Decoupling the effects of food and density on life history plasticity of wild animals using field experiments: Insights from the steward who sits in the shadow of its tail, the North American red squirrel

Long-term studies of wild animals provide the opportunity to investigate
how phenotypic plasticity is used to cope with environmental
fluctuations, and how the relationships between phenotypes and
fitness can be dependent upon the ecological context. Most previous
studies have only investigated life history plasticity in response to
changes in temperature, yet wild animals often experience
multiple environmental fluctuations simultaneously. This requires field
experiments to decouple which ecological factor induces plasticity in
fitness-relevant traits to better understand their population-level
responses to those environmental fluctuations. For the past 32 years, we
have conducted a long-term integrative study of individually marked North
American red squirrels (Tamiasciurus hudsonicus Erxleben) in the
Yukon, Canada. We have used multi-year field experiments to examine the
physiological and life history responses of individual red squirrels to
fluctuations in food abundance and conspecific density. Our long-term
observational study and field experiments show that squirrels can
anticipate increases in food availability and density, thereby decoupling
the usual pattern where animals respond to, rather than anticipate, an
ecological change. As in many other study systems, ecological factors that
can induce plasticity (such as food and density) co-vary. However, our
field experiments that manipulate food availability and social cues of
density (frequency of territorial vocalizations) indicate that increases
in social (acoustic) cues of density in the absence of additional food can
induce similar life history plasticity, as does experimental food
supplementation. Changes in the levels of metabolic hormones
(glucocorticoids) in response to variation in food and density are one
mechanism that seems to induce this adaptive life history
plasticity.  Although we have not yet investigated the energetic
response of squirrels to elevated density or its association with life
history plasticity, energetics research in red squirrels has overturned
several standard pillars of knowledge in physiological ecology. We show
how a tractable model species combined with integrative studies can reveal
how animals cope with resource fluctuations through life history
plasticity.