Macroevolution of the plant–hummingbird pollination system

ABSTRACTPlant–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

The macroecology of phylogenetically structured hummingbird-plant networks

Aim To investigate the association between species richness, species' phylogenetic signal, insularity and historical and current climate with hummingbird-plant network structure. Location 54 communities along a c. 10,000 kilometer latitudinal gradient across the Americas (39ºN - 32ºS), ranging from sea level to c. 3700 m asl, located on the mainland and on islands, and covering a wide range of climate regimes. Methods We measured null-modeled corrected complementary specialization and bipartite modularity (compartmentalization) in networks of quantitative interactions between hummingbird and plant species. Using an ordinary least squares multi-model approach, we examined the influence of species richness, phylogenetic signal, insularity, and current and historical climate conditions on network structure. Results Phylogenetically-related species, especially plants, showed a tendency to interact with a similar array of partners. The spatial variation in network structure exhibited a constant association with species' phylogeny (R2=0.18-0.19). Species richness and environmental factors showed the strongest associations with network structure (R2=0.20-0.44; R2138 =0.32-0.45, respectively). Specifically, higher levels of complementary specialization and modularity were associated to species-rich communities and communities in which closely-related hummingbirds visited distinct sets of flowering species. On the mainland, warmer temperatures and higher historical temperature stability associated to higher levels of complementary specialization. Main conclusions Previous macroecological studies of interaction networks have highlighted the importance of environment and species richness in determining network structure. Here, for the first time, we report an association between species phylogenetic signal and network structure at macroecological scale. Specifically, null model corrected complementary specialization and modularity exhibited a positive association with species richness and a negative association with hummingbird phylogenetic signal, indicating that both high richness and high inter-specific competition among closely-related 150 hummingbirds exhibit important relationships with specialization in hummingbird-plant networks. Our results document how species richness, phylogenetic signal and climate associate with network structure in complex ways at macroecological scale

Global patterns of interaction specialization in bird-flower networks

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), 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 honeyeater-flower networks. Specifically, hummingbird-flower networks had a lower proportion of realized interactions (lower C), decreased niche overlap (greater H-2) and greater modularity (greater Q(B)). However, we found no significant differences between hummingbird- and sunbird-flower networks, nor between sunbird- and honeyeater-flower networks. Main conclusions As expected, hummingbirds and their floral resources have greater interaction specialization than honeyeaters, possibly because of greater phenotypic specialization and greater floral resource richness in the New World. Interaction specialization in sunbird-flower communities was similar to both hummingbird-flower and honeyeater-flower communities. This may either be due to the relatively small number of sunbird-flower networks available, or because sunbird-flower communities share features of both hummingbird-flower communities (specialized floral shapes) and honeyeater-flower communities (fewer floral resources). These results suggest a link between interaction specialization and both phenotypic specialization and floral resource richness within bird-flower communities at a global scale.CAPES Foundation [8105/2014-6, 8012/2014-08]; CNPq [309453/2013-5, 445405/2014-7]; Czech Science Foundation [14-36098G]; British Ornithologists' Union; Wolfson College, University of Oxford; FAPESP [2015/21457-4]; FAPEMIG; FUNDECT; Oticon Fonden Denmark; Danish Council for Independent Research Natural Sciences; University of Aarhus; CACyPI-Uatx-GK; FACEPE; OeAD; FAPESB; CONICIT; MICIT; CCT; UNED; OTS; DAAD; DFG; Hesse's Ministry of Higher Education, Research, and the ArtsSCI(E)ARTICLE81891-19104

Ecological mechanisms explaining interactions within plant–hummingbird networks: morphological matching increases towards lower latitudes

No embargoInteractions 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.</jats:p

¿Podemos transformar las situaciones conflictivas? : un aporte desde el pensamiento sistémico y complejo

Resumen: El estudio de los conflictos como fenómenos sociales complejos exige una diversidad de miradas y análisis para delinear, por una parte, los elementos constitutivos de los mismos: identificar los actores y sus interacciones, sus lenguajes y formas comunicativas, los contextos desde los cuales se relacionan, las estrategias de transformación o solución; y, por otra, es también necesario para evaluar los modos de intervención de los diversos operadores (facilitadores, mediadores, negociadores), sus estrategias y las herramientas aplicables a los distintos casos. Este ensayo propone una descripción integrada desde el pensamiento sistémico de Gregory Bateson y el pensamiento complejo de Edgar Morin, quienes, entre otros autores, han contribuido a una visión alternativa y superadora de las tradicionales posturas positivistas, conductistas o meramente estructurales, para acercarnos a estos fenómenos sociales con nuevos postulados teóricos y aplicaciones prácticas transformadoras.Abstract: The study of conflicts as complex social phenomena requires a diversity of views and analysis to delineate the constituent elements of them: identify the actors and their interactions, their languages and communicative forms, the contexts from which they relate to each other, strategies of transformation or solution. Also, it is necessary to evaluate the modes of intervention of the various operators (facilitators, mediators, negotiators), their strategies and the tools applicable to the different cases. This essay proposes an integrated description from the systemic thinking of Gregory Bateson and the complex thinking of Edgar Morin, who, among other authors, have contributed to an alternative vision, overcoming the traditional positivist, behavioral or merely structural positions, to approach these social phenomena with new theoretical postulates and transformative practical applications

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

Aim: To 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. Location: Mainland and insular Americas. Methods: We 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. Results: Within 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 conclusions: Once 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