Macroevolution of the plant-hummingbird pollination system.

Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.

Elevated alpha diversity in disturbed sites obscures regional decline and homogenization of amphibian taxonomic, functional and phylogenetic diversity.

Loss of natural habitat due to land-use change is one of the major threats to biodiversity worldwide. It not only affects the diversity of local species communities (alpha diversity) but can also lead to large-scale homogenization of community composition (reduced beta diversity) and loss of regional diversity (gamma diversity), but these effects are still rarely investigated. We assessed the impact of land-use change on taxonomic, functional and phylogenetic diversity of amphibians in Rwanda, both on the local (community-level) and regional scale (country-wide). Alpha diversity in local communities was higher in farmland than in natural habitats; however, species turnover among farmland sites was much lower than among natural sites, resulting in highly homogenized communities and reduced taxonomic, functional and phylogenetic gamma diversity in farmland across Rwanda. Amphibians found in farmland were mostly disturbance-tolerant species that are widespread in eastern Africa and beyond. In contrast, most of the regionally endemic frog species that make this region a continent-wide hotspot of amphibian diversity were found only in the natural habitats. Ongoing habitat conversion might result in further homogenization of amphibian communities across sub-Saharan Africa and the loss of regional endemism, unique evolutionary lineages, and multifunctionality.

Global and regional ecological boundaries explain abrupt spatial discontinuities in avian frugivory interactions.

Species interactions can propagate disturbances across space via direct and indirect effects, potentially connecting species at a global scale. However, ecological and biogeographic boundaries may mitigate this spread by demarcating the limits of ecological networks. We tested whether large-scale ecological boundaries (ecoregions and biomes) and human disturbance gradients increase dissimilarity among plant-frugivore networks, while accounting for background spatial and elevational gradients and differences in network sampling. We assessed network dissimilarity patterns over a broad spatial scale, using 196 quantitative avian frugivory networks (encompassing 1496 plant and 1004 bird species) distributed across 67 ecoregions, 11 biomes, and 6 continents. We show that dissimilarities in species and interaction composition, but not network structure, are greater across ecoregion and biome boundaries and along different levels of human disturbance. Our findings indicate that biogeographic boundaries delineate the world's biodiversity of interactions and likely contribute to mitigating the propagation of disturbances at large spatial scales.

The contribution of mutualistic interactions to functional and phylogenetic diversity.

Reduction of functional diversity (FD) and phylogenetic diversity (PD) likely affects ecosystem functions and reduces the potential of communities to respond to changes, such as climate change. Mutualistic interactions are essential for maintaining diversity, but their role has largely been ignored in conservation planning. We propose using a species' interaction niche - the diversity of its interaction partners - to measure a species' contribution to the maintenance of FD and PD via mutualistic interactions, and thus identify species and interspecific interactions that are particularly important for the conservation of ecosystem functions and evolutionary lineages in ecological communities. Our approach represents a switch in perspective that allows a direct assessment of the importance of mutualistic interactions for the maintenance of biodiversity and ecosystem functioning.

Niche Packing and Local Coexistence in a Megadiverse Guild of Frugivorous Birds Are Mediated by Fruit Dependence and Shifts in Interaction Frequencies.

AbstractNiche packing is one of the prevailing mechanisms underlying the increase in the number of co-occurring species and the extraordinary diversity of tropical ecosystems. However, it is not yet understood whether niche packing is facilitated by higher specialization and reduced niche overlap or, rather, by diffuse competition and increased niche overlap. We combined highly resolved bird-plant interaction networks, bird phylogenies, and plant functional traits to compare dietary niche overlap and foraging frequencies among frugivorous birds at seven sites in the tropical Andes. We quantified niche overlap on the basis of the traits of the plants used by each bird and related it to the degree of niche packing at the different sites. Niche complementarity decreased with increasing niche packing, suggesting that increasingly dense niche packing is facilitated by increased niche overlap. Pairwise niche overlap was mediated by shifts in foraging frequencies away from shared resources, and it decreased with decreasing phylogenetic relatedness and increasing dependence on fruit as resource. Our findings suggest that foraging choices are a key axis of diversification in frugivorous birds and that differences in resource use frequencies are already sufficient to reduce potential competition between ecologically similar species and facilitate niche packing, especially if species differ in their dependence on particular resources.

The recovery of functional diversity with restoration.

