Abstract
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: Φ SC) and between sites (among forest fragments: Φ CT). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ SC = 0.0506), and weaker, statistically significant differentiation among sites (Φ 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.
Highlights
Most species of flowering plants depend on animals for successful pollination (Ollerton et al, 2011)
Estimates of pollen pool differentiation among mothers within sites were about two times higher than estimates of pollen pool differentiation among sites, even after accounting for potential spurious pollen pool differentiation due to a combination of selfing (Table 1A) and non-independent pollination events (Table 1B). This pattern of hierarchical pollen pool differentiation is consistent with the foraging strategy of traplining hummingbirds (Figures 2C, E), but not with the movement patterns of territorial hummingbirds (Figures 2B, D)
We argue that pollen pool differentiation among neighboring mothers is a landscape genetic signature of the traplining foraging strategy, as it cannot be explained by the spatial scale of pollen flow alone but requires neighboring mothers to consistently receive pollen from a distinct set of fathers, such as the repeated sequence of plants or inflorescences a traplining hummingbird is expected to visit along its established foraging route (Figure 2A)
Summary
Most species of flowering plants depend on animals for successful pollination (Ollerton et al, 2011). Due to the vast biodiversity of flowering plants and animal pollinators found in these environments, tropical pollination networks have often been thought to be highly generalized (Jordano, 1987; Olesen and Jordano, 2002); that is, a single plant species can rely on multiple functional groups of floral visitors for effective pollen transfer (Waser et al, 1996; Bascompte et al, 2006). Accumulating evidence suggests that different functional groups of floral visitors vary widely in their effectiveness as pollinators (Waser et al, 1996; Fenster et al, 2004), leading to a reduction in the number of realized pollinators and an increase in the degree of plant-pollinator specialization (Pellmyr and Thompson, 1996; Schleuning et al, 2016) This “cryptic specialization” may increase the susceptibility of pollination to the decline of particular species of pollinators. In the face of ongoing pollination declines (Potts et al, 2010; Hadley and Betts, 2012; González-Varo et al, 2013), it is imperative to understand how different functional groups of pollinators contribute to pollination success
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