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Dendritic Connectivity Controls Biodiversity Patterns in Experimental Metacommunities

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Dendritic Connectivity Controls Biodiversity Patterns in Experimental Metacommunities This document is the accepted manuscript version of the following article: Carrara, F., Altermatt, F., Rodriguez-Iturbe, I., & Rinaldo, A. (2012). Dendritic connectivity controls biodiversity patterns in experimental metacommunities. Proceedings of the National Academy of Sciences of the United States of America PNAS, 109(15), 5761-5766. https://doi.org/10.1073/pnas.1119651109 Dendritic connectivity controls biodiversity patterns in experimental metacommunities Francesco Carrara ∗ y,Florian Altermatt z y ,Ignacio Rodriguez-Iturbe x and Andrea Rinaldo ∗ { ∗Laboratory of Ecohydrology ECHO/IEE/ENAC, Ecole´ Polytechnique F´ed´eraleLausanne, 1015 Lausanne, Switzerland,zDepartment of Aquatic Ecology, Eawag, 8600 D¨ubendorf, Switzerland,xDepartment of Civil and Environmental Engineering, Princeton University, Princeton, NJ 08544, USA,{Dipartimento IMAGE, Universit`adi Padova, 35131 Padova, Italy, and yThese authors contributed equally to this work. Submitted to Proceedings of the National Academy of Sciences of the United States of America Biological communities often occur in spatially structured habitats vation. Directional dispersal refers to the pathway constrained where connectivity directly affects dispersal and metacommunity by the habitat connectivity and does not imply downstream- processes. Recent theoretical work suggests that dispersal con- biased dispersal kernels, that is, in all treatments dispersal strained by the connectivity of specific habitat structures, such as kernels were identical and symmetric. Disturbance consisted dendrites like river networks, can explain observed features of bio- of medium replacement and reflects the spatial environmen- diversity, but direct evidence is still lacking. We experimentally show that connectivity per se shapes diversity patterns in microcosm tal heterogeneity inherent to many natural systems (Materials metacommunities at different levels. Local dispersal in isotropic and Methods). lattice landscapes homogenizes local species richness and leads to The microcosm communities were composed of nine proto- pronounced spatial persistence. On the contrary, dispersal along zoan and one rotifer species, which are naturally co-occurring dendritic landscapes leads to higher variability in local diversity and in freshwater habitats, with bacteria as common food resource among-community composition. Although headwaters exhibit rela- [21]. These species cover a wide range of body sizes (Fig. 1B), tively lower species richness, they are crucial for the maintenance of intrinsic growth rates and other important biological traits regional biodiversity. Our results establish that spatially constrained [23] (see Table S1). Thus, the microcosm communities cover dendritic connectivity is a key factor for community composition and substantial biological complexity in terms of more structured population persistence. trophic levels and species interactions that can not be en- tirely captured by any model [24] (see Materials and Methods microbial metacommunities j directional dispersal j dendritic ecosystems j and SI ). Previous microbial experiments found that spatio- community ecology temporal heterogeneity among local communities induced by disturbance [25] and dispersal [26, 27, 28] events have a strong major aim of community ecology is to identify processes influence on species coexistence and biodiversity. In previous Athat define large-scale biodiversity patterns [1, 2, 3, 4, 5, works [28, 22, 20, 26] the focus was mostly on dispersal dis- 6, 7, 8]. For simplified landscapes, often described geometri- tance, dispersal rates and dispersal kernels, and how they af- cally by linear or lattice structures, a variety of local environ- fect diversity patterns in relatively simple landscapes. These mental factors have been brought forward as the elements cre- factors, directly affecting the history of community assembly ating and maintaining diversity among habitats [9, 10, 11, 12]. [29, 30], introduce variability in community composition in Many highly diverse landscapes, however, exhibit hierarchical term of abundances and local species richness. We specifically spatial structures that are shaped by geomorphological pro- studied basic mechanisms of dispersal and landscape structure cesses and neither linear nor two-dimensional environmental on diversity patterns in metacommunities mimicking realis- matrices may be appropriate to describe biodiversity of species tic network structures. Thus, our replicated and controlled living within dendritic ecosystems [13, 14]. Furthermore, in experimental design sheds light on the role of connectivity many environments intrinsic disturbance events