Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia

The most conspicuous and species-rich ant-plant mutualism in the Malesian region is found in the important pioneer tree genus Macaranga , yet little is known about the identities or community ecology of the species involved. Our studies have revealed a far more complex system than previously thought. This paper presents the first extensive investigation in the whole distribution area of myrmecophytic Macaranga. All ant-inhabited species were restricted to the moister parts of SE Asia: Peninsular Malaysia, South and East Thailand, Sumatra and Borneo. We found a rather strict and similar altitudinal zonation of myrmecophytic Macaranga species in all regions. Here we focus on the majority of the 19 Macaranga species obligatorily associated with ants of the genus Crematogaster. We identified a total of 2163 ant queens which belonged to at least eight (morpho)species of the small subgenus Decacrema as well as to one non-Decacrema (probably from Atopogyne ). The ant species were not randomly distributed among the Macaranga species but distinct patterns of associations emerged. Despite common sympatric distribution of Macaranga species, in most cases a surprisingly high specificity of ant colonization was maintained which was, however, often not species-specific but groups of certain plant species with identical ant partners could be found. These colonization patterns usually but not always mirror existing taxonomic sections within the genus Macaranga. Possible mechanisms of specificity are discussed. The results are compared with other ant-plant mutualisms.     

The specialization and structure of antagonistic and mutualistic networks of beetles on rainforest canopy trees

Different kinds of species interactions can lead to different structures within ecological networks. Antagonistic interactions (such as between herbivores and host plants) often promote increasing host specificity within a compartmentalized network structure, whereas mutualistic networks (such as pollination networks) are associated with higher levels of generalization and form nested network structures. However, we recently showed that the host specificity of flower‐visiting beetles from three different feeding guilds (herbivores, fungivores, and predators) in an Australian rainforest canopy was equal to that of herbivores on leaves, suggesting that antagonistic herbivores on leaves are no more specialized than flower‐visitors. We therefore set out to test whether similarities in the host specificity of these different assemblages reflect similarities in underlying network structures. As shown before at the species level, mutualistic communities on flowers showed levels of specialization at the network scale similar to those of the antagonistic herbivore community on leaves. However, the network structure differed, with flower‐visiting assemblages displaying a significantly more nested structure than folivores, and folivores displaying a significantly more compartmentalized structure than flower‐visitors. These results, which need further testing in other forest systems, demonstrate that both antagonistic and mutualistic interactions can result in equally high levels of host specialization among beetle assemblages in tropical rainforests. If this is a widespread phenomenon, it may alter our current perceptions of food web dynamics, species diversity patterns, and co‐evolution in tropical rainforests. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 287–295.     

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.     

Missing and forbidden links in mutualistic networks

Ecological networks are complexes of interacting species, but not all potential links among species are realized. Unobserved links are either missing or forbidden. Missing links exist, but require more sampling or alternative ways of detection to be verified. Forbidden links remain unobservable, irrespective of sampling effort. They are caused by linkage constraints. We studied one Arctic pollination network and two Mediterranean seed-dispersal networks. In the first, for example, we recorded flower-visit links for one full season, arranged data in an interaction matrix and got a connectance C of 15 per cent. Interaction accumulation curves documented our sampling of interactions through observation of visits to be robust. Then, we included data on pollen from the body surface of flower visitors as an additional link ‘currency’. This resulted in 98 new links, missing from the visitation data. Thus, the combined visit–pollen matrix got an increased C of 20 per cent. For the three networks, C ranged from 20 to 52 per cent, and thus the percentage of unobserved links (100 − C) was 48 to 80 per cent; these were assumed forbidden because of linkage constraints and not missing because of under-sampling. Phenological uncoupling (i.e. non-overlapping phenophases between interacting mutualists) is one kind of constraint, and it explained 22 to 28 per cent of all possible, but unobserved links. Increasing phenophase overlap between species increased link probability, but extensive overlaps were required to achieve a high probability. Other kinds of constraint, such as size mismatch and accessibility limitations, are briefly addressed.     

