Macroevolution of the plant-hummingbird pollination system.

Plant-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.

Ecological filtering shapes the impacts of agricultural deforestation on biodiversity.

The biodiversity impacts of agricultural deforestation vary widely across regions. Previous efforts to explain this variation have focused exclusively on the landscape features and management regimes of agricultural systems, neglecting the potentially critical role of ecological filtering in shaping deforestation tolerance of extant species assemblages at large geographical scales via selection for functional traits. Here we provide a large-scale test of this role using a global database of species abundance ratios between matched agricultural and native forest sites that comprises 71 avian assemblages reported in 44 primary studies, and a companion database of 10 functional traits for all 2,647 species involved. Using meta-analytic, phylogenetic and multivariate methods, we show that beyond agricultural features, filtering by the extent of natural environmental variability and the severity of historical anthropogenic deforestation shapes the varying deforestation impacts across species assemblages. For assemblages under greater environmental variability-proxied by drier and more seasonal climates under a greater disturbance regime-and longer deforestation histories, filtering has attenuated the negative impacts of current deforestation by selecting for functional traits linked to stronger deforestation tolerance. Our study provides a previously largely missing piece of knowledge in understanding and managing the biodiversity consequences of deforestation by agricultural deforestation.

Inter- and intra-island speciation and their morphological and ecological correlates in Aeonium (Crassulaceae), a species-rich Macaronesian radiation.

BACKGROUND AND AIMS: The most species-rich and ecologically diverse plant radiation on the Canary Islands is the Aeonium alliance (Crassulaceae). In island radiations like this, speciation can take place either within islands or following dispersal between islands. Aiming at quantifying intra- and inter-island speciation events in the evolution of Aeonium, and exploring their consequences, we hypothesized that (1) intra-island diversification resulted in stronger ecological divergence of sister lineages, and that (2) taxa on islands with a longer history of habitation by Aeonium show stronger ecological differentiation and produce fewer natural hybrids. METHODS: We studied the biogeographical and ecological setting of diversification processes in Aeonium with a fully sampled and dated phylogeny inferred using a ddRADseq approach. Ancestral areas and biogeographical events were reconstructed in BioGeoBEARS. Eleven morphological characters and three habitat characteristics were taken into account to quantify the morphological and ecological divergence between sister lineages. A co-occurrence matrix of all Aeonium taxa is presented to assess the spatial separation of taxa on each island. KEY RESULTS: We found intra- and inter-island diversification events in almost equal numbers. In lineages that diversified within single islands, morphological and ecological divergence was more pronounced than in lineages derived from inter-island diversification, but only the difference in morphological divergence was significant. Those islands with the longest history of habitation by Aeonium had the lowest percentages of co-occurring and hybridizing taxon pairs compared with islands where Aeonium arrived later. CONCLUSIONS: Our findings illustrate the importance of both inter- and intra-island speciation, the latter of which is potentially sympatric speciation. Speciation on the same island entailed significantly higher levels of morphological divergence compared with inter-island speciation, but ecological divergence was not significantly different. Longer periods of shared island habitation resulted in the evolution of a higher degree of spatial separation and stronger reproductive barriers.

The best of two worlds: ecology and evolution of ambophilous plants.

