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.     

Trophic Niche in a Raptor Species: The Relationship between Diet Diversity,Habitat Diversity and Territory Quality

Recent research reports that many populations of species showing a wide trophic niche (generalists) are made up of both generalist individuals and individuals with a narrow trophic niche (specialists), suggesting trophic specializations at an individual level. If true, foraging strategies should be associated with individual quality and fitness. Optimal foraging theory predicts that individuals will select the most favourable habitats for feeding. In addition, the “landscape heterogeneity hypothesis” predicts a higher number of species in more diverse landscapes. Thus, it can be predicted that individuals with a wider realized trophic niche should have foraging territories with greater habitat diversity, suggesting that foraging strategies, territory quality and habitat diversity are inter-correlated. This was tested for a population of common kestrels Falco tinnunculus. Diet diversity, territory occupancy (as a measure of territory quality) and habitat diversity of territories were measured over an 8-year period. Our results show that: 1) territory quality was quadratically correlated with habitat diversity, with the best territories being the least and most diverse; 2) diet diversity was not correlated with territory quality; and 3) diet diversity was negatively correlated with landscape heterogeneity. Our study suggests that niche generalist foraging strategies are based on an active search for different prey species within or between habitats rather than on the selection of territories with high habitat diversity.     

Persistence of flower visitors and pollination services of a generalist tree in modified forests

Flower‐visiting insects provide essential pollination services to many plant species. It is thus of critical importance to understand the effects of anthropogenic landscape modification on these animals. Particularly at the landscape scale, we still lack information on how flower visitors are affected by different intensities of human disturbance. In this study, we chose six representative types of forest modification across a heterogeneous South African landscape. At 36 study sites we observed insect visitation to Celtis africana flowers in two consecutive years. This generalist tree species has small unspecialized flowers which we found to be pollinated by a diverse array of insects as well as by wind. Visitation rates to flowers of C. africana differed significantly among the six forest types and between two study years. Visitation rates were enhanced in modified forests, facilitated by a high abundance of feral honeybees (Apis mellifera). Fruit set in C. africana showed significant positive associations with insect visitation and with the diversity of flower visitors, but was only weakly predicted by forest type. Our findings imply that even though forest modification can strongly alter flower visitors, pollination services for trees with unspecialized flowers may persist at a landscape scale. We advise conservation managers to maintain modified forest fragments in addition to natural forests as these may contribute to sustain pollination services in human‐modified landscapes.     

Floral traits and reproduction of Avicennia schaueriana Moldenke (Acanthaceae): a generalist pollination system in the Lamiales

Pollination systems may vary in their degree of specialization from generalist to specialist and this is associated with the frequency and efficiency of pollinators. Self‐compatibility and a generalist pollination system appear to be adaptations that enhance the ability for colonizing new areas, which is typical of mangrove species. Avicennia schaueriana is a western mangrove species included in Acanthaceae, Lamiales, an order known to have specialized pollination. We aimed to describe the floral morphology and analyze the pollination and reproductive systems of A. schaueriana in a mangrove area on the northern coast of the state of Pernambuco, Brazil, to analyze the possible adaptations of this species to the environment. Avicennia schaueriana is self‐compatible; however, pollination activity is essential because there is no spontaneous formation of fruit. Reproductive efficacy was high, indicating pollinator efficiency. Some floral attributes of A. schaueriana suggest specialization; however, the broad spectrum of pollinators observed suggests that it has a generalist pollination system. The way in which pollinators interact with flowers and the environmental conditions may have exerted a selective force on the floral attributes of A. schaueriana, characterizing an adaptive generalized pollination system, which is somewhat specialized.     

Pollination systems, biogeography, and divergence times of three allopatric species of Schisandra in North America, China, and Japan

