Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism

Abstract

The interaction between granivorous scatterhoarding mammals and plants is a conditional mutualism: scatterhoarders consume seeds (acting as predators), but the movement of seed by scatterhoarders may contribute to dispersal (acting as mutualists). Understanding the ecological factors that shape this relationship is highly relevant in anthropogenically disturbed tropical forests where large‐bodied frugivores are extirpated. In such forests, large‐seeded trees that once depended on these frugivores for dispersal may now only have scatterhoarders as prospective dispersers. We studied Carapa oreophila (Meliaceae) in an Afromontane forest, to test the hypotheses that the proportion of seeds immediately consumed or hoarded (dispersed) would vary over a disturbance gradient. Temporal replication also afforded exploration of how habitat effects might vary with food availability. Using a Bayesian framework, we demonstrate that seeds were more likely to be hoarded in less disturbed forest, irrespective of temporal variation in food abundance. In contrast, forest disturbance only appeared to increase seed predation in temporal replicates that coincided with sustained food availability. These results highlight the potential variability in the dynamics between plants and scatterhoarders over fine temporal scales, elucidating possible ecological scenarios where scatterhoarders might act as mutualists (contributing positively to plant recruitment). Our study also fills important knowledge gaps about the importance of scatterhoarders as dispersers in tropical forests depleted of large‐bodied frugivores, particularly in Africa where scatterhoarding mutualisms have not been extensively studied.

Synzoochory: the ecological and evolutionary relevance of a dual interaction

“…For example, the proportion of Quercus ilex acorns cached by rodents is influenced by the presence of red deer Cervus elaphus (Muñoz & Bonal, ; Muñoz, Bonal & Díaz, ). The spatial structure of vegetation, both at local and landscape scales, may also determine the proportion of seeds cached versus eaten (Puerta‐Piñero et al, ; Yang & Yi, ; Puerta‐Piñero, Pino & Gómez, ; Castro et al ., ; Morán‐López et al ., , b ; Aliyu et al ., ). For example, the proportion of seed effectively dispersed by Eurasian jays is significantly influenced by the presence of pine woodlands and afforestation (Rolando, ; Gómez, ; Pons & Pausas, ; Sheffer et al ., ; Pesendorfer et al ., ).…”

“…The dual role played by synzoochorous dispersers has two main consequences for the dynamics and evolution of synzoochory. A first consequence is that the positive (effective seed dispersal) and negative (seed predation) outcomes of the interactions are expressed simultaneously (Hulme, ; Aliyu et al ., ). Even the removal of several seeds by a single animal can result in a fraction of them being successfully dispersed while others are directly preyed upon.…”

“…Even the removal of several seeds by a single animal can result in a fraction of them being successfully dispersed while others are directly preyed upon. For this reason this interaction is considered to be a conditional mutualism (Jorge & Howe, 2009; Aliyu et al ., ), becoming mutualistic when the benefit of effective seed dispersal exceeds the cost of seed predation (Theimer, ). It is widely acknowledged that mutualistic organisms can confer benefits to their partners while also imposing fitness costs (Bronstein, ).…”

Converting Larch Plantations to Larch-Walnut Mixed Stands: Effects of Spatial Distribution Pattern of Larch Plantations on the Rodent-Mediated Seed Dispersal of Juglans mandshurica

“…Besides spatial distribution types of LPs within the SFs, fluctuated seed production (masting seed: the intermittent production of large seed crops by a plant population) and seed shedding (seed rain) have effects on animal-plant interactions [31,32]. Seed abundance and availability changing with masting year and seed rain arekey factors likely to influence scatterhoarder's strategy [33,34]. In the secondary forest ecosystems of Northeast China, Juglans mandshurica Maxim., Quercus mongolica Fishch.…”

“…Because of high economic value, harvest of Korean pine seeds by humans is very serious and rodents have lost the competition for the dispersal of Korean pine seeds [37]. Highly nutritious and palatable walnut and low nutritious and unpalatable acorn are alternative food for rodents [38,39] and the fates of alternative seeds handled by scatter-hoarding rodents may vary with forest disturbance and seasonal food availability [34].…”