Plant-hummingbird Networks Research Articles

Evolutionary history as a driver of ecological networks: a case study of plant–hummingbird interactions

Multiple factors drive species interactions in ecological networks, such as morphological barriers, spatio–temporal distribution, abundances and evolutionary histories of species. Novel methods are making it possible to evaluate the relative importance of each of these drivers. However, the lack of appropriate methods has prevented evaluating the extent to which interaction networks are shaped by species’ evolutionary histories. This study includes the evolutionary histories of species among the potential drivers of interactions, allowing the comparative analysis of its importance in structuring ecological networks. We hypothesized different possible phylogenetic scenarios to predict frequencies of interactions between species by combining concepts from the fields of ecological networks and ecophylogenetics. The usage of these scenarios is illustrated in a plant–hummingbird interaction network database from the Atlantic Forest, southeastern Brazil. We first evaluated which phylogenetic hypotheses better predict the observed network; subsequently, we evaluated the relative importance of species evolutionary histories, abundances, and matching on species morphologies and phenologies as drivers of their frequencies of interactions. The results suggest that the evolutionary histories of hummingbirds are more important than the species abundances in structuring the studied plant–hummingbird network but less important than the morphological and phenological matching among species. The approach developed here offers the potential to advance our understanding of the multiple factors structuring ecological networks.

The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity.

Plant species within communities may overlap in pollinators' use and influence visitation patterns of shared pollinators, potentially engaging in indirect interactions (e.g., facilitation or competition). While several studies have explored the mechanisms regulating insect-pollination networks, there is a lack of studies on bird-pollination systems, particularly in species-rich tropical areas. Here, we evaluated if phenotypic similarity, resource availability (floral abundance), evolutionary relatedness and flowering phenology affect the potential for indirect effects via shared pollinators in hummingbird-pollinated plant species within four communities in the Brazilian Atlantic forest. Among the evaluated factors, phenotypic similarity (corolla length and anther height) was the most important variable, while resource availability (floral abundance) had a secondary importance. On the other hand, evolutionary relatedness and flowering phenology were less important, which altogether highlights the relevance of convergent evolution and that the contribution of a plant to the diet of the pollinators of another plant is independent of the level of temporal overlap in flowering in this tropical system. Interestingly, our findings contrast with results from multiple insect-pollinated plant communities, mostly from temperate regions, in which floral abundance was the most important driver, followed by evolutionary relatedness and phenotypic similarity. We propose that these contrasting results are due to high level of specialization inherent to tropical hummingbird-pollination systems. Moreover, our results demonstrated that factors defining linkage rules of plant-hummingbird networks also determinate plant-plant potential indirect effects. Future studies are needed to test if these findings can be generalized to other highly specialized systems. Overall, our results have important implications for the understanding of ecological processes due resource sharing in mutualistic systems.

Corrigendum.

Journal of Animal EcologyVolume 85, Issue 4 p. 1131-1131 CorrigendumFree Access Corrigendum This article corrects the following: Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant–hummingbird network Jeferson Vizentin-Bugoni, Pietro K. Maruyama, Vanderlei J. Debastiani, L. da S. Duarte, Bo Dalsgaard, Marlies Sazima, Daniel Stouffer, Volume 85Issue 1Journal of Animal Ecology pages: 262-272 First Published online: November 30, 2015 First published: 10 May 2016 https://doi.org/10.1111/1365-2656.12520AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Vizentin-Bugoni, J., Maruyama, P.K., Debastiani, V.J., da S. Duarte, L., Dalsgaard, B. & Sazima, M. (2016) Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network. Journal of Animal Ecology, 85, 262-272. An error has been identified by the authors in the plant abundance data published in Vizentin-Bugoni et al. (2016). The correction results in a slight alteration to the trajectories of models including abundances (Figure 2 in Vizentin-Bugoni et al. 2016). However, the order of the best models remained the same. The corrected Fig. 2 is provided below. Figure 2Open in figure viewerPowerPoint Ability of eight models to predict observed frequency of interaction between pairwise species over increasing sampling effort in a plant–hummingbird network. Models are probability matrices based on species abundance (A), phenological overlap (P), morphological matching (M) and all possible combinations among them. The Null model is a benchmark model that assumes all interactions have the same probability to occur. Note that after 5 h of sampling effort, the model PM, which includes both phenological overlap and bill-corolla (morphological) matching, had the best ability to predict pairwise interaction, while those models including A had worst fits, even worse than the Null model. This means that the higher importance of forbidden links in detriment of abundances was identified even under low sampling. We also show the change in coefficient of correlation between the observed frequency of pairwise interactions and the frequency predicted by the best model PM (right axe, black line with dots in the plot). Note that the correlation coefficient tends to increase with sampling effort (up to c. 15 h). All correlations were P < 0·001. Corrections have also been made to the Supporting Information Tables A1 and A10 in Vizentin-Bugoni et al. (2016). Reference Vizentin-Bugoni, J., Maruyama, P.K., Debastiani, V.J., da S. Duarte, L., Dalsgaard, B. & Sazima, M. (2016) Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network. Journal of Animal Ecology, 85, 262– 272. doi: 10.1111/1365-2656.12459. Volume85, Issue4July 2016Pages 1131-1131 FiguresReferencesRelatedInformation