This study analyses the pollination systems and biogeography of three allopatdc species of Schisandra (Section Euschisandra) consisting of S.glabra (North America),S.bicolor (China),and S.repanda (Japan); the clade is delimited in a phylogenetic tree of Schisandraceae constructed with nuclear and plastid genes.The male and female flowers of these species have similar floral structures,but exhibit different pollination systems.At the base of the clade,S.glabra is pollinated by a wide variety of beetles and flies in a generalist pollination system that also includes floral heat and the use of male and female flowers as brood sites for insects.In Asia,however,S.bicolor and S.repanda are pollinated exclusively by one or two different species of gall midges (Resseliella spp.) in a specialist pollination system.In this system only female,pollen-eating gall midges pollinate the flowers and breed on nearby spiderwebs.The gall midge pollination system is specialized and derived from the generalist system in S.glabra,and basal in the clade.Pollen is the main floral resource,and we hypothesize it is exploited to enrich eggs,and as a result species of gall midges could increase reproductive fitness by feeding on a single dependable food source.Subsequently the life cycles of the plants and insects evolved into a tight association in old stable plant communities in the Sino-Japanese flora.Divergence times for the plant species are presented and correlated with past distributions and migration routes.     

地下结实植物白番红花的繁育系统与传粉生物学

地下结实是植物用来防御不利环境的一种策略, 研究地下结实植物的繁殖特性, 可以揭示它们的繁殖对策多样性, 对于探讨环境选择压力对其繁育系统及后代适合度的影响具有重要意义。白番红花(Crocus alatavicus)是一种分布在天山西部亚高山带、具地下芽和地下结实特性的早春短命植物。我们采用野外观测和统计分析方法, 对该物种的繁育系统与传粉生物学及其对亚高山环境的适应进行了研究。研究结果表明: 白番红花具有先花后叶的特性, 于4月上中旬始花, 呈爆发式开花式样; 花白色, 无花蜜无气味; 开花时, 下位子房位于地下, 花蕾在地上开放并随光照变化而开闭; 单花花期为6–9 d, 花萎蔫时花粉活性仍保持在75.39±5.69%, 柱头可授期为8 d。人工授粉实验结果显示, 该物种属于兼性异交繁育系统, 且具有自主自花授粉能力。白番红花属于泛化传粉系统, 鲁熊蜂 (Bombus lucorum)、老条蜂 (Anthophora senilis)和黄腹地花蜂 (Andrena capillosa)是有效传粉昆虫, 通过采食花粉进行传粉, 访花频率分别为0.50±0.27次•花–1•h–1、0.18±0.08次•花–1•h–1和0.13±0.05次•花–1•h–1。在天山西部亚高山早春环境中, 白番红花不仅利用其开花式样、泛化传粉系统及早春空白生态位来提高传粉效率, 而且通过自交亲和及主动自花授粉等繁育系统特征来弥补传粉昆虫少及访花频率低的不足, 从而保障繁殖成功。     

Generalized pollination,floral scent chemistry,and a possible case of hybridization in the African orchid Disa fragrans

Pollination systems in orchids tend to be specialized as a consequence of restrictive floral morphology and specific advertising signals. Here we document a notable exception: Disa fragrans subsp. fragrans, a taxon from the Drakensberg Mountains of South Africa, which is pollinated by insects belonging to at least four orders (flies, beetles, bees, and moths). Pollinaria of D. fragrans are attached to the feet of these visitors and pollination thus occurs in a rather haphazard fashion. Nevertheless, its pollination success and pollen transfer efficiency are comparable to those of its close relative, Disa sankeyi, which is pollinated by a single genus of wasps. D. fragrans has an exceptionally strong floral scent: volatile emission is 19–86 μg per inflorescence per hour, which is up to 100 fold greater than in D. sankeyi. The scent bouquet is comprised of at least 46 compounds, mostly benzenoids and phenylpropanoids, which are known to be general attractants to a wide range of insects. In contrast to D. sankeyi, the flowers of D. fragrans have a high level of spectral purity (chroma) as is typical of many generalist insect-pollinated plants. At a site where D. fragrans co-occurs with D. sankeyi we found a plant with intermediate characteristics that may be a hybrid between the two taxa. The novel case of generalist pollination in D. fragrans documented here serves as an example of how floral advertising traits might evolve during an evolutionary shift from specialized to generalized pollination.     

Evolution of pollination niches and floral divergence in the generalist plant Erysimum mediohispanicum

Background and Aims

How generalist plants diverge in response to pollinator selection without becoming specialized is still unknown. This study explores this question, focusing on the evolution of the pollination system in the pollination generalist Erysimum mediohispanicum (Brassicaceae).

Methods

Pollinator assemblages were surveyed from 2001 to 2010 in 48 geo-referenced populations covering the entire geographic distribution of E. mediohispanicum. Bipartite modularity, a complex network tool, was used to find the pollination niche of each population. Evolution of the pollination niches and the correlated evolution of floral traits and pollination niches were explored using within-species comparative analyses.

