Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation

Abstract

The predator satiation hypothesis posits that masting helps plants escape seed predation through starvation of predators in lean years, followed by satiation of predators in mast years. Importantly, successful satiation requires sufficiently delayed bottom-up effects of seed availability on seed consumers. However, some seed consumers may be capable of quick aggregative and reproductive responses to masting, which may jeopardize positive density dependence of seed survival. We used a 17-yr data set on seed production and insect (Curculio weevils) infestation of three North American oaks species (northern red Quercus rubra, white Q. alba, and chestnut oak Q. montana) to test predictions of the predation satiation hypothesis. Furthermore, we tested for the unlagged numerical response of Curculio to acorn production. We found that masting results in a bottom-up effect on the insect population; both through increased reproductive output and aggregation at seed-rich trees. Consequently, mast seeding in two out of three studied oaks (white and chestnut oak) did not help to escape insect seed predation, whereas, in the red oak, the escape depended on the synchronization of mast crops within the population. Bottom-up effects of masting on seed consumer populations are assumed to be delayed, and therefore to have negligible effects on seed survival in mast years. Our research suggests that insect populations may be able to mount rapid reproductive and aggregative responses when seed availability increases, possibly hindering satiation effects of masting. Many insect species are able to quickly benefit from pulsed resources, making mechanisms described here potentially relevant in many other systems.

Climate warming disrupts mast seeding and its fitness benefits in European beech

“…The temporal decrease in variability and synchrony of seed production provides a natural experiment of how long-term changes in climate alter seed crop patterns and thereby alter the effectiveness of economies of scale. The predator satiation hypothesis consists of two parts, in which the starvation of seed predators in years of low seed production results in the satiation of reduced populations of predators in subsequent mast years 35,36 . More regular seeding of European beech and the reduction in the frequency of seed failures in this study weakened the starvation effect which in turn lowered the effectiveness of predispersal predator satiation.…”

Seed depredation negates the benefits of midstory hardwood removal on longleaf pine seedling establishment

“…Also, theory and empirical evidence suggest that invertebrate seed predators should become satiated during a mast year due to their seed specialization and relative immobility compared to vertebrate seed predators (Holling ; Holling ; Soler et al ). Nevertheless, recent evidence demonstrates that some invertebrate seed predators are capable of overcoming satiation during mast years through rapid reproduction and aggregative responses to seed availability (Bogdziewicz et al ), suggesting that strong invertebrate seed depredation is possible.…”

Spatial and temporal patterns of a pulsed resource dynamically drive the distribution of specialist herbivores

“…Masting is a common, but not universal, reproductive strategy of long-lived tree species 48,49 , and it has been widely acknowledged as a strong demographic and evolutionary driving force of seed specialized insects 46,50,51 . In this line, the present study provided critical support for the need to consider seed densities at both tree and populations levels when assessing distributions of insect seed predators 69,70 . Different mechanisms may however arise in other plant-insect interaction systems, depending on whether they involve more generalist insect herbivores, insects with more limited dispersal abilities among tree populations, or important interferences of local neighbouring vegetation with insects’ behaviour.…”

“…Monophagous and oligophagous predispersal seed predators showed diverging spatial distribution responses to masting patterns in seed production of a jointly exploited perennial herb 68 . Moreover, compared to highly mobile seed wasps, Curculio weevil species with low dispersal abilities rather respond to oak masting by aggregating on seed-rich trees 69,70 or entering prolonged diapause (i.e temporal dispersal) as an alternative strategy to face local resource unpredictability 71 . Finally, the spatial dynamics of insect herbivory may also relate to the relative densities of both host conspecifics and heterospecific neighbours 72 .…”