Resilient networks of ant-plant mutualists in amazonian forest fragments

Background

The organization of networks of interacting species, such as plants and animals engaged in mutualisms, strongly influences the ecology and evolution of partner communities. Habitat fragmentation is a globally pervasive form of spatial heterogeneity that could profoundly impact the structure of mutualist networks. This is particularly true for biodiversity-rich tropical ecosystems, where the majority of plant species depend on mutualisms with animals and it is thought that changes in the structure of mutualist networks could lead to cascades of extinctions.

Methodology/Principal Findings

We evaluated effects of fragmentation on mutualistic networks by calculating metrics of network structure for ant-plant networks in continuous Amazonian forests with those in forest fragments. We hypothesized that networks in fragments would have fewer species and higher connectance, but equal nestedness and resilience compared to forest networks. Only one of the nine metrics we compared differed between continuous forest and forest fragments, indicating that networks were resistant to the biotic and abiotic changes that accompany fragmentation. This is partially the result of the loss of only specialist species with one connection that were lost in forest fragments.

Conclusions/Significance

We found that the networks of ant-plant mutualists in twenty-five year old fragments are similar to those in continuous forest, suggesting these interactions are resistant to the detrimental changes associated with habitat fragmentation, at least in landscapes that are a mosaic of fragments, regenerating forests, and pastures. However, ant-plant mutualistic networks may have several properties that may promote their persistence in fragmented landscapes. Proactive identification of key mutualist partners may be necessary to focus conservation efforts on the interactions that insure the integrity of network structure and the ecosystems services networks provide.     

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.     

Reciprocal specialization in ecological networks

Theories suggest that food webs might consist of groups of species forming 'blocks', 'compartments' or 'guilds'. We consider ecological networks – subsets of complete food webs – involving species at adjacent trophic levels. Reciprocal specializations occur when (say) a pollinator (or group of pollinators) specializes on a particular flower species (or group of such species) and vice versa. Such specializations tend to group species into guilds. We characterize the level of reciprocal specialization for both antagonistic interactions – particularly parasitoids and their hosts – and mutualistic ones – such as insects and the flowers that they pollinate. We also examine whether trophic patterns might be 'palimpsests'– that is, there might be reciprocal specialization within taxonomically related species within a network, but these might be obscured when these relationships are combined. Reciprocal specializations are rare in all these systems when tested against the most conservative null model.     

Fitness consequences of centrality in mutualistic individual-based networks

The relationships among the members of a population can be visualized using individual networks, where each individual is a node connected to each other by means of links describing the interactions. The centrality of a given node captures its importance within the network. We hypothesize that in mutualistic networks, the centrality of a node should benefit its fitness. We test this idea studying eight individual-based networks originated from the interaction between Erysimum mediohispanicum and its flower visitors. In these networks, each plant was considered a node and was connected to conspecifics sharing flower visitors. Centrality indicates how well connected is a given E. mediohispanicum individual with the rest of the co-occurring conspecifics because of sharing flower visitors. The centrality was estimated by three network metrics: betweenness, closeness and degree. The complex relationship between centrality, phenotype and fitness was explored by structural equation modelling. We found that the centrality of a plant was related to its fitness, with plants occupying central positions having higher fitness than those occupying peripheral positions. The structural equation models (SEMs) indicated that the centrality effect on fitness was not merely an effect of the abundance of visits and the species richness of visitors. Centrality has an effect even when simultaneously accounting for these predictors. The SEMs also indicated that the centrality effect on fitness was because of the specific phenotype of each plant, with attractive plants occupying central positions in networks, in relation to the distribution of conspecific phenotypes. This finding suggests that centrality, owing to its dependence on social interactions, may be an appropriate surrogate for the interacting phenotype of individuals.     

Do mutualistic networks follow power distributions?

