Land-use changes are expected to affect plant-disperser conditional mutualisms through changes in animal behavior. We analyzed the oak-rodent conditional mutualism in Mediterranean fragmented forests at two climatically different locations. We quantified fragmentation effects on seed dispersal effectiveness and assessed if such effects were due to changes in habitat structure and intraspecific competition for acorns in fragmented areas. Fragmentation decreased cover from predators within mouse territories as well as intraspecific competition for acorns. This resulted in lower dispersal effectiveness in small forest fragments. Globally, habitat structure was the main driver in mouse foraging decisions. In small fragments, low shelter availability precluded mouse movements, leading to short mobilization distances and low caching rates. However, as the proportion of cover from predators increased, mice were able to modulate their foraging decisions depending on intraspecific competition for acorns, resulting in higher dispersal quality. In addition to fragmentation effects, delayed breeding in the southern locality caused lower number of rodents during the dispersal season, which reduced acorn mobilization rates. Our study shows that seed dispersal patterns in managed systems can be analyzed as the result of management effects on key environmental factors in dispersers' foraging decisions.
Network metrics are widely used to infer the roles of mutualistic animals in plant communities and to predict the effect of species' loss. However, their empirical validation is scarce. Here we parameterized a joint species model of frugivory and seed dispersal with bird movement and foraging data from tropical and temperate communities. With this model, we investigate the effect of frugivore loss on seed rain, and compare our predictions to those of standard coextinction models and network metrics. Topological coextinction models underestimated species loss after the removal of highly linked frugivores with unique foraging behaviours. Network metrics informed about changes in seed rain quantity after frugivore loss. However, changes in seed rain composition were only predicted by partner diversity. Nestedness, closeness, and d’ specialisation could not anticipate the effects of rearrangements in plant–frugivore communities following species loss. Accounting for behavioural differences among mutualists is critical to improve predictions from network models.
Wood mice Apodemus sylvaticus are the main dispersers of acorns in highly managed Mediterranean holm-oak woodlands. Mice mobilize and cache acorns to store them for winter consumption. They carry acorns away from potential competitors, face predation risks during mobilization, and cache acorns in areas where pilfering risks are low. However, mice can act either as net predators or as moderately efficient dispersers, depending on the way landscape management affects intraspecific competition for acorns and shelter availability. To assess the influence of landscape structure and mouse behavior on acorn dispersal, we developed an agent-based model (ABM) that translates forest management into changes in key environmental factors driving mouse foraging decisions.The model was able to predict accurately acorn dispersal patterns in a wide range of forest management practices based on information on forest habitat availability, stem density and shrub cover. Sensitivity analysis revealed that caching rates emerged from the interplay between intraspecific competition for seeds and predation risk accepted during mobilization. It also showed that intraspecific competition for acorns decreased with increasing habitat loss (due to positive edge effects on acorn production) while landscape resistance to mouse movements increased. As a result, the net benefits of caching declined and acorn predation became the dominant strategy. Finally, we assessed the effects of shrub encroachment as a management practice to enhance dispersal services in savanna-like landscapes (dehesas). The model predicted non-linear responses with a 65% threshold of shrub cover needed to achieve relatively high levels of acorn dispersal. This value may not be compatible with the traditional exploitation of dehesas (livestock rearing). Our study shows that integrated approaches that combine environmental change driven by management with behavioral responses of dispersers improve our understanding of the causes of recruitment bottlenecks, and are useful tools for evaluating conservation strategies aimed at enhancing dispersal services.
Frugivores may play a key role in plant species coexistence by equalizing the species' representation in the seed rain. Rare species may benefit from enhanced dispersal if frugivores prefer locally scarce fruits, or if rare plants are found in neighborhoods of high fruit density. Using a simulation model of frugivorous birds foraging on landscapes we tested if increased diversity in the seed rain could emerge from rare-biased fruit selection, from the spatial configuration of plants, or both. In the absence of rare-biased fruit selection, frugivores were not able to increase the diversity of the seed rain in any of our simulated landscapes. In contrast, when frugivores were attracted to locally scarce fruits, we found increased diversity in the seed rain whenever frugivore mobility across the landscape was high and plant species were well-mixed in the fruiting neighborhoods. Irrespectively of the behavioral mechanism involved, landscape fragmentation lead to losses in diversity and species richness of simulated communities. In all simulations, density-dependent mortality of dispersed seeds increased diversity in the community of seedlings. However, landscape homogenization at the scale of frugivores movements decreased the magnitude of this diversification effect. In summary, our study shows that frugivory has the potential to increase diversity in the seed rain when frugivores display rare-biased fruit choices, provided that rare and common plants form heterogeneous neighborhoods. They also show that fragmentation is a major threat for diversity maintenance in the early-regenerating community. Finally, they show that rarity confers advantages during regeneration only if it occurs at the scale of frugivores' foraging decisions.
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