Species interactions in an Andean bird-flowering plant network: phenology is more important than abundance or morphology.
ABSTRACT: Biological constraints and neutral processes have been proposed to explain the properties of plant-pollinator networks. Using interactions between nectarivorous birds (hummingbirds and flowerpiercers) and flowering plants in high elevation forests (i.e., "elfin" forests) of the Andes, we explore the importance of biological constraints and neutral processes (random interactions) to explain the observed species interactions and network metrics, such as connectance, specialization, nestedness and asymmetry. In cold environments of elfin forests, which are located at the top of the tropical montane forest zone, many plants are adapted for pollination by birds, making this an ideal system to study plant-pollinator networks. To build the network of interactions between birds and plants, we used direct field observations. We measured abundance of birds using mist-nets and flower abundance using transects, and phenology by scoring presence of birds and flowers over time. We compared the length of birds' bills to flower length to identify "forbidden interactions"-those interactions that could not result in legitimate floral visits based on mis-match in morphology. Diglossa flowerpiercers, which are characterized as "illegitimate" flower visitors, were relatively abundant. We found that the elfin forest network was nested with phenology being the factor that best explained interaction frequencies and nestedness, providing support for biological constraints hypothesis. We did not find morphological constraints to be important in explaining observed interaction frequencies and network metrics. Other network metrics (connectance, evenness and asymmetry), however, were better predicted by abundance (neutral process) models. Flowerpiercers, which cut holes and access flowers at their base and, consequently, facilitate nectar access for other hummingbirds, explain why morphological mis-matches were relatively unimportant in this system. Future work should focus on how changes in abundance and phenology, likely results of climate change and habitat fragmentation, and the role of nectar robbers impact ecological and evolutionary dynamics of plant-pollinator (or flower-visitor) interactions.
Project description:Geographical variations in environmental factors can affect species diversity and consequently influence the structure of interspecific ecological interactions. Relationships between flowering plants and animal flower visitors are among the most important ecological interactions and can structure and maintain ecological diversity in different environments. Additionally, many animal and plant species participate in these interactions, which shape the specific characteristics of these communities, in terms of both the responses of the interacting species involved and environmental differences. Therefore, in the present study we investigated geographical and environmental effects on the architecture of Neotropical flower-visitor networks of vertebrates and invertebrates. To this end, we used data regarding interaction networks available in the literature and constructed binary interaction networks of plants and plant-visitors (hummingbirds and insects) and tested the effects of altitude, latitude, vegetation type and number of plant families on the structure of these networks. In total, we analyzed 55 networks of flower-visitor interactions with 746 species of flower-visiting animals and 1,185 species of plants, totaling 5,463 distinct plant-animal interactions. In general, the architecture of flower-visitor networks varied along latitudinal and altitudinal gradients, with more pronounced effects for flower-insect networks in which latitude influenced network size, modularity, and nestedness, and altitude influenced network size and connectance. Flower-hummingbird networks in open vegetation (grassland) were more modular than networks in other environments. The number of plant families positively influenced the size of insect and hummingbird networks, and positively affected connectance and nestedness and negatively affected modularity in the flower-insect networks. So, the patterns we found indicate that plant-visitor interactions in flower-insect and flower-hummingbird networks are differently affected by geographical and plant-related factors, possibly due to the differences in taxonomic and functional groups involved in these interactions.
Project description:Pollinators mediate the evolution of secondary floral traits through both natural and sexual selection. Gender-biased nectar, for example, could be maintained by one or both, depending on the interactions between plants and pollinators. Here, I investigate pollinator responses to gender-biased nectar using the dichogamous herb Chrysothemis friedrichsthaliana (Gesneriaceae) which produces more nectar during the male floral phase. Previous research showed that the hummingbird pollinator Phaethornis striigularis visited male-phase flowers more often than female-phase flowers, and multiple visits benefited male more than female fecundity. If sexual selection maintains male-biased rewards, hummingbirds should prefer more-rewarding flowers independent of floral gender. If, however, differential rewards are partially maintained through natural selection, hummingbirds should respond to asymmetry with visits that reduce geitonogamy, i.e. selfing and pollen discounting. In plants with male biases, these visit types include single-flower visits and movements from low to high rewards. To test these predictions, I manipulated nectar asymmetry between pairs of real or artificial flowers on plants and recorded foraging behaviour. I also assessed maternal costs of selfing using hand pollinations. For plants with real flowers, hummingbirds preferred more-rewarding flowers and male-phase morphology, the latter possibly owing to previous experience. At artificial arrays, hummingbirds responded to extreme reward asymmetry with increased single-flower visits; however, they moved from high to low rewards more often than low to high. Finally, selfed flowers did not produce inferior seeds. In summary, sexual selection, more so than geitonogamy avoidance, maintains nectar biases in C. friedrichsthaliana, in one of the clearest examples of sexual selection in plants, to date.
