The effect of space in plant–animal mutualistic networks: insights from a simulation study

The topology of plant–animal mutualistic networks has the potential to determine the ecological and evolutionary dynamics of interacting species. Many mechanisms have been proposed as explanations of observed network patterns; however, the fact that plant–animal interactions are inherently spatial has so far been ignored. Using a simulation model of frugivorous birds foraging in spatially explicit landscapes we evaluated how plant distribution and the scale of bird movement decisions influenced species interaction probabilities and the resulting network properties. Spatial aggregation and limited animal mobility restricted encounter probabilities, so that the distribution of animal visits per plant deviated strongly from the binomial distribution expected for a well-mixed system. Lack of mixing in turn resulted in a strong decrease in network connectance, a weak decrease in nestedness, stronger interactions, greater strength asymmetry and the unexpected presence/absence of some interactions. Our results suggest that spatial processes may contribute substantially to structure plant–animal mutualistic networks.     

A neutral‐niche theory of nestedness in mutualistic networks

Recently, there has been a vigorous interest in community ecology about the structure of mutualistic networks and its importance for species persistence and coevolution. However, the mechanisms shaping mutualistic networks have been rarely explored. Here we extend for the first time the neutral theory of biodiversity to a multi trophic system. We focus on nestedness, a distinctive pattern of mutualistic community assembly showing two characteristics, namely, asymmetrical specialization (specialists interacting with generalists) and a generalist core (generalists interacting with generalists). We investigate the importance of relative species abundance (RSA) for the nested assembly of plant–animal mutualistic networks. Our results show that neutral mutualistic communities give rise to networks considerably more nested than real communities. RSA explains 60–70% of nested patterns in two real communities studied here, while 30–40% of nestedness is still unexplained. The nested pattern in real communities is better explained when we introduce interaction‐specific species traits such as forbidden links and intensity of dependence (relative importance of fruits for the diet of a frugivore) in our analysis. The fact that neutral mutualistic communities exhibit a perfectly nested structure and do not show a random or compartmentalized structure, underlines the importance of RSA in the assembly of mutualistic networks.     

Does asymmetric specialization differ between mutualistic and trophic networks?

Recently, plant–pollinator networks have been found to be highly structured in a nested pattern in which specialists interact with generalist species. This structure is often assumed to be particular to mutualistic interactions in opposition to the compartmentalized pattern expected for antagonistic networks. We investigated the presence of asymmetric specialization in a data set assembled from the literature of 20 highly resolved plant–insect herbivore networks and compared them with 24 plant–pollinator networks. Our results indicate that these two types of networks differ, but not in the way it is generally assumed. Asymmetric specialization is present in plant–herbivore networks even if it appears less frequently than in plant–pollinator networks. Indeed, mean and median percentages of species showing asymmetric specialisation in herbivory webs are 33% and 14% respectively, compared to 57% and 60% in pollination webs. Furthermore, the amount of asymmetry is linked with species diversity and not to connectance in plant-pollinator networks whereas the opposite pattern is found in plant–herbivore networks. Our results offer promising perspectives for understanding both the mechanisms that structure ecological communities and their impact on community dynamics depending on the type of interaction.     

Diversity in a complex ecological network with two interaction types

Most studies on ecological networks consider only a single interaction type (e.g. competitive, predatory or mutualistic), and try to developrules for system stability based exclusively on properties of this interaction type. However, the stability of ecological networks may be more dependent on the way different interaction types are combined in real communities. To address this issue, we start by compiling an ecological network in the Doñana Biological Reserve, southern Spain, with 390 species and 798 mu-tualistic and antagonistic interactions. We characterize network structure by looking at how mutualistic and antagonistic interactions are combined across all plant species. Both the ratio of mutualistic to antagonistic interactions per plant, and the number of basic modules with an antagonistic and a mutualistic interaction are very heterogeneous across plant species, with a few plant species showing very high values for these parameters. To assess the implications of these network patterns on species diversity, we study analytically and by simulation a model of this ecological network. We find that the observed correlation between strong interaction strengths and high mutualistic to antagonistic ratios in a few plant species significantly increases community diversity. Thus, to predict the persistence of biodiversity we need to understand how interaction strength and the architecture of ecological networks with different interaction types are combined.     