Ambophily, the mixed mode of wind and insect pollination is still poorly understood, even though it has been known to science for over 130 years. While its presence has been repeatedly inferred, experimental data remain regrettably rare. No specific suite of morphological or ecological characteristics has yet been identified for ambophilous plants and their ecology and evolution remain uncertain. In this review we summarise and evaluate our current understanding of ambophily, primarily based on experimental studies. A total of 128 ambophilous species - including several agriculturally important crops - have been reported from most major habitat types worldwide, but this probably represents only a small subset of ambophilous species. Ambophilous species have evolved both from wind- and insect-pollinated ancestors, with insect-pollinated ancestors mostly representing pollination by small, generalist flower visitors. We compiled floral and reproductive traits for known ambophilous species and compared our results to traits of species pollinated either by wind or by small generalist insects only. Floral traits were found to be heterogeneous and strongly overlap especially with those of species pollinated by small generalist insects, which are also the prominent pollinator group for ambophilous plants. A few ambophilous species are only pollinated by specialised bees or beetles in addition to pollination by wind. The heterogeneity of floral traits and high similarity to generalist small insect-pollinated species lead us to conclude that ambophily is not a separate pollination syndrome but includes species belonging to different insect- as well as wind-pollination syndromes. Ambophily therefore should be regarded as a pollination mode. We found that a number of ecological factors promoted the evolution of ambophily, including avoidance of pollen limitation and self-pollination, spatial flower interference and population density. However, the individual ecological factors favouring the transition to ambophily vary among species depending on species distribution, habitat, population structure and reproductive system. Finally, a number of experimental studies in combination with observations of floral traits of living and fossil species and dated phylogenies may indicate evolutionary stability. In some clades ambophily has likely prevailed for millions of years, for example in the castanoid clade of the Fagaceae.

Temporal changes in the Swiss flora: implications for flower-visiting insects.

BACKGROUND: Local floristic diversity has massively decreased during the twentieth century in Central Europe even though in the 1990s diversity began increasing again in several regions. However, little is known whether this increase is equally distributed among plant groups with different reproductive traits. METHODS: Our study is based on data of the Swiss Biodiversity Monitoring Program. In this program, plant species occurrence is recorded since 2001 in 450 regularly distributed 1 km2 study sites. For all 1774 plant species registered in the study, we researched data on flower/pseudanthium type and colour, reproductive system, and groups of flower visitors. We then tested whether temporal changes in species frequency were equally distributed among species with different trait states. RESULTS: Species richness and functional richness significantly increased in the study sites while functional evenness decreased. The frequency of wind-pollinated species increased more strongly than that of insect-pollinated species. Further, the frequency of species with simple, open insect-pollinated flowers and pseudanthia visited by generalist groups of insects increased slightly more strongly than the frequency of species with complex flowers visited by more specialized groups of flower visitors. Additionally, the frequency of self-compatible species increased significantly more than that of self-incompatible species. Thus, the overall increase in local plant species richness in Switzerland is mostly driven by wind- and generalist insect-pollinated, self-compatible species. In contrast, species with complex flowers, which are essential for specialized groups of flower visitors and species with self-incompatible reproductive systems profited less. CONCLUSIONS: Our study thus emphasizes the need to consider functional traits in the planning and monitoring of conservation activities, and calls for a special focus on plant species with specialized reproductive traits.

Influence of plant reproductive systems on the evolution of hummingbird pollination.

Many hummingbird-pollinated plant species evolved from bee-pollinated ancestors independently in many different habitats in North and South America. The mechanisms leading to these transitions are not completely understood. We conducted pollination and germination experiments and analyzed additional reproductive traits in three sister species pairs of which one species is bee- and the other hummingbird-pollinated. All hummingbird-pollinated species showed higher seed set and germination rates in cross-pollinated than in self-pollinated flowers. In the self-compatible, bee-pollinated sister species this difference did not exist. As expected, seed set and germination rate were higher after cross-pollination in the largely self-incompatible genus Penstemon independently of the pollination syndrome. However, the bird-pollinated species produce only half of the amount of ovules and pollen grains per flower compared to the bee-pollinated sister species. This indicates that hummingbird pollination is much more efficient in self-incompatible populations because hummingbirds waste less pollen and provide higher outcrossing rates. Therefore, hummingbird pollination is less resource costly. Overall, we suggest that hummingbirds may increase the reproductive success compared to bees, influencing the evolution of hummingbird pollination in ecosystems with diverse bee assemblages.

Pre- and postzygotic mechanisms preventing hybridization in co-occurring species of the Impatiens purpureoviolacea complex.

