Hummingbird Plant 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.

Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities

Summary Understanding how ecological processes structure species assemblages is a central issue in community ecology. While the influence of plant–pollinator interactions on each other's evolution is well recognized, their role in the assembly of interdependent communities of plants and pollinators is still unclear. Using data from seven communities of hummingbirds and plants that they pollinate from two tropical rain forest types (lowland and montane), we evaluated phylogenetic relationships and signal of functional traits, over space and time, to test predictions on the main processes (environmental filtering, facilitation or competition) that are driving these hummingbird–plant assemblages. Our findings suggest that the main processes driving these assemblages varied between hummingbirds and plants and between habitats, and even among communities at the same habitat. The non‐conserved floral trait and the phylogenetic patterns (even or random) give support to the hypothesis of facilitation or competition as processes regulating the composition of plant assemblages. Moreover, the positive relationship between fitness and flowering synchrony suggests facilitation as the most important mechanism for montane plant communities. Distinctively, for lowland plant communities, the combination of non‐conserved traits and clustered phylogenetic patterns may be a result of either adaptive radiation or biotic filtering driven by a particular pollinator species that plays a main role as plant community organizer. Lastly, evidence of trait conservatism, together with clustered or even phylogenetic patterns, suggests that facilitation or competition may drive the assembly of montane hummingbird communities, despite the predominance of random phylogenetic patterns. Synthesis. Overall, we present a pathway to identify central ecological processes that may drive the assembly of plant–pollinator communities. We show that different processes related with pollination that vary in space and time may contribute to the assembly of the interdependent tropical communities of plants and pollinators. These findings highlight the importance of considering ecological interactions when evaluating community assembly processes.

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.

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas.

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.

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.

The macroecology of phylogenetically structured hummingbird–plant networks

AbstractAimTo investigate the association between hummingbird–plant network structure and species richness, phylogenetic signal on species' interaction pattern, insularity and historical and current climate.LocationFifty‐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.MethodsWe 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).ResultsPhylogenetically 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 conclusionsOur 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.

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.

MotionMeerkat: integrating motion video detection and ecological monitoring

Summary Human observation is expensive and limits the breadth of data collection. For this reason, remotely placed video cameras are increasingly used to monitor animals. One drawback of field‐based video recordings is extensive review time. Computer vision can mitigate this cost and enhance data collection by extracting biological information from images with minimal time investment. MotionMeerkat is a new standalone program that identifies motion events from a video stream. After running a video, the user reviews a folder of candidate motion frames for the target organism. This tool reduces the time needed to review videos and accommodates a variety of inputs. I tested MotionMeerkat using hummingbird–plant videos recorded in a tropical montane forest. To validate the optimal parameter set for finding motion events, I counted hummingbirds observed from direct video review compared to events found in images returned from MotionMeerkat. To show the generality of the approach, MotionMeerkat was tested on a set of terrestrial and underwater videos. To assess the performance of the background subtraction for further image analysis, I hand counted the number of frames with target organisms and compared them to the MotionMeerkat output. MotionMeerkat was highly successful in finding motion events and often reduced the number of frames needed to capture hummingbird visitation by over 90%. Both background approaches effectively found a variety of organisms in ecological videos. I provide general recommendations for parameter settings and extending this approach in the future.

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.

Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird–plant network

Understanding the relative importance of multiple processes on structuring species interactions within communities is one of the major challenges in ecology. Here, we evaluated the relative importance of species abundance and forbidden links in structuring a hummingbird-plant interaction network from the Atlantic rainforest in Brazil. Our results show that models incorporating phenological overlapping and morphological matches were more accurate in predicting the observed interactions than models considering species abundance. This means that forbidden links, by imposing constraints on species interactions, play a greater role than species abundance in structuring the ecological network. We also show that using the frequency of interaction as a proxy for species abundance and network metrics to describe the detailed network structure might lead to biased conclusions regarding mechanisms generating network structure. Together, our findings suggest that species abundance can be a less important driver of species interactions in communities than previously thought.

The assembly of plants used as nectar sources by hummingbirds in a Cerrado area of Central Brazil

Studies on hummingbird–plant interactions commonly use a pollination approach emphasizing mutualistic relationships. But floral resources are often used opportunistically by these birds. Plant–pollinator assemblies and pollination sustainability will depend both on the well-adapted plants and other potential floral resources. The Cerrado, Neotropical savannas of Central Brazil, has ca. 7.5 % of its flora supposedly adapted to hummingbird pollination. But detailed information about flowers effectively used by hummingbirds at community level is still lacking. Hence, we recorded all plant species visited by hummingbirds, to determine how these nectariferous flowers were distributed in time and space in different plant formations of a Cerrado area, and also the hummingbird species that visit them. The study was conducted between March 2007 and December 2008 in the Panga Ecological Station. Data regarding flowering phenology, floral morphology and visitation were collected monthly. Forty-six nectariferous species from 39 genera and 17 families were recorded, most with annual flowering dynamics and tubular flowers. But only 21 species had a combination of traits fitting classic ornithophilous syndrome. For the remaining species hummingbird visitation was ascertained from observations at the study site or other sites in the region. Eight hummingbird species occurred in the area and were recorded visiting directly 36 plant species. The study area presented a relatively low number of ornithophilous plants, but a great habitat diversity and many non-ornithophilous plants that hummingbirds used as nectar sources. Therefore, in the studied Cerrado, the diversity of environments and nectariferous plants favour the maintenance of resident and migrant hummingbirds.