Key Results

Despite being generalists, the E. mediohispanicum populations studied can be classified into five pollination niches. The boundaries between niches were not sharp, the niches differing among them in the relative frequencies of the floral visitor functional groups. The absence of spatial autocorrelation and phylogenetic signal indicates that the niches were distributed in a phylogeographic mosaic. The ancestral E. mediohispanicum populations presumably belonged to the niche defined by a high number of beetle and ant visits. A correlated evolution was found between pollination niches and some floral traits, suggesting the existence of generalist pollination ecotypes.

Conclusions

It is conjectured that the geographic variation in pollination niches has contributed to the observed floral divergence in E. mediohispanicum. The process mediating this floral divergence presumably has been adaptive wandering, but the adaptation to the local pollinator faunas has been not universal. The outcome is a landscape where a few populations locally adapted to their pollination environment (generalist pollination ecotypes) coexist with many populations where this local adaptation has failed and where the plant phenotype is not primarily shaped by pollinators.     

The phylogeny of the louse genus Brueelia does not reflect host phylogeny

The general flowering (GF) events of forests in south-east Asia are perhaps the most spectacular phenomena in tropical biology. GF events occur at multiyear intervals. In GF, most dipterocarp species and many plants of other families come into flower and set fruit massively; these species and plants rarely flower except during GF events. GF is unique, because it can occur over thousands of kilometers and involve hundreds of plant species representing diverse families and lifeforms. It also involves strict mast fruiting. Satiation of generalist seed predators has been considered a primary force for GF. However, recent observations indicate that several selective agents rather than a single major factor may shape GF. In addition to the satiation of generalist predators, promotion of pollination could be one of the selective factors for GF, since synchronized flowering of many species causes an increase in pollinator activity through immigration and population growth. Although environmental prediction for better establishment of seedlings may also be involved in GF, no field data have been reported to support this idea. Long-term monitoring and further understanding of GF are essential for the conservation of this unique and diverse tropical forest in south-east Asia, especially in a period of global climatic change. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 233–247.     

Pollinator Interactions with Yellow Starthistle (Centaurea solstitialis) across Urban,Agricultural, and Natural Landscapes

Pollinator-plant relationships are found to be particularly vulnerable to land use change. Yet despite extensive research in agricultural and natural systems, less attention has focused on these interactions in neighboring urban areas and its impact on pollination services. We investigated pollinator-plant interactions in a peri-urban landscape on the outskirts of the San Francisco Bay Area, California, where urban, agricultural, and natural land use types interface. We made standardized observations of floral visitation and measured seed set of yellow starthistle (Centaurea solstitialis), a common grassland invasive, to test the hypotheses that increasing urbanization decreases 1) rates of bee visitation, 2) viable seed set, and 3) the efficiency of pollination (relationship between bee visitation and seed set). We unexpectedly found that bee visitation was highest in urban and agricultural land use contexts, but in contrast, seed set rates in these human-altered landscapes were lower than in natural sites. An explanation for the discrepancy between floral visitation and seed set is that higher plant diversity in urban and agricultural areas, as a result of more introduced species, decreases pollinator efficiency. If these patterns are consistent across other plant species, the novel plant communities created in these managed landscapes and the generalist bee species that are favored by human-altered environments will reduce pollination services.     

Competition,facilitation and the Allee effect

Individuals of different species may interact in many different ways, such as competition, mutualism, or predation, to name but a few. Recent theory and experiments reveal that whether an interaction is beneficial or detrimental to the dynamics of a population often depends on species densities and other environmental factors. Here, we explore how, for suitable densities, facilitation may arise between two competing species with an Allee effect. We consider two different mechanisms for the Allee effect: 1) plant species with obligate insect pollination, and 2) generalist predation. In the first case, a second plant species, competing for nutrients, may have a facilitative effect by attracting more pollinators. In the second case, another potentially competing species may serve to satiate the same generalist predator and thereby have a facilitative effect. We explore three aspects of facilitation in each of the two systems. The focal species may benefit from the presence of a ‘competitor’ if it experiences 1) the removal of the Allee threshold, 2) a lowering of the Allee threshold, or 3) an increase in carrying capacity. We find that the latter two effects occur in both study systems whereas the first only occurs for the generalist predation system but not for the plant‐pollination system. We give precise conditions on when such a facilitative effect can be expected. We also demonstrate several unexpected outcomes of these two‐species interactions with multiple steady states, such as obligate co‐occurence; we draw parallels to the dynamics of species known as ‘ecosystem engineers’, and we discuss implications for conservation and management.     