Ecological restoration aims at recovering biodiversity in degraded ecosystems, and it is commonly assessed via species richness. However, it is unclear whether increasing species richness in a site also recovers its functional diversity (FD), which has been shown to be a better representation of ecosystem functioning. We conducted a quantitative synthesis of 30 restoration projects and tested whether restoration improves FD. We compared actively and passively restored sites with degraded and reference sites with respect to four key measures of FD (functional richness, evenness, dispersion, and turnover) and two measures of species diversity (richness and evenness). We separately analyzed longitudinal studies (which monitor degraded, reference, and restored sites through time) and space-for-time substitutions (which compare at one point in time degraded and reference sites with restored sites of different ages). Space-for-time studies suggested that species diversity and FD improved over time. However, replicated longitudinal data showed no sustained benefits of active or passive restoration for FD measures, relative to degraded sites. This could suggest that the positive results in space-for-time designs may have been unreliable, but the relatively short duration of longitudinal studies suggests a need for longer-term longitudinal research to robustly demonstrate the absence of any effect. These differences across study designs may explain the variable results found in recent studies directly measuring the response of FD to restoration. We recommend that future assessments of ecological community dynamics include control sites in monitoring, to ensure that the consequences of treatments, including but not limited to restoration, are correctly partitioned from unassisted temporal changes.

Tricky partners: native plants show stronger interaction preferences than their exotic counterparts.

In ecological networks, neutral predictions suggest that species' interaction frequencies are proportional to their relative abundances. Deviations from neutral predictions thus correspond to interaction preferences (when positive) or avoidances (when negative), driven by nonneutral (e.g., niche-based) processes. Exotic species interact with many partners with which they have not coevolved, and it remains unclear whether this systematically influences the strength of neutral processes on interactions, and how these interaction-level differences scale up to entire networks. To fill this gap, we compared interactions between plants and frugivorous birds at nine forest sites in New Zealand varying in the relative abundance and composition of native and exotic species, with independently sampled data on bird and plant abundances from the same sites. We tested if the strength and direction of interaction preferences differed between native and exotic species. We further evaluated whether the performance of neutral predictions at the site level was predicted by the proportion of exotic interactions in each network from both bird and plant perspectives, and the species composition in each site. We found that interactions involving native plants deviated more strongly from neutral predictions than did interactions involving exotics. This "pickiness" of native plants could be detrimental in a context of global biotic homogenization where they could be increasingly exposed to novel interactions with neutrally interacting mutualists. However, the realization of only a subset of interactions in different sites compensated for the neutrality of interactions involving exotics, so that neutral predictions for whole networks did not change systematically with the proportion of exotic species or species composition. Therefore, the neutral and niche processes that underpin individual interactions may not scale up to entire networks. This shows that seemingly simplistic neutral assumptions entail complex processes and can provide valuable understanding of community assembly or invasion dynamics.

Strength of niche processes for species interactions is lower for generalists and exotic species.

Niche and neutral processes jointly influence species interactions. Predictions of interactions based on these processes assume that they operate similarly across all species. However, species characteristics could systematically create differences in the strength of niche or neutral processes for each interspecific interaction. We used national-level records of plant-frugivore interactions, species traits, biogeographic status (native vs. exotic), phylogenies and species range sizes to test the hypothesis that the strength of niche processes in species interactions changes in predictable ways depending on trophic generalism and biogeographic status of the interacting species. The strength of niche processes (measured as trait matching) decreased when the generalism of the interacting partners increased. Furthermore, the slope of this negative relationship between trait matching and generalism of the interacting partners was steeper (more negative) for interactions between exotic species than those between native species. These results remained significant after accounting for the potential effects of neutral processes (estimated by species range size). These observed changes in the strength of niche processes in generating species interactions, after accounting for effects of neutral processes, could improve predictions of ecological networks from species trait data. Specifically, due to their shorter co-evolutionary history, exotic species tend to interact with native species even when lower trait matching occurs than in interactions among native species. Likewise, interactions between generalist bird species and generalist plant species should be expected to occur despite low trait matching between species, whereas interactions between specialist species involve higher trait matching.

Similar composition of functional roles in Andean seed-dispersal networks, despite high species and interaction turnover.