Species interactions are central to the structure and dynamics of biological communities. Recently, of particular interest, is the analysis of ecological networks where the number of species to species interactions vary depending on the degree of specialization. For mutualistic networks, species degree has been suggested to follows a power distribution or a truncated power distribution. In this paper, I discuss previously estimated parameters and associated model selection may be unreliable. I use the likelihood approach and compare the results from previous findings and show that the parameter estimates as well as model selection results are indeed very different. Furthermore, the likelihood approach reveals that many mutualistic networks do not follow either power distribution or truncated power distribution.     

Trait-mediated interaction leads to structural emergence in mutualistic networks

As asymmetric structures of mutualistic networks can potentially contribute to system resilience, elucidating drivers behind the emergence of particular network architectures remains a major endeavour in ecology. Here, using an eco-evolutionary model for bipartite mutualistic networks with trait-mediated interactions, we explore how particular levels of connectance, nestedness and modularity are affected by three network assembly forces: resource accessibility, tolerance to trait difference between mutualistic pairs and competition intensity. We found that a moderate accessibility to intra-trophic resources and cross-trophic mutualistic support can result in a highly nested web, while low tolerance to trait difference between interacting pairs leads to a high level of modularity. Network-level trait complementarity leads to low connectance and high modularity, while network-level specialization can result in nested structures. Consequently, we argue that the interplay of ecological and evolutionary processes through trait-mediated interactions can explain these widely observed architectures in mutualistic networks.     

Build-up mechanisms determining the topology of mutualistic networks

The frequency distribution of the number of interactions per species (i.e., degree distribution) within plant-animal mutualistic assemblages often decays as a power-law with an exponential truncation. Such a truncation suggests that there are ecological factors limiting the frequency of supergeneralist species. However, it is not clear whether these patterns can emerge from intrinsic features of the interacting assemblages, such as differences between plant and animal species richness (richness ratio). Here, we show that high richness ratios often characterize plant-animal mutualisms. Then, we demonstrate that exponential truncations are expected in bipartite networks generated by a simple model that incorporates build-up mechanisms that lead to a high richness ratio. Our results provide a simple interpretation for the truncations commonly observed in the degree distributions of mutualistic networks that complements previous ones based on biological effects.     

Specialization, constraints, and conflicting interests in mutualistic networks

The topology of ecological interaction webs holds important information for theories of coevolution, biodiversity, and ecosystem stability . However, most previous network analyses solely counted the number of links and ignored variation in link strength. Because of this crude resolution, results vary with scale and sampling intensity, thus hampering a comparison of network patterns at different levels . We applied a recently developed quantitative and scale-independent analysis based on information theory to 51 mutualistic plant-animal networks, with interaction frequency as measure of link strength. Most networks were highly structured, deviating significantly from random associations. The degree of specialization was independent of network size. Pollination webs were significantly more specialized than seed-dispersal webs, and obligate symbiotic ant-plant mutualisms were more specialized than nectar-mediated facultative ones. Across networks, the average specialization of animal and plants was correlated, but is constrained by the ratio of plant to animal species involved. In pollination webs, rarely visited plants were on average more specialized than frequently attended ones, whereas specialization of pollinators was positively correlated with their interaction frequency. We conclude that quantitative specialization in ecological communities mirrors evolutionary trade-offs and constraints of web architecture. This approach can be easily expanded to other types of biological interactions.     

Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks

The structure of mutualistic networks provides clues to processes shaping biodiversity [1-10]. Among them, interaction intimacy, the degree of biological association between partners, leads to differences in specialization patterns [4, 11] and might affect network organization [12]. Here, we investigated potential consequences of interaction intimacy for the structure and coevolution of mutualistic networks. From observed processes of selection on mutualistic interactions, it is expected that symbiotic interactions (high-interaction intimacy) will form species-poor networks characterized by compartmentalization [12, 13], whereas nonsymbiotic interactions (low intimacy) will lead to species-rich, nested networks in which there is a core of generalists and specialists often interact with generalists [3, 5, 7, 12, 14]. We demonstrated an association between interaction intimacy and structure in 19 ant-plant mutualistic networks. Through numerical simulations, we found that network structure of different forms of mutualism affects evolutionary change in distinct ways. Change in one species affects primarily one mutualistic partner in symbiotic interactions but might affect multiple partners in nonsymbiotic interactions. We hypothesize that coevolution in symbiotic interactions is characterized by frequent reciprocal changes between few partners, but coevolution in nonsymbiotic networks might show rare bursts of changes in which many species respond to evolutionary changes in a single species.     