Pollinators of tropical dioecious angiosperms: a reassessment? No,not yet

The association between dioecy and generalist mode of pollination suggested about 20 years ago has been recently questioned. It is argued that there is evidence to indicate that a disproportionate number of dioecious species have relatively smaller flowers and a more generalist mode of pollination than hermaphroditic taxa. This trend seems to hold at the community level as well as within genera containing dioecious and hermaphroditic species. Like other correlations among characters, correlations among dioecy, small flower size, and pollination systems provide important insights into mechanisms of plant evolution.     

Are there pollination syndromes in the Australian epacrids (Ericaceae: Styphelioideae)? A novel statistical method to identify key floral traits per syndrome

Background and Aims

Convergent floral traits hypothesized as attracting particular pollinators are known as pollination syndromes. Floral diversity suggests that the Australian epacrid flora may be adapted to pollinator type. Currently there are empirical data on the pollination systems for 87 species (approx. 15 % of Australian epacrids). This provides an opportunity to test for pollination syndromes and their important morphological traits in an iconic element of the Australian flora.

Methods

Data on epacrid–pollinator relationships were obtained from published literature and field observation. A multivariate approach was used to test whether epacrid floral attributes related to pollinator profiles. Statistical classification was then used to rank floral attributes according to their predictive value. Data sets excluding mixed pollination systems were used to test the predictive power of statistical classification to identify pollination models.

Key Results

Floral attributes are correlated with bird, fly and bee pollination. Using floral attributes identified as correlating with pollinator type, bird pollination is classified with 86 % accuracy, red flowers being the most important predictor. Fly and bee pollination are classified with 78 and 69 % accuracy, but have a lack of individually important floral predictors. Excluding mixed pollination systems improved the accuracy of the prediction of both bee and fly pollination systems.

Conclusions

Although most epacrids have generalized pollination systems, a correlation between bird pollination and red, long-tubed epacrids is found. Statistical classification highlights the relative importance of each floral attribute in relation to pollinator type and proves useful in classifying epacrids to bird, fly and bee pollination systems.     

The pollination niche and its role in the diversification and maintenance of the southern African flora

The flora of southern Africa has exceptional species richness and endemism, making it an ideal system for studying the patterns and processes of evolutionary diversification. Using a wealth of recent case studies, I examine the evidence for pollinator-driven diversification in this flora. Pollination systems, which represent available niches for ecological diversification, are characterized in southern Africa by a high level of ecological and evolutionary specialization on the part of plants, and, in some cases, by pollinators as well. These systems are asymmetric, with entire plant guilds commonly specialized for a particular pollinator species or functional type, resulting in obvious convergent floral evolution among guild members. Identified modes of plant lineage diversification involving adaptation to pollinators in these guilds include (i) shifts between pollination systems, (ii) divergent use of the same pollinator, (iii) coevolution, (iv) trait tracking, and (v) floral mimicry of different model species. Microevolutionary studies confirm that pollinator shifts can be precipitated when a plant species encounters a novel pollinator fauna on its range margin, and macroevolutionary studies confirm frequent pollinator shifts associated with lineage diversification. As Darwin first noted, evolutionary specialization for particular pollinators, when resulting in ecological dependency, may increase the risk of plant extinction. I thus also consider the evidence that disturbance provokes pollination failure in some southern African plants with specialized pollination systems.     

