Evolution and coevolution in mutualistic networks

A major current challenge in evolutionary biology is to understand how networks of interacting species shape the coevolutionary process. We combined a model for trait evolution with data for twenty plant-animal assemblages to explore coevolution in mutualistic networks. The results revealed three fundamental aspects of coevolution in species-rich mutualisms. First, coevolution shapes species traits throughout mutualistic networks by speeding up the overall rate of evolution. Second, coevolution results in higher trait complementarity in interacting partners and trait convergence in species in the same trophic level. Third, convergence is higher in the presence of super-generalists, which are species that interact with multiple groups of species. We predict that worldwide shifts in the occurrence of super-generalists will alter how coevolution shapes webs of interacting species. Introduced species such as honeybees will favour trait convergence in invaded communities, whereas the loss of large frugivores will lead to increased trait dissimilarity in tropical ecosystems.

The Missing Part of Seed Dispersal Networks: Structure and Robustness of Bat-Fruit Interactions

Mutualistic networks are crucial to the maintenance of ecosystem services. Unfortunately, what we know about seed dispersal networks is based only on bird-fruit interactions. Therefore, we aimed at filling part of this gap by investigating bat-fruit networks. It is known from population studies that: (i) some bat species depend more on fruits than others, and (ii) that some specialized frugivorous bats prefer particular plant genera. We tested whether those preferences affected the structure and robustness of the whole network and the functional roles of species. Nine bat-fruit datasets from the literature were analyzed and all networks showed lower complementary specialization (H(2)' = 0.3760.10, mean 6 SD) and similar nestedness (NODF = 0.5660.12) than pollination networks. All networks were modular (M=0.32 +/- 0.07), and had on average four cohesive subgroups (modules) of tightly connected bats and plants. The composition of those modules followed the genus-genus associations observed at population level (Artibeus-Ficus, Carollia-Piper, and Sturnira-Solanum), although a few of those plant genera were dispersed also by other bats. Bat-fruit networks showed high robustness to simulated cumulative removals of both bats (R = 0.55 +/- 0.10) and plants (R = 0.68 +/- 0.09). Primary frugivores interacted with a larger proportion of the plants available and also occupied more central positions; furthermore, their extinction caused larger changes in network structure. We conclude that bat-fruit networks are highly cohesive and robust mutualistic systems, in which redundancy is high within modules, although modules are complementary to each other. Dietary specialization seems to be an important structuring factor that affects the topology, the guild structure and functional roles in bat-fruit networks.

The modularity of seed dispersal: differences in structure and robustness between bat- and bird-fruit networks

In networks of plant-animal mutualisms, different animal groups interact preferentially with different plants, thus forming distinct modules responsible for different parts of the service. However, what we currently know about seed dispersal networks is based only on birds. Therefore, we wished to fill this gap by studying bat-fruit networks and testing how they differ from bird-fruit networks. As dietary overlap of Neotropical bats and birds is low, they should form distinct mutualistic modules within local networks. Furthermore, since frugivory evolved only once among Neotropical bats, but several times independently among Neotropical birds, greater dietary overlap is expected among bats, and thus connectance and nestedness should be higher in bat-fruit networks. If bat-fruit networks have higher nestedness and connectance, they should be more robust to extinctions. We analyzed 1 mixed network of both bats and birds and 20 networks that consisted exclusively of either bats (11) or birds (9). As expected, the structure of the mixed network was both modular (M = 0.45) and nested (NODF = 0.31); one module contained only birds and two only bats. In 20 datasets with only one disperser group, bat-fruit networks (NODF = 0.53 +/- A 0.09, C = 0.30 +/- A 0.11) were more nested and had a higher connectance than bird-fruit networks (NODF = 0.42 +/- A 0.07, C = 0.22 +/- A 0.09). Unexpectedly, robustness to extinction of animal species was higher in bird-fruit networks (R = 0.60 +/- A 0.13) than in bat-fruit networks (R = 0.54 +/- A 0.09), and differences were explained mainly by species richness. These findings suggest that a modular structure also occurs in seed dispersal networks, similar to pollination networks. The higher nestedness and connectance observed in bat-fruit networks compared with bird-fruit networks may be explained by the monophyletic evolution of frugivory in Neotropical bats, among which the diets of specialists seem to have evolved from the pool of fruits consumed by generalists.

