Tropical deforestation reduces plant mating quality by shifting the functional composition of pollinator communities

Torres-Vanegas, Felipe; Hadley, Adam S.; Kormann, Urs G.; Jones, F. Andrew; Betts, Matthew G.; Wagner, Helene H.

doi:10.1111/1365-2745.13594

Cited by 10 publications

(14 citation statements)

References 110 publications

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“…Determining whether this is the case is important for two reasons. First, we agree with Betts et al [18] that filtering the short-billed, territorial hummingbirds could promote outcrossing and enhance the genetic diversity of pollen grains that reach the ovules, a hypothesis that is supported by landscape genetic studies of H. tortuosa populations in Costa Rica [9,10]. Given the potential for fitness benefits, pollinator recognition could be present in many related taxa and could be one means through which tight morphological matching evolves despite apparently generalized interaction networks.…”

Section: Introductionsupporting

confidence: 91%

“…This would be adaptive if plants suffer from inbreeding depression. Indeed, Torres-Vanegas et al [21,52] found genetic signatures in H. tortuosa populations that are consistent with this hypothesis; inbreeding was greatly reduced in large, connected forest patches where morphologically matched, traplining hummingbirds were more prevalent. In H. rostrata styles, visits from clean hummingbirds to hand-pollinated flowers also increased pollen tube rates, but regardless of the bird species.…”

Section: Implications Of Pollinator Recognitionmentioning

confidence: 72%

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Testing for pollinator recognition in multiple species ofHeliconia

Gannon

et al. 2021

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Plant-pollinator generalization increases the robustness of plant-pollinator communities to fluctuations in the availability of mutualistic partners. However, natural selection may reinforce floral traits that filter pollinator communities to promote pollination by efficient pollinators, which reduces the number of potential partners. We tested the generality of a recently described, cryptic pollinator filter termed ‘pollinator recognition’ (PR) which could reduce the realized number of pollinators compared to the number of floral visitors. PR was first documented experimentally in Heliconia tortuosa whereby pollen tube germination – a proxy for reproduction – was enhanced following visits from morphologically specialized pollinators, but not generalists. We tested for PR in four taxa spread widely across the Heliconiaceae. With aviary experiments that standardized pollen quality and minimized variation in pollen quantity, we demonstrated that visits by pollen-free hummingbirds increased pollen tube rates compared to hand pollination alone in two species; we also corroborated previous results that visits by long-billed, but not short-billed hummingbirds increased pollen tubes in H. tortuosa . Based on these results, we suggest that the PR mechanism likely exists beyond a single species in the Heliconiaceae and could promote outcrossing in two ways. First, promoting pollen tube growth following a cue from a visiting pollinator could allow a plant to invest in seed production when pollen on the stigma is less likely to be composed entirely of self pollen. Second, because hummingbirds with long, decurved bills tend to be less territorial and more mobile than those with short, straight bills, pollinator recognition could act in conjunction with physical exploitation barriers, such as long and curved corolla tubes, to filter the community of floral visitors in favor of those that are more likely to carry pollen from geographically and therefore genetically distance sources. While the mechanism underlying PR remains equivocal, cryptic pollinator filters may be more common than previously anticipated and could alter perspectives on redundancy in plant-pollinator communities.

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Section: Introductionsupporting

confidence: 91%

Section: Implications Of Pollinator Recognitionmentioning

confidence: 72%

Testing for pollinator recognition in multiple species ofHeliconia

Gannon

et al. 2021

Preprint

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“…When markers were designed and modified from the above studies (Table S1), primer combinations showing evidence of null alleles were eliminated from the genotyping panel. Furthermore, mother–offspring arrays examined in a separate study using the same marker system and individuals from many of the same forest patches did not reveal the presence of null alleles (Torres‐Venegas et al 2019, Torres‐Vanegas et al, 2021). Finally, to confirm the absence of null alleles, analyses using the program inest , which jointly estimates null allele frequency and inbreeding levels, were conducted (Chybicki & Burczyk, 2009) for all individual populations in our study.…”

Section: Methodsmentioning

confidence: 94%

“…Furthermore, a recent study has shown that the relative abundance of traplining birds can affect both the mating system and levels of genetic diversity of H. tortuosa seeds. Higher abundances of traplining birds within stands are correlated with increased pollen pool genetic diversity and lower levels of biparental inbreeding in predispersed ungerminated embryos inferred from mother-offspring genotype arrays (Torres-Vanegas et al, 2021). However, additional factors affecting genetic diversity should be studied, such as the persistence of genetic diversity through later juvenile and adult life stages, differences between populations in primary and secondary forest patches, and the impact of landscape variables and bird community species composition.…”

