Granivore abundance shapes mutualism quality in plant-scatterhoarder interactions.

Conditional mutualisms involve costs and benefits that vary with environmental factors, but mechanisms driving these dynamics remain poorly understood. Scatterhoarder-plant interactions are a prime example of this phenomenon, as scatterhoarders can either increase or reduce plant recruitment depending on the balance between seed dispersal and predation. We explored factors that drive the magnitude of net benefits for plants in this interaction using a mathematical model, with parameter values based on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). We measured benefits as the percentage of germinating seeds, and examined how varying rodent survival (reflecting, e.g. changes in predation pressure), the rate of seed loss to other granivores, the abundance of alternative food resources, and changes in masting patterns affect the quality of mutualism. We found that increasing granivore abundance can degrade the quality of plant-scatterhoarder mutualism due to increased cache pilferage. Scatterhoarders are predicted to respond by increasing immediate consumption of gathered seeds, leading to higher costs and reduced benefits for plants. Thus, biotic changes that are detrimental to rodent populations can be beneficial for tree recruitment due to adaptive behavior of rodents. When scatterhoarder populations decline too drastically (< 5 individuals ha-1 ); however, tree recruitment may also suffer.

Small mammal personalities generate context dependence in the seed dispersal mutualism.

Mutualisms are foundational components of ecosystems with the capacity to generate biodiversity through adaptation and coevolution and give rise to essential services such as pollination and seed dispersal. To understand how mutualistic interactions shape communities and ecosystems, we must identify the mechanisms that underlie their functioning. One mechanism that may drive mutualisms to vary in space and time is the unique behavioral types, or personalities, of the individuals involved. Here, our goal was to examine interindividual variation in the seed dispersal mutualism and identify the role that different personalities play. In a field experiment, we observed individual deer mice (Peromyscus maniculatus) with known personality traits predating and dispersing seeds in a natural environment and classified all observed interactions made by individuals as either positive or negative. We then scored mice on a continuum from antagonistic to mutualistic and found that within a population of scatter hoarders, some individuals are more mutualistic than others and that one factor driving this distinction is animal personality. Through this empirical work, we provide a conceptual advancement to the study of mutualism by integrating it with the study of intraspecific behavioral variation. These findings indicate that animal personality is a previously overlooked mechanism generating context dependence in plant­animal interactions and suggest that behavioral diversity may have important consequences for the functioning of mutualisms.

The ecological and evolutionary significance of effectiveness landscapes in mutualistic interactions.

Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (quantity component) multiplied by the probability that an immediate outcome results in a new individual (quality component). These components form a two-dimensional effectiveness landscape with each species' location determined by its values of quantity (x-axis) and quality (y-axis). We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness values: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components. We illustrate this approach using a large dataset on synzoochory, seed dispersal by seed-caching animals. The synzoochory landscape was clumped, with effectiveness determined primarily by the quality component, and with quantity and quality positively correlated. We suggest this type of landscape structure is common in generalised coevolved mutualisms, where multiple functionally equivalent, high-quality partners exert similarly strong selection. Presumably, only those organisms located in high-quality regions will impact the evolution of their partner. Exploring properties of effectiveness landscapes in other mutualisms will provide new insight into the evolutionary and ecological consequences of mutualisms.

Mast seeding promotes evolution of scatter-hoarding.

Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of 'shared' seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Sowing forests: a synthesis of seed dispersal and predation by agoutis and their influence on plant communities.