Geographical variation in mutualistic networks: similarity, turnover and partner fidelity

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Disentangling social networks from spatiotemporal dynamics: the temporal structure of a dolphin society

Social networks are static illustrations of dynamic societies, within which social interactions are constantly changing. Fundamental sources of variation include ranging behaviour and temporal demographic changes. Spatiotemporal dynamics can favour or limit opportunities for individuals to interact, and then a network may not essentially represent social processes. We examined whether a social network can embed such nonsocial effects in its topology, whereby emerging modules depict spatially or temporally segregated individuals. To this end, we applied a combination of spatial, temporal and demographic analyses to a long-term study of the association patterns of Guiana dolphins, Sotalia guianensis. We found that association patterns are organized into a modular social network. Space use was unlikely to reflect these modules, since dolphins' ranging behaviour clearly overlapped. However, a temporal demographic turnover, caused by the exit/entrance of individuals (most likely emigration/immigration), defined three modules of associations occurring at different times. Although this factor could mask real social processes, we identified the temporal scale that allowed us to account for these demographic effects. By looking within this turnover period (32 months), we assessed fission-fusion dynamics of the poorly known social organization of Guiana dolphins. We highlight that spatiotemporal dynamics can strongly influence the structure of social networks. Our findings show that hypothetical social units can emerge due to the temporal opportunities for individuals to interact. Therefore, a thorough search for a satisfactory spatiotemporal scale that removes such nonsocial noise is critical when analysing a social system. (C) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms

Mutualistic interactions involving pollination and ant-plant mutualistic networks typically feature tightly linked species grouped in modules. However, such modularity is infrequent in seed dispersal networks, presumably because research on those networks predominantly includes a single taxonomic animal group (e.g. birds). Herein, for the first time, we examine the pattern of interaction in a network that includes multiple taxonomic groups of seed dispersers, and the mechanisms underlying modularity. We found that the network was nested and modular, with five distinguishable modules. Our examination of the mechanisms underlying such modularity showed that plant and animal trait values were associated with specific modules but phylogenetic effect was limited. Thus, the pattern of interaction in this network is only partially explained by shared evolutionary history. We conclude that the observed modularity emerged by a combination of phylogenetic history and trait convergence of phylogenetically unrelated species, shaped by interactions with particular types of dispersal agents.

Mistletoes Play Different Roles in a Modular Host-Parasite Network

Antagonistic interactions between host plants and mistletoes often form complex networks of interacting species. Adequate characterization of network organization requires a combination of qualitative and quantitative data. Therefore, we assessed the distribution of interactions between mistletoes and hosts in the Brazilian Pantanal and characterized the network structure in relation to nestedness and modularity. Interactions were highly asymmetric, with mistletoes presenting low host specificity (i.e., weak dependence) and with hosts being highly susceptible to mistletoe-specific infections. We found a non-nested and modular pattern of interactions, wherein each mistletoe species interacted with a particular set of host species. Psittacanthus spp. infected more species and individuals and also caused a high number of infections per individual, whereas the other mistletoes showed a more specialized pattern of infection. For this reason, Psittacanthus spp. were regarded as module hubs while the other mistletoe species showed a peripheral role. We hypothesize that this pattern is primarily the result of different seed dispersal systems. Although all mistletoe species in our study are bird dispersed, the frugivorous assemblage of Psittacanthus spp. is composed of a larger suite of birds, whereas Phoradendron are mainly dispersed by Euphonia species. The larger assemblage of bird species dispersing Psittacanthus seeds may also increase the number of hosts colonized and, consequently, its dominance in the study area. Nevertheless, other restrictions on the interactions among species, such as the differential capacity of mistletoe infections, defense strategies of hosts and habitat types, can also generate or enhance the observed pattern.

CLEANING ASSOCIATIONS BETWEEN BIRDS AND HERBIVOROUS MAMMALS IN BRAZIL: STRUCTURE AND COMPLEXITY

Birds that remove ectoparasites and other food material from their hosts are iconic illustrations of mutualistic-commensalistic cleaning associations. To assess the complex pattern of food resource use embedded in cleaning interactions of an assemblage of birds and their herbivorous mammal hosts in open habitats in Brazil, we used a network approach that characterized their patterns of association. Cleaning interactions showed a distinctly nested pattern, related to the number of interactions of cleaners and hosts and to the range of food types that each host species provided. Hosts that provided a wide range of food types (flies, ticks, tissue and blood, and organic debris) were attended by more species of cleaners and formed the core of the web. On the other hand, core cleaner species did not exploit the full range of available food resources, but used a variety of host species to exploit these resources instead. The structure that we found indicates that cleaners rely on cleaning interactions to obtain food types that would not be available otherwise (e.g., blood-engorged ticks or horseflies, wounded tissue). Additionally, a nested organization for the cleaner bird mammalian herbivore association means that both generalist and selective species take part in the interactions and that partners of selective species form an ordered subset of the partners of generalist species. The availability of predictable protein-rich food sources for birds provided by cleaning interactions may lead to an evolutionary pathway favoring their increased use by birds that forage opportunistically. Received 30 June 2011, accepted 10 November 2011.

