diversity levels. Though a consensus on this subject has not been reached (Cornell and Lawton 1992; Shurin et al. 2000), the possibility exists that local community interactions may regulate regional species richness for fishes in neotropical rivers.
Much attention has focused on spatiotemporal dynamics in lotic environments as a mechanism for maintaining biodiversity (e.g. Schlosser 1987; Townsend 1989; Ward 1989, 1998; Poff and Allan 1995; Matthews 1998; Schlosser and Kallemeyn 2000; Oberdorf, Hugueny and Vigneron 2001). Recent work conducted on European floodplain rivers has characterized landscape attributes of floodplain rivers as shifting mosaics of habitat features with varying levels of among-habitat connectivity (Ward, Tockner, Arscot et al. 2002; Amoros and Bornette 2002). The combination of landscape heterogeneity and temporally variable among-patch connectivity are common features of floodplain rivers that result in observed patterns and levels of biodiversity (Ward 1998; Ward et al. 1999; Ward et al. 2001; Tockner et al. 1999; Amoros and Bornette 2002; Robinson et al. 2002). The general synopsis is that a dynamic landscape composed of a mosaic of habitat patches in various successional states maintains the high regional diversity levels observed in floodplain rivers. This should be the case whether or not local communities are saturated, because effects of landscape and temporal heterogeneity should overcome competitive exclusion (Levin and Paine 1974; Chesson and Huntley 1997; Hurtt and Pacala 1995).
In this limited review, we hope to address the following questions based on experience with fish assemblages in neotropical floodplain rivers. How are neotropical fishes organized across the river-floodplain landscape? What factors influence assemblage structure in these local communities? How are such large regional species pools maintained?
ORGANIZATION OF FISH DIVERSITY IN TROPICAL FLOODPLAIN RIVERS
Characterization of patterns of species occurrences and relative abundance is a major goal in community ecology (Hubbell 2001). A central debate among community ecologists has been the role of deterministic versus stochastic processes often inferred through examination of random or non-random patterns in assemblage data. Studies of fish assemblages in temperate streams have demonstrated both random (Grossman, Moyle and Whitaker 1982; Grossman et al. 1998) and non-random patterns (Meffe and Sheldon 1990; Jackson, Somers and Harvey 1992; Taylor 1996), with results often strongly dependent on the spatial, temporal and numerical scale of the study (Rahel 1990, Angermeier and Winston 1998). Tropical floodplain rivers have been studied less frequently and have yielded mixed results. Goulding, Carvalho and Ferreira (1988) concluded that fish assemblages of the Río Negro (Brazil) were random associations of species. More recent studies also support the random association hypothesis (Jepsen 1997; Saint-Paul et al. 2000).
A few studies in tropical river systems have concluded fish assemblages are structured in a nonrandom manner. Working in the same system as Jepsen (1997), Arrington (2002) documented non-random structure of fish and macroinvertebrate assemblages among major habitat types (e.g. sandbank, leaf litter, submerged wood) located in the moving littoral. Fish assemblages in these local habitats were maximally structured during the low-water period and less structured in rising- and falling-water periods. Consequently, juxtaposition of multiple habitat types and the resulting landscape heterogeneity resulted in high levels of observed beta diversity, which substantially influenced the estimate of the regional species pool. Similarly, fish assemblages on the floodplain of the Brazillian Amazon were found to be non-randomly structured among major habitat types (Petry, Bayley and Markle 2003), though habitats in this study were characterized by dominant macrophytes. Others have shown fish assemblage structure in tropical rivers is influenced by water type (Ibarra and Stewart 1989; Cox Fernandes 1999), sample depth (Lundberg et al. 1987; Stewart, Ibarra and Barriga-Salazar 2002; Hoeinghaus et al. 2003), seasonally falling water levels (Cox Fernandes 1999) and diel period sampled (Arrington and Winemiller 2003). Rodriguez and Lewis (1997) found structured assemblage patterns in Orinoco floodplain lakes that were correlated with water clarity. They inferred predation by alternative predators in clear or turbid lakes was driving assemblage structure. As Winemiller (1996) hypothesized, tropical floodplain river fish assemblages appear to be structured by both stochastic and deterministic processes and the magnitude of these processes varies seasonally (Arrington 2002).