contribute to in more structured metacommunities, disentangling complex spatio-temporal heterogeneity [14, 15]. Riverine ecosystems, natural systems' behavior [31]. among the most diverse habitats on earth [16], represent an outstanding example of such mechanisms [17, 18, 19, 7]. Here, we investigate the effects of directional dispersal im- posed by the habitat-network structure on the biodiversity Results and Discussion of metacommunities (`MC's), by conducting a laboratory ex- We compared the RN and the 2D landscapes focusing on three periment using aquatic microcosms. Experiments were con- measures of biodiversity: the number of species present in ducted in 36-well culture plates (Figure 1), thus imposing by a local community (훼-diversity), among-community diversity construction a metacommunity structure [20, 21]: each well (훽-diversity) and the number of LCs in which a given species hosted a local community (`LC') within the whole landscape is present (species occupancy) [7]. We found a significantly and dispersal occurred by periodic transfer of culture medium broader 훼-diversity distribution (Figs. 2 and 3A, B) in the among connected LCs [22], following two different geometries RN compared to the 2D landscapes (measured as the coeffi- [see Materials and Methods and Supporting Information (SI)]. We compared spatially heterogeneous MCs following a river network geometry (`RN'; Fig. 1D), with spatially homoge- Reserved for Publication Footnotes neous MCs, in which every LC has 2D lattice four nearest neighbors (`2D'; Fig. 1E). The coarse-grained RN landscape is derived from a scheme [13] known to reproduce the scaling properties observed in real river systems (Fig. 1A). To single out the effects of connectivity, we deliberately avoided reproducing other geomorphic features of real river networks, such as the bias in downstream dispersal, the grow- ing habitat capacity with accumulated contributing area or other environmental conditions connected to topographic ele- www.pnas.org/cgi/doi/10.1073/pnas.0709640104 PNAS Issue Date Volume Issue Number 1{9 cient of variation CV, CV RN = 0.265, CV 2D = 0.122, paired of the river network exhibits on average a higher species rich- t-test, t5 = 7.05, P = 0.0009). Furthermore 훽-diversity, here ness with respect to peripheral communities. described by the spatial decay of the Jaccard's similarity in- To explain the variability of the local species richness in dex (Materials and Methods, see also SI ), was higher in the the RN, we included two other factors in our analysis: the RN compared to the 2D landscapes (Fig. 3C). Mean local `ecological diameter' li of the LC i (strictly related to its species richness in RN was significantly lower compared to closeness centrality), and the temporal distribution of distur- bance events. The ecological diameter is simply defined as 2D landscapes (Fig. 2A-D, h훼iRN = 5.72, h훼i2D = 6.72, paired t-test, t5 = 9.23, P = 0.0003). These results confirm the average distance li = hdij ij of i from all the other LCs theoretical predictions on the role of directional dispersal from j in the RN, where dij represent the shortest (geodesic) dis- both individual- or metacommunity-based models [32, 7, 33]. tance between i and j [34]. We found that connectivity sig- Specifically, we experimentally observe that the anisotropy nificantly affected 훼-diversity in the RN landscape (ANOVA, induced by directional dispersal has a strong impact on the F1;5 = 12.09, P = 0.0006), whereas neither time to the last spatial configuration of the species occupancy, reflected in 훼- disturbance nor network centrality significantly affected local and 훽-diversity (Figs. 2A-D, 3E). This is a direct consequence species richness (ANOVA, F6;5 = 1.66, P = 0.13; and F4;5 = of the radically different distributions of closeness centrality, 0.71, P = 0.59) (see Fig. S3 and SI Text ). i.e., the mean geometric geodesic distance [34] and the mean We obtained 훽-diversity separately for headwaters and distance l between all LCs pairs (Fig. S6) in RN vs. 2D confluences, to test the difference in species composition landscapes (lRN = 5.33, l2D = 3) (see SI ). within the river network structure. Headwaters exhibit not In parallel to the experiment we developed a stochastic only a higher variability in 훼-diversity, but also a higher 훽- model, generalizing across spatial and temporal scales (Mate- diversity compared to confluences (Fig. 4B), confirming pat- rials and Methods). The model embeds spatio-temporal en- terns found in natural river basins [16, 18]. Therefore, the vironmental heterogeneity, and is based on a Lotka-Volterra difference in the loss of spatial correlation relative to lattice competition model. We simulated the dynamics of species landscapes appeared even higher when only headwaters were competing for space and food resources on the same trophic considered in the comparison. These results reveal the
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