Section: Introductionmentioning

confidence: 99%

Elevated inbreeding in Heliconia tortuosa is determined by tropical forest stand age, isolation and loss of hummingbird functional diversity

et al. 2022

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Forest conversion and habitat loss are major threats to biological diversity. Forest regeneration can mitigate the negative effects of old‐growth forest loss on species diversity, but less is known about the extent to which forest loss reduces genetic diversity in remnant populations and whether secondary forests play a role in the maintenance of genetic diversity. We quantified genetic diversity in a tropical hummingbird‐pollinated understorey herb, Heliconia tortuosa, across a landscape mosaic of primary and secondary forest regrowth. Using microsatellite genotypes from >850 adult and juvenile plants within 33 forest patches and extensive bird surveys, we examined the effect of contemporary and historical landscape features including forest age (primary vs. secondary forest), stand isolation and pollinator assemblages on genetic diversity and levels of inbreeding in H. tortuosa. We found that inbreeding was up to three times higher in secondary forest, and this effect was amplified with reductions in primary forest in the surrounding landscape through reduced observed heterozygosity in isolated fragments. Inbreeding in forest patches was negatively correlated with the local frequency of specialist long‐distance foraging traplining hummingbirds. Traplining hummingbirds therefore appear to facilitate mating among unrelated plants—an inference we tested using empirically parameterized simulations. Higher levels of inbreeding in H. tortuosa are therefore associated with reduced functional diversity of hummingbirds in secondary forests and forest patches isolated from primary forests. Our findings suggest a cryptic consequence of primary forest loss and secondary forest regeneration through the disruption of mutualistic interactions resulting in the erosion of genetic diversity in a common understorey plant.

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“…Pollen quantity can be measured by counting conspecific pollen grains delivered to a stigma during a single visit (‘single‐visit deposition’: King et al ., 2013; Ballantyne et al ., 2015), while pollen quality depends on numerous plant‐specific variables (e.g. genetic compatibility, relatedness, presence of multiple sires) and is best ascertained through seed set (Ne’eman et al ., 2010; Santiago‐Hernández et al ., 2019) or genetic measures (Torres‐Vanegas et al ., 2021). Additionally, in plant species with pollinator filtering mechanisms (i.e.…”

Section: Ecological Relationships Between Hummingbirds and Plantsmentioning

confidence: 99%

The evolution, ecology, and conservation of hummingbirds and their interactions with flowering plants

et al. 2022

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The ecological co-dependency between plants and hummingbirds is a classic example of a mutualistic interaction: hummingbirds rely on floral nectar to fuel their rapid metabolisms, and more than 7000 plant species rely on hummingbirds for pollination. However, threats to hummingbirds are mounting, with 10% of 366 species considered globally threatened and 60% in decline. Despite the important ecological implications of these population declines, no recent review has examined plant-hummingbird interactions in the wider context of their evolution, ecology, and conservation. To provide this overview, we (i) assess the extent to which plants and hummingbirds have coevolved over millions of years, (ii) examine the mechanisms underlying plant-hummingbird interaction frequencies and hummingbird specialization, (iii) explore the factors driving the decline of hummingbird populations, and (iv) map out directions for future research and conservation. We find that, despite close associations between plants and hummingbirds, acquiring evidence for coevolution (versus one-sided adaptation) is difficult because data on fitness outcomes for both partners are required. Thus, linking plant-hummingbird interactions to plant reproduction is not only a major avenue for future coevolutionary work, but also for studies of interaction networks, which rarely incorporate pollinator effectiveness. Nevertheless, over the past decade, a growing body of literature on plant-hummingbird networks suggests that hummingbirds form relationships with plants primarily based on overlapping phenologies and trait-matching between bill length and flower length. On the other hand, species-level specialization appears to depend primarily on local community context, such as hummingbird abundance and nectar availability. Finally, although hummingbirds are commonly viewed as resilient opportunists that thrive in brushy habitats, we find that range size and forest dependency are key predictors of hummingbird extinction risk. A critical direction for future research is to examine how potential stressorssuch as habitat loss and fragmentation, climate change, and introduction of non-native plantsmay interact to affect hummingbirds and the plants they pollinate.

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Tropical deforestation reduces plant mating quality by shifting the functional composition of pollinator communities

Cited by 10 publications

References 110 publications

Testing for pollinator recognition in multiple species ofHeliconia

Testing for pollinator recognition in multiple species ofHeliconia

Elevated inbreeding in Heliconia tortuosa is determined by tropical forest stand age, isolation and loss of hummingbird functional diversity

The evolution, ecology, and conservation of hummingbirds and their interactions with flowering plants

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