MAINTENANCE OF FISH DIVERSITY IN TROPICAL FLOODPLAIN RIVERS
We suggest that the flood pulse paradigm be expanded to include a potential mechanistic understanding of maintenance of high levels of beta and gamma diversity in floodplain rivers. We hypothesize that the flood pulse (Junk, Bayley and Sparks 1989), i.e. the annual hydrologic pattern of predictable flooding of lateral floodplain habitats in large tropical rivers, regulates community assembly patterns and regional diversity levels. As conceived by Junk et al. (1989), the flood pulse concept linked riverine productivity to predictable annual patterns of flooding and characterized the main channel as a passageway for fish migrations. Although some fish species undoubtedly use the main channel for migration (Junk et al. 1989; Fernandes 1997; Wei et al. 1997; Duque, Taphorn and Winemiller 1998), many species either seasonally (low water) or consistently occupy main channel habitats (e.g. deep channel, shifting sandbanks, snag complexes). We shift our focus from the main channel/highway analogy (Junk et al. 1989) to the moving littoral as a dynamic habitat template. We define the moving littoral as the dynamic land-water ecotone occurring along main channel margins and extending onto the floodplain during high water. The moving littoral, thus, represents a highly dynamic component (i.e. shallow water) of the landscape composed of a mosaic of habitat templets upon which local communities are assembled (Southwood 1988; Townsend 1989; Bayley 1995; Arrington 2002; Petry et al. 2003). Furthermore, local habitat templates in the moving littoral may be thought of as being disturbed at some intermediate level (Connell 1978; Townsend, Scarsbrook and Dolédec 1997; Ward et al. 1999; Sheil and Burslem 2003) due to the seasonally predictable patterns of drying and wetting in lowland rivers (Junk et al. 1989; Arrington and Winemiller 2003).
As discussed above, there is considerable debate regarding the roles of deterministic and stochastic processes regulating local fish assemblages. A new hypothesis receiving considerable attention is Hubbell’s (2001) "neutral theory", which assumes per capita equivalence of within-trophic-level community members. Community change is assumed to occur through stochastic ecological processes and random speciation. Application of the neutral theory has resulted in the generation of multiple testable predictions, which can serve as working null hypotheses in community studies. For example, local communities are expected to be sub-sets of the larger metacommunity, with species relative abundance equal between the two when migration rates into the local community are non-trivial (Hubbell 2001).
Previous studies have shown the importance of immigration rates on the structure (including richness) of local communities (MacArthur and Wilson 1967). Dispersal rates determine the importance of local community regulators in zooplankton assemblages (Jenkins and Buikema 1998) and predominantly limit diversity in newly formed assemblages (Shurin et al. 2000). Temporal variation of fish assemblage structure in a Brazilian estuary has been linked to fish immigration and emigration dynamics (Garcia, Vieira and Winemiller 2001). For temperate streams, Schlosser (1987) offered a conceptual model indicating the generalized importance of immigration and extinction processes for the development of fish assemblage attributes. Using Schlosser’s model as a starting point, Taylor and Warren (2001) showed stream fish immigration rates were positively related to stream size and negatively related to flow variability. They then documented patterns of nestedness in fish assemblage structure that were positively related to extinction rates and negatively related to immigration rates. They also observed that colonization and extinction dynamics of species appeared "more or less random" in habitats with high immigration rates, a result predicted by Townsend’s (1989) patch dynamics concept.
