Two of the predictions of the metacommunity model (Fig. 1a and c) are fully confirmed in stream periphytic diatoms and fish, but partially in benthic invertebrates (due to the lack of body size data): (1) body size controls directly and/or indirectly species properties manifested from the organismal to the metapopulation level, including niche breadth, maximum local abundance and regional distribution; and (2) the strong positive relationship between abundance and distribution reflects their equivalent response to common determinants, namely body size and niche breadth. Across groups, species with the highest maximum abundance and regional prevalence possess the broadest niches; however, the influence of body size is group-specific. In diatoms, these species are small, whereas in fish, they are of intermediate body size within a very narrow range, i.e. between 41 and 62 g. Thus, the prediction for positive relationships of body size with niche breadth, abundance and distribution in macroorganisms (Fig. 1c) is not confirmed in fish. This divergence from the model expectation is attributed to the complex life history tradeoffs in fish, imposing constraints on extreme body sizes, i.e. small fish experience higher mortality and reproductive effort, while large fish reach maturity later (Gunderson 1997). Collectively, these limitations should give advantage to intermediate sizes, as seen not only here but also in fish from different areas of the marine environment, including the demersal zone and the coral reefs (Blackburn & Lawton 1994; Ackerman et al. 2004). A peak population density at intermediate threshold body size was also reported in birds and explained with the operation of energetic constraints below the threshold (i.e. increased energy requirements per unit mass) vs. energetic tradeoffs above it (i.e. energy controlled biomass-for-density tradeoff) (Brown & Maurer 1987). Evidently, the density-body size relationship in large macroorganisms is frequently unimodal, but further research is necessary to elucidate whether life history or energetic constraints or both are responsible for this pattern. Diatoms, on the other hand, conform to the model expectations – the small size is beneficial all around, promoting faster turnover rates, broader dispersal and greater disturbance resistance, all leading to high abundance and distribution. Similar inverse relationships of body size with abundance and distribution were found in herbivorous insects (Gaston & Lawton 1988), suggesting that this trend may persist among smaller organisms both protists and multicellular forms across aquatic and terrestrial environments, as predicted in Fig. 1a.
The metacommunity model sheds light on a long-standing controversy in ecology as to whether species characteristics, i.e. niche breadth (Brown 1984), or environmental properties, i.e. resource availability (Hanski et al. 1993), define the relationship of species abundance with distribution. Criticism of the resource use hypothesis points to unclarity as to why species with broader niches should exhibit greater local abundance and redundancy in comparison with the resource availability hypothesis, which explains the same patterns, but without invoking variability in niche breadth (Gaston et al. 1997). The present results disagree with this assessment of the resource use hypothesis. Across all major freshwater organismal groups, niche breadth is a dominant factor behind the variability in maximum abundance (R 2 = 0.27–0.40) and regional distribution, including occurrence and geographical range (R 2 = 0.55–0.92). On the contrary, habitat and resource availability appears to be of little consequence as species with a preference for common or rare conditions have highly significantly narrower distributions than species with no environmental preference (Suppl. Figure S3). In diatoms, species with a preference for common conditions exceed in distribution those with a preferential occurrence in the pristine, but rare habitats, whereas in invertebrates and fish, this trend disappears. Therefore, an adaptation for common environments is insufficient to confer a species broad distribution. Finally, body size underlies all relationships depicted in the metacommunity model (Fig. 3d; Figures S4c, S5d) – species with the widest niches, highest abundances and broadest distributions have optimised body sizes, i.e. small in diatoms, but intermediate in fish.
