Ecological fitting is a sufficient driver of tight interactions between sunbirds and ornithophilous plants.
ABSTRACT: Plant-bird pollination interactions evolved independently on different continents. Specific adaptations can lead to their restriction when potential partners from distant evolutionary trajectories come into contact. Alternatively, these interactions can be enabled by convergent evolution and subsequent ecological fitting.We studied the interactions between New World plants from the genus Heliconia, Asian plants of genus Etlingera and African sunbirds on a local farm in Cameroon. Heliconia spp. evolved together with hummingbirds and Etlingera spp. with spiderhunters -an oriental subgroup of the sunbird family.Sunbirds fed on all studied plants and individual plant species were visited by a different sunbird spectrum. We experimentally documented a higher number of germinated pollen grains in sunbird-visited flowers of Etlingera spp. For Heliconia spp., this experiment was not successful and pollen tubes were rarely observed, even in hand-pollinated flowers, where enough pollen was deposited. The analyses of contacts with plant reproductive organs nevertheless confirmed that sunbirds are good pollen vectors for both Heliconia and Etlingera species.Our study demonstrated a high ecological fit between actors of distinct evolutionary history and the general validity of bird-pollination syndrome. We moreover show that trait matching and niche differentiation are important ecological processes also in semi-artificial plant-pollinator systems.
Project description:Geographic variation in the reproductive traits of animal-pollinated plants can be shaped by spatially variable selection imposed by differences in the local pollination environment. We investigated this process in Babiana ringens (Iridaceae), an enigmatic species from the Western Cape region of South Africa. B. ringens has evolved a specialized perch facilitating cross-pollination by sunbirds and displays striking geographic variation in perch size and floral traits. Here, we investigate whether this variation can be explained by geographic differences in the pollinator communities. We measured floral and inflorescence traits, and abiotic variables (N, P, C, and rainfall) and made observations of sunbirds in populations spanning the range of B. ringens. In each population, we recorded sunbird species identity and measured visitation rates, interfloral pollen transfer, and whether the seed set of flowers was pollen limited. To evaluate whether competition from co-occurring sunbird-pollinated species might reduce visitation, we quantified nectar rewards in B. ringens and of other co-flowering bird-pollinated species in local communities in which populations occurred. Variation in abiotic variables was not associated with geographical variation of traits in B. ringens. Malachite sunbirds were the dominant visitor (97% of visits) and populations with larger-sized traits exhibited higher visitation rates, more between-flower pollen transfer and set more seed. No sunbirds were observed in four populations, all with smaller-sized traits. Sunbird visitation to B. ringens was not associated with local sunbird activity in communities, but sunbird visitation was negatively associated with the amount of B. ringens sugar relative to the availability of alternative nectar sources. Our study provides evidence that B. ringens populations with larger floral traits are visited more frequently by sunbirds, and we propose that visitation rates to B. ringens may be influenced, in part, by competition with other sunbird-pollinated species.
Project description:Bird pollination systems are dominated by specialist nectarivores, such as hummingbirds in the Americas and sunbirds in Africa. Opportunistic (generalist) avian nectarivores such as orioles, weavers and bulbuls have also been implicated as plant pollinators, but their effectiveness as agents of pollen transfer is poorly known. Here, we compare the single-visit effectiveness of specialist and opportunistic avian nectarivores as pollinators of Aloe ferox, a plant that relies almost exclusively on birds for seed production. We found that the number of pollen grains on stigmas of flowers receiving single visits by opportunistic avian nectarivores was approximately threefold greater than on those receiving single visits by specialist sunbirds and about twofold greater than on those that received single visits by honeybees. The number of pollen grains on stigmas of flowers visited by sunbirds was similar to that on stigmas of unvisited flowers. These results show that opportunistic birds are highly effective pollinators of A. ferox, supporting the idea that some plants are specialized for pollination by opportunistic birds.
Project description:Aeschynanthus (Gesneriaceae), a genus comprising approximately 160 species in subtropical Southeast Asia, has red, tubular flowers, typical of a sunbird pollination syndrome. A. acuminatus, the species that is distributed extending to the northern edge of the genus, where the specialized nectarivorous sunbirds are absent, possesses reddish-green flowers and a wide-open corolla tube, flowering time shifts from summer to winter and the species achieves high fruiting success. This atypical flower led us to investigate the pollination biology of this species. Three species of generalist passerines, Grey-cheeked Fulvetta (Alcippe morrisonia, Sylviidae), White-eared Sibia (Heterophasia auricularis, Leiothrichidae) and Taiwan Yuhina (Yuhina brunneiceps, Zosteropidae), were recorded visiting A. acuminatus flowers. Pollination effectiveness was quantified via conspecific pollen presence on stigmas and natural fruit set. The significantly high natural fruit set (60%) and conspecific pollen transfer rate (94%) indicate high reproductive success facilitated by the accurate pollen placement on the birds. The existence of copious (61?µL) and highly diluted (7%) hexose-dominant nectar, together with a major reflectance peak of corolla lobe in the long-wavelength red color spectrum, is consistent with the pollination syndrome of generalist passerines. The high pollination effectiveness of A. acuminatus due to the recruitment of generalist passerines as pollinators, and the specializations of floral traits to match generalist bird pollination, appear crucial in the successful colonization on islands such as Taiwan that lack specialized bird pollinators.
