Abstract
For many squirrel species, their intense—arguably coevolutionary— interactions with seed and nut producing trees have significantly shaped their biology and diversity. Here we provide an overview of this relationship in a range of forest types worldwide. We first review the evidence for how forest composition (conifer, hardwood, mixed hardwood and overall diversity of tree species) influences interactions between squirrels and seed trees and, ultimately, the role of squirrels as either seed predators or seed dispersers. We review, for example, the intense selective pressure squirrels exert on conifer trees as seed predators and the diversity of morphological traits and behavioral strategies that allow them to efficiently exploit this critical resource. In contrast, we show how the squirrel's role shifts to one of seed disperser in hardwood forests and how the specifics of this interaction varies further with forest structure, forest composition and climactic conditions. We then review the growing evidence for the tight ecological and evolutionary dance between the squirrels and the oaks that has shaped the biology of both across the globe. We show how a suite of seed (acorn) characteristics (e.g., chemical gradients, germination schedules, seedling morphology and tolerance-resistance strategies) are all intimately tied to the scatter-hoarding decisions of several squirrel species. And, based on studies in oak forests in Central America, Mexico, North America, and Eurasia–many by the authors–we also highlight the behavioral strategy of embryo excision now reported for six species across at least four genera of squirrels. This behavior, glaringly absent in other scatter-hoarding rodents worldwide, is now known be an innate trait in at least two species, one in Asia and another in North America. We review extensive recent research on one species of squirrel, the Siberian chipmunk (Tamias sibiricus), which exhibits a suite of behavioral strategies unique to that of other squirrels that independently contributes to seed dispersal and establishment. Finally, we outline numerous remaining questions concerning plants and other taxa of squirrels still open to investigation.
Highlights
Among the squirrels, the intensive use of tree seeds has clearly shaped both the biology of trees and their diaspores, which in turn have significantly influenced evolution of the squirrels’ behavior, ecology and even some aspects of their morphology
We review recent intensive studies of the Siberian chipmunk (Tamias sibiricus) a resident of conifer, mixed, and hardwood forests across northern Asia, which suggest a relatively tight evolutionary relationship with the oaks, somewhat distinct from that of other squirrel species
Opposite of that reported by Hadj-Chikh et al (1996), this study suggests that seed size was a more immediate determinant of caching decisions
Summary
The intensive use of tree seeds has clearly shaped both the biology of trees and their diaspores, which in turn have significantly influenced evolution of the squirrels’ behavior, ecology and even some aspects of their morphology. A limited number of squirrel species (six, Table 1) worldwide are reported to perform embryo excision on early germinating acorns, adaptations of these early germinating oaks present a significant challenge to numerous other seed predators that disperse or feed on these acorns, including several rodents, corvids and insect larvae (e.g., Curculio). Numerous early germinating oak species can even sustain complete acorn removal once the radicle is established (Yi et al, 2012b, 2013a, 2015, 2019a) Together these observations suggest a diffuse co-evolutionary relationship between multiple seed predators, including the squirrels, and the oaks that quite likely results in significant dispersal of oaks under conditions of high seed abundance. Similar observations in North America have been attributed to eastern chipmunks
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