An earlier study on Finnish diatoms demonstrated that even though niche breadth was a significant predictor of regional distribution, it was secondary to niche position (a measure of how common species' habitat was) (Heino & Soininen 2006). Investigations on French riverine fish (Tales et al. 2004) and British breeding birds (Gregory & Gaston 2000) found that local density and distribution correlated with niche position, but not niche breadth. Although the use of different methods for measuring niche breadth and habitat commonness may have contributed to the divergent conclusions of these studies and the present work, the main cause is most likely the dissimilarity in taxonomic diversity and in the number and length of the underlying environmental gradients and with this, the ability to adequately measure species niche breadth. In particular, the Finnish diatom study was restricted to near pristine sites in the boreal region (Heino & Soininen 2006) and the fish study, to a small number of most common and native fish (29 species) across undisturbed, reference sites only (Tales et al. 2004). This investigation, on the other hand, is based on continental variability in climate, topography, nutrient supply and human impact as well as the occurrence of all members of a particular group, including native and introduced, common and uncommon. In the bird study (Gregory & Gaston 2000), resource variables were not explicitly incorporated, while the used descriptors, reflecting primarily land use, might have been incapable of capturing important niche properties. As recently shown, even substantial anthropogenic modifications of the terrestrial landscape, such as urbanisation, are not strong enough to generate commensurate community responses because remnant habitats are sufficient to maintain the bird community structure (Pautasso et al. 2011). In contrast, cultural eutrophication of aquatic ecosystems leads to pronounced alterations across communities (Smith & Schindler 2009), which can explain why invertebrates and fish conform to the hypothesised patterns even though their niche is defined here by habitat, but not resource variables.
The present findings also provide an answer to two fundamental, but still open questions in ecology, i.e. are resource generalists broadly distributed, while specialists, uncommon and does this pattern hold in microbial communities with theoretically unlimited dispersal (Finlay et al. 2002; Telford et al. 2006; Pither 2007; Bennett et al. 2010). As revealed here, the distribution of freshwater organisms scales strongly and positively with niche breadth, indicating that narrowing of the niche brings about a corresponding decline in distribution. Contrary to perceptions that body size diminution expands distribution, but only in larger bodied species, e.g. over 1–10 mm in length (Finlay 2002), I demonstrate that: (1) size matters even within microbial communities with small species having significantly greater distributions than large forms and (2) the influence of body size is not always linear, i.e. a decrease in body size beyond a certain optimum in fish is not beneficial for maintaining high abundance and distribution.
The community model (Fig. 1b and d) is confirmed in diatoms, but to a lesser extent in fish. The lack of body size data in invertebrates results in a partial support of the model. Richness determines the relationships of population density with body size and distribution, regardless of their shape, described by either power laws or quadratic functions. In diatoms, the environment constrains both richness and slopes b and d, but its effect on the two slopes is mostly indirect through richness. Pure environment in invertebrates and fish and environment-richness covariance in fish contribute to the explained variance in slope d and parameter b 2 (in fish), whereas richness is a weaker predictor compared to diatoms. This may be due to the fact that, unlike diatoms, invertebrates and fish encompass multiple trophic levels and habitat guilds. Richness, which gives the same weight to all taxa, regardless of their ecological differences, may underrepresent the true diversity of these communities and consequently, correlates less strongly with the scaling exponents and regression parameters. Therefore, further tests of the hierarchical theory at a functional level are necessary.
A pathway of watershed impact on stream diatom biodiversity through local control of nutrient concentrations has already been established (Passy 2010), but I show here that important community scaling relationships across freshwater groups are too part of this pathway. In diatoms, the negatively correlated slopes b and d become the flattest in productive species-rich streams with elevated nutrient concentrations due to cultural eutrophication or proximity to large and Fe-abundant wetlands. In contrast, the steepest b and d slopes are found in species-poor oligotrophic streams in undeveloped watersheds with extensive forest or barren land covers. Thus, rich communities have a greater proportion of their biomass derived from large and rare species, whereas the biomass of impoverished communities comes primarily from small and common species, as predicted (Fig. 1b). A community shift towards greater numbers of large diatoms with Fe and macronutrient enrichment is a well-documented phenomenon in many parts of the world's ocean (de Baar et al. 2005). Here, I report a similar transition across the continental stream network, evident in the positive correlations of slope b with Fe and N fertilisation. It has already been suggested that Fe controls diatom richness globally (Passy 2010) and now it becomes clear that diatom body size organisation is influenced by Fe across aquatic environments as well.