Habitat loss and the structure of plant-animal mutualistic networks

Recent papers have described the structure of plant–animal mutualistic networks. However, no study has yet explored the dynamical implications of network structure for the persistence of such mutualistic communities. Here, we develop a patch-model of a whole plant–animal community and explore its persistence. To assess the role of network structure, we build three versions of the model. In the first version, we use the exact network of interactions of two real mutualistic communities. In the other versions, we randomize the observed network of interactions using two different null models. We show that the community response to habitat loss is affected by network structure. Real communities start to decay sooner than random communities, but persist for higher destruction levels. There is a destruction threshold at which the community collapses. Our model is the first attempt to describe the dynamics of whole mutualistic metacommunities interacting in realistic ways.     

Spatial structure of ant–plant mutualistic networks

The structure of mutualistic networks provides insights into ecological and coevolutionary dynamics of interacting species. However, the spatial effect has only recently been incorporated as a factor structuring mutualistic networks. In this study, we evaluated how the topological structure and species turnover of ant–plant mutualistic networks vary over a spatial gradient. We showed that although the ant and plant composition of networks changed over space, the central core of generalist species and the structure of networks remained unaltered on a geographic distance of up to 5099 m in the southern Brazilian Amazon. This finding indicates that independently of variation in local and landscape environmental factors, the nonrandom pattern organization of these interacting assemblages do not change. Finally, we suggest that a stable core can increase the potential for coevolutionary convergence of traits among species from both sides of the interaction within the community. These findings contribute to our understanding of the maintenance of biodiversity and coevolutionary processes.     

The impact of individual variation on abrupt collapses in mutualistic networks

Individual variation is central to species involved in complex interactions with others in an ecological system. Such ecological systems could exhibit tipping points in response to changes in the environment, consequently leading to abrupt transitions to alternative, often less desirable states. However, little is known about how individual trait variation could influence the timing and occurrence of abrupt transitions. Using 101 empirical mutualistic networks, I model the eco-evolutionary dynamics of such networks in response to gradual changes in strength of co-evolutionary interactions. Results indicated that individual variation facilitates the timing of transition in such networks, albeit slightly. In addition, individual variation significantly increases the occurrence of large abrupt transitions. Furthermore, topological network features also positively influence the occurrence of such abrupt transitions. These findings argue for understanding tipping points using an eco-evolutionary perspective to better forecast abrupt transitions in ecological systems.     

Multiple effects of mutualistic ants improve the performance of a neotropical ant-plant: A long-term study with the Cecropia-Azteca system

Comprehension of the benefits involved in mutualisms is crucial to disentangle the role of interactions in the structure and functioning of populations, communities and ecosystems. In ant-plant mutualisms, benefits provided by plants to ants are immediately recognizable, but reverse benefits are less obvious, conditional and accumulate over longer time spans. Here we tested the hypothesis that the ant Azteca muelleri simultaneously provides multiple benefits to its host plant (Cecropia glaziovii), ultimately increasing plant performance. We planted seedlings and experimentally prevented ant colonization for half of them. Over 4.5 years we quantified the effects of ant presence or absence on plant growth, herbivory levels, fungal infection, fertilization via ant debris and changes in defense strategies. Ant colonization increased plant height by 125% compared to ant-free plants. Such an improvement in plant performance can be explained because plants with ants faced less herbivory, lower prevalence of pathogenic fungi, invested less in foliar trichomes and had more foliar nitrogen. We thus confirmed that ant mutualists provide cumulative benefits including nutritional benefits, effective defense and lower investment into other defenses – which result in increased plant growth. We highlight the importance of long-term experiments that simultaneously evaluate a multiplicity of potential ant effects to better understand their relative contribution to the performance of the mutualistic partner.     

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.