Nested species interactions promote feasibility over stability during the assembly of a pollinator community

The foundational concepts behind the persistence of ecological communities have been based on two ecological properties: dynamical stability and feasibility. The former is typically regarded as the capacity of a community to return to an original equilibrium state after a perturbation in species abundances and is usually linked to the strength of interspecific interactions. The latter is the capacity to sustain positive abundances on all its constituent species and is linked to both interspecific interactions and species demographic characteristics. Over the last 40 years, theoretical research in ecology has emphasized the search for conditions leading to the dynamical stability of ecological communities, while the conditions leading to feasibility have been overlooked. However, thus far, we have no evidence of whether species interactions are more conditioned by the community''s need to be stable or feasible. Here, we introduce novel quantitative methods and use empirical data to investigate the consequences of species interactions on the dynamical stability and feasibility of mutualistic communities. First, we demonstrate that the more nested the species interactions in a community are, the lower the mutualistic strength that the community can tolerate without losing dynamical stability. Second, we show that high feasibility in a community can be reached either with high mutualistic strength or with highly nested species interactions. Third, we find that during the assembly process of a seasonal pollinator community located at The Zackenberg Research Station (northeastern Greenland), a high feasibility is reached through the nested species interactions established between newcomer and resident species. Our findings imply that nested mutualistic communities promote feasibility over stability, which may suggest that the former can be key for community persistence.     

Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands

Confined within a volcanic caldera at 2000 m a.s.l., the sub-alpine desert of Tenerife, Canary Islands, harbors a distinct biota. At this altitude the climate is harsh and the growing season short. Hence, plant and animal communities, constituting the sub-alpine plant–flower-visitor network, are clearly delimited, both spatially and temporally. We investigated species composition and interaction structure of this system. A total of 11 plant species (91% endemics) and 37 flower-visiting animal species (62% endemics) formed 108 interactions. Numbers of interactions among species varied ten-fold within both plant and animal communities. Generalization level of a species was positively correlated with its local abundance. Two separate network analyses revealed a significantly nested structure. In relation to a plant–flower-visitor system, nestedness implies that specialized species (animals or plants) interact with a subset of the species pool visiting (animals) or being visited (plants) by more generalized species. Therefore, specialized, locally rare plants tend to be visited by generalized, locally abundant animals, and specialized, locally rare animals tend to utilize generalized, locally abundant food plants. Such patterns could have implications for conservation of the sub-alpine network, and stress the importance of preserving not only rare species, but also the more abundant ones, which may be key food resources or pollinators in the plant–flower-visitor network.     

The architecture of weighted mutualistic networks

Several ecosystem services directly depend on mutualistic interactions. In species rich communities, these interactions can be studied using network theory. Current knowledge of mutualistic networks is based mainly on binary links; however, little is known about the role played by the weights of the interactions between species. What new information can be extracted by analyzing weighted mutualistic networks? In performing an exhaustive analysis of the topological properties of 29 weighted mutualistic networks, our results show that the generalist species, defined as those with a larger number of interactions in a network, also have the strongest interactions. Though most interactions of generalists are with specialists, the strongest interactions occur between generalists. As a result and by defining binary and weighted clustering coefficients for bipartite networks, we demonstrate that generalists form strongly‐interconnected groups of species. The existence of these strong clusters reinforces the idea that generalist species govern the coevolution of the whole community.     

Congruence between visitation and pollen-transport networks in a California plant–pollinator community

Most recent studies describing pollination networks are based on observed flower visits, and few have explicitly tested if the floral visitors actually carry pollen. Since floral visitors can vary in their ability to remove and transfer pollen, it is important to show that visitation patterns reflect effective pollination. Given the difficulty of measuring per-visit pollen deposition at the community scale, a first step is to examine the amount of conspecific pollen carried by insect visitors. Here I compared the plant–animal visitation network with the pollen-transport network, estimated from insect pollen loads, for a montane meadow community from southern California, USA. Visitation and pollen-transport networks were positively associated with each other in both 2001 and 2002. However, the exclusion of visitors that do not carry any conspecific pollen reveals that pollen-transport networks are more specialized from the plants' perspective and that species are involved in fewer mutualistic interactions compared with estimates derived from visitation frequencies. Although conspecific pollen loads were smaller in 2002, bees tended to carry the largest conspecific loads in both years and were responsible for transporting the most pollen. These results suggest that, although visitation networks are suitable first-order approximations of pollination networks, information on which visitors carry conspecific pollen, and in what amounts, is crucial for distinguishing between antagonistic and mutualistic interactions.     