The predictable deviation of slope b from −0.75 (Fig. 4a), i.e. the condition necessary for energetic equivalence (Damuth 1981), allows estimation of the resource partitioning patterns among coexisting diatoms. Communities of about 15 species, clustered at the low end of the richness gradient, have slopes approaching −0.75. In communities of higher richness, which are the majority, large species acquire disproportionately more of the shared resources (b > −0.75), whereas the opposite is true in the few communities of richness lower than 15. Previous studies on organisms, ranging from plants to mammals, demonstrated that large species monopolised greater resource amounts and attributed this to their lower energy requirements per unit biomass, tolerance to broader environmental gradients, greater mobility, weaker predation pressure and stronger aggression than small species (Brown & Maurer 1986; Pagel et al. 1991). As seen here, both small and large diatoms reach densities much higher than expected under the energetic equivalence rule, although it is much more common for large species to do so. However, most of the aforementioned reasons for this disparity are inapplicable to diatoms. The shift from small species' to large species' control of the energy flow across diatom communities is environmentally determined (Fig. 5a), which is expected under the benthic model (Passy 2008a) and the present community model (Fig. 1b). Large species are unable to grow well in oligotrophic environments (slope b < −0.75), but their advantageous position in the overstory under high nutrient supply, affording unimpeded access to resources, results in substantial biomass accumulation (slope b > −0.75). Conversely, small species persist across all environments due to their high tolerance to nutrient limitation and even though with reduced biomass when overgrown in eutrophic conditions, their density consistently exceeds this of large species (slope b < 0). Thus, the energy distribution among differently sized diatoms is a function of environmental inputs, having an impact on reproduction, and biofilm three-dimensional spatial organisation, with an influence on both reproduction and competition.
A comparatively overlooked aspect of the density-body size relationship is that species not only consume resources but also contribute to community biomass, which is then used by higher trophic levels (Cohen et al. 2003). As established here, species of different size and distribution are responsible for biomass accrual in communities of contrasting biodiversity. Diatoms are major producers in streams and their body size organisation influences herbivore composition, e.g. invertebrate grazers preferentially ingest diatoms with sizes commensurate with their head width (Tall et al. 2006). This implies that rich diatom communities, with more equitable biomass distribution across the body size spectrum (i.e. flatter b slopes), provide food resources for a broader diversity of herbivores.
In invertebrates, the highest values of slope d are found in poor communities, which unlike diatoms, are located in impacted habitats. In contrast, pristine forested watersheds are inhabited by rich invertebrate fauna exhibiting lower values of slope d, consistent with the model prediction for a negative richness–slope d relationship (Fig. 1b). Agriculture and/or urbanisation are associated with: (1) deforestation and subsequent stream bank erosion, elevated stream turbidity and siltation and decreased leaf litter inputs; (2) an increased area of impervious surfaces, affecting the intensity of urban runoffs and (3) benthic habitat loss and homogenisation, all with negative consequences for invertebrate community richness (Allan 2004; Walsh et al. 2007; Bêche & Statzner 2009; Death & Collier 2010). Here, we see that these stream alterations are also correlated with significant density reductions in regionally rare invertebrates, evident in the significant increase in slope d (Suppl. Figure S7b). Diatom local richness, on the other hand, is not as sensitive to the aforementioned habitat modifications (Passy & Blanchet 2007), but responds positively to nutrient enrichment, which explains why diatoms and invertebrates display contrasting patterns along the anthropogenic impact gradient.