Project description:Understanding the factors determining the spatial and temporal variation of ecological networks is fundamental to the knowledge of their dynamics and functioning. In this study, we evaluate the effect of elevation and time on the structure of plant-flower-visitor networks in a Colombian mountain forest. We examine the level of generalization of plant and animal species and the identity of interactions in 44 bipartite matrices obtained from eight altitudinal levels, from 2200 to 2900 m during eight consecutive months. The contribution of altitude and time to the overall variation in the number of plant (P) and pollinator (A) species, network size (M), number of interactions (I), connectance (C), and nestedness was evaluated. In general, networks were small, showed high connectance values and non-nested patterns of organization. Variation in P, M, I and C was better accounted by time than elevation, seemingly related to temporal variation in precipitation. Most plant and insect species were specialists and the identity of links showed a high turnover over months and at every 100 m elevation. The partition of the whole system into smaller network units allowed us to detect small-scale patterns of interaction that contrasted with patterns commonly described in cumulative networks. The specialized but erratic pattern of network organization observed in this tropical mountain suggests that high connectance coupled with opportunistic attachment may confer robustness to plant-flower-visitor networks occurring at small spatial and temporal units.
Project description:Species flower production and flowering phenology vary from year to year due to extrinsic factors. Inter-annual variability in flowering patterns may have important consequences for attractiveness to pollinators, and ultimately, plant reproductive output. To understand the consequences of flowering pattern variability, a community approach is necessary because pollinator flower choice is highly dependent on flower context. Our objectives were: 1) To quantify yearly variability in flower density and phenology; 2) To evaluate whether changes in flowering patterns result in significant changes in pollen/nectar composition. We monitored weekly flowering patterns in a Mediterranean scrubland community (23 species) over 8 years. Floral resource availability was estimated based on field measures of pollen and nectar production per flower. We analysed inter-annual variation in flowering phenology (duration and date of peak bloom) and flower production, and inter-annual and monthly variability in flower, pollen and nectar species composition. We also investigated potential phylogenetic effects on inter-annual variability of flowering patterns. We found dramatic variation in yearly flower production both at the species and community levels. There was also substantial variation in flowering phenology. Importantly, yearly fluctuations were far from synchronous across species, and resulted in significant changes in floral resources availability and composition at the community level. Changes were especially pronounced late in the season, at a time when flowers are scarce and pollinator visitation rates are particularly high. We discuss the consequences of our findings for pollinator visitation and plant reproductive success in the current scenario of climate change.
Project description:G. L. Stebbins' most effective pollinator principle states that when pollinators are not limiting, plants are expected to specialize and adapt to the most abundant and effective pollinator species available. In this study, we quantify the effectiveness of bees, hummingbirds and hawkmoths in a Chilean population of Erythranthe lutea (Phrymaceae), and examine whether flower traits are subject to pollinator-mediated selection by the most effective pollinator species during two consecutive years. Unlike most species in the pollinator community, the visitation rate of the recently arrived Bombus terrestris did not change substantially between years, which together with its high and stable pollen delivery to flower stigmas made this species the most important in the pollinator assemblage, followed by the solitary bee Centris nigerrima Flower traits were under significant selection in the direction expected for short-tongue bees, suggesting that E. lutea is in the initial steps of adaptation to the highly effective exotic bumblebee. Our results illustrate the applicability of Stebbins' principle for new invasive pollinators, and stress their importance in driving flower adaptation of native plant species, a critical issue in the face of biotic exchange and homogenization.