Recent work by Arrington, Winemiller and Layman (in review) examined the influence of colonization rate and habitat complexity on the dynamics of local fish assemblages in the Cinaruco River, a floodplain river located in the Venezuelan llanos. Habitat patches of varying complexity and colonization rates were created within broad main-channel sandbanks and were colonized by fishes and macroinvertebrates for a period of 21 days. In accordance with island biogeography theory, Arrington et al. found a significant positive influence of colonization rate on the number of species in local habitat patches. Furthermore, they observed more complex habitats contained significantly more species. Results varied when treatment effects were evaluated separately for two distinct subsets of the fish assemblage. Richness of fish taxa with low vagility was positively related to colonization rate and habitat patch complexity, whereas richness of highly vagile fishes was positively related to patch complexity but not colonization rate. Presumably, increased colonization ability by vagile species swamped the influence of habitat patch isolation. These results suggest local community dynamics in this neotropical floodplain river are dominated by near continuous dispersal and colonization of habitat patches in the moving littoral (sensu "patch dynamics concept" Townsend 1989) by adult fishes (Arrington et al. in review). Furthermore, low concordance was observed between ranks of species from the meta-community and local habitat patches; thus falsifying one of Hubbell’s (2001) hypotheses (see above). In a parallel experiment, Arrington et al. (in review) documented largely stochastic structure of local assemblages in newly formed habitat patches, but increasing levels of non-random organization were observed in patches as time progressed (> 24 days). Taken together, these data suggest dispersal is most important in structuring assemblages in newly formed patches, whereas the influence of local processes on assemblage structure increases as time progresses.
A considerable body of ecological theory has been developed that indicates tradeoffs in colonization and competitive abilities should preclude competitively dominant species from occupying all suitable habitats in a spatially heterogeneous landscape (i.e. the moving littoral of floodplain rivers) and as a consequence competitive subordinates should persist in the regional species pool (Levin and Paine 1974; Hurtt and Pacala 1995). The experiments by Arrington et al. lend support to an implicit theoretical trade off between colonization and competition ability in fishes of tropical floodplain rivers, where littoral species are forced to continually disperse across the landscape in association with a moving land-water interface. This continual disassembly and reassembly (due to dispersal) of local communities across a spatially heterogeneous landscape should result in low extinction rates (i.e. at the regional level) and could theoretically maintain a nearly infinite regional species pool (Hurtt and Pacala 1995).
Additional studies on the Cinaruco River appear to support such a mechanism in maintaining a very large regional species pool in a tropical floodplain river (Arrington 2002). Through most of 1999, six habitats were sampled from the moving littoral zone in the Cinaruco River. These habitats function as habitat templets, upon which local communities are assembled (Arrington 2002) and their spatial distribution in the main channel and floodplain is a dominant component of spatial habitat heterogeneity. Each month seven replicate diurnal samples were collected using the same seine (see Arrington 2002 for a description of methods). We plotted fish species accumulation curves for each habitat independently (Figure 1). In each habitat, we observed a continual and positive slope of the accumulation curve, with observed total assemblage richness (ã diversity) reaching 50 to 80 fish species per habitat type. In addition to observed species richness values, we estimated ã diversity for specific littoral zone habitats using a non-parametric estimator based on observed relative abundance data. The technique, known as abundance-based coverage estimator, assumes information about un-sampled species is held in the rarest classes of species collected (Chao and Lee 1992; Colwell and Coddington 1994; Chazdon et al. 1998) and can be computed using freely-available soft- ware (Estimate S, Colwell 1997). In some habitats, such as river rock (Figure 1), the estimated size of the species pool far exceeds observed values. These local communities were consistently composed of relatively rare species. Thus, it appears that community assembly within isolated habitat patches, such as our river rock habitats, are more dependent upon stochastic colonization processes (i.e. colonization limitation). Furthermore, these patches often contained species characteristic of adjacent open sandbank habitats, which suggests leaky boundaries may lead to "mass effects" (Townsend 1989) in local patches that are not biologically saturated. Others have hypothesized that low dispersal or connectivity among patches should result in lowered á diversity, but promote â and ã diversity (Hubbell 1997), particularly in floodplain rivers that are characterized by high levels of spatiotemporal heterogeneity (Ward et al. 1999; Tockner et al. 1999; Amoros and Bornette 2002). In more contiguous (higher connectivity) patches, lower estimates of total richness may reflect reduced persistence of rare (Hubbell 2001) or competitively inferior (Hurt and Pacala 1995) species with higher colonization rates (higher á diversity but lower â diversity; Amoros and Bornette 2002). At present we are unable to identify the mechanism(s) driving the difference between observed and expected diversity (Figure 1). But, our experimental results indicate that a combination of colonization limitation (dispersal) and biotic interactions result in low á diversity but high â diversity (Arrington et al. in review). We submit that the annual flood pulse interacts with basin geomorphology and adds temporal heterogeneity to an already spatially heterogeneous landscape, both of which are critical in maintaining high levels of ã diversity observed in lowland tropical rivers (Figure 2).