The nested assembly of individual-resource networks

P>1. Much of the current understanding of ecological systems is based on theory that does not explicitly take into account individual variation within natural populations. However, individuals may show substantial variation in resource use. This variation in turn may be translated into topological properties of networks that depict interactions among individuals and the food resources they consume (individual-resource networks). 2. Different models derived from optimal diet theory (ODT) predict highly distinct patterns of trophic interactions at the individual level that should translate into distinct network topologies. As a consequence, individual-resource networks can be useful tools in revealing the incidence of different patterns of resource use by individuals and suggesting their mechanistic basis. 3. In the present study, using data from several dietary studies, we assembled individual-resource networks of 10 vertebrate species, previously reported to show interindividual diet variation, and used a network-based approach to investigate their structure. 4. We found significant nestedness, but no modularity, in all empirical networks, indicating that (i) these populations are composed of both opportunistic and selective individuals and (ii) the diets of the latter are ordered as predictable subsets of the diets of the more opportunistic individuals. 5. Nested patterns are a common feature of species networks, and our results extend its generality to trophic interactions at the individual level. This pattern is consistent with a recently proposed ODT model, in which individuals show similar rank preferences but differ in their acceptance rate for alternative resources. Our findings therefore suggest a common mechanism underlying interindividual variation in resource use in disparate taxa.

Changes of a mutualistic network over time: reanalysis over a 10-year period

We analyzed the structure of a multispecific network or interacting ants and plants bearing extrafloral nectaries recorded in 1990 and again in 2000 in La Mancha, Veracruz, Mexico. We assessed the replicability of the number of interactions found among species and also whether there had been changes in the network structure associated with appearance of new ant and plant species during. that 10-year period. Our results show that the nested topology of the network was similar between sampling dates, group dissimilarity increased, mean number of interactions for ant species increased, the frequency distribution of standardized degrees reached higher values for plant species, more ant species and fewer plant species constituted the core of the more recent network, and the presence of new ant and plant species increased while their contribution to nestedness remained the same. Generalist species (i.e., those with the most links or interactions) appeared to maintain the stability of the network because the new species incorporated into the communities were linked to this core of generalists. Camponotus planatus was the most extreme generalist ant species (the one with the most links) in both networks, followed by four other ant species; but other species changed either their position along the continuum of generalists relative to specialists or their presence or absence within the network. Even though new species moved into the area during the decade between the surveys, the overall network structure remained unmodified.

Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

The dimensionality of ecological networks

How many dimensions (trait-axes) are required to predict whether two species interact? This unanswered question originated with the idea of ecological niches, and yet bears relevance today for understanding what determines network structure. Here, we analyse a set of 200 ecological networks, including food webs, antagonistic and mutualistic networks, and find that the number of dimensions needed to completely explain all interactions is small (< 10), with model selection favouring less than five. Using 18 high-quality webs including several species traits, we identify which traits contribute the most to explaining network structure. We show that accounting for a few traits dramatically improves our understanding of the structure of ecological networks. Matching traits for resources and consumers, for example, fruit size and bill gape, are the most successful combinations. These results link ecologically important species attributes to large-scale community structure. © 2013 Blackwell Publishing Ltd/CNRS.

The role of predator overlap in the robustness and extinction of a four species predator-prey network

Predators and preys often form species networks with asymmetric patterns of interaction. We study the dynamics of a four species network consisting of two weakly connected predator-prey pairs. We focus our analysis on the effects of the cross interaction between the predator of the first pair and the prey of the second pair. This is an example where the predator overlap, which is the proportion of predators that a given prey shares with other preys, is not uniform across the network due to asymmetries in patterns of interaction. We explore the behavior of the system under different interaction strengths and study the dynamics of survival and extinction. In particular, we consider situations in which the four species have initial populations lower than their long-term equilibrium, simulating catastrophic situations in which their abundances are reduced due to human action or environmental change. We show that, under these reduced initial conditions, and depending on the strength of the cross interaction, the populations tend to oscillate before re-equilibrating, disturbing the community equilibrium and sometimes reaching values that are only a small fraction of the equilibrium population, potentially leading to their extinction. We predict that, contrary to one`s intuition, the most likely scenario is the extinction of the less predated preys. (C) 2010 Elsevier B.V. All rights reserved.

Abiotic factors shape temporal variation in the structure of an ant-plant network

Despite recognition of key biotic processes in shaping the structure of biological communities, few empirical studies have explored the influences of abiotic factors on the structural properties of mutualistic networks. We tested whether temperature and precipitation contribute to temporal variation in the nestedness of mutualistic ant-plant networks. While maintaining their nested structure, nestedness increased with mean monthly precipitation and, particularly, with monthly temperature. Moreover, some species changed their role in network structure, shifting from peripheral to core species within the nested network. We could summarize that abiotic factors affect plant species in the vegetation (e.g., phenology), meaning presence/absence of food sources, consequently an increase/decrease of associations with ants, and finally, these variations to fluctuations in nestedness. While biotic factors are certainly important, greater attention needs to be given to abiotic factors as underlying determinants of the structures of ecological networks.