Pollination outcomes reveal negative density‐dependence coupled with interspecific facilitation among plants

Bergamo, Pedro Joaquim; Streher, Nathália Susin; Traveset, Anna; Wolowski, Marina; Sazima, Marlies

doi:10.1111/ele.13415

Cited by 63 publications

(72 citation statements)

References 59 publications

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“…Tropical mountaintop communities, as the one here studied, are highly vulnerable to climatic variations, which makes the pollination environment very unpredictable ( Freitas and Sazima 2006 ). For this plant community, it has been shown that species that flower nearby heterospecifics get more CP and grow more pollen tubes suggesting that the joint attraction of pollinators is advantageous under low pollinator availability circumstances ( Bergamo et al 2020a ), but the role of HP receipt in such outcomes was not considered. Therefore, we hypothesize that the positive effect found when S. wettsteinii received HP distantly related in our study could be a reflex of the pollinator scarcity context, especially because this interspecific facilitation mentioned before was a trend among the generalist-pollinated species of this community ( Bergamo et al 2020a , b ).…”

Section: Discussionmentioning

confidence: 99%

“…We considered congeners as phylogenetically close and species from different families as phylogenetically distant. Based on this assumptions, the recipients chosen included two Fuchsia hummingbird-pollinated species, considered as specialists (previously classified in Bergamo et al 2020a ): Fuchsia campos-portoi , that has 113.7 ± 20.83 (mean ± standard deviation) ovules per ovary and a stigmatic surface area of 0.01 cm 2 and F. regia , that has 122.38 ± 25.23 (mean ± standard deviation) ovules per ovary and a stigmatic surface area of 0.05 cm 2 . The other recipient was Sisyrinchium wettsteinii that has 60.5 ± 16.8 (standard deviation) ovules per ovary, a stigmatic surface area of 0.001 cm 2 and is visited by various insects (i.e.…”

Section: Methodsmentioning

confidence: 99%

“…The other recipient was Sisyrinchium wettsteinii that has 60.5 ± 16.8 (standard deviation) ovules per ovary, a stigmatic surface area of 0.001 cm 2 and is visited by various insects (i.e. bees, flies and beetles), considered a generalist-pollinated species (previously classified in Bergamo et al 2020a ). Besides fitting the assumptions described before, these species were chosen to be recipients also due to their high flower abundance in field, their pollination system and the fact that they experience HP deposition naturally (e.g.…”

Section: Methodsmentioning

confidence: 99%

“…Here, we used an experimental approach to assess the post-pollination HP effects between sets of species with similar flowers that share pollinators in a tropical highland community. The species studied here were categorized as specialist- or generalist-pollinated depending on whether they were visited by one or more than one group of pollinators, respectively (see Bergamo et al 2020a ). The taxonomic classification of these species (genus and family) was used to establish pairs of closely related taxa (species in the same genus) vs. more distantly related (species in different families).…”

Section: Introductionmentioning

confidence: 99%

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Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient

et al. 2020

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Abstract Co-flowering plant species may interact via pollinators leading to heterospecific pollen transfer with consequences for plant reproduction. What determines the severity of heterospecific pollen effect on conspecific pollen performance is unclear, but it may depend on the phylogenetic relatedness of the interactors (pollen donors and recipient). The heterospecific pollen effect might also depend on the extent to which plants are exposed to heterospecific pollen over ecological or evolutionary timescales. For instance, generalist-pollinated plant species might tolerate heterospecific pollen more than specialists. Here, we tested whether heterospecific pollen effects are stronger between closely related species than phylogenetically distant ones in a tropical highland community. Then, based on these results, we determined whether responses to heterospecific pollen were stronger in generalized vs. specialized plant species. We applied heterospecific pollen from close (congeneric) or distant (different families) donors alone or with conspecific pollen on stigmas of three recipient species (one generalist, Sisyrinchium wettsteinii; and two specialists, Fuchsia campos-portoi and Fuchsia regia) and scored pollen tube performance in styles. In all species, pollen from closely related donors grew pollen tubes to the base of the style indicating a high potential to interfere with seed set. Conversely, distantly related heterospecific pollen had no effect on either specialist Fuchsia species, whereas enhanced performance of conspecific pollen was observed in generalist S. wettsteinii. The strong effect of phylogenetic relatedness of donor and recipient might have obscured the role of pollination specialization, at least for the three species examined here. Therefore, phylogenetic relatedness mediated the effect of heterospecific pollen on post-pollination success, with possible consequences for reproductive trait evolution and community assembly for further studies to explore.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient

et al. 2020

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“…However, the dominant interaction may switch from facilitative to competitive as the number of flowering species and/or floral density increases during the rainy season, as plants will start to compete for a limited pollinator pool (Fontaine, Collin, & Dajoz, 2008;Rathcke, 1983). Although this type of densitydependent relationship has been shown for pairs of interacting plant species (Brown, Mitchell, & Graham, 2002;Jakobsson, Lázaro, & Totland, 2009;Rathcke, 1983Rathcke, , 1988Seifan, Hoch, Hanoteaux, & Tielbörger, 2014), knowledge of density-dependent effects in structuring species interactions at the community level is limited (but see Bergamo, Streher, Traveset, Wolowski, & Sazima, 2020). As a result, along the entire study area, the density and diversity of co-flowering species can be up to 10 and 2 times higher in the rainy season compared to the dry season, respectively (Albor et al, 2019;Parra-Tabla et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Integrating floral trait and flowering time distribution patterns help reveal a more dynamic nature of co‐flowering community assembly processes

2020

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1. Species' floral traits and flowering times are known to be the major drivers of pollinator-mediated plant-plant interactions in diverse co-flowering communities. However, their simultaneous role in mediating plant community assembly and plant-pollinator interactions is still poorly understood. Since not all species flower at the same time, inference of facilitative and competitive interactions based on floral trait distribution patterns should account for fine phenological structure (intensity of flowering overlap) within co-flowering communities. Such an approach may also help reveal the simultaneous action of competitive and facilitative interactions in structuring co-flowering communities. 2. Here we used modularity within a co-flowering network context, as a novel approach to detect convergent and/or over-dispersed patterns in floral trait distribution and pollinator sharing. Specifically, we evaluate differences in floral trait and pollinator distribution patterns within (high temporal flowering overlap) and among co-flowering modules (low temporal flowering overlap). We further evaluate the consistency of observed floral trait and pollinator sharing distribution patterns across space (three geographical regions) and time (dry and rainy seasons). 3. We found that floral trait similarity was significantly higher in plant species within co-flowering modules than in species among them. This suggests pollinator facilitation may lead to floral trait convergence, but only within co-flowering modules. However, our results also revealed seasonal and spatial shifts in the underlying interactions (facilitation or competition) driving co-flowering assembly, suggesting that the prevalent dominant interactions are not static. 4. Synthesis. Overall, we provide strong evidence showing that the use of flowering time and floral trait distribution alone may be insufficient to fully uncover the role of pollinator-mediated interactions in community assembly. Integrating this information along with patterns of pollinator sharing will greatly help reveal the simultaneous action of facilitative and competitive pollinator-mediated interactions in co-flowering communities. The spatial and temporal variation in flowering and trait distribution patterns observed further emphasize the importance of adopting a more dynamic view of community assembly processes. Co-flowering Module 1 Co-flowering Module 1 Co-flowering Module 2 Co-flowering Module 2 Co-flowering Module 1 Co-flowering Module 2 Example of clustering in floral color and overdispersion in flowering time (co-flowering modularity) Floral trait similarity: greater among than within co-flowering modules Associated predictions Floral trait and flowering time distribution patterns Sp1

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Patterns of frequency and density dependence are highly variable in diverse annual flowering plant communities

James

Mayfield

Dwyer

2023

Ecology

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Applications of ecological theory to natural communities often assume that competitive, negative density‐dependent processes are the only type of interaction important for diversity maintenance. Recent advances suggest that positive interactions within trophic levels (e.g., plant–plant) may also affect plant coexistence. Though positive plant–plant interactions theoretically might result in positive or nonmonotonic frequency or density dependence (FD/DD), less is known about how commonly these patterns occur or which ecological processes might result in such patterns in natural plant communities. In this study we tested for signals of variable frequency and density dependence in annual flowering plant communities in Western Australia and searched for evidence that interactions among plants during flowering might induce positive or nonmonotonic FD/DD in flowering plants. Using four common annual wildflower species, we ask if plant fecundity exhibited positive or nonmonotonic FD/DD and if pollinator‐mediated plant–plant interactions during flowering change patterns of FD/DD relative to pollinator‐independent plant interactions. Three species exhibited nonmonotonic (hump‐shaped) density dependence, and only one species experienced strictly negative density dependence. Each species exhibited a different pattern of frequency dependence (positive, negative, weakly nonmonotonic, and no detectable frequency dependence). Pollinator‐mediated plant–plant interactions during flowering induced both nonmonotonic density dependence and negative frequency dependence in one species. Importantly, the extent of variation in FD/DD observed in our study brings into question the dominance of negative density and frequency dependence in theory, suggesting instead that demographic responses of plants to their communities fall along a continuum of possible density‐ and frequency‐dependent patterns.

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Pollination outcomes reveal negative density‐dependence coupled with interspecific facilitation among plants

Cited by 63 publications

References 59 publications

Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient

Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient

Integrating floral trait and flowering time distribution patterns help reveal a more dynamic nature of co‐flowering community assembly processes

Patterns of frequency and density dependence are highly variable in diverse annual flowering plant communities

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