High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas.
ABSTRACT: 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.
Project description: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.
Project description:BACKGROUNDS AND AIMS:Tropical plant species are already suffering the effects of climate change and projections warn of even greater changes in the following decades. Of particular concern are alterations in flowering phenology, given that it is considered a fitness trait, part of plant species ecological niche, with potential cascade effects in plant-pollinator interactions. The aim of the study was to assess the potential impacts of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants. METHODS:We implemented ecological niche modelling (ENM) to investigate the potential impacts of different climate change scenarios on the geographical distribution and flowering phenology of 62 hummingbird-pollinated plant species in the Brazilian Atlantic Forest. KEY RESULTS:Distribution models indicate future changes in the climatic suitability of their current habitats, suggesting a tendency towards discontinuity, reduction and spatial displacement. Flowering models indicate that climate can influence species phenology in different ways: some species may experience increased flowering suitability whereas others may suffer decreased suitability. CONCLUSIONS:Our results suggest that hummingbird-pollinated species are prone to changes in their geographical distribution and flowering under different climate scenarios. Such variation may impact the community structure of ecological networks and reproductive success of tropical plants in the near future.
Project description:The 361 species of hummingbirds that occur from Alaska to Patagonia pollinate ~7,000 plant species with flowers morphologically adapted to them. To better understand this asymmetric diversity build-up, this study analyzes the origin of hummingbird/plant mutualisms in North America and temperate South America, based on new compilations of the 184 hummingbird-adapted species in North America, the 56 in temperate South America, and complete species-level phylogenies for the relevant hummingbirds in both regions, namely five in temperate South America and eight in North America. Because both floras are relatively well sampled phylogenetically, crown or stem ages of many representative clades could be inferred. The hummingbird chronogram was calibrated once with fossils, once with substitutions rates, while plant chronograms were taken from the literature or in 13 cases newly generated.The 184 North American hummingbird-adapted species belong to ca. 70 lineages for 19 of which (comprising 54 species) we inferred divergence times. The 56 temperate South American hummingbird-adapted species belong to ca. 35 lineages, for 17 of which (comprising 25 species) we inferred divergence times. The oldest hummingbirds and hummingbird-adapted plant lineages in the South American assemblage date to 16-17 my, those in the North American assemblage to 6-7 my. Few hummingbird-pollinated clades in either system have >4 species.The asymmetric diversity build-up between hummingbirds and the plants dependent on them appears to arise not from rapid speciation within hummingbird-pollinated clades, but instead from a gradual and continuing process in which independent plant species switch from insect to bird pollination. Diversification within hummingbird-pollinated clades in the temperate regions of the Americas appears mainly due to habitat specialization and allopatric speciation, not bird pollination per se. Interaction tanglegrams, even if incomplete, indicate a lack of tight coevolution as perhaps expected for temperate-region mutualisms involving nectar-feeding vertebrates.
Project description:Intra and interspecific competition for nectar play an important role in hummingbird communities. Larger sized species usually exclude smaller species from the rich floral resources. However, it has been recently postulated that the competitive advantages of a large body size decline as the evolutionary distance between the contending species increases. In this study, we analyzed dominance hierarchy dynamics in a hummingbird assemblage in central Mexico. By monitoring hummingbird territories established in three plant species through 1 year, we assessed the effects of energy within territories and the territory owners identity in the frequency of inter and intraspecific encounters. We also evaluated if these factors affect the dominance of larger species when they compete against smaller distantly related contenders. Our results show that their frequency of intraspecific encounters was related with the identity of the territory's owner. On the contrary, the frequency of interspecific encounters was related with both the territory and the identity of the territory's owner. We did not find a significant difference between the number of encounters dominated by larger and smaller species and their contenders. However, the increase in genetic distance between contenders was positively associated with a higher frequency of encounters dominated by small hummingbirds. Our results showed that the ecological factors and evolutionary relationships among contenders play important roles in the dominance hierarchy dynamics.
Project description:The effects of specific functional groups of pollinators in the diversification of angiosperms are still to be elucidated. We investigated whether the pollination shifts or the specific association with hummingbirds affected the diversification of a highly diverse angiosperm lineage in the Neotropics. We reconstructed a phylogeny of 583 species from the Gesneriaceae family and detected diversification shifts through time, inferred the timing and amount of transitions among pollinator functional groups, and tested the association between hummingbird pollination and speciation and extinction rates. We identified a high frequency of pollinator transitions, including reversals to insect pollination. Diversification rates of the group increased through time since 25 Ma, coinciding with the evolution of hummingbird-adapted flowers and the arrival of hummingbirds in South America. We showed that plants pollinated by hummingbirds have a twofold higher speciation rate compared with plants pollinated by insects, and that transitions among functional groups of pollinators had little impact on the diversification process. We demonstrated that floral specialization on hummingbirds for pollination has triggered rapid diversification in the Gesneriaceae family since the Early Miocene, and that it represents one of the oldest identified plant-hummingbird associations. Biotic drivers of plant diversification in the Neotropics could be more related to this specific type of pollinator (hummingbirds) than to shifts among different functional groups of pollinators.