The species composition of local communities varies in space, and its similarity generally decreases with increasing geographic distance between communities, a phenomenon known as distance decay of similarity. It is, however, not known how changes in local species composition affect ecological processes, that is, whether they lead to differences in the local composition of species' functional roles. We studied eight seed-dispersal networks along the South American Andes and compared them with regard to their species composition and their composition of functional roles. We tested (1) if changes in bird species composition lead to changes in the composition of bird functional roles, and (2) if the similarity in species composition and functional-role composition decreased with increasing geographic distance between the networks. We also used cluster analysis to (3) identify bird species with similar roles across all networks based on the similarity in the plants they consume, (i) considering only the species identity of the plants and (ii) considering the functional traits of the plants. Despite strong changes in species composition, the networks along the Andes showed similar composition of functional roles. (1) Changes in species composition generally did not lead to changes in the composition of functional roles. (2) Similarity in species composition, but not functional-role composition, decreased with increasing geographic distance between the networks. (3) The cluster analysis considering the functional traits of plants identified bird species with similar functional roles across all networks. The similarity in functional roles despite the high species turnover suggests that the ecological process of seed dispersal is organized similarly along the Andes, with similar functional roles fulfilled locally by different sets of species. The high species turnover, relative to functional turnover, also indicates that a large number of bird species are needed to maintain the seed-dispersal process along the Andes.

Trait-Based Assessments of Climate-Change Impacts on Interacting Species.

Plant-animal interactions are fundamentally important in ecosystems, but have often been ignored by studies of climate-change impacts on biodiversity. Here, we present a trait-based framework for predicting the responses of interacting plants and animals to climate change. We distinguish three pathways along which climate change can impact interacting species in ecological communities: (i) spatial and temporal mismatches in the occurrence and abundance of species, (ii) the formation of novel interactions and secondary extinctions, and (iii) alterations of the dispersal ability of plants. These pathways are mediated by three kinds of functional traits: response traits, matching traits, and dispersal traits. We propose that incorporating these traits into predictive models will improve assessments of the responses of interacting species to climate change.

Projected impacts of climate change on functional diversity of frugivorous birds along a tropical elevational gradient.

Climate change forces many species to move their ranges to higher latitudes or elevations. Resulting immigration or emigration of species might lead to functional changes, e.g., in the trait distribution and composition of ecological assemblages. Here, we combined approaches from biogeography (species distribution models; SDMs) and community ecology (functional diversity) to investigate potential effects of climate-driven range changes on frugivorous bird assemblages along a 3000 m elevational gradient in the tropical Andes. We used SDMs to model current and projected future occurrence probabilities of frugivorous bird species from the lowlands to the tree line. SDM-derived probabilities of occurrence were combined with traits relevant for seed dispersal of fleshy-fruited plants to calculate functional dispersion (FDis; a measure of functional diversity) for current and future bird assemblages. Comparisons of FDis between current and projected future assemblages showed consistent results across four dispersal scenarios, five climate models and two representative concentration pathways. Projections indicated a decrease of FDis in the lowlands, an increase of FDis at lower mid-elevations and little changes at high elevations. This suggests that functional dispersion responds differently to global warming at different elevational levels, likely modifying avian seed dispersal functions and plant regeneration in forest ecosystems along tropical mountains.

Functionally specialised birds respond flexibly to seasonal changes in fruit availability.

Interactions between resource and consumer species result in complex ecological networks. The overall structure of these networks is often stable in space and time, but little is known about the temporal stability of the functional roles of consumer species in these networks. We used a trait-based approach to investigate whether consumers (frugivorous birds) show similar degrees of functional specialisation on resources (plants) in ecological networks across seasons. We additionally tested whether closely related bird species have similar degrees of functional specialisation and whether birds that are functionally specialised on specific resource types within a season are flexible in switching to other resource types in other seasons. We analysed four seasonal replicates of two species-rich plant-frugivore networks from the tropical Andes. To quantify fruit preferences of frugivorous birds, we projected their interactions with plants into a multidimensional plant trait space. To measure functional specialisation of birds, we calculated a species' functional niche breadth (the extent of seasonal plant trait space utilised by a particular bird) and functional originality (the extent to which a bird species' fruit preference functionally differs from those of other species in a seasonal network). We additionally calculated functional flexibility, i.e. the ability of bird species to change their fruit preference across seasons in response to variation in plant resources. Functional specialisation of bird species varied more among species than across seasons, and phylogenetically similar bird species showed similar degrees of functional niche breadth (phylogenetic signal λ = 0·81) and functional originality (λ = 0·89). Additionally, we found that birds with high functional flexibility across seasons had narrow functional niche breadth and high functional originality per season, suggesting that birds that are seasonally specialised on particular resources are most flexible in switching to other fruit resources across seasons. The high flexibility of functionally specialised bird species to switch seasonally to other resources challenges the view that consumer species rely on functionally similar resources throughout the year. This flexibility of consumer species may be an important, but widely neglected mechanism that could potentially stabilise consumer-resource networks in response to human disturbance and environmental change.

