Effects of hummingbird morphology on specialization in pollination networks vary with resource availability

Specialization of species in interaction networks influences network stability and ecosystem functioning. Spatial and temporal variation in resource availability may provide insight into how ecological factors, such as resource abundance, and evolutionary factors, such as phylogenetically conserved morphological traits, influence specialization within mutualistic networks. We used independent measures of hummingbird abundance and resources (nectar), information on hummingbird traits and plant–hummingbird interactions to examine how resource availability and species' morphology influence the specialization of hummingbirds in three habitat types (forest, shrubs, cattle ranch) sampled over 10 sessions across two years in the southern Andes of Ecuador. Specialization of hummingbird species in the networks was measured by three indices: d' (related to niche partitioning), generality (related to niche width) and PSI (related to pollination services). Specialization indices d', generality and PSI of hummingbird species were influenced by resource availability. All indices indicated that specialization of hummingbirds increased when the availability of resources decreased. Variation in d' was also explained by an interaction between resource availability and bill length; hummingbirds with a long bill switched from being more specialized than other species when resource availability was low to being similarly specialized when availability was high. Overall, our results highlight the importance of ecological and evolutionary factors determining the specialization of species in interaction networks. We demonstrate in particular that ecological gradients in resource availability cause substantial changes in consumers' foraging behavior contingent on their morphology. Changes in pollinator specialization along resource gradients can have impacts on ecosystem functions, such as pollination by animals.     

Network analyses reveal the role of large snakes in connecting feeding guilds in a species‐rich Amazonian snake community

In ecological communities, interactions between consumers and resources lead to the emergence of ecological networks and a fundamental problem to solve is to understand which factors shape network structure. Empirical and theoretical studies on ecological networks suggest predator body size is a key factor structuring patterns of interaction. Because larger predators consume a wider resource range, including the prey consumed by smaller predators, we hypothesized that variation in body size favors the rise of nestedness. In contrast, if resource consumption requires specific adaptations, predators are expected to consume distinct sets of resources, thus favoring modularity. We investigate these predictions by characterizing the trophic network of a species‐rich Amazonian snake community (62 species). Our results revealed an intricate network pattern resulting from larger species feeding on higher diversity of prey and therefore promoting nestedness, whereas snakes with specific lifestyles and feeding on distinct resources, promoting modularity. Species removal simulations indicated that the nested structure is favored mainly by the presence of five species of the family Boidae, which because of their body size and generalist lifestyles connect modules in the network. Our study highlights the particular ways traits affect the structure of interactions among consumers and resources at the community level.     

Trophic network structure emerges through antagonistic coevolution in temporally varying environments

Understanding the mechanisms underlying ecological specialization is central to our understanding of community ecology and evolution. Although theoretical work has investigated how variable environments may affect specialization in single species, little is known about how such variation impacts bipartite network structure in antagonistically coevolving systems. Here, we develop and analyse a general model of victim-enemy coevolution that explicitly includes resource and population dynamics. We investigate how temporal environmental heterogeneity affects the evolution of specialization and associated community structure. Environmental productivity influences victim investment in resistance, which will shape patterns of specialization through its regulating effect on enemy investment in infectivity. We also investigate the epidemiological consequences of environmental variability and show that enemy population density is maximized for intermediate lengths of productive seasons, which corresponds to situations where enemies can evolve higher infectivity than victims can evolve defence. We discuss our results in the light of empirical studies, and further highlight ways in which our model applies to a range of natural systems.     

Experiments with humans indicate that decision accuracy drives the evolution of niche width

One theory to explain the high incidence of niche specialization in many animals is that it reduces attentional load during resource-seeking behaviour and thus leads to more accurate resource selection. A recent neural network model refined the predictions of this theory, indicating that a cognitive advantage in specialists is likely to occur under realistic ecological conditions, namely when 'mistakes' (i.e. selection of non-host resources) contribute moderately but positively to fitness. Here, we present a formal empirical test of the predictions of this model. Using a human-computer interactive, we demonstrate that the central prediction of the model is supported: specialist humans are more accurate decision-makers than generalists when their mistakes are rewarded, but not when mistakes are punished. The idea that increased decision accuracy drives the evolution of niche width in animals has been supported in almost all empirical systems in which it has been investigated. Theoretical work supports the idea, and now the predictions of a key theoretical model have been demonstrated in a real biological information-processing system. Considering these interlocking pieces of evidence, we argue that specialization through increased decision accuracy may contribute significantly, along with other mechanisms, to promote niche specialization in animals.     

