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ABSTRACT Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in suites of matching frugivore and plant traits that structure fruit consumption. Recent work has suggested fruit traits can represent adaptations to broad groups of functionally similar frugivores, but the role of frugivore traits and within‐species variation in structuring fruit consumption is less understood. To address these knowledge gaps, we assess the presence of reciprocal trait matching for the mutualistic ecological network comprising ofCarolliabats that feed on and dispersePiperseeds. We used generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of frugivore adaptation to their dietary composition and suggesting niche partitioning amongCarolliabats, we find differential consumption of a suite ofPiperspecies influenced by bat traits such as body size; however, thePipermorphological traits considered had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such asPiperchemical bouquets, may explain the lack of association between batPiperconsumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant–frugivore interactions, providing a template for future trait analyses of plant–animal networks. As intraspecific trait variation is rarely included in studies on trait matching, this paper contributes to closing that important knowledge gap.
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Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism
Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats ( Carollia spp.) and plants ( Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper . Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper , our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity.
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- PAR ID:
- 10299795
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 288
- Issue:
- 1956
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20210312
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in suites of matching frugivore and plant traits that structure fruit consumption. Recent work has suggested fruit traits can represent adaptations to broad groups of functionally similar frugivores, but the role of frugivore traits and within-species variation in structuring fruit consumption is less understood. To address these knowledge gaps, we assess the presence of reciprocal trait matching for the mutualistic ecological network comprising of Carollia bats that feed on and disperse Piper seeds. We used generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of frugivore adaptation to their dietary composition and suggesting niche partitioning among Carollia bats, we find differential consumption of a suite of Piper species influenced by bat traits such as body size; however, the Piper morphological traits considered had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such as Piper chemical bouquets, may explain the lack of association between bat Piper consumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant–frugivore interactions, providing a template for future trait analyses of plant–animal networks. As intraspecific trait variation is rarely included in studies on trait matching, this paper contributes to closing that important knowledge gap. # Data from: Frugivore traits predict plant-frugivore interactions using generalized joint attribute modeling [https://doi.org/10.5061/dryad.2v6wwpzwg](https://doi.org/10.5061/dryad.2v6wwpzwg) Bayesian models relating: 1\. head.R: relates *Carollia* traits to bite force (performance) via hierarchical ML models 2\. carollia3_0.R: relates *Carollia* traits to bite force (performance) via hierarchical Bayesian models 3\. gjam generated model of consumption relationship to traits for *Carollia* bats 4\. gjam processed model outputs 5\. piper.R: relates *Piper* traits and GJAM coefficients obtained from 3 and 4 ## Description of the data and file structure All cells marked as NA lacked data and correspond to missing data. ## Code/Software 1\. head.R: relates *Carollia* traits to bite force (performance) via hierarchical ML models. Requires data file bat_l_biteBody.csv and R library lme4. Prints results to .txt file. 2\. carollia3_0.R: relates *Carollia* traits to bite force (performance) via hierarchical Bayesian models. Requires data file bat_l_biteBody.csv, R library R2Jags, and 3 Jags files. The three Jags files are: * carollia_bf_size.txt * carollia_bf_mass.txt * carollia_bf_head.txt carollia3_0.R prints out the results of hierarchical Bayesian regressions in txt and saves an Rdata file. 3\. niche_Carollia.R: generates gjam model of consumption relationship t traits for *Carollia* bats Requires data files: * carollia_niche_xdata.csv: x or explanatory variables, bat traits * carollia_niche_ydata_trim.csv: y or response variables, bat consumption of *Piper* fruit from different species * carollia_type.csv: individual bat assignment to one of 3 species * and R libraries gjam, reshape2 and plyr plus function * bayesReg.R (which codes a function to run a Tobit and Bayesian regression from the NEON example here: [https://rstudio-pubs-static.s3.amazonaws.com/710083_480b1b43b4f0470691e95302483fdc08.html](https://rstudio-pubs-static.s3.amazonaws.com/710083_480b1b43b4f0470691e95302483fdc08.html)). This script generates the bayesian gjam model and saves an Rdata file. 4\. plot_Carollia_v2.r processes gjam model outputs. Requires data files: * models_Carollia.Rdata * and R libraries gjam, reshape2, plyr, ggplot2, MCMCvis and wesanderson This script generates the standardized summary and prints out a file called piper_medians.csv 5\. piper.R relates *Piper* traits and gjam coefficients obtained from steps 3 and 4.. Requires data files: * piper.nex: phylogeny of *Piper* plants * piper_k_traits.csv: correspondence between *Piper* traits and *Piper* species * output.csv: this is processed from piper_medians.csv to separate relate Piper species to bat trait values resulting from gjam * Requires R libraries MCMCglmm and geiger This script prints out the results of phylogenetic Bayesian regressions of gjam outputs as a function of *Piper* traits in txt and saves a Rdata file.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2021.0312