Project description:A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.
Project description:<h4>Background and aims</h4>Although pollen limitation of reproduction (PL) has been widely studied, our understanding of its occurrence in tropical communities, especially for bird-pollinated plants, is underdeveloped. In addition, inclusion of both quantity and quality aspects in studies of PL are generally lacking. Within hummingbird-pollinated plants, a prediction was made for higher PL for the quality than quantity aspects and a minor effect of temporal variation because hummingbirds are constant and efficient pollen vectors but they may transfer low quality pollen.<h4>Methods</h4>Field hand and open pollination experiments were conducted on 21 species in a tropical montane rain forest over 2 years. The quantity (fruit set and seeds per fruit) and quality (seed weight and germination) aspects of reproduction were assessed as the response to open pollination relative to outcross hand pollination. The relationships between the effect size of quantity and quality aspects of reproduction and predictive plant features (self-incompatibility, autogamy, density and pollinator specialization level) were assessed with phylogenetic generalized linear models.<h4>Key results</h4>Just over half of all the species expressed PL for one or more response variables. On average, the severity of PL was strong for one quality variable (seed germination; 0·83), but insignificant for another (seed weight; -0·03), and low to moderate for quantity variables (0·31 for seeds per fruit and 0·39 for fruit set). There was only a minor contribution of temporal variation to PL within the studied species. Common predictors of PL, i.e. phylogenetic relatedness, self-incompatibility, autogamy, plant density and pollinator specialization level, did not adequately explain variation in PL within this community.<h4>Conclusions</h4>Despite the measurable degree of PL within these hummingbird-pollinated plants, the causes of pollen quality and quantity insufficiency are not clear. Variables other than those tested may contribute to PL or causes of PL may vary among species and cannot adequately be accounted for when assessed from the within-community perspective.
Project description:BACKGROUND:The ridges and valleys of the Andes create physical barriers that limit animal dispersal and cause deterministic local variation in rainfall. This has resulted in physical isolation of animal populations and variation in habitats, each of which has likely contributed to the evolution of high species diversity in the region. However, the relative influences of geographic isolation, ecoclimatic conditions, and their potential interactions remain poorly understood. To address this, we compared patterns of genetic and morphological diversity in Peruvian populations of the hummingbird Metallura tyrianthina. RESULTS:Phylogenetic and variation partitioning analyses showed that geographic isolation rather than climatic dissimilarity explained the greatest proportion of genetic variance. In contrast, bill length variation was explained by climatic seasonality, but not by genetic divergence. We found that mutation-scaled migration rate (m) between persistently humid and semi-humid environments was nearly 20 times higher when the habitats were contiguous (m?=?39.9) than when separated by a barrier, the Cordillera de Vilcanota (m?=?2.1). Moreover, the population experiencing more gene flow exhibited a lesser degree of bill length divergence despite similar differences in climate. CONCLUSIONS:Geographic isolation is necessary for genetic divergence. Ecological differences, represented here by climate characteristics, are necessary for functional divergence. Gene flow appears to hinder the evolution of functional traits toward local adaptive optima. This suggests that functional diversification requires geographic isolation followed or accompanied by a shift in ecological conditions. Andean topography causes both isolation and climatic variation, underscoring its dual role in biotic diversification.
Project description:BACKGROUND AND AIMS:Because distylous species have two hermaphroditic style-length floral morphs, they face two sex allocation problems: the equilibrium morph ratio and the optimal allocation to pollen and seed production in each floral morph. Gender specialization is expected among distylous species when floral morphs differ in reproductive output. However, spatio-temporal variability in female reproductive output between morphs needs to be investigated to fully understand patterns of sexual expression and gender specialization in distylous plants. Between-year variation in flower and fruit production of hummingbird-pollinated Palicourea padifolia (Rubiaceae) was examined, focusing on functional gender expression of long- and short-styled morphs and comparing their reproductive performance in five consecutive years (1998-2002). METHODS:Between-year variation in inflorescence, floral bud and fruit production was monitored and quantified. These traits were then used as parameters to determine functional gender differences between floral morphs through time. KEY RESULTS:Inflorescence production varied among years but no significant differences were found between floral morphs. Long-styled plants initiated more floral buds per inflorescence every year than short-styled plants, suggesting higher allocation to pollinator attraction and, potentially, an increase in male fitness through pollen donation. Although fruit production was similar between morphs, their functional gender shifted across years. CONCLUSIONS:The gender expression inconsistency across years is surprising because a number of floral characters and attributes that contribute to differently attracting and rewarding effective pollinators in P. padifolia suggest gender specialization. The evidence that morphs of distylous species might specialize in functional gender mostly comes from differences among populations in seed production and non-equilibrium morph ratios based on 1-year field population surveys. The results suggest that more sampling through time is needed to detect gender specialization among distylous species with a perennial habit.
Project description: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.