Whole community invasions and the integration of novel ecosystems

The impact of invasion by a single non-native species on the function and structure of ecological communities can be significant, and the effects can become more drastic–and harder to predict–when multiple species invade as a group. Here we modify a dynamic Boolean model of plant-pollinator community assembly to consider the invasion of native communities by multiple invasive species that are selected either randomly or such that the invaders constitute a stable community. We show that, compared to random invasion, whole community invasion leads to final stable communities (where the initial process of species turnover has given way to a static or near-static set of species in the community) including both native and non-native species that are larger, more likely to retain native species, and which experience smaller changes to the topological measures of nestedness and connectance. We consider the relationship between the prevalence of mutualistic interactions among native and invasive species in the final stable communities and demonstrate that mutualistic interactions may act as a buffer against significant disruptions to the native community.     

Structure–stability relationships in networks combining mutualistic and antagonistic interactions

The relationship between the structure of ecological networks and community stability has been studied for decades. Recent developments highlighted that this relationship depended on whether interactions were antagonistic or mutualistic. Different structures promoting stability in different types of ecological networks, i.e. mutualistic or antagonistic, have been pointed out. However, these findings come from studies considering mutualistic and antagonistic interactions separately whereas we know that species are part of both types of networks simultaneously. Understanding the relationship between network structure and community stability, when mutualistic and antagonistic interactions are merged in a single network, thus appears as the next challenge to improve our understanding of the dynamics of natural communities. Using a theoretical approach, we test whether the structural characteristics known to promote stability in networks made of a single interaction type still hold for network merging mutualistic and antagonistic interactions. We show that the effects of diversity and connectance remain unchanged. But the effects of nestedness and modularity are strongly weakened in networks combining mutualistic and antagonistic interactions. By challenging the stabilizing mechanisms proposed for networks with a single interaction type, our study calls for new measures of structure for networks that integrate the diversity of interaction.     

Network structural properties mediate the stability of mutualistic communities

Key advances are being made on the structures of predator–prey food webs and competitive communities that enhance their stability, but little attention has been given to such complexity–stability relationships for mutualistic communities. We show, by way of theoretical analyses with empirically informed parameters, that structural properties can alter the stability of mutualistic communities characterized by nonlinear functional responses among the interacting species. Specifically, community resilience is enhanced by increasing community size (species diversity) and the number of species interactions (connectivity), and through strong, symmetric interaction strengths of highly nested networks. As a result, mutualistic communities show largely positive complexity–stability relationships, in opposition to the standard paradox. Thus, contrary to the commonly-held belief that mutualism's positive feedback destabilizes food webs, our results suggest that interplay between the structure and function of ecological networks in general, and consideration of mutualistic interactions in particular, may be key to understanding complexity–stability relationships of biological communities as a whole.     

COEVOLUTION AND THE ARCHITECTURE OF MUTUALISTIC NETWORKS

Although coevolution is widely recognized as an important evolutionary process for pairs of reciprocally specialized species, its importance within species‐rich communities of generalized species has been questioned. Here we develop and analyze mathematical models of mutualistic communities, such as those between plants and pollinators or plants and seed‐dispersers to evaluate the importance of coevolutionary selection within complex communities. Our analyses reveal that coevolutionary selection can drive significant changes in trait distributions with important consequences for the network structure of mutualistic communities. One such consequence is greater connectance caused by an almost invariable increase in the rate of mutualistic interaction within the community. Another important consequence is altered patterns of nestedness. Specifically, interactions mediated by a mechanism of phenotype matching tend to be antinested when coevolutionary selection is weak and even more strongly antinested as increasing coevolutionary selection favors the emergence of reciprocal specialization. In contrast, interactions mediated by a mechanism of phenotype differences tend to be nested when coevolutionary selection is weak, but less nested as increasing coevolutionary selection favors greater levels of generalization in both plants and animals. Taken together, our results show that coevolutionary selection can be an important force within mutualistic communities, driving changes in trait distributions, interaction rates, and even network structure.     