Radiation of pollination systems in the Iridaceae of sub-Saharan Africa

BACKGROUND: Seventeen distinct pollination systems are known for genera of sub-Saharan African Iridaceae and recurrent shifts in pollination system have evolved in those with ten or more species. Pollination by long-tongued anthophorine bees foraging for nectar and coincidentally acquiring pollen on some part of their bodies is the inferred ancestral pollination strategy for most genera of the large subfamilies Iridoideae and Crocoideae and may be ancestral for the latter. Derived strategies include pollination by long-proboscid flies, large butterflies, night-flying hovering and settling moths, hopliine beetles and sunbirds. Bee pollination is diverse, with active pollen collection by female bees occurring in several genera, vibratile systems in a few and non-volatile oil as a reward in one species. Long-proboscid fly pollination, which is apparently restricted to southern Africa, includes four separate syndromes using different sets of flies and plant species in different parts of the subcontinent. Small numbers of species use bibionid flies, short-proboscid flies or wasps for their pollination; only about 2 % of species use multiple pollinators and can be described as generalists. SCOPE: Using pollination observations for 375 species and based on repeated patterns of floral attractants and rewards, we infer pollination mechanisms for an additional 610 species. Matching pollination system to phylogeny or what is known about species relationships based on shared derived features, we infer repeated shifts in pollination system in some genera, as frequently as one shift for every five or six species of southern African Babiana or Gladiolus. Specialized systems using pollinators of one pollination group, or even a single pollinator species are the rule in the family. Shifts in pollination system are more frequent in genera of Crocoideae that have bilaterally symmetric flowers and a perianth tube, features that promote adaptive radiation by facilitating precise shifts in pollen placement, in conjunction with changes in flower colour, scent and tube length. CONCLUSIONS: Diversity of pollination systems explains in part the huge species diversity of Iridaceae in sub-Saharan Africa, and permits species packing locally. Pollination shifts are, however, seen as playing a secondary role in speciation by promoting reproductive isolation in peripheral, ecologically distinct populations in areas of diverse topography, climate and soils. Pollination of Iridaceae in Eurasia and the New World, where the family is also well represented, is poorly studied but appears less diverse, although pollination by both pollen- and oil-collecting bees is frequent and bird pollination rare.     

Spatio-temporal variation in the pollination mode of Buxus balearica (Buxaceae), an ambophilous and selfing species: mainland-island comparison

Mixed-pollination systems may allow plants to achieve stable seed production when unpredictable conditions cause variation in the relative success of different pollination modes. We studied variation in time (two years) and space (in five populations, three from an island and two from mainland) in the pollination mode of Buxus balearica , an ambophilous (i.e. pollinated by wind and insects) and selfing species distributed in the Mediterranean Basin, by means of direct observations and experimental manipulations (bagging with different material). The relative importance of each pollination mode differed among populations; however, levels of selfing and wind pollination were similar between island and mainland. Flowers of B. balearica were visited only by generalist insects, and species composition and abundance of flower visitors varied both in space and time. Frequency of insect visits to plants were not higher in mainland than island populations, although insects on the mainland were more diverse, visited a proportionally greater number of flowers, and remained longer on the plants than insects on the island. Frequency of insect visits was negatively correlated with flowering synchrony (all populations pooled) and was found to increase seed set in one of the mainland populations (that with highest frequency of insect visits and highest flower visitation rate). Fruit and seed mass were found to be not affected by pollination mode. Scarcity of pollinators in the island seems to have an effect on the pollination mode, although the greatest variation in breeding system was found at a more local scale.     

Response diversity to land use occurs but does not consistently stabilise ecosystem services provided by native pollinators

More diverse biological communities may provide ecosystem services that are less variable over space or time. However, the mechanisms underlying this relationship are rarely investigated empirically in real‐world ecosystems. Here, we investigate how a potentially important stabilising mechanism, response diversity, the differential response to environmental change among species, stabilises pollination services against land‐use change. We measured crop pollination services provided by native bees across land‐use gradients in three crop systems. We found that bee species responded differentially to increasing agricultural land cover in all three systems, demonstrating that response diversity occurs. Similarly, we found response diversity in pollination services in two of the systems. However, there was no evidence that response diversity, in general, stabilised ecosystem services. Our results suggest that either response diversity is not the primary stabilising mechanism in our system, or that new measures of response diversity are needed that better capture the stabilising effects it provides.     

农田-荒地边缘地带中蝗虫边缘反应分析

探讨了中华蚱蜢等10种蝗总科昆虫对农田－荒地的边缘反应。研究发现,就同一边缘而言,有些物种的多度在靠近边缘时上升,而有些物种则下降。从科的水平上分析的结果与物种水平上的分析有差异。为了更精确地了解边缘对蝗虫的分布格局的影响,从物种水平上对其进行分析是 很有必要的。