Complex 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.
Aim To investigate the association between hummingbird–plant network structure and species richness, phylogenetic signal on species' interaction pattern, insularity and historical and current climate. Location Fifty‐four communities along a c. 10,000 km latitudinal gradient across the Americas (39° N–32° S), ranging from sea level to c. 3700 m a.s.l., located on the mainland and on islands and covering a wide range of climate regimes. Methods We measured the level of specialization and modularity in mutualistic plant–hummingbird interaction networks. Using an ordinary least squares multimodel approach, we examined the influence of species richness, phylogenetic signal, insularity and current and historical climate conditions on network structure (null‐model‐corrected specialization and modularity). Results Phylogenetically related species, especially plants, showed a tendency to interact with a similar array of mutualistic partners. The spatial variation in network structure exhibited a constant association with species phylogeny (R2 = 0.18–0.19); however, network structure showed the strongest association with species richness and environmental factors (R2 = 0.20–0.44 and R2 = 0.32–0.45, respectively). Specifically, higher levels of specialization and modularity were associated with species‐rich communities and communities in which closely related hummingbirds visited distinct sets of flowering species. On the mainland, specialization was also associated with warmer temperatures and greater historical temperature stability. Main conclusions Our results confirm the results of previous macroecological studies of interaction networks which have highlighted the importance of species richness and the environment in determining network structure. Additionally, for the first time, we report an association between network structure and species phylogenetic signal at a macroecological scale, indicating that high specialization and modularity are associated with high interspecific competition among closely related hummingbirds, subdividing the floral niche. This suggests a tighter co‐evolutionary association between hummingbirds and their plants than in previously studied plant–bird mutualistic systems.
Generalization prevails in flower-animal interactions, and although animal visitors are not equally effective pollinators, most interactions likely represent an important energy intake for the animal visitor. Hummingbirds are nectar-feeding specialists, and many tropical plants are specialized toward hummingbird-pollination. In spite of this, especially in dry and seasonal tropical habitats, hummingbirds may often rely on non-ornithophilous plants to meet their energy requirements. However, quantitative studies evaluating the relative importance of ornithophilous vs. non-ornithophilous plants for hummingbirds in these areas are scarce. We here studied the availability and use of floral resources by hummingbirds in two different areas of the Cerrado, the seasonal savannas in Central Brazil. Roughly half the hummingbird visited plant species were non-ornithophilous, and these contributed greatly to increase the overall nectar availability. We showed that mean nectar offer, at the transect scale, was the only parameter related to hummingbird visitation frequency, more so than nectar offer at single flowers and at the plant scale, or pollination syndrome. Centrality indices, calculated using hummingbird-plant networks, showed that ornithophilous and non-ornithophilous plants have similar importance for network cohesion. How this foraging behaviour affects reproduction of non-ornithophilous plants remains largely unexplored and is probably case specific, however, we suggest that the additional energy provided by non-ornithophilous plants may facilitate reproduction of truly ornithophilous flowers by attracting and maintaining hummingbirds in the area. This may promote asymmetric hummingbird-plant associations, i.e., pollination depends on floral traits adapted to hummingbird morphology, but hummingbird visitation is determined more by the energetic "reward" than by pollination syndromes.
Interactions between species are influenced by different ecological mechanisms, such as morphological matching, phenological overlap and species abundances. How these mechanisms explain interaction frequencies across environmental gradients remains poorly understood. Consequently, we also know little about the mechanisms that drive the geographical patterns in network structure, such as complementary specialization and modularity. Here, we use data on morphologies, phenologies and abundances to explain interaction frequencies between hummingbirds and plants at a large geographical scale. For 24 quantitative networks sampled throughout the Americas, we found that the tendency of species to interact with morphologically matching partners contributed to specialized and modular network structures. Morphological matching best explained interaction frequencies in networks found closer to the equator and in areas with low-temperature seasonality. When comparing the three ecological mechanisms within networks, we found that both morphological matching and phenological overlap generally outperformed abundances in the explanation of interaction frequencies. Together, these findings provide insights into the ecological mechanisms that underlie geographical patterns in resource specialization. Notably, our results highlight morphological constraints on interactions as a potential explanation for increasing resource specialization towards lower latitudes.