The geographical variation of network structure is scale dependent: understanding the biotic specialization of host–parasitoid networks

Research on the structure of ecological networks suggests that a number of universal patterns exist. Historically, biotic specialization has been thought to increase towards the Equator. Yet, recent studies have challenged this view showing non‐conclusive results. Most studies analysing the geographical variation in biotic specialization focus, however, only on the local scale. Little is known about how the geographical variation of network structure depends on the spatial scale of observation (i.e. from local to regional spatial scales). This should be remedied, as network structure changes as the spatial scale of observation changes, and the magnitude and shape of these changes can elucidate the mechanisms behind the geographical variation in biotic specialization. Here we analyse four facets of biotic specialization in host–parasitoid networks along gradients of climatic constancy, classifying the networks according to their spatial extension (local or regional). Namely, we analyse network connectance, consumer diet overlap, consumer diet breadth, and resource vulnerability at both local and regional scales along the gradients of both current climatic constancy and historical climatic change. While at the regional scale none of the climatic variables are associated to biotic specialization, at the local scale, network connectance, consumer diet overlap, and resource vulnerability decrease with current climatic constancy, whereas consumer generalism increases (i.e. broader diet breadths in tropical areas). Similar patterns are observed along the gradient of historical climatic change. We provide an explanation based on different beta‐diversity for consumers and resources across the geographical gradients. Our results show that the geographical gradient of biotic specialization is not universal. It depends on both the facet of biotic specialization and the spatial scale of observation.     

How ecology shapes caste evolution: linking resource use,morphology, performance and fitness in a superorganism

Caste evolution is a central process in the adaptive diversification of insect superorganisms. Nevertheless, how ecology shapes adaptive caste evolution remains poorly understood. Recent work with the ant genus Cephalotes has provided new comparative evidence that ecological specialization may drive adaptive caste specialization. Here, three key predictions of this adaptive hypothesis are supported, using a representative of the highest level of ecological specialization and the most specialized soldier phenotype. First, soldier defensive performance was maximal for the specific nesting resource used most often in nature. Second, colonies only used a specialized subset of available nesting resources and preferred the specific resource that maximizes soldier performance. Third, soldier performance and its limitations on resource use were found to have both direct and indirect consequences for colony reproduction. These findings suggest that the most specialized soldier phenotype in Cephalotes is indeed an adaptation to ecological specialization on a narrowly defined subset of available nesting resources.     

Coevolution of resource trade-offs driving species interactions in a host–parasite network: an exploratory model

Patterns of specialization asymmetry, where specialist species interact mainly with generalists while generalists interact with both generalists and specialists, are often observed in mutualistic and antagonistic bipartite ecological networks. These have been explained in terms of the relative abundance of species, using a null model that assigns links in proportion to abundance, but doubts have been raised as to whether this offers a complete explanation. In particular, host–parasite networks offer a variety of examples in which the reverse patterns are observed. We propose that the link between specificity and species richness may also be driven by the coevolution of hosts and parasites, as hosts allocate resources to optimize defense against parasites, and parasites to optimize attack on hosts. In this hypothesis, species interactions are a result of resource allocations. This novel concept, linking together many different arguments for network structures, is introduced through the adaptive dynamics of a simple ecological toy system of two hosts and two parasites. We analyze the toy model and its functionality, demonstrating that coevolution leads to specialization asymmetry in networks with closely related parasites or fast host mutation rates, but not in networks with more distantly related species. Having constructed the toy model and tested its applicability, our model can now be expanded to the full problem of a larger system.     

Pollinators visit related plant species across 29 plant–pollinator networks

Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant–pollinator networks of varying sizes, with “clade specialization” increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization.     