In the species-rich genus Impatiens, few natural hybrids are known, even though closely related species often occur sympatrically. In this study, we aim to bridge the gap between micro- and macro-evolution to disentangle pre- and postzygotic mechanisms that may prevent hybridization in the Impatiens purpureoviolacea complex from Central Africa. We analyzed habitat types, species distribution, pollination syndromes, pollinator dependency, genome sizes, and chromosome numbers of seven out of the ten species of the complex as well as of one natural hybrid and reconstructed the ancestral chromosome numbers of the complex. Several species of the complex occur in sympatry or geographically very close to each other. All of them are characterized by pre- and/or postzygotic mechanisms potentially preventing hybridization. We found four independent polyploidization events within the complex. The only known natural hybrid always appears as single individual and is self-fertile. But the plants resulting from self-pollinated seeds often die shortly after first flowering. These results indicate that the investigated mechanisms in combination may effectively but not absolutely prevent hybridization in Impatiens and probably occur in other genera with sympatric species as well.

Shifts in food plant abundance for flower-visiting insects between 1900 and 2017 in the canton of Zurich, Switzerland.

Adult flower-visiting insects feed on nectar and pollen and partly collect floral resources to feed their larvae. The reduction in food availability has therefore been proposed as one of the main causes for the drastic decline in flower-visiting insects in Central Europe. We compared the current (2012-2017) abundances of food plants of different groups of flower-visiting insects to that of 1900-1930 in the canton of Zurich, Switzerland. Comparisons were done separately for different vegetation types, flowering months, and groups of diurnal flower-visiting insects, such as bees, bumble bees, wasps, butterflies, hoverflies, flies, and beetles. We found a general decrease in food plant abundance for all groups of flower-visiting insects and in all vegetation types except ruderal areas. Reductions of food plant abundance were most pronounced for wetlands and agricultural fields, reflecting the massive transformation of wetlands into other habitat types and the intensified management of agricultural fields. Food plant abundance for specialized flower visitors (bees, bumble bees, butterflies) of wetlands decreased most strongly in May and for generalized flower visitors (wasps, hoverflies, flies, beetles) in July. Specialized plant species, i.e., species with few groups of flower visitors, decreased more strongly in abundance than species with many groups of flower visitors. Finally, we found a homogenization of food plant assemblages in all vegetation types except ruderal areas, where the opposite pattern emerged. Our results suggest a significant reduction in the diversity and abundance of food plants for flower-visiting insects over the past century, which has been most severe for the more specialized insect groups. The trend of insect decline, in particular those specialized on few plant species, can only be stopped by extending suitable habitats, i.e., by increasing food availability and reestablish selected plant populations.

Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide.

Thousands of plant species worldwide are dependent on birds for pollination. While the ecology and evolution of interactions between specialist nectarivorous birds and the plants they pollinate is relatively well understood, very little is known on pollination by generalist birds. The flower characters of this pollination syndrome are clearly defined but the geographical distribution patterns, habitat preferences and ecological factors driving the evolution of generalist-bird-pollinated plant species have never been analysed. Herein I provide an overview, compare the distribution of character states for plants growing on continents with those occurring on oceanic islands and discuss the environmental factors driving the evolution of both groups. The ecological niches of generalist-bird-pollinated plant species differ: on continents these plants mainly occur in habitats with pronounced climatic seasonality whereas on islands generalist-bird-pollinated plant species mainly occur in evergreen forests. Further, on continents generalist-bird-pollinated plant species are mostly shrubs and other large woody species producing numerous flowers with a self-incompatible reproductive system, while on islands they are mostly small shrubs producing fewer flowers and are self-compatible. This difference in character states indicates that diverging ecological factors are likely to have driven the evolution of these groups: on continents, plants that evolved generalist bird pollination escape from pollinator groups that tend to maintain self-pollination by installing feeding territories in single flowering trees or shrubs, such as social bees or specialist nectarivorous birds. This pattern is more pronounced in the New compared to the Old World. By contrast, on islands, plants evolved generalist bird pollination as an adaptation to birds as a reliable pollinator group, a pattern previously known from plants pollinated by specialist nectarivorous birds in tropical mountain ranges. Additionally, I discuss the evolutionary origins of bird pollination systems in comparison to systems involving specialist nectarivorous birds and reconstruct the bird pollination system of Hawaii, which may represent an intermediate between a specialist and generalist bird pollination system. I also discuss the interesting case of Australia, where it is difficult to distinguish between specialist and generalist bird pollination systems.