Interspecific interactions affect species and community responses to climate shifts

The response of individual species to climate change may alter the composition and dynamics of communities. Here, we show that the impacts of environmental change on communities can depend on the nature of the interspecific interactions: mutualistic communities typically respond differently than commensalistic or parasitic communities. We model and analyse the geographic range shifting of metapopulations of two interacting species – a host and an obligate species. Different types of interspecific interactions are implemented by modifying local extinction rates according to the presence/absence of the other species. We distinguish and compare three fundamentally different community types: mutualism, commensalism and parasitism. We find that community dynamics during geographic range shifting critically depends on the type of interspecific interactions. Parasitic interactions exacerbate the negative effect of environmental change whereas mutualistic interactions only partly compensate it. Commensalistic interactions exhibit an intermediate response. Based on these model outcomes, we predict that parasitic species interactions may be more vulnerable to geographic range shifting than commensalistic or mutualistic ones. However, we observe that when climate stabilises following a period of change, the rate of community recovery is largely independent of the type of interspecific interactions. These results emphasize that communities respond delicately to environmental change, and that local interspecific interactions can affect range shifting communities at large spatial scales.     

Top‐down network analysis characterizes hidden termite–termite interactions

The analysis of ecological networks is generally bottom‐up, where networks are established by observing interactions between individuals. Emergent network properties have been indicated to reflect the dominant mode of interactions in communities that might be mutualistic (e.g., pollination) or antagonistic (e.g., host–parasitoid communities). Many ecological communities, however, comprise species interactions that are difficult to observe directly. Here, we propose that a comparison of the emergent properties from detail‐rich reference communities with known modes of interaction can inform our understanding of detail‐sparse focal communities. With this top‐down approach, we consider patterns of coexistence between termite species that live as guests in mounds built by other host termite species as a case in point. Termite societies are extremely sensitive to perturbations, which precludes determining the nature of their interactions through direct observations. We perform a literature review to construct two networks representing termite mound cohabitation in a Brazilian savanna and in the tropical forest of Cameroon. We contrast the properties of these cohabitation networks with a total of 197 geographically diverse mutualistic plant–pollinator and antagonistic host–parasitoid networks. We analyze network properties for the networks, perform a principal components analysis (PCA), and compute the Mahalanobis distance of the termite networks to the cloud of mutualistic and antagonistic networks to assess the extent to which the termite networks overlap with the properties of the reference networks. Both termite networks overlap more closely with the mutualistic plant–pollinator communities than the antagonistic host–parasitoid communities, although the Brazilian community overlap with mutualistic communities is stronger. The analysis raises the hypothesis that termite–termite cohabitation networks may be overall mutualistic. More broadly, this work provides support for the argument that cryptic communities may be analyzed via comparison to well‐characterized communities.     

Global versus local extinction in a network model of plant–pollinator communities

The loss of a species from an ecological community can trigger a cascade of additional extinctions; the complex interactions that comprise ecological communities make the dynamics and impacts of such a cascade challenging to predict. Previous studies have typically considered global extinctions, where a species cannot re-enter a community once it is lost. However, in some cases a species only becomes locally extinct, and may be able to reinvade from surrounding communities. Here, we use a dynamic, Boolean network model of plant–pollinator community assembly to analyze the differences between global and local extinction events in mutualistic communities. As expected, we find that compared to global extinctions, communities respond to local extinctions with lower biodiversity loss, and less variation in topological network properties. We demonstrate that in the face of global extinctions, larger communities suffer greater biodiversity loss than smaller communities when similar proportions of species are lost. Conversely, smaller communities suffer greater loss in the face of local extinctions. We show that targeting species with the most interacting partners causes more biodiversity loss than random extinctions in the case of global, but not local, extinctions. These results extend our understanding of how mutualistic communities respond to species loss, with implications for community management and conservation efforts.     