In fish, temperature and land use have strong effects on richness as well as parameter b 2 and slope d. Consistent with previous observations (Oberdorff et al. 1995; Knouft & Page 2011), streams of higher temperature, found at lower elevations, have greater richness. As these streams are often located in human-modified watersheds, fish richness also responds positively to agriculture, which too has been previously reported (Strayer et al. 2003). On the contrary, shrublands occur in watersheds of higher elevation and lower temperature and they are a negative predictor of fish richness. The comparatively limited dispersal of fish and their strong response to stochastic flow disturbance (Grossman et al. 1998) are probably the reasons why parameter b 2 and slope d are generally non-significant. Their greater variability at low richness suggests that species-poor fish communities are more susceptible to environmental stochasticity and thus more unpredictable. In comparison, fish parameter b 2 and slope d are highly significant in the metacommunity, where they are derived from the continental metapopulations, transcending the local environmental vagaries. Diatom and invertebrate communities, on the other hand, even though subjected to the same environmental fluctuations as fish, display generally significant scaling exponents, varying predictably along the richness- and habitat gradients. There are multiple reasons why diatom and invertebrate patterns persist at a community level despite local disturbance, including shorter generation times (allowing proliferation between major flow events), adaptations for withstanding drag (e.g. substrate attachment and growth on sheltered surfaces), benefit from the higher supply of resources in faster currents and comparatively unlimited dispersal, facilitated by small sizes and large local population densities, providing a continuous supply of colonists. In the cases where fish parameter b 2 and slope d are significant, they exhibit opposite responses along the richness gradient. Thus, in species-poor communities, found in non-impacted watersheds of low temperature, rare fish of generally extreme body sizes maintain high densities. Conversely, common fish of intermediate body size predominate in speciose communities, inhabiting streams of high temperature and human disturbance. This discrepancy with the model prediction for a negative richness–slope d relationship across all groups (Fig. 1b and d) is due to the already discussed erratic behaviour of species-poor fish communities, where slope d is frequently negative, driving the relationship with richness in a positive direction. These results reveal a tendency of rare species of both invertebrates and fish to maintain greater density in the vanishing pristine streams, which may be a contributing factor to the unprecedentedly high extinction rates in freshwater fauna (Ricciardi & Rasmussen 1999).
As shown here, the response of population density to body size and distribution cannot be described by an invariant power law, but by a wide variety of power laws or quadratic models with scaling exponents or coefficients dependent on the environment and richness. Consistent with other field observations (Cyr 2000; Knouft 2002), energetic equivalence in the trophically homogenous diatoms is inconceivable, whereas in fish, encompassing different consumer guilds, it is improbable, given the distinct quadratic abundance-average body weight relationship at the level of the whole community. The combination of two factors is most likely responsible for this departure from energetic equivalence: (1) size is coupled with niche breadth – broad niches are associated with small sizes in diatoms, but intermediate sizes in fish and (2) environmental variability in streams is substantial, e.g. resource supply ranges from extreme natural limitation to extreme anthropogenic enrichment and flow disturbance, from intermittent to continuous. Therefore, species of different size will produce biomass along the wide resource and disturbance gradients, giving rise to environmentally constrained abundance-body size and abundance-distribution relationships. Considering that other important power laws too depend on the environment, e.g. the home range-body size (Haskell et al. 2002), ecologists should broaden their search for environmental causes of community scaling behaviour.
The novel mathematical formulation of the abundance-distribution relationship, i.e. N ~ D −ln S , has profound implications for conservation planning, which is faced with the difficult challenges of selecting the right targets of conservation action and managing their landscape requirements (Schwenk & Donovan 2011). The new power function, showing that as community richness increases so does the abundance of rare species, is confirmed in both diatoms and invertebrates. If a similar richness dependence of the abundance-distribution relationship is found in communities of threatened species, changes in environmental protection and species conservation policies may ensue. Specifically, broad community-based conservation efforts to promote biodiversity will be adequate for increasing the abundance, and with this, the chance of survival of rare and potentially endangered species.
In conclusion, the present hierarchical theory explains the variability of the relationships among body size, abundance and distribution in the major organismal groups in streams from a metacommunity to a community level. It elucidates that the driving mechanisms differ along this hierarchy with evolutionarily constrained species traits, e.g. body size and niche breadth, giving way to environmental forces, e.g. resource supply, temperature and human impact. These findings emphasise the necessity for better integration of macroecology and environmental science.