Marco A. Pizo, Juan M. Morales, Otso Ovaskainen, and Tomás A. Carlo (Feb 2021)
New paper shows the importance of fruit chemistry as a factor structuring the interactions between frugivores and plants
“Frugivory specialization in birds and fruit chemistry structure mutualistic networks across the Neotropics”
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(Photo: Tomás A. Carlo)
The issue of fruit choice by fruit-eating animals has long intrigued ecologists. With such a variety of fruits available out there, how do frugivorous animals chose a given fruit to eat? This is not a trivial question as fruit eating is at the same time the final act of a long evolutionary history that enabled frugivores and fruits to interact with each other, and the first step of the process that led to the dispersal of seeds and regeneration of plant populations. We know that fruit morphology is part of the answer, but other fruit traits should also be considered. Lipid content varies a lot in fruits and is, interestingly, negatively correlated with sugar content. Compared to sugars, lipids demand longer processing in the gut to be absorbed. Scattered published observations and the experience accumulated by Marco Pizo and Tomas Carlo with fruits and frugivores in the field has provided evidence that lipid-rich and lipid-poor (sugary) fruits might attract different bird species. They formally tested this possibility by compiling from the literature over 35 thousand feeding visits of 317 bird species to 165 fleshy-fruited plant species. The analytical expertise of Juan Morales and Otso Ovaskainen was pivotal in analyzing this huge dataset to reveal that the relative contribution of predominantly insectivorous birds (which also eat some fruit) to feeding visits to lipid-rich fruits is higher than birds that include a greater amount of fruits in the diet, while the reverse is true for lipid-poor fruits. The digestive physiology of predominantly insectivorous birds adapted to deal with arthropods that normally are richer in lipids than fruits likely permits them to process lipid-rich fruits, while the rapid food passage typical of heavily frugivorous species makes lipid-poor fruits better suited to them. This balance between the degree of frugivory of birds and the pattern of visitation to lipid-poor and lipid-rich fruits helps to illuminate community-wide interactions between frugivorous birds and plants.
Abstract
The interaction between fruit chemistry and the physiological traits of frugivores is expected to shape the structure of mutualistic seed dispersal networks, but it has been understudied compared to the role of morphological trait-matching in structuring interaction patterns. For instance, highly frugivorous birds (i.e., birds that have fruits as the main component of their diets), which characteristically have fast gut-passage times, are expected to avoid feeding on lipid-rich fruits because of the long gut-retention times associated with lipid digestion. Here we compiled data from 84 studies conducted in the Neotropics that used focal-plant methods to record 35,815 feeding visits made by 317 bird species (155 genera in 28 families) on 165 plant species (82 genera in 48 families). We investigated the relationship between the degree of frugivory of birds (i.e., how much of their diet is composed by fruit) at the genus level and their visits to plant genera that vary in fruit-lipid content. We used a Hierarchical Modeling of Species Communities approach that accounted for the effects of differences in body size, the bird and plant phylogeny, and the spatial location of study sites. We found that birds with low degree of frugivory (e.g., predominantly insectivores) tend to have the highest increase in visitation rates as fruits get more lipid-rich, while birds that are more frugivorous tend to increase visits at a lower rate or even decrease visitation rates as lipids increase in fruits. This balance between degree of frugivory and visitation rates to lipid-poor and lipid-rich fruits provides a mechanism to explain specialized dispersal systems and the occurrence of certain physiological-nutritional filters, ultimately helping to understand community-wide interaction patterns between birds and plants.
A especialização na dieta das aves e a química dos frutos estruturam as redes de frugivoria nos Neotrópicos
Apesar de potencialmente influenciar a estrutura das redes de interações entre animais frugívoros e frutos carnosos, as características químicas dos frutos e a fisiologia digestiva dos frugívoros tem sido pouco estudada em comparação com o papel de características morfológicas na estruturação dos padrões de interação. Por exemplo, aves altamente frugívoras (ou seja, aves que têm os frutos como principal componente de suas dietas), que caracteristicamente processam rapidamente os frutos no intestino, devem evitar frutos ricos em lipídios que demandam longo tempo de retenção intestinal para sua completa digestão. Para testar esta hipótese, compilamos dados de 84 estudos conduzidos nos Neotrópicos que registraram 35.815 visitas de alimentação feitas por 317 espécies de aves (155 gêneros, 28 famílias) em 165 espécies de plantas (82 gêneros, 48 famílias). Investigamos a relação entre o grau de frugivoria das aves (ou seja, quanto de sua dieta é composta por frutos) em nível de gênero e a frequência de suas visitas a gêneros de plantas que variaram quanto ao teor de lipídeos dos frutos. Usamos uma abordagem de Modelagem Hierárquica de Comunidades que levou em consideração os efeitos das diferenças no tamanho do corpo, da filogenia das aves e plantas e da localização das áreas de estudo. As aves com baixo grau de frugivoria (por exemplo, predominantemente insetívoros) tendem a aumentar a taxa de visitas à medida que os frutos se tornam mais ricos em lipídios, enquanto as taxas de visita das aves mais frugívoras tendem a aumentar menos ou mesmo diminuir à medida que aumenta o conteúdo lipídico dos frutos. Esse balanço entre o grau de frugivoria das aves e a frequência de alimentação em frutos pobres e ricos em lipídios representa um mecanismo para explicar os sistemas especializados de dispersão de sementes e a ocorrência de filtros fisiológicos-nutricionais que ajudam a entender os padrões de interação entre as aves frugívoras e as plantas.