Pollination decays in biodiversity hotspots

Abstract

As pollinators decline globally, competition for their services is expected to intensify, and this antagonism may be most severe where the number of plant species is the greatest. Using metaanalysis and comparative phylogenetic analysis, we provide a global-scale test of whether reproduction becomes more limited by pollen receipt (pollen limitation) as the number of coexisting plant species increases. As predicted, we find a significant positive relationship between pollen limitation and species richness. In addition, this pattern is particularly strong for species that are obligately outcrossing and for trees relative to herbs or shrubs. We suggest that plants occurring in species-rich communities may be more prone to pollen limitation because of interspecific competition for pollinators. As a consequence, plants in biodiversity hotspots may have a higher risk of extinction and͞or experience increased selection pressure to specialize on certain pollinators or diversify into different phenological niches. The combination of higher pollen limitation and habitat destruction represents a dual risk to tropical plant species that has not been previously identified.extinction ͉ latitudinal gradients ͉ speciation ͉ competition ͉ pollen delivery W ild plant species in biodiversity hotspots are an important world resource for the products and ecosystem services they provide, including medicine, food, nutrient cycling, and alternative resources for pollinators of domesticated crops (1). Maintaining plant biodiversity in hotspots is a critical challenge for conservation biologists because individual species may have reduced mean fitness in species-rich communities because of increased interspecific competition (2-4). In flowering plants, the presence of coflowering species can reduce pollination success at a local scale because of reduced visitation of generalist pollinators to the focal species, decreased delivery of conspecific pollen, or stigma interference by heterospecific pollen (5-8). However, whether the number of competing species within broad geographic regions influences global patterns in pollination biology has not yet been examined.Adaptations for effective pollination are widely accepted to have contributed to the tremendous radiation of angiosperms (9, 10). Pollen limitation may decrease as plants evolve traits that reduce reliance on pollinators (e.g., self-compatible breeding systems and vegetative reproduction), attract more specialized pollinators that deliver less heterospecific pollen, or reduce competition for pollinators (e.g., shifts in flowering time) (11). Studies have found that diversity in flowering phenologies and pollinator fauna is indeed higher in species-rich areas (12, 13). If plants in species-rich regions are more often pollen limited than those in species-depauperate areas, they may experience relatively strong natural selection favoring traits that reduce pollen limitation, making current biodiversity hotspots an even more valuable global resource as centers for future adaptation and...

Floral adaptation and diversification under pollen limitation

“…In this context, Vamosi et al (2006) found that global 'hotspots' of angiosperm diversity also tend to be areas of common PL. They interpreted this association as an ecological consequence of heightened competition for pollinators (see also Armbruster & Muchhala 2009).…”

“…Even when supplementation indicates PL during a single flowering season, iteroparous species may not suffer lifetime limitation, which is most relevant for population dynamics and natural selection, because elevated reproductive effort stimulated by supplementation during one flowering season typically reduces a plant's seed production during subsequent seasons . Finally, the populations and species for which published results of pollen supplementation experiments are available may not be representative because of unequal geographic and taxonomic sampling (Vamosi et al 2006) and a publication bias favouring statistically significant responses . Given the preceding problems, the finding that roughly 60 per cent of pollen supplementation experiments significantly elevate seed production (Larson & Barrett 2000;Knight et al 2005a) must overestimate the general incidence of PL; however, it still suggests that incomplete ovule fertilization compromises seed production by many plants.…”

Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana

“…Recent genetic studies on other birdpollinated plants in the SWAFR have demonstrated an impact on the mating system, with increased selfing and increased correlated paternity associated with reduced population size following habitat fragmentation . Introduced, non-native pollinators such as European honeybees (A. mellifera), and increased competition for declining vertebrate pollinators, strongest in biodiversity hotspots (Vamosi et al, 2006), affect pollen limitation and seed set in many species with already low conversions of flowers to fruits (Ayre and Whelan, 1989;England et al, 2001), increasing extinction risk. Our results highlight the additional conservation genetic concerns from bird-pollinator disruption that may result in a significant increase in near-neighbour pollen dispersal, correlated paternity and inbreeding through bi-parental mating.…”

An overview of the applicability of functional diversity in Biological Conservation

“…Functional diversity responds differently to changes in land use and management than other measures, particularly the traditional ones showing that conserving other diversity components (such as species number or abundance) will not necessarily conserve functional diversity (Bennett et al, 2014;Katovai et al, 2012;Van Capelle et al, 2012). In some cases measures of functional diversity or trait-based approach responded more precisely than other measures (Dengler et al, 2014;Pelosi et al, 2014), suggesting that this approach can potentially better predict the impacts, although other corroborative studies are needed.…”

“…As most part of Europe lies in the northern temperate climate zone, current conclusions and recommendations regarding functional diversity and conservation tend to be less suitable to ecosystems from outside that climate. Because tropical species communities are prone to be more complex (Janzen, 1975;Vamosi et al, 2006), relationships between ecosystem functioning and functional diversity in the tropics may not be as straightforward, as is usually assumed (Freitas et al, 2012;Martins and Batalha, 2006). Testing hypothesis in tropical ecosystems would contribute to expanding the current understanding of functional diversity in conservation strategies' applicability.…”