A question of data quality-Testing pollination syndromes in Balsaminaceae.

Pollination syndromes and their predictive power regarding actual plant-animal interactions have been controversially discussed in the past. We investigate pollination syndromes in Balsaminaceae, utilizing quantitative respectively categorical data sets of flower morphometry, signal and reward traits for 86 species to test for the effect of different types of data on the test patterns retrieved. Cluster Analyses of the floral traits are used in combination with independent pollinator observations. Based on quantitative data we retrieve seven clusters, six of them corresponding to plausible pollination syndromes and one additional, well-supported cluster comprising highly divergent floral architectures. This latter cluster represents a non-syndrome of flowers not segregated by the specific data set here used. Conversely, using categorical data we obtained only a rudimentary resolution of pollination syndromes, in line with several earlier studies. The results underscore that the use of functional, exactly quanitified trait data has the power to retrieve pollination syndromes circumscribed by the specific data used. Data quality can, however, not be replaced by sheer data volume. With this caveat, it is possible to identify pollination syndromes from large datasets and to reliably extrapolate them for taxa for which direct observations are unavailable.

The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project.

The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.

Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases.

Land-use change and intensification threaten bee populations worldwide, imperilling pollination services. Global models are needed to better characterise, project, and mitigate bees' responses to these human impacts. The available data are, however, geographically and taxonomically unrepresentative; most data are from North America and Western Europe, overrepresenting bumblebees and raising concerns that model results may not be generalizable to other regions and taxa. To assess whether the geographic and taxonomic biases of data could undermine effectiveness of models for conservation policy, we have collated from the published literature a global dataset of bee diversity at sites facing land-use change and intensification, and assess whether bee responses to these pressures vary across 11 regions (Western, Northern, Eastern and Southern Europe; North, Central and South America; Australia and New Zealand; South East Asia; Middle and Southern Africa) and between bumblebees and other bees. Our analyses highlight strong regionally-based responses of total abundance, species richness and Simpson's diversity to land use, caused by variation in the sensitivity of species and potentially in the nature of threats. These results suggest that global extrapolation of models based on geographically and taxonomically restricted data may underestimate the true uncertainty, increasing the risk of ecological surprises.

Contrasting biodiversity-ecosystem functioning relationships in phylogenetic and functional diversity.

It is well known that ecosystem functioning is positively influenced by biodiversity. Most biodiversity-ecosystem functioning experiments have measured biodiversity based on species richness or phylogenetic relationships. However, theoretical and empirical evidence suggests that ecosystem functioning should be more closely related to functional diversity than to species richness. We applied different metrics of biodiversity in an artificial biodiversity-ecosystem functioning experiment using 64 species of green microalgae in combinations of two to 16 species. We found that phylogenetic and functional diversity were positively correlated with biomass overyield, driven by their strong correlation with species richness. At low species richness, no significant correlation between overyield and functional and phylogenetic diversity was found. However, at high species richness (16 species), we found a positive relationship of overyield with functional diversity and a negative relationship with phylogenetic diversity. We show that negative phylogenetic diversity-ecosystem functioning relationships can result from interspecific growth inhibition. The opposing performances of facilitation (functional diversity) and inhibition (phylogenetic diversity) we observed at the 16 species level suggest that phylogenetic diversity is not always a good proxy for functional diversity and that results from experiments with low species numbers may underestimate negative species interactions.