Antagonists and their effects in a hummingbird—plant interaction: Field experiments

In the plant—hummingbird interaction both the rewards offered by plants and the pollen transport effected by hummingbirds are usually exploited by antagonists such as herbivores and nectar robbers, which do not provide a benefit to either mutualistic partner. These antagonists can directly and indirectly affect plant fitness by forcing hummingbirds to modify their foraging behaviour. The ecological significance of antagonists for the plant—hummingbird interaction is largely unknown. The goal of this work was to investigate the combined effects of herbivores and nectar robbers on the interaction between the distylous herb Bouvardia ternifolia and its hummingbird visitors. By simulating different intensities of herbivory and nectar theft, we studied (1) changes in the foraging behaviour of visiting hummingbirds, (2) differences in the use of floral morphs, (3) changes in nectar characteristics, and (4) their effects on plant fitness. On plants of both morphs, higher levels of leaf defoliation and nectar removal were related to a decrease in the number of visited flowers, an increase in the time-to-arrival of hummingbirds, and a reduction in nectar availability and sugar production. The pollination experiments showed that seed production on both floral morphs was significantly reduced by herbivory and nectar removal. These results suggest that herbivores and nectar robbers can directly affect hummingbird foraging patterns and reduce the fitness of the host plants.

The Hummingbird Plant Community of a Tropical Montane Rain Forest in Southern Ecuador

Abstract: The diversity of a hummingbird plant community in the eastern Andes of southern Ecuador was studied on the equivalent of a hectare (two 500 ′ 10 m transects) at 1920 ‐ 2100 m a.s.l. over the course of a year. A total of 3186 flowering individuals, representing 12 plant families, 29 genera and 72 species, were found to be visited by hummingbirds. Bromeliaceae had the most species visited, followed by Orchidaceae and Ericaceae. The majority of visited plant species were represented by a very few individuals, and only a few species of the Bromeliaceae and Orchidaceae appeared in large numbers of visited individuals. With regard to life forms visited by hummingbirds, epiphytes predominated (59 %), followed by trees and shrubs (29 %), vines (8 %) and herbs (4 %). Visited flowers usually had short‐ to medium‐long floral tubes which were either functionally or morphologically tubiform or campanulate. Fifty percent of the species had red‐coloured flowers, and a considerable number of the blossoms (43 %) displayed contrasting colours. The 72 plant species received visits from 26 species of Trochilidae (hummingbirds) and two species of Coerebidae (honeycreepers). A mere eight species of hummingbirds were seen frequently at the study area; the remaining species were only occasionally sighted. The eight frequently sighted species of hummingbirds made use of a total of 74 % of all hummingbird‐visited plant species growing in the study area.

Flower mites and nectar production in six hummingbird-pollinated plants with contrasting flower longevities

Hummingbird flower mites and hummingbirds may compete intensely for the nectar secreted by their host plants. Here, we present the results from field experiments in which flower mites were excluded from flowers of six hummingbird-pollinated plants with contrasting flower longevities. Nectar measurements were taken on flowers from which mites were excluded and those without mite exclusion over their lifespans. The exclusion of mites had a significant positive effect on the amount of nectar available in plants with long-lived flowers. In contrast, nectar availability in short-lived flowers was not significantly reduced after mite exclusion. The significance of the mite-exclusion treatment was independent of floral morph and flower age. Results also suggest that the magnitude of the mite-exclusion treatment depends on the volume of nectar produced by the flower throughout its lifetime. The treatment effect was detected when nectar consumption, presumably by flower mites, exceeded 13% of the nectar produced by the flowers; nectar availability was not significantly reduced when nectar volume was &lt; 7 µL per flower. It appears that flower mites consume proportionately more nectar in long-lived flowers than in short-lived flowers. Parasitic hummingbird flower mites seem to be preferentially taking advantage of plant-pollinator interactions in which flowers last several days and produce large volumes of nectar. The consequences of this finding concerning plant–hummingbird–mite interactions await further investigation. As a working hypothesis, we propose that nectar production has increased over evolutionary time not only by the selective pressures imposed by the pollinators, but also to compensate for the reduction they suffer after exploitation by nectar robbers and thieves such as flower mites.Key words: Ascidae, flower longevity, hummingbird pollination, multiple-species interactions, mutualism exploitation, nectar theft.

Rufous hummingbird feeding territoriality in a suboptimal habitat

Postbreeding migratory female and immature rufous hummingbirds (Selasphorus rufus) establish feeding territories in dense meadows of several 'typical hummingbird plant species' and in individual Rhamnus purshiana shrubs. Resource utilization patterns and activity budgets of individuals in meadows are typical of territorial hummingbirds. Individuals in Rhamnus forage a high proportion of the time and are absent from their territories frequently and for long durations early and late in the day, and feed on other species during these absences. Rhamnus is marginally profitable to feed on and defend, but it may be the only available habitat for the individuals that utilize it.