Ecological networks are more sensitive to plant than to animal extinction under climate change.

Impacts of climate change on individual species are increasingly well documented, but we lack understanding of how these effects propagate through ecological communities. Here we combine species distribution models with ecological network analyses to test potential impacts of climate change on >700 plant and animal species in pollination and seed-dispersal networks from central Europe. We discover that animal species that interact with a low diversity of plant species have narrow climatic niches and are most vulnerable to climate change. In contrast, biotic specialization of plants is not related to climatic niche breadth and vulnerability. A simulation model incorporating different scenarios of species coextinction and capacities for partner switches shows that projected plant extinctions under climate change are more likely to trigger animal coextinctions than vice versa. This result demonstrates that impacts of climate change on biodiversity can be amplified via extinction cascades from plants to animals in ecological networks.

Morphology predicts species' functional roles and their degree of specialization in plant-frugivore interactions.

Species' functional roles in key ecosystem processes such as predation, pollination or seed dispersal are determined by the resource use of consumer species. An interaction between resource and consumer species usually requires trait matching (e.g. a congruence in the morphologies of interaction partners). Species' morphology should therefore determine species' functional roles in ecological processes mediated by mutualistic or antagonistic interactions. We tested this assumption for Neotropical plant-bird mutualisms. We used a new analytical framework that assesses a species's functional role based on the analysis of the traits of its interaction partners in a multidimensional trait space. We employed this framework to test (i) whether there is correspondence between the morphology of bird species and their functional roles and (ii) whether morphologically specialized birds fulfil specialized functional roles. We found that morphological differences between bird species reflected their functional differences: (i) bird species with different morphologies foraged on distinct sets of plant species and (ii) morphologically distinct bird species fulfilled specialized functional roles. These findings encourage further assessments of species' functional roles through the analysis of their interaction partners, and the proposed analytical framework facilitates a wide range of novel analyses for network and community ecology.

Specialization of mutualistic interaction networks decreases toward tropical latitudes.

Species-rich tropical communities are expected to be more specialized than their temperate counterparts. Several studies have reported increasing biotic specialization toward the tropics, whereas others have not found latitudinal trends once accounting for sampling bias or differences in plant diversity. Thus, the direction of the latitudinal specialization gradient remains contentious. With an unprecedented global data set, we investigated how biotic specialization between plants and animal pollinators or seed dispersers is associated with latitude, past and contemporary climate, and plant diversity. We show that in contrast to expectation, biotic specialization of mutualistic networks is significantly lower at tropical than at temperate latitudes. Specialization was more closely related to contemporary climate than to past climate stability, suggesting that current conditions have a stronger effect on biotic specialization than historical community stability. Biotic specialization decreased with increasing local and regional plant diversity. This suggests that high specialization of mutualistic interactions is a response of pollinators and seed dispersers to low plant diversity. This could explain why the latitudinal specialization gradient is reversed relative to the latitudinal diversity gradient. Low mutualistic network specialization in the tropics suggests higher tolerance against extinctions in tropical than in temperate communities.

Habitat stability affects dispersal and the ability to track climate change.

Habitat persistence should influence dispersal ability, selecting for stronger dispersal in habitats of lower temporal stability. As standing (lentic) freshwater habitats are on average less persistent over time than running (lotic) habitats, lentic species should show higher dispersal abilities than lotic species. Assuming that climate is an important determinant of species distributions, we hypothesize that lentic species should have distributions that are closer to equilibrium with current climate, and should more rapidly track climatic changes. We tested these hypotheses using datasets from 1988 and 2006 containing all European dragon- and damselfly species. Bioclimatic envelope models showed that lentic species were closer to climatic equilibrium than lotic species. Furthermore, the models over-predicted lotic species ranges more strongly than lentic species ranges, indicating that lentic species track climatic changes more rapidly than lotic species. These results are consistent with the proposed hypothesis that habitat persistence affects the evolution of dispersal.