Project description:<h4>Background and aims</h4>According to the Grant-Stebbins model of pollinator-driven divergence, plants that disperse beyond the range of their specialized pollinator may adapt to a new pollination system. Although this model provides a compelling explanation for pollination ecotype formation, few studies have directly tested its validity in nature. Here we investigate the distribution and pollination biology of several subspecies of the shrub Erica plukenetii from the Cape Floristic Region in South Africa. We analyse these data in a phylogenetic context and combine these results with information on pollinator ranges to test whether the evolution of pollination ecotypes is consistent with the Grant-Stebbins model.<h4>Methods and key results</h4>Pollinator observations showed that the most common form of E. plukenetii with intermediate corolla length is pollinated by short-billed Orange-breasted sunbirds. Populations at the northern fringe of the distribution are characterized by long corollas, and are mainly pollinated by long-billed Malachite sunbirds. A population with short corollas in the centre of the range was mainly pollinated by insects, particularly short-tongued noctuid moths. Bird exclusion in this population did not have an effect on fruit set, while insect exclusion reduced fruit set. An analysis of floral scent across the range, using coupled gas chromatography-mass spectrometry, showed that the scent bouquets of flowers from moth-pollinated populations are characterized by a larger number of scent compounds and higher emission rates than those in bird-pollinated populations. This was also reflected in clear separation of moth- and bird-pollinated populations in a two-dimensional phenotype space based on non-metric multidimensional scaling analysis of scent data. Phylogenetic analyses of chloroplast and nuclear DNA sequences strongly supported monophyly of E. plukenetii, but not of all the subspecies. Reconstruction of ancestral character states suggests two shifts from traits associated with short-billed Orange-breasted sunbird pollination: one towards traits associated with moth pollination, and one towards traits associated with pollination by long-billed Malachite sunbirds. The latter shift coincided with the colonization of Namaqualand in which Orange-breasted sunbirds are absent.<h4>Conclusions</h4>Erica plukenetii is characterized by three pollination ecotypes, but only the evolutionary transition from short- to long-billed sunbird pollination can be clearly explained by the Grant-Stebbins model. Corolla length is a key character for both ecotype transitions, while floral scent emission was important for the transition from bird to moth pollination.
Project description:BACKGROUND AND AIMS: Floral variation, pollination biology and mating patterns were investigated in sunbird-pollinated Babiana (Iridaceae) species endemic to the Western Cape of South Africa. The group includes several taxa with specialized bird perches and it has been proposed that these function to promote cross-pollination. METHODS: Pollinator observations were conducted in 12 populations of five taxa (B. ringens subspp. ringens, australis, B. hirsuta, B. avicularis, B. carminea) and geographic variation in morphological traits investigated in the widespread B. ringens. Experimental pollinations were used to determine the compatibility status, facility for autonomous self-pollination and intensity of pollen limitation in six populations of four taxa. Allozyme markers were employed to investigate mating patterns in four populations of three species. KEY RESULTS: Sunbirds were the primary pollinators of the five Babiana taxa investigated. Correlated geographical variation in perch size, flower size and stigma-anther separation was evident among B. ringens populations. Experimental pollinations demonstrated that B. ringens and B. avicularis were self-compatible with variation in levels of autonomous self-pollination and weak or no pollen limitation of seed set. In contrast, B. hirsuta was self-incompatible and chronically pollen limited. Estimates of outcrossing rate indicated mixed mating with substantial self-fertilization in all species investigated. CONCLUSIONS: Despite the possession of specialized bird perches in B. ringens and B. avicularis, these structures do not prevent considerable selfing from occurring, probably as a result of autonomous self-pollination. In eastern populations of B. ringens, smaller flowers and reduced herkogamy appear to be associated with a shift to predominant selfing. Relaxed selection on perch function due to increased selfing may explain the increased incidence of apical flowers in some populations.
Project description:Understanding the mechanisms enabling coevolution in complex mutualistic networks remains a central challenge in evolutionary biology. We show for the first time, to our knowledge, that a tropical plant species has the capacity to discriminate among floral visitors, investing in reproduction differentially across the pollinator community. After we standardized pollen quality in 223 aviary experiments, successful pollination of Heliconia tortuosa (measured as pollen tube abundance) occurred frequently when plants were visited by long-distance traplining hummingbird species with specialized bills (mean pollen tubes = 1.21 ± 0.12 SE) but was reduced 5.7 times when visited by straight-billed territorial birds (mean pollen tubes = 0.20 ± 0.074 SE) or insects. Our subsequent experiments revealed that plants use the nectar extraction capacity of tropical hummingbirds, a positive function of bill length, as a cue to turn on reproductively. Furthermore, we show that hummingbirds with long bills and high nectar extraction efficiency engaged in daily movements at broad spatial scales (?1 km), but that territorial species moved only short distances (<100 m). Such pollinator recognition may therefore affect mate selection and maximize receipt of high-quality pollen from multiple parents. Although a diffuse pollinator network is implied, because all six species of hummingbirds carry pollen of H. tortuosa, only two species with specialized bills contribute meaningfully to its reproduction. We hypothesize that this pollinator filtering behavior constitutes a crucial mechanism facilitating coevolution in multispecies plant-pollinator networks. However, pollinator recognition also greatly reduces the number of realized pollinators, thereby rendering mutualistic networks more vulnerable to environmental change.