Project description:When plant species compete for pollinators, climate warming may cause directional change in flowering overlap, thereby shifting the strength of pollinator-mediated plant-plant interactions. Such shifts are likely accentuated in the rapidly warming Arctic. Targeting a plant community in Northeast Greenland, we asked (a) whether the relative phenology of plants is shifting with spatial variation in temperature, (b) whether local plants compete for pollination, and (c) whether shifts in climatic conditions are likely to affect this competition. We first searched for climatic imprints on relative species phenology along an elevational gradient. We then tested for signs of competition with increasing flower densities: reduced pollinator visits, reduced representation of plant species in pollen loads, and reduced seed production. Finally, we evaluated how climate change may affect this competition. Compared to a dominant species, Dryas integrifolia × octopetala, the relative timing of other species shifted along the environmental gradient, with Silene acaulis and Papaver radicatum flowering earlier toward higher elevation. This shift resulted in larger niche overlap, allowing for an increased potential for competition for pollination. Meanwhile, Dryas emerged as a superior competitor by attracting 97.2% of flower visits. Higher Dryas density resulted in reduced insect visits and less pollen of S. acaulis being carried by pollinators, causing reduced seed set by S. acaulis. Our results show that current variation in climate shifts the timing and flowering overlap between dominant and less-competitive plant species. With climate warming, such shifts in phenology within trophic levels may ultimately affect interactions between them, changing the strength of competition among plants.
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:Plant-pollinator interactions have a fundamental influence on flower evolution. Flower color signals are frequently tuned to the visual capabilities of important pollinators such as either bees or birds, but far less is known about whether flower shape influences the choices of pollinators. We tested European honeybee Apis mellifera preferences using novel achromatic (gray-scale) images of 12 insect-pollinated and 12 bird-pollinated native Australian flowers in Germany; thus, avoiding influences of color, odor, or prior experience. Independent bees were tested with a number of parameterized images specifically designed to assess preferences for size, shape, brightness, or the number of flower-like shapes present in an image. We show that honeybees have a preference for visiting images of insect-pollinated flowers and such a preference is most-likely mediated by holistic information rather than by individual image parameters. Our results indicate angiosperms have evolved flower shapes which influence the choice behavior of important pollinators, and thus suggest spatial achromatic flower properties are an important part of visual signaling for plant-pollinator interactions.
Project description: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.
Project description:Petunia is endemic to South America grasslands; member of this genus exhibit variation in flower colour and shape, attracting bees, hawkmoths or hummingbirds. This group of plants is thus an excellent model system for evolutionary studies of diversification associated with pollinator shifts. Our aims were to identify the legitimate pollinator of Petunia secreta, a rare and endemic species, and to assess the importance of floral traits in pollinator attraction in this Petunia species. To determine the legitimate pollinator, field observations were conducted, and all floral visitors were recorded and evaluated. We also measured the nectar volume and sugar concentration. To characterize morphological cues for pollinators, we assessed the ultraviolet (UV)-light response in detached flowers, and characterized the floral pigments and pollen volatile scents for four different Petunia species that present different pollination syndromes. Petunia secreta shares the most recent ancestor with a white hawkmoth-pollinated species, P. axillaris, but presents flavonols and anthocyanin pigments responsible for the pink corolla colour and UV-light responses that are common to bee-pollinated Petunia species. Our study showed that a solitary bee in the genus Pseudagapostemon was the most frequent pollinator of P. secreta, and these bees collect only pollen as a reward. Despite being mainly bee-pollinated, different functional groups of pollinators visit P. secreta. Nectar volume, sugar concentration per flower, morphology and components of pollen scent would appear to be attractive to several different pollinator groups. Notably, the corolla includes a narrow tube with nectar at its base that cannot be reached by Pseudagapostemon, and flowers of P. secreta appear to follow an evolutionary transition, with traits attractive to several functional groups of pollinators. Additionally, the present study shows that differences in the volatiles of pollen scent are relevant for plant mutualistic and antagonist interactions in Petunia species and that pollen scent profile plays a key role in characterizing pollination syndromes.