Functional structure and specialization in three tropical plant–hummingbird interaction networks across an elevational gradient in Costa Rica

Understanding causes of variation in multispecies assemblages along spatial environmental gradients is a long‐standing research topic in ecology and biogeography. Ecological networks comprising interacting species of plants and pollinators are particularly suitable for testing effects of environmental gradients on the functional structure and specialization in multispecies assemblages. In this study, we investigated patterns in functional assemblage structure and specialization of hummingbirds at the individual and species level along a tropical elevational gradient. We mist‐netted hummingbirds at three elevations in Costa Rica in seven temporally distinct sampling periods and used the pollen carried by hummingbird individuals to construct plant–hummingbird networks at each elevation. We measured four functional traits of hummingbird species and quantified different metrics of functional community structure. We tested the effect of elevation on functional metrics of hummingbird assemblages and specialization within the networks, employing the variability across sampling periods and hummingbird species to compare the respective metrics among elevations. Hummingbird species and individuals were more specialized at low and mid elevations than at the highest elevation. This pattern corresponded to a more even and over‐dispersed assemblage structure at the lower elevations throughout the year and suggests a high level of floral resource partitioning in functionally diversified communities. In contrast, an uneven and clustered functional structure of the highland assemblage across all sampling periods suggests that this assemblage was structured by environmental filtering and by niche expansion of hummingbird individuals and species at this elevation. We conclude that high degrees of specialization on specific floral resources might be crucial for the coexistence of hummingbird species in diversified lowland communities. Spatial variation in animal resource use may be an important crucial driver of spatial patterns in the functional structure of diversified species assemblages also in other types of ecological networks.     

Sexual selection's impacts on ecological specialization: an experimental test

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs—distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.     

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas

Ecological communities that experience stable climate conditions have been speculated to preserve more specialized interspecific associations and have higher proportions of smaller ranged species (SRS). Thus, areas with disproportionally large numbers of SRS are expected to coincide geographically with a high degree of community-level ecological specialization, but this suggestion remains poorly supported with empirical evidence. Here, we analysed data for hummingbird resource specialization, range size, contemporary climate, and Late Quaternary climate stability for 46 hummingbird–plant mutualistic networks distributed across the Americas, representing 130 hummingbird species (ca 40% of all hummingbird species). We demonstrate a positive relationship between the proportion of SRS of hummingbirds and community-level specialization, i.e. the division of the floral niche among coexisting hummingbird species. This relationship remained strong even when accounting for climate, furthermore, the effect of SRS on specialization was far stronger than the effect of specialization on SRS, suggesting that climate largely influences specialization through species'' range-size dynamics. Irrespective of the exact mechanism involved, our results indicate that communities consisting of higher proportions of SRS may be vulnerable to disturbance not only because of their small geographical ranges, but also because of their high degree of specialization.     

Effects of partitioning allochthonous and autochthonous resources on food web stability

The flux of energetic and nutrient resources across habitat boundaries can exert major impacts on the dynamics of the recipient food web. Competition for these resources can be a key factor structuring many ecological communities. Competition theory suggests that competing species should exhibit some partitioning to minimize competitive interactions. Species should partition both in situ (autochthonous) resources and (allochthonous) resources that enter the food web from outside sources. Allochthonous resources are important sources of energy and nutrients in many low productivity systems and can significantly influence community structure. The focus of this paper is on: (i) the influence of resource partitioning on food web stability, but concurrently we examine the compound effects of; (ii) the trophic level(s) that has access to allochthonous resources; (iii) the amount of allochthonous resource input; and (iv) the strength of the consumer–resource interactions. We start with a three trophic level food chain model (resource–consumer–predator) and separate the higher two trophic levels into two trophospecies. In the model, allochthonous resources are either one type available to both consumers and predators or two distinct types, one for consumers and one for predators. The feeding preferences of the consumer and predator trophospecies were varied so that they could either be generalists or specialists on allochthonous and/or autochthonous resources. The degree of specialization influenced system persistence by altering the structure and, therefore, the indirect effects of the food web. With regard to the trophic level(s) that has access to allochthonous resources, we found that a single allochthonous resource available to both consumers and predators is more unstable than two allochthonous resources. The results demonstrate that species populating food webs that experience low to moderate allochthonous resources are more persistent. The results also support the notion that strong links destabilize food web dynamics, but that weak to moderate strength links stabilize food web dynamics. These results are consistent with the idea that the particular structure, resource availability, and relative strength of links of food webs (such as degree of specialization) can influence the stability of communities. Given that allochthonous resources are important resources in many ecosystems, we argue that the influence of such resources on species and community persistence needs to be examined more thoroughly to provide a clearer understanding of food web dynamics.     

