Accounting for age: uncovering the nuanced drivers of mammal body-size responses to climate change

Abstract

Shifts in mean body size coinciding with environmental change are well documented across animal species and populations, serving as a widespread and complex indicator of climate-change response. In mammal research, identifying and disentangling the potential drivers of these trends (e.g., thermoregulation, resource availability) is hindered by treating adult size as fixed, ignoring morphological changes that occur throughout life in many species. However, observed population-level size trends may reflect underlying shifts in age structure (i.e., change in the proportion of older, potentially larger individuals in the population). Here, we assessed the role of age structure by explicitly evaluating age as a contributor to temporal variation in skull size (a proxy for body size) in 2 carnivorans, Canadian Lynx (Lynx canadensis) and American Marten (Martes americana). Using a series of linear and nonlinear models, we tested age in years (determined by cementum-layer analysis) as a predictor of skull size alongside other factors previously proposed to be important drivers of body-size trends, including population density for lynx and growing season conditions for martens. In both species, age was a significant predictor of skull size indicating a rapid year-to-year increase in young adult size that diminished in later adulthood. However, temporal shifts in age structure alone did not explain the observed changes in size over time, indicating that age structure acts in concert with other as-yet unidentified factors to drive body-size change. By explicitly evaluating the role of age, we can both refine models of temporal body-size trends and gain insights into size change as a signal of underlying demographic shifts-such as age-specific survivorship-providing a more holistic understanding of how mammals are responding to climate change.

Keywords: Lynx canadensis; Martes americana; age structure; body size; climate-change response.

