Pollination decays in biodiversity hotspots (original) (raw)
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Plant Ecology & Diversity, 2013
Background: Plant species in biodiversity hotspots suffer more from pollen limitation than those in lower diversity regions, though this pattern is largely restricted to self-incompatible species. It is unknown whether higher pollen limitation is due to increased pollinator sharing or declines in pollinator abundance. Aims: Macroecological examinations of pollen limitation have been challenged by statistical confounds of phylogenetic non-independence and interrelationships between variables. Here, we perform phylogenetically corrected analyses of pollen limitation, examining an ensemble dataset of endemicity, abundance, species diversity, breeding system, floral symmetry, and pollinator richness. Methods: We apply model selection and path analysis to a large dataset of published studies of pollen limitation on 275 plant species distributed worldwide. Results: Plant diversity and breeding system were included in the best model. Even the best model explained only 13% of the among-species variation in pollen limitation, indicating a stochastic component in pollen receipt. Pollinator richness remained a consistent determinant of pollen limitation, influenced by floral symmetry and, to a lesser extent, plant diversity. Conclusions: Our results suggest that many traits examined thus far explain relatively little of the variation in pollen limitation, partly because their effects are subsumed by the roles played by breeding system and plant diversity. 10 15 20
Oikos, 2008
Pollen limitation on a plant community level has received little attention, although it might show which pollinationrelated traits may cause pollen limitation to vary among species. To address several central questions in plant reproductive biology, we investigated pollen limitation in 11 plant species, including visitation and specialisation levels of all species. The female reproductive success of most species within the studied plant community was not pollen limited, but a general tradeoff between seed production and seed weight occurred as a response to supplemental pollination. In contrast to general notion, we did not find that less visited species were most pollen limited. Instead, it appears that species with high visitation rates were most pollen limited. Our study provided conflicting evidence to whether specialisation levels may affect the degree of pollen limitation within the study community. We discuss these findings in the context of recent reviews on the occurrence, causes and consequences of pollen limitation in plants. In particular, we propose that, although pollen limitation is an important phenomenon, 1) the majority of species within a plant community may not experience pollen limitation at a given moment, 2) that common notions of which plant species should experience pollen limited reproductive success do not hold true in the studied plant community, and 3) that offspring quality is as likely affected by surplus pollen loads as is the number of offspring.
Is reproduction of endemic plant species particularly pollen limited in biodiversity hotspots
Oikos, 2010
Current evidence suggests that plants in biodiversity hotspots suffer more from pollen limitation of reproduction than those in lower diversity regions, primarily due to the response of self-incompatible species. Species in biodiversity hotspots may thus be more at risk of limited reproduction and subsequent population decline. Should these species have restricted ranges (i.e. be endemics to a certain region), pollen limitation within highly diverse regions may pose an important threat to global plant biodiversity. We further dissect the global pattern by exploring whether pollen limitation of range-restricted (endemic) species is distinctive and/or relates differently to species diversity than that of widespread (non-endemic) species. To provide a preliminary test of this prediction we conducted both cross-species and comparative phylogenetic meta-analyses to determine the effect of endemism on the magnitude of pollen limitation and its relationship with regional species richness. Our data set included 287 plant species belonging to 78 families distributed world-wide. Our results revealed that endemism and self-compatibility contribute to the global association between pollen limitation and species richness. Self-incompatible species were more pollen limited than self-compatible ones, and the PICs analysis indicated that transitions to endemism were associated with transitions to self-compatibility. The relationship between pollen limitation and species richness was significant only for the self-incompatible species, and was monotonically increasing in non-endemic species but accelerating in the endemic species. Thus, self-incompatible endemic species from biodiversity hotspots are at the greatest risk of pollination failure, a previously unknown aspect suggesting this group of species as a top priority for future development of conservation strategies. In contrast, reproduction of self-compatible species appears to be unrelated to plant diversity, although we caution that current data do not account for the reproductive limitation due to the quality of pollen received. Understanding the mechanisms underlying these patterns requires further investigation into plant–plant pollinator mediated interactions and the dynamics of pollen transfer in communities differing in species diversity.
Journal of Ecology, 2010
1. Pollen limitation may be a consequence of changes in pollinator abundance, diversity and identity. However, no empirical evidence exists concerning the consequences that the spatial variation in pollinator fauna has on pollen limitation intensity and plant reproduction. In this study, we test the effect that changes in flower-visitor abundance, diversity and identity exert on the occurrence and strength of pollen limitation by experimentally quantifying pollen limitation in eight populations of Erysimum mediohispanicum, a pollination-generalist plant native to the Iberian Peninsula. 2. Pollen limitation was accounted for by using a comprehensive estimator, the net reproductive rate (R 0 ). Nevertheless, we also determined which components of plant reproduction, from ovule fertilization to seedling survival, were more intensely pollen-limited. Finally, we explored whether the spatial variation in pollen limitation intensity was related to among-population changes in flower-visitor abundance, diversity and identity. 3. The whole reproductive cycle of E. mediohispanicum was pollen-limited, although pollen limitation occurred more strongly during the ovule fertilization and seed-production phases than during fruit ripening or seedling emergence and establishment. 4. There was a significant among-population difference in pollen limitation intensity. Pollen limitation strength was associated with variations in flower-visitor diversity, and identity. Populations with lower flower-visitor diversity and with many low-efficiency pollinators (i.e. beetles) showed stronger pollen limitation. 5. Synthesis. Our study shows that the intensity of pollen limitation at the population level may depend on several characteristics of the assemblage of flower-visiting insects, such as their abundance, diversity and identity. Our results suggest that any impoverishment of pollinator diversity or any alteration in the specific composition of the pollinator assemblage may exacerbate pollen limitation.