Aim: Among the world's three major nectar-feeding bird taxa, hummingbirds are the most phenotypically specialized for nectarivory, followed by sunbirds, while the honeyeaters are the least phenotypically specialized taxa. We tested whether this phenotypic specialization gradient is also found in the interaction patterns with their floral resources.Location: Americas, Africa, Asia and Oceania/Australia. Methods:We compiled interaction networks between birds and floral resources for 79 hummingbird, nine sunbird and 33 honeyeater communities. Interaction specialization was quantified through connectance (C), complementary specialization (H 2 0 ), binary (Q B ) and weighted modularity (Q), with both observed and null-model corrected values. We compared interaction specialization among the three types of bird-flower communities, both independently and while controlling for potential confounding variables, such as plant species richness, asymmetry, latitude, insularity, topography, sampling methods and intensity.Results: Hummingbird-flower networks were more specialized than honeyeaterflower networks. Specifically, hummingbird-flower networks had a lower proportion of realized interactions (lower C), decreased niche overlap (greater H 2 0 ) and greater modularity (greater Q B ). However, we found no significant differences between hummingbird-and sunbird-flower networks, nor between sunbird-and honeyeaterflower networks.
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.
Aim We examined the effects of space, climate, phylogeny and species traits on module composition in a cross‐biomes plant–hummingbird network. Location Brazil, except Amazonian region. Methods We compiled 31 local binary plant–hummingbird networks, combining them into one cross‐biomes metanetwork. We conducted a modularity analysis and tested the relationship between species’ module membership with traits, geographical location, climatic conditions and range sizes, employing random forest models. We fitted reduced models containing groups of related variables (climatic, spatial, phylogenetic, traits) and combinations of groups to partition the variance explained by these sets into unique and shared components. Results The Brazilian cross‐biomes network was composed of 479 plant and 42 hummingbird species, and showed significant modularity. The resulting six modules conformed well to vegetation domains. Only plant traits, not hummingbird traits, differed between modules, notably plants’ growth form, corolla length, flower shape and colour. Some modules included plant species with very restricted distributions, whereas others encompassed more widespread ones. Widespread hummingbirds were the most connected, both within and between modules, whereas widespread plants were the most connected between modules. Among traits, only nectar concentration had a weak effect on among‐module connectivity. Main conclusions Climate and spatial filters were the main determinants of module composition for hummingbirds and plants, potentially related to resource seasonality, especially for hummingbirds. Historical dispersal‐linked contingency, or environmental variations not accounted for by the explanatory factors here evaluated, could also contribute to the spatial component. Phylogeny and morphological traits had no unique effects on the assignment of species to modules. Widespread species showed higher within‐ and/or among‐module connectivity, indicating their key role connecting biomes, and, in the case of hummingbirds, communities within biomes. Our results indicate that biogeography and climate not only determine the variation of modularity in local plant–animal networks, as previously shown, but also affect the cross‐biomes network structure.
Agora é tempo de agradecer: À Deus, base da minha Força e Coragem. "Deus que faz as cruzes faz também os ombros. Ninguém o iguala na arte das proporções" (P. Prin). À Professora Ariuska, agradeço pela confiança ao aceitar-me como sua primeira orientanda de doutorado e pela oportunidade em permitir-me desenvolver as habilidades em pesquisas e inovações, elaboração de projetos visando financiamentos, nas co-orientações de TCC e ICs. Obrigada pela compreensão nos meus momentos de incertezas. À Professora Cristina Brandão, minha Conselheira, um exemplo de dedicação e paixão pela Academia e de moral e compromisso com a ciência de qualidade. Ao Professor Koide, mais do que um Professor, outro exemplo de desprendimento, moral e compromisso. Aprendi muito com nossas conversas sobre a vida, o mundo administrativo da academia, sobre política e, lógico, sobre Engenharia. Obrigada por todo o apoio financeiro. Aos membros da Banca Examinadora, à Professora Cynthia Kyaw, minha admiração e agradecimento. À Professora Lenora, agradeço pelas discussões e por descomplicar a biologia molecular. Aos Professores Silvana Queiroz, Marcos von Sperling e Marco Antonio Almeida de Souza pelas valiosas contribuições na discussão da tese. Aos professores do PTARH, Nestor (Compromisso e Responsabilidade), Yovanka (pela amizade e discussões de métodos analíticos), Oscar (Diplomacia), Marco Antônio (pela dedicação e por abrir a sua casa para as festas tão animadas do PTARH), Ricardo Bernardes (Ciência e Filosofia), aprendi muito com cada um de vocês. Ao Carlos, Conceição e Dirceu, ainda que pelos corredores do PTARH, também fizeram parte da minha formação. Ao amigo Leonardo Damasceno que me incentivou a buscar um Programa de Pós-Graduação que me faria uma profissional com verdadeira competência técnica.
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