Project description:Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: ? SC ) and between sites (among forest fragments: ? CT ). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (? SC = 0.0506), and weaker, statistically significant differentiation among sites (? CT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.
Project description:BACKGROUND: Animals fertilize thousands of angiosperm species whose floral-display sizes can significantly influence pollinator behavior and plant reproductive success. Many studies have measured the interactions among pollinator behavior, floral-display size, and plant reproductive success, but few studies have been able to separate the effects of pollinator behavior and post-pollination processes on angiosperm sexual reproduction. In this study, we utilized the highly self-incompatible pollinium-pollination system of Asclepias syriaca (Common Milkweed) to quantify how insect visitors influenced male reproductive success measured as pollen removal, female reproductive success measured as pollen deposition, and self-pollination rate. We also determined how floral-display size impacts both visitor behavior and self-pollination rate. RESULTS: Four insect taxonomic orders visited A. syriaca: Coleoptera, Diptera, Hymenoptera, and Lepidoptera. We focused on three groups of visitor taxa within two orders (Hymenoptera and Lepidoptera) with sample sizes large enough for quantitative analysis: Apis mellifera (Western Honey Bee), Bombus spp. (bumble bees) and lepidopterans (butterflies and moths). Qualitatively, lepidopterans had the highest pollinator importance values, but the large variability in the lepidopteran data precluded meaningful interpretation of much of their behavior. The introduced A. mellifera was the most effective and most important diurnal pollinator with regard to both pollen removal and pollen deposition. However, when considering the self-incompatibility of A. syriaca, A. mellifera was not the most important pollinator because of its high self-pollination rate as compared to Bombus spp. Additionally, the rate of self-pollination increased more rapidly with the number of flowers per inflorescence in A. mellifera than in the native Bombus spp. CONCLUSIONS: Apis mellifera's high rate of self-pollination may have significant negative effects on both male and female reproductive successes in A. syriaca, causing different selection on floral-display size than native pollinators.
Project description:Animal pollination mediates both reproduction and gene flow for the majority of plant species across the globe. However, past functional studies have focused largely on seed production; although useful, this focus on seed set does not provide information regarding species-specific contributions to pollen-mediated gene flow. Here we quantify pollen dispersal for individual pollinator species across more than 690 ha of tropical forest. Specifically, we examine visitation, seed production, and pollen-dispersal ability for the entire pollinator community of a common tropical tree using a series of individual-based pollinator-exclusion experiments followed by molecular-based fractional paternity analyses. We investigate the effects of pollinator body size, plant size (as a proxy of floral display), local plant density, and local plant kinship on seed production and pollen-dispersal distance. Our results show that while large-bodied pollinators set more seeds per visit, small-bodied bees visited flowers more frequently and were responsible for more than 49% of all long-distance (beyond 1 km) pollen-dispersal events. Thus, despite their size, small-bodied bees play a critical role in facilitating long-distance pollen-mediated gene flow. We also found that both plant size and local plant kinship negatively impact pollen dispersal and seed production. By incorporating genetic and trait-based data into the quantification of pollination services, we highlight the diversity in ecological function mediated by pollinators, the influential role that plant and population attributes play in driving service provision, and the unexpected importance of small-bodied pollinators in the recruitment of plant genetic diversity.
Project description:The reproductive biology encompassing phenology, floral biology, pollination and breeding systems, of Butea monosperma, a beautiful tree of the Indian subcontinent, was investigated in a protected dry, deciduous forest located in New Delhi. Phenological studies indicated that although the species shows a regular flowering season, all trees do not flower every year. Flowers are typically papilionaceous; the stigma is wet papillate and the style is hollow. The flowers show characteristics of bird pollination being large and bright orange-red in colour with copious amounts of nectar, and exhibiting diurnal anthesis. Although the flowers are frequented by as many as seven species of birds belonging to six families, only one species, the purple sunbird (Nectarinia asiatica), is the effective pollinator. The flowers are also pollinated by the three-striped squirrel (Funambulus tristiatus). Unlike other flower visitors, these two pollinators forage the nectar from the open side of the keel (legitimate path) during which pollen grains are deposited on their body parts. After the first visit of a sunbird or a squirrel, virgin flowers showed pollen load on the stigma and developed into fruits. B. monosperma shows a weak form of self-incompatibility. Fruit set following manual self-pollination (5.25 %) was comparable with open-pollination (approx. 5 %) but was significantly lower than manual cross-pollination (22.51 %). This indicates that there is a high degree of geitonogamous pollination in this species, which may lead to a weakening of self-incompatibility as a means of reproductive assurance. The results are analysed in the light of prevailing discussions on specialized vs. generalized pollination systems.