Changes in pollinator fauna cause spatial variation in pollen limitation
Journal of Ecology, 2010
1. Pollen limitation may be a consequence of changes in pollinator abundance, diversity and identity. However, no empirical evidence exists concerning the consequences that the spatial variation in pollinator fauna has on pollen limitation intensity and plant reproduction. In this study, we test the effect that changes in flower-visitor abundance, diversity and identity exert on the occurrence and strength of pollen limitation by experimentally quantifying pollen limitation in eight populations of Erysimum mediohispanicum, a pollination-generalist plant native to the Iberian Peninsula. 2. Pollen limitation was accounted for by using a comprehensive estimator, the net reproductive rate (R 0 ). Nevertheless, we also determined which components of plant reproduction, from ovule fertilization to seedling survival, were more intensely pollen-limited. Finally, we explored whether the spatial variation in pollen limitation intensity was related to among-population changes in flower-visitor abundance, diversity and identity. 3. The whole reproductive cycle of E. mediohispanicum was pollen-limited, although pollen limitation occurred more strongly during the ovule fertilization and seed-production phases than during fruit ripening or seedling emergence and establishment. 4. There was a significant among-population difference in pollen limitation intensity. Pollen limitation strength was associated with variations in flower-visitor diversity, and identity. Populations with lower flower-visitor diversity and with many low-efficiency pollinators (i.e. beetles) showed stronger pollen limitation. 5. Synthesis. Our study shows that the intensity of pollen limitation at the population level may depend on several characteristics of the assemblage of flower-visiting insects, such as their abundance, diversity and identity. Our results suggest that any impoverishment of pollinator diversity or any alteration in the specific composition of the pollinator assemblage may exacerbate pollen limitation.
Botany, 2012
Recent work on the ecosystem service of biodiversity suggests that higher pollinator diversity could lower pollen limitation, but these two aspects of plant–pollinator communities have only rarely been causally connected. Here we present a review of studies that produced quantitative assessments of both pollinator diversity and evenness as well as pollen limitation of focal plant species. Although pollen limitation is expected to be lower when pollinator diversity is high, our analysis suggests this relationship is weak. The relationship may be obscured when features of the plant species (e.g., average level of specialization) are confounded with features of the plant communities (e.g., habitat). We encourage researchers investigating pollen limitation to consider including measures of diversity of the floral visitors, and their effectiveness. These data would permit a more powerful test of the relationships among these variables and improve our understanding of the critical elements of stable plant–pollinator networks.
Ecology, 2012
Mutualisms are well known to influence individual fitness and the population dynamics of partner species, but little is known about whether they influence species distributions and the location of geographic range limits. Here, we examine the contribution of plant-pollinator interactions to the geographic range limit of the California endemic plant Clarkia xantiana ssp. xantiana. We show that pollinator availability declined from the center to the margin of the geographic range consistently across four years of study. This decline in pollinator availability was caused to a greater extent by variation in the abundance of generalist rather than specialist bee pollinators. Climate data suggest that patterns of precipitation in the current and previous year drove variation in bee abundance because of its effects on cues for bee emergence in the current year and the abundance of floral resources in the previous year. Experimental floral manipulations showed that marginal populations had greater outcross pollen limitation of reproduction, in parallel with the decline in pollinator abundance. Although plants are self-compatible, we found no evidence that autonomous selfing contributes to reproduction, and thus no evidence that it alleviates outcross pollen limitation in marginal populations. Furthermore, we found no association between the distance to the range edge and selfing rate, as estimated from sequence and microsatellite variation, indicating that the mating system has not evolved in response to the pollination environment at the range periphery. Overall, our results suggest that dependence on pollinators for reproduction may be an important constraint limiting range expansion in this system.
Botany, 2012
Recent work on the ecosystem service of biodiversity suggests that higher pollinator diversity could lower pollen limitation, but these two aspects of plant-pollinator communities have only rarely been causally connected. Here we present a review of studies that produced quantitative assessments of both pollinator diversity and evenness as well as pollen limitation of focal plant species. Although pollen limitation is expected to be lower when pollinator diversity is high, our analysis suggests this relationship is weak. The relationship may be obscured when features of the plant species (e.g., average level of specialization) are confounded with features of the plant communities (e.g., habitat). We encourage researchers investigating pollen limitation to consider including measures of diversity of the floral visitors, and their effectiveness. These data would permit a more powerful test of the relationships among these variables and improve our understanding of the critical elements of stable plant-pollinator networks.