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.

The temporal build-up of hummingbird/plant mutualisms in North America and temperate South America.

BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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.

The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts.

Biodiversity continues to decline in the face of increasing anthropogenic pressures such as habitat destruction, exploitation, pollution and introduction of alien species. Existing global databases of species' threat status or population time series are dominated by charismatic species. The collation of datasets with broad taxonomic and biogeographic extents, and that support computation of a range of biodiversity indicators, is necessary to enable better understanding of historical declines and to project - and avert - future declines. We describe and assess a new database of more than 1.6 million samples from 78 countries representing over 28,000 species, collated from existing spatial comparisons of local-scale biodiversity exposed to different intensities and types of anthropogenic pressures, from terrestrial sites around the world. The database contains measurements taken in 208 (of 814) ecoregions, 13 (of 14) biomes, 25 (of 35) biodiversity hotspots and 16 (of 17) megadiverse countries. The database contains more than 1% of the total number of all species described, and more than 1% of the described species within many taxonomic groups - including flowering plants, gymnosperms, birds, mammals, reptiles, amphibians, beetles, lepidopterans and hymenopterans. The dataset, which is still being added to, is therefore already considerably larger and more representative than those used by previous quantitative models of biodiversity trends and responses. The database is being assembled as part of the PREDICTS project (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems - http://www.predicts.org.uk). We make site-level summary data available alongside this article. The full database will be publicly available in 2015.

Can joint carbon and biodiversity management in tropical agroforestry landscapes be optimized?

Managing ecosystems for carbon storage may also benefit biodiversity conservation, but such a potential 'win-win' scenario has not yet been assessed for tropical agroforestry landscapes. We measured above- and below-ground carbon stocks as well as the species richness of four groups of plants and eight of animals on 14 representative plots in Sulawesi, Indonesia, ranging from natural rainforest to cacao agroforests that have replaced former natural forest. The conversion of natural forests with carbon stocks of 227-362 Mg C ha(-1) to agroforests with 82-211 Mg C ha(-1) showed no relationships to overall biodiversity but led to a significant loss of forest-related species richness. We conclude that the conservation of the forest-related biodiversity, and to a lesser degree of carbon stocks, mainly depends on the preservation of natural forest habitats. In the three most carbon-rich agroforestry systems, carbon stocks were about 60% of those of natural forest, suggesting that 1.6 ha of optimally managed agroforest can contribute to the conservation of carbon stocks as much as 1 ha of natural forest. However, agroforestry systems had comparatively low biodiversity, and we found no evidence for a tight link between carbon storage and biodiversity. Yet, potential win-win agroforestry management solutions include combining high shade-tree quality which favours biodiversity with cacao-yield adapted shade levels.

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.

The influence of climatic seasonality on the diversity of different tropical pollinator groups.

Tropical South America is rich in different groups of pollinators, but the biotic and abiotic factors determining the geographical distribution of their species richness are poorly understood. We analyzed the species richness of three groups of pollinators (bees and wasps, butterflies, hummingbirds) in six tropical forests in the Bolivian lowlands along a gradient of climatic seasonality and precipitation ranging from 410 mm to 6250 mm. At each site, we sampled the three pollinator groups and their food plants twice for 16 days in both the dry and rainy seasons. The richness of the pollinator groups was related to climatic factors by linear regressions. Differences in species numbers between pollinator groups were analyzed by Wilcoxon tests for matched pairs and the proportion in species numbers between pollinator groups by correlation analyses. Species richness of hummingbirds was most closely correlated to the continuous availability of food, that of bees and wasps to the number of food plant species and flowers, and that of butterflies to air temperature. Only the species number of butterflies differed significantly between seasons. We were not able to find shifts in the proportion of species numbers of the different groups of pollinators along the study gradient. Thus, we conclude that the diversity of pollinator guilds is determined by group-specific factors and that the constant proportions in species numbers of the different pollinator groups constitute a general pattern.