The integration of alien plants in mutualistic plant–hummingbird networks across the Americas: the importance of species traits and insularity

AbstractAimTo investigate the role of alien plants in mutualistic plant–hummingbird networks, assessing the importance of species traits, floral abundance and insularity on alien plant integration.LocationMainland and insular Americas.MethodsWe used species‐level network indices to assess the role of alien plants in 21 quantitative plant–hummingbird networks where alien plants occur. We then evaluated whether plant traits, including previous adaptations to bird pollination, and insularity predict these network roles. Additionally, for a subset of networks for which floral abundance data were available, we tested whether this relates to network roles. Finally, we tested the association between hummingbird traits and the probability of interaction with alien plants across the networks.ResultsWithin the 21 networks, we identified 32 alien plant species and 352 native plant species. On average, alien plant species attracted more hummingbird species (i.e. aliens had a higher degree) and had a higher proportion of interactions across their hummingbird visitors than native plants (i.e. aliens had a higher species strength). At the same time, an average alien plant was visited more exclusively by certain hummingbird species (i.e. had a higher level of complementary specialization). Large alien plants and those occurring on islands had more evenly distributed interactions, thereby acting as connectors. Other evaluated plant traits and floral abundance were unimportant predictors of network roles. Short‐billed hummingbirds had higher probability of including alien plants in their interactions than long‐billed species.Main conclusionsOnce incorporated into plant‐hummingbird networks, alien plants appear strongly integrated and, thus, may have a large influence on network dynamics. Plant traits and floral abundance were generally poor predictors of how well alien species are integrated. Short‐billed hummingbirds, often characterized as functionally generalized pollinators, facilitate the integration of alien plants. Our results show that plant–hummingbird networks are open for invasion.

Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network.

Virtually all empirical ecological interaction networks to some extent suffer from undersampling. However, how limitations imposed by sampling incompleteness affect our understanding of ecological networks is still poorly explored, which may hinder further advances in the field. Here, we use a plant-hummingbird network with unprecedented sampling effort (2716h of focal observations) from the Atlantic Rainforest in Brazil, to investigate how sampling effort affects the description of network structure (i.e. widely used network metrics) and the relative importance of distinct processes (i.e. species abundances vs. traits) in determining the frequency of pairwise interactions. By dividing the network into time slices representing a gradient of sampling effort, we show that quantitative metrics, such as interaction evenness, specialization (H2 '), weighted nestedness (wNODF) and modularity (Q; QuanBiMo algorithm) were less biased by sampling incompleteness than binary metrics. Furthermore, the significance of some network metrics changed along the sampling effort gradient. Nevertheless, the higher importance of traits in structuring the network was apparent even with small sampling effort. Our results (i) warn against using very poorly sampled networks as this may bias our understanding of networks, both their patterns and structuring processes, (ii) encourage the use of quantitative metrics little influenced by sampling when performing spatio-temporal comparisons and (iii) indicate that in networks strongly constrained by species traits, such as plant-hummingbird networks, even small sampling is sufficient to detect their relative importance for the frequencies of interactions. Finally, we argue that similar effects of sampling are expected for other highly specialized subnetworks.

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.

Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure

Interactions between flowers and their visitors span the spectrum from mutualism to antagonism. The literature is rich in studies focusing on mutualism, but nectar robbery has mostly been investigated using phytocentric approaches focused on only a few plant species. To fill this gap, we studied the interactions between a nectar-robbing hermit hummingbird, Phaethornis ruber, and the array of flowers it visits. First, based on a literature review of the interactions involving P. ruber, we characterized the association of floral larceny to floral phenotype. We then experimentally examined the effects of nectar robbing on nectar standing crop and number of visits of the pollinators to the flowers of Canna paniculata. Finally, we asked whether the incorporation of illegitimate interactions into the analysis affects plant-hummingbird network structure. We identified 97 plant species visited by P. ruber and found that P. ruber engaged in floral larceny in almost 30% of these species. Nectar robbery was especially common in flowers with longer corolla. In terms of the effect on C. paniculata, the depletion of nectar due to robbery by P. ruber was associated with decreased visitation rates of legitimate pollinators. At the community level, the inclusion of the illegitimate visits of P. ruber resulted in modifications of how modules within the network were organized, notably giving rise to a new module consisting of P. ruber and mostly robbed flowers. However, although illegitimate visits constituted approximately 9% of all interactions in the network, changes in nestedness, modularity, and network-level specialization were minor. Our results indicate that although a flower robber may have a strong effect on the pollination of a particular plant species, the inclusion of its illegitimate interactions has limited capacity to change overall network structure.

Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics

Ecological communities are organized in complex ecological networks. Trait‐based analyses of the structure of these networks in highly diversified species assemblages are crucial for improving our understanding of the ecological and evolutionary processes causing specialization in mutualistic networks. In this study, we assessed the importance of morphological traits for structuring plant–hummingbird networks in Neotropical forests by using a novel combination of quantitative analytical approaches. We recorded the visitation of hummingbirds to plant species over an entire year at three different elevations in Costa Rica and constructed quantitative networks based on interaction frequencies. Three morphological traits were measured in hummingbirds (bill length, bill curvature, and body mass) and plants (corolla length, curvature, and volume). We tested the effects of avian morphological traits and abundance on ecological specialization of hummingbird species. All three morphological traits of hummingbirds were positively associated with ecological specialization, especially bill curvature. We tested whether interaction strength in the networks was associated with the degree of trait matching between corresponding pairs of morphological traits in plant and hummingbird species and explore whether this was related to resource handling times by hummingbird species. We found strong and significant associations between interaction strength and the degree of trait matching. Moreover, the degree of trait matching, particularly between bill and corolla length, was associated with the handling time of nectar resources by hummingbirds. Our findings show that bill morphology structures tropical plant–hummingbird networks and patterns of interactions are closely associated with morphological matches between plant and bird species and the efficiency of hummingbirds' resource use. These results are consistent with the findings of seminal studies in plant–hummingbird systems from the neotropics. We conclude that trait‐based analyses of quantitative networks contribute to a better mechanistic understanding of the causes of specialization in ecological networks and could be valuable for studying processes of complementary trait evolution in highly diversified species assemblages.

Morphological and Spatio‐Temporal Mismatches Shape a Neotropical Savanna Plant‐Hummingbird Network

AbstractComplex networks of species interactions might be determined by species traits but also by simple chance meetings governed by species abundances. Although the idea that species traits structure mutualistic networks is appealing, most studies have found abundance to be a major structuring mechanism underlying interaction frequencies. With a well‐resolved plant–hummingbird interaction network from the Neotropical savanna in Brazil, we asked whether species morphology, phenology, nectar availability and habitat occupancy and/or abundance best predicted the frequency of interactions. For this, we constructed interaction probability matrices and compared them to the observed plant‐hummingbird matrix through a likelihood approach. Furthermore, a recently proposed modularity algorithm for weighted bipartite networks was employed to evaluate whether these factors also scale‐up to the formation of modules in the network. Interaction frequencies were best predicted by species morphology, phenology and habitat occupancy, while species abundances and nectar availability performed poorly. The plant–hummingbird network was modular, and modules were associated to morphological specialization and habitat occupancy. Our findings highlight the importance of traits as determinants of interaction frequencies and network structure, corroborating the results of a previous study on a plant–hummingbird network from the Brazilian Atlantic Forest. Thus, we propose that traits matter more in tropical plant–hummingbird networks than in less specialized systems. To test the generality of this hypothesis, future research could employ geographic or taxonomic cross‐system comparisons contrasting networks with known differences in level of specialization.

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.

Specialization in plant-hummingbird networks is associated with species richness, contemporary precipitation and quaternary climate-change velocity.

Large-scale geographical patterns of biotic specialization and the underlying drivers are poorly understood, but it is widely believed that climate plays an important role in determining specialization. As climate-driven range dynamics should diminish local adaptations and favor generalization, one hypothesis is that contemporary biotic specialization is determined by the degree of past climatic instability, primarily Quaternary climate-change velocity. Other prominent hypotheses predict that either contemporary climate or species richness affect biotic specialization. To gain insight into geographical patterns of contemporary biotic specialization and its drivers, we use network analysis to determine the degree of specialization in plant-hummingbird mutualistic networks sampled at 31 localities, spanning a wide range of climate regimes across the Americas. We found greater biotic specialization at lower latitudes, with latitude explaining 20–22% of the spatial variation in plant-hummingbird specialization. Potential drivers of specialization - contemporary climate, Quaternary climate-change velocity, and species richness - had superior explanatory power, together explaining 53–64% of the variation in specialization. Notably, our data provides empirical evidence for the hypothesized roles of species richness, contemporary precipitation and Quaternary climate-change velocity as key predictors of biotic specialization, whereas contemporary temperature and seasonality seem unimportant in determining specialization. These results suggest that both ecological and evolutionary processes at Quaternary time scales can be important in driving large-scale geographical patterns of contemporary biotic specialization, at least for co-evolved systems such as plant-hummingbird networks.