Invading a mutualistic network: to be or not to be similar

Biological invasion remains a major threat to biodiversity in general and a disruptor to mutualistic interactions in particular. While a number of empirical studies have directly explored the role of invasion in mutualistic pollination networks, a clear picture is yet to emerge and a theoretical model for comprehension still lacking. Here, using an eco‐evolutionary model of bipartite mutualistic networks with trait‐mediated interactions, we explore invader trait, propagule pressure, and network features of recipient community that contribute importantly to the success and impact of an invasion. High level of invasiveness is observed when invader trait differs from those of the community average, and level of interaction generalization equals to that of the community average. Moreover, multiple introductions of invaders with declining propagules enhance invasiveness. Surprisingly, the most successful invader is not always the one having the biggest impact on the recipient community. The network structure of recipient community, such as nestedness and modularity, is not a primary indicator of its invasibility; rather, the invasibility is best correlated with measurements of network stability such as robustness, resilience, and disruptiveness (a measure of evolutionary instability). Our model encompasses more general scenarios than previously studied in predicting invasion success and impact in mutualistic networks, and our results highlight the need for coupling eco‐evolutionary processes to resolve the invasion dilemma.     

Predicting the effect of competition on secondary plant extinctions in plant–pollinator networks

What are the limitations of models that predict the behavior of an ecological community based on a single type of species interaction? Using plant–pollinator network models as an example, we contrast the predicted vulnerability of a community to secondary extinctions under the assumption of purely mutualistic interactions versus mutualistic and competitive interactions. We find that competition among plant species increases the risk of secondary extinctions and extinction cascades. Simulations over a number of different network structures indicate that this effect is stronger in larger networks, more strongly connected networks and networks with higher plant:pollinator ratios. We conclude that efforts to model plant–pollinator communities will systematically over‐estimate community robustness to species loss if plant competition is ignored. However, because the effect of plant competition depends on network architecture, and because characterization of plant competition is work intensive, we suggest that efforts to account for plant competition in plant–pollinator network models should be focused on large, strongly connected networks with high plant:pollinator ratios.     

Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human‐driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.     

Adaptive foraging behaviour of individual pollinators and the coexistence of co-flowering plants

Although pollinators can play a central role in determining the structure and stability of plant communities, little is known about how their adaptive foraging behaviours at the individual level, e.g. flower constancy, structure these interactions. Here, we construct a mathematical model that integrates individual adaptive foraging behaviour and population dynamics of a community consisting of two plant species and a pollinator species. We find that adaptive foraging at the individual level, as a complementary mechanism to adaptive foraging at the species level, can further enhance the coexistence of plant species through niche partitioning between conspecific pollinators. The stabilizing effect is stronger than that of unbiased generalists when there is also strong competition between plant species over other resources, but less so than that of multiple specialist species. This suggests that adaptive foraging in mutualistic interactions can have a very different impact on the plant community structure from that in predator–prey interactions. In addition, the adaptive behaviour of individual pollinators may cause a sharp regime shift for invading plant species. These results indicate the importance of integrating individual adaptive behaviour and population dynamics for the conservation of native plant communities.     

Structure and dynamics of pollination networks: the role of alien plants

Research on ecological communities, and plant–pollinator mutualistic networks in particular, has increasingly benefited from the theory and tools of complexity science. Nevertheless, up to now there have been few attempts to investigate the interplay between the structure of real pollination networks and their dynamics. This study is one of the first contributions to explore this issue. Biological invasions, of major concern for conservation, are also poorly understood from the perspective of complex ecological networks. In this paper we assess the role that established alien species play within a host community by analyzing the temporal changes in structural network properties driven by the removal of non‐native plants. Three topological measures have been used to represent the most relevant structural properties for the stability of ecological networks: degree distribution, nestedness, and modularity. Therefore, we investigate for a detailed pollination network, 1) how its dynamics, represented as changes in species abundances, affect the evolution of its structure, 2) how topology relates to dynamics focusing on long‐term species persistence; and 3) how both structure and dynamics are affected by the removal of alien plant species. Network dynamics were simulated by means of a stochastic metacommunity model. Our results showed that established alien plants are important for the persistence of the pollination network and for the maintenance of its structure. Removal of alien plants decreased the likelihood of species persistence. On the other hand, both the full network and the subset native network tended to lose their structure through time. Nevertheless, the structure of the full network was better preserved than the structure of the network without alien plants. Temporal topological shifts were evident in terms of degree distribution, nestedness, and modularity. However the effects of removing alien plants were more pronounced for degree distribution and modularity of the network. Therefore, elimination of alien plants affected the evolution of the architecture of the interaction web, which was closely related to the higher species loss found in the network where alien plants were removed.