Figure 1. Species accumulation curves for standardized seine samples collected from six habitats located in the moving littoral zone of the Cinaruco River, Venezuela reveal the diversity of tropical floodplain fish assemblages. Samples were collected through most of 1999, excluding the peak-wet season (see Arrington 2002). Number of samples collected per habitat was: river rock 45, river sand 69, river snag 47, lagoon leaf 36, lagoon sand 36 and lagoon snag 31. Each point along the solid line represents an estimate of the total community richness (including taxa not sampled) for specific littoral zone habitats based on the relative abundances of the most rare species in our samples (see Colwell 1997).
THREATS TO FISH DIVERSITY IN TROPICAL FLOODPLAIN RIVERS
Rivers face a number of anthropogenic threats (Allan and Flecker 1993; Crisman et al. 2003) and dam building appears particularly damaging to tropical riverine biodiversity (Grossman, Dowd and Crawford 1990; Goulding, Smith and Mahar 1996; Pringle et al. 2000). Large floodplain rivers are characterized by a remarkable degree of spatiotemporal heterogeneity in their natural state (Ward et al. 1999, 2001, 2002) and this heterogeneity is maintained by fluvial dynamics acting on landscape features. In the Tagliamento River (Italy) corridor, for example, landscape features experienced up to 80 percent turnover in a 3-year period, but features maintained similar relative proportions across the landscape (Ward et al. 2001). Construction of dams for flood control or hydroelectric power generation constrains these fluvial dynamics and can result in dramatic loss of spatial heterogeneity (Toth et al. 1995; Schmidt et al. 1998). If the interaction between the natural rise and fall of flood waters and floodplain spatial heterogeneity (habitat templates for organisms) maintains regional diversity levels in tropical floodplain rivers (Figure 2), then loss of the flood pulse not only will impact biological production (Junk et al. 1989; Bayley 1995), but impoverish regional species pools (Grossman et al. 1990; Ward et al. 1999). Furthermore, reduction of landscape heterogeneity may impair the resilience typically observed in these systems (Townsend 1989; Meffe and Sheldon 1990; Townsend et al. 1997). Consequently, restoration strategies for floodplain rivers must emphasize the return of hydrologic variability characteristic of the pre-impacted system (e.g. Toth, Arrington and Begue 1997) as well as re-establishing among-habitat connectivity (Toth et al. 1998).
Figure 2. A conceptual model illustrating the importance of spatiotemporal heterogeneity in maintaining biological diversity in floodplain rivers. This model is derived from the intermediate disturbance hypothesis (Connell 1978; Shiel and Burslem 2003) and the "patch dynamics concept" (Townsend 1989) and is supported by fish data collected from the Cinaruco River, Venezuela, an unregulated, tropical lowland river. Anthropogenic alterations such as channelization and flow regulation are expected to result in compromised heterogeneity; direction of impact is indicated by dotted lines.
Interactions among seasonal hydrology, variability in habitat structural complexity and landscape heterogeneity appear to maintain high aquatic species richness in these lowland rivers. It follows that alteration of seasonal water level fluctuation (e.g. damming) and habitat heterogeneity (e.g. channelization) should have substantial and negative consequences on the maintenance of regional biodiversity pools in floodplain rivers. Better ecological understanding is needed to properly manage and preserve biological diversity in tropical floodplain rivers.
ACKNOWLEDGEMENTS
Our research was funded by the National Science Foundation (NSF DEB-0107456), The National Geographic Society, L.T. Jordan Institute and the International Sportfish Fund. This work would not have been possible without the help and assistance of J. Arrington, C. Garcia, J. Garcia, C. Layman, C. Lofgren, C. Marzuola, J. Marzuola, E. Pelaez, A. Stergios, B. Stergios, D. Taphorn and G. Webb. C. Layman and an anonymous reviewer provided helpful comments on this manuscript.
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