Pollination success increases with plant diversity in high-Andean communities
Scientific Reports, 2021
Pollinator-mediated plant-plant interactions have traditionally been viewed within the competition paradigm. However, facilitation via pollinator sharing might be the rule rather than the exception in harsh environments. Moreover, plant diversity could be playing a key role in fostering pollinatormediated facilitation. Yet, the facilitative effect of plant diversity on pollination remains poorly understood, especially under natural conditions. By examining a total of 9371 stigmas of 88 species from nine high-Andean communities in NW Patagonia, we explored the prevalent sign of the relation between conspecific pollen receipt and heterospecific pollen diversity, and assessed whether the incidence of different outcomes varies with altitude and whether pollen receipt relates to plant diversity. Conspecific pollen receipt increased with heterospecific pollen diversity on stigmas. In all communities, species showed either positive or neutral but never negative relations between the number of heterospecific pollen donor species and conspecific pollen receipt. The incidence of species showing positive relations increased with altitude. Finally, stigmas collected from communities with more co-flowering species had richer heterospecific pollen loads and higher abundance of conspecific pollen grains. Our findings suggest that plant diversity enhances pollination success in high-Andean plant communities. This study emphasizes the importance of plant diversity in fostering indirect plant-plant facilitative interactions in alpine environments, which could promote species coexistence and biodiversity maintenance. Understanding the mechanisms that drive species coexistence is challenging, especially given the underlying belief that interspecific competition is the overriding ecological force determining diversity 1. A growing number of studies, however, have shown that plant-plant interactions can range from competitive to facilitative 2-5 and animal-mediated interactions are not an exception 6-8. Given that most flowering plant species are animal-pollinated 9 and generalization in plant-pollinator interactions is widespread 10,11 , pollinator sharing is common among co-flowering plants. Shared pollinators move pollen not only between conspecific but also among heterospecific flowers, and as a result interspecific pollen transfer is ubiquitous in communities worldwide 12. Interspecific pollen transfer has certainly been seen as one of the mechanisms underlying competition among plants for pollinators 13,14 , notwithstanding it can also reflect facilitation 7,15-18. Ultimately, the study of interspecific pollen transfer can be useful to better understand the role of pollinator-mediated plant-plant interactions as drivers of plant species coexistence and diversity. Pollen transfer among flowers from different species is particularly common in natural communities 12 and several recent studies show that heterospecific pollen loads on stigmas, albeit highly variable, can be large and diverse 7,19-21. Commonly, more than 50% of the flowers of outcrossing plant species receive some heterospecific pollen, and in amounts that constitute from ~ 1 to 70-80% of the total pollen load deposited on the stigmas 19-22. Moreover, heterospecific pollen grains can come from a single or multiple donor species 7,20,23. This substantial variation within and among species in both the magnitude and diversity of heterospecific pollen loads may be due to several factors such as differences in plant specialization, flower symmetry and size, flower lifespan, floral display, and associated pollinator group 12,22,24. However, beyond all these intrinsic factors, the size and diversity of pollen loads on flowers' stigmas might reflect local plant community diversity, and be a consequence of the processes triggered by several species flowering together. The outcome of pollinator sharing on plant pollination success can range from negative to positive 8. Specifically, heterospecific pollen deposited by shared pollinators can have negative effects when it interferes either mechanically or physiologically with conspecific pollen receipt and performance (i.e., pollen germination and
Annals of Botany, 2013
Aims Insufficient pollination is a function of quantity and quality of pollen receipt, and the relative contribution of each to pollen limitation may vary with intrinsic plant traits and extrinsic ecological properties. Community-level studies are essential to evaluate variation across species in quality limitation under common ecological conditions. This study examined whether endemic species are more limited by pollen quantity or quality than non-endemic co-flowering species in three endemic-rich plant communities located in biodiversity hotspots of different continents (Andalusia, California and Yucatan). † Methods Natural variations in pollen receipt and pollen tube formation were analysed for 20 insect-pollinated plants. Endemic and non-endemic species that co-flowered were paired in order to estimate and compare the quantity and quality components of pre-zygotic pollination success, obtained through piecewise regression analysis of the relationship between pollen grains and pollen tubes of naturally pollinated wilted flowers. † Key Results Pollen tubes did not frequently exceed the number of ovules per flower. Only the combination of abundant and good quality pollen and a low number of ovules per flower conferred relief from pre-zygotic pollen limitation in the three stochastic pollination environments studied. Quality of pollen receipt was found to be as variable as quantity among study species. The relative pollination success of endemic and non-endemic species, and its quantity and quality components, was community dependent. † Conclusions Assessing both quality and quantity of pollen receipt is key to determining the ovule fertilization potential of both endemic and widespread plants in biodiverse hotspot regions. Large natural variation among flowers of the same species in the two components and pollen tube formation deserves further analysis in order to estimate the environmental, phenotypic and intraindividual sources of variation that may affect how plants evolve to overcome this limitation in different communities worldwide.