Granivorous rodents have been traditionally regarded as antagonistic seed predators. Agoutis (Dasyprocta spp.), however, have also been recognized as mutualistic dispersers of plants because of their role as scatter-hoarders of seeds, especially for large-seeded species. A closer look shows that such definitions are too simplistic for these Neotropical animals because agoutis can influence plant communities not only through seed dispersal of large seeds but also through predation of small seeds and seedlings, evidencing their dual role. Herein, we summarize the literature on plant-agouti interactions, decompose agouti seed dispersal into its quantitative and qualitative components, and discuss how environmental factors and plant traits determine whether these interactions result in mutualisms or antagonisms. We also look at the role of agoutis in a community context, assessing their effectiveness as substitutes for extinct megafaunal frugivores and comparing their ecological functions to those of other extant dispersers of large seeds. We also discuss how our conclusions can be extended to the single other genus in the Dasyproctidae family (Myoprocta). Finally, we examine agoutis' contribution to carbon stocks and summarize current conservation threats and efforts. We recorded 164 interactions between agoutis and plants, which were widespread across the plant phylogeny, confirming that agoutis are generalist frugivores. Seed mass was a main factor determining seed hoarding probability of plant species and agoutis were found to disperse larger seeds than other large-bodied frugivores. Agoutis positively contributed to carbon storage by preying upon seeds of plants with lower carbon biomass and by dispersing species with higher biomass. This synthesis of plant-agouti interactions shows that ecological services provided by agoutis to plant populations and communities go beyond seed dispersal and predation, and we identify still unanswered questions. We hope to emphasise the importance of agoutis in Neotropical forests.

Topological Interlocking and Geometric Stiffening as Complementary Strategies for Strong Plant Shells.

Many organisms encapsulate their embryos in hard, protective shells. While birds and reptiles largely rely on mineralized shells, plants often develop highly robust lignocellulosic shells. Despite the abundance of hard plant shells, particularly nutshells, it remains unclear which fundamental properties drive their mechanical stability. This multiscale analysis of six prominent (nut)shells (pine, pistachio, walnut, pecan, hazelnut, and macadamia) reveals geometric and structural strengthening mechanisms on the cellular and macroscopic length scales. The strongest tissues, found in walnut and pistachio, exploit the topological interlocking of 3D-puzzle cells and thereby outperform the fiber-reinforced structure of macadamia under tensile and compressive loading. On the macroscopic scale, strengthening occurs via an increased shell thickness, spherical shape, small size, and a lack of extended sutures. These functional interrelations suggest that simple geometric modifications are a powerful and resource-efficient strategy for plants to enhance the fracture resistance of entire shells and their tissues. Understanding the interplay between structure, geometry, and mechanics in hard plant shells provides new perspectives on the evolutionary diversification of hard seed coats, as well as insights for nutshell-based material applications.

The parakeet Brotogeris tirica feeds on and disperses the fruits of the palm Syagrus romanzoffiana in Southeastern Brazil / O periquito Brotogeris tirica come e dispersa os frutos da palmeira Syagrus romanzoffiana no sudeste do Brasil

Small psittacids remain unrecorded as dispersal agents of palm fruits in Brazil. I record here the plain parakeet (Brotogeris tirica), an Atlantic forest endemic, feeding on and dispersing the fruits of the palm Syagrus romanzoffiana at Ubatuba, northern coast of São Paulo, Southeastern Brazil. The birds removed the fruit and carried it away from the mother-tree in about 40 percent of the feeding records. While perched on trees and shrubs of the understorey, the parakeets removed and ingested most of the mesocarp, dropping the partly consumed fruit. As the parakeets damaged no the embryo and may feed at a distance from the mother-tree, they act as primary dispersal agents. This is the first substantiated record of a small Neotropical psittacid as a stomatochorous dispersal agent of palm fruits the size of A. romanzoffiana drupes.

Psitacídeos de pequeno porte não constam como dispersores de frutos de palmeiras no Brasil. Registro aqui o periquito-rico (Brotogeris tirica), endêmico da mata Atlântica, alimentando-se em e dispersando frutos da palmeira Syagrus romanzoffiana em Ubatuba, litoral norte do Estado de São Paulo. As aves removiam o fruto e, em cerca de 40 por cento dos registros alimentares, carregavam-no à distância da árvore-mãe. Empoleirados em ramos de arvoretas e arbustos no sub-bosque, os periquitos retiravam e ingeriam a maior parte do mesocarpo, deixando cair o resto do fruto. Uma vez que estas aves se alimentam sem danificar o embrião e podem fazê-lo a certa distância da árvore-mãe, agem como dispersores primários. Este é o primeiro registro documentado de um psitacídeo Neotropical de pequeno porte como dispersor estomatocórico de frutos de palmeira com as dimensões das drupas de S. romanzoffiana.