Individual variation in resource use by opossums leading to nested fruit consumption

Despite recent findings on the ecological relevance of within population diet variation far less attention has been devoted to the role diet variation for ecological services. Seed dispersal is a key ecological service, affecting plant fitness and regeneration based on foraging by fruit‐eating vertebrates. Here we used a network approach, widely used to understand how seed‐dispersal is organized at the species level, to gain insights into the patterns that emerge at the individual‐level. We studied the individual fruit consumption behavior of a South American didelphid Didelphis albiventris, during the cool–dry and warm–wet seasons. In species–species networks the heterogeneity in specialization levels generates patterns such as nestedness and asymmetry. Because generalist populations may be comprised of specialized individuals, we hypo thesized that network structural properties, such as nestedness, should also emerge at the individual level. We detected variation in fruit consumption that was not related to resource availability, ontogenetic or sexual factors or sampling biases. Such variation resulted in the structural patterns often found in species–species seed‐dispersal networks: low connectance, a high degree of nestedness and the absence of modules. Moreover structure varied between the warm–wet and cool–dry seasons, presumably as a consequence of seasonal fluctuation in fruit availability. Our findings suggest individuals may differ in selectivity causing asymmetries in seed dispersal efficiency within the population. In this sense the realized dispersal would differ from the expected dispersal estimated from their average dispersal potential. Additionally the results suggest possible frequency‐dependent effects on seed dispersal that might affect individual plant performance and plant community composition.     

Nested diets: a novel pattern of individual-level resource use

Many generalist populations may actually be composed of relatively specialist individuals. This 'individual specialization' may have important ecological and evolutionary implications. Although this phenomenon has been documented in more than one hundred taxa, it is still unclear how individuals within a population actually partition resources. Here we applied several methods based on network theory to investigate the intrapopulation patterns of resource use in the gracile mouse opossum Gracilinanus microtarsus . We found evidence of significant individual specialization in this species and that the diets of specialists are nested within the diets of generalists. This novel pattern is consistent with a recently proposed model of optimal foraging and implies strong asymmetry in the interactions among individuals of a population.     

Vive le difference! Sexual dimorphism and adaptive patterns in lizards of the genus Anolis

The repeated, convergent evolution of body shape and microhabitat use in Greater Antillean lizards of the genus Anolis (anoles) provides compelling evidence of the importance of microhabitat specialization in shaping morphology. Interestingly, sexual dimorphism is also extensive, with males and females differing in body size as well as in shape. It is important to note that the components of shape analyzed in these studies is related to locomotion and are size-adjusted, including: relative limb and body lengths and mass of the body. Numbers of lamellae were also used and these do not vary with size. Furthermore, dimorphism in both size and shape differs by habitat type. Thus, does functionally-relevant sexual dimorphism imply that one sex is the "ecological" sex, with the other being maladapted to it's environment? Alternatively, sexual dimorphism may interact with adaptive diversification. Different classes of individuals within a species may act as separate ecological units if they play ecologically different roles. Here, I reanalyze a data set of morphological data for 15 species of Puerto Rican and Jamaican Anolis, which represent two largely independent adaptive radiations of lizards. I test for concordance between size and shape dimorphism and microhabitat (ecomorph) type, and for "parallel" patterns of sexual dimorphism among species. I integrate these results and, in the light of previous research, evaluate the relative influence that larger-scale ecological patterns have on sexual dimorphism, as well as the influence of sexual dimorphism on community structuring. I conclude that the presence of ecologically-relevant dimorphism may in fact increase the adaptive diversity present within a community.     

Population dynamics of plant and pollinator communities: stability reconsidered

Plant-pollinator networks are systems of outstanding ecological and economic importance. A particularly intriguing aspect of these systems is their high diversity. However, earlier studies have concluded that the specific mechanisms of plant-pollinator interactions are destabilizing and should lead to a loss of diversity. Here we present a mechanistic model of plant and pollinator population dynamics with the ability to represent a broad spectrum of interaction structures. Using this model, we examined the influence of pollinators on the stability of a plant community and the relationship between pollinator specialization and stability. In accordance with earlier work, our results show that plant-pollinator interactions may severely destabilize plant coexistence, regardless of the degree of pollinator specialization. However, if plant niche differentiation, a classical stabilizing mechanism, is sufficiently strong to overcome the minority disadvantage with respect to pollination, interactions with pollinators may even increase the stability of a plant community. In addition to plant niche differentiation, the relationship between specialization and stability depends on a number of parameters that affect pollinator growth rates. Our results highlight the complex effects of this particular type of mutualism on community stability and call for further investigations of the mechanisms of diversity maintenance in plant-pollinator systems.     

Ant-Plant Interaction in a Tropical Savanna: May the Network Structure Vary over Time and Influence on the Outcomes of Associations?

Plant-animal interactions occur in a community context of dynamic and complex ecological interactive networks. The understanding of who interacts with whom is a basic information, but the outcomes of interactions among associates are fundamental to draw valid conclusions about the functional structure of the network. Ecological networks studies in general gave little importance to know the true outcomes of interactions and how they may change over time. We evaluate the dynamic of an interaction network between ants and plants with extrafloral nectaries, by verifying the temporal variation in structure and outcomes of mutualism for the plant community (leaf herbivory). To reach this goal, we used two tools: bipartite network analysis and experimental manipulation. The networks exhibited the same general pattern as other mutualistic networks: nestedness, asymmetry and low specialization and this pattern was maintained over time, but with internal changes (species degree, connectance and ant abundance). These changes influenced the protection effectiveness of plants by ants, which varied over time. Our study shows that interaction networks between ants and plants are dynamic over time, and that these alterations affect the outcomes of mutualisms. In addition, our study proposes that the set of single systems that shape ecological networks can be manipulated for a greater understanding of the entire system.     

On the evolution of omnivory in a community context

Omnivory is extremely common in animals, yet theory predicts that when given a choice of resources specialization should be favored over being generalist. The evolution of a feeding phenotype involves complex interactions with many factors other than resource choice alone, including environmental heterogeneity, resource quality, availability, and interactions with other organisms. We applied an evolutionary simulation model to examine how ecological conditions shape evolution of feeding phenotypes (e.g., omnivory), by varying the quality and availability (absolute and relative) of plant and animal (prey) resources. Resulting feeding phenotypes were defined by the relative contribution of plants and prey to diets of individuals. We characterized organisms using seven traits that were allowed to evolve freely in different simulated environments, and we asked which traits are important for different feeding phenotypes to evolve among interacting organisms. Carnivores, herbivores, and omnivores all coexisted without any requirement in the model for a synergistic effect of eating plant and animal prey. Omnivores were most prevalent when ratio of plants and animal prey was low, and to a lesser degree, when habitat productivity was high. A key result of the model is that omnivores evolved through many different combinations of trait values and environmental contexts. Specific combinations of traits tended to form emergent trait complexes, and under certain environmental conditions, are expressed as omnivorous feeding phenotypes. The results indicate that relative availabilities of plants and prey (over the quality of resources) determine an individual's feeding class and that feeding phenotypes are often the product of convergent evolution of emergent trait complexes under specific environmental conditions. Foraging outcomes appear to be consequences of degree and type of phenotypic specialization for plant and animal prey, navigation and exploitation of the habitat, reproduction, and interactions with other individuals in a heterogeneous environment. Omnivory should not be treated as a fixed strategy, but instead a pattern of phenotypic expression, emerging from diverse genetic sources and coevolving across a range of ecological contexts.     

Conservatism and Adaptability during Squirrel Radiation: What Is Mandible Shape Telling Us?

Both functional adaptation and phylogeny shape the morphology of taxa within clades. Herein we explore these two factors in an integrated way by analyzing shape and size variation in the mandible of extant squirrels using landmark-based geometric morphometrics in combination with a comparative phylogenetic analysis. Dietary specialization and locomotion were found to be reliable predictors of mandible shape, with the prediction by locomotion probably reflecting the underlying diet. In addition a weak but significant allometric effect could be demonstrated. Our results found a strong phylogenetic signal in the family as a whole as well as in the main clades, which is in agreement with the general notion of squirrels being a conservative group. This fact does not preclude functional explanations for mandible shape, but rather indicates that ancient adaptations kept a prominent role, with most genera having diverged little from their ancestral clade morphologies. Nevertheless, certain groups have evolved conspicuous adaptations that allow them to specialize on unique dietary resources. Such adaptations mostly occurred in the Callosciurinae and probably reflect their radiation into the numerous ecological niches of the tropical and subtropical forests of Southeastern Asia. Our dietary reconstruction for the oldest known fossil squirrels (Eocene, 36 million years ago) show a specialization on nuts and seeds, implying that the development from protrogomorphous to sciuromorphous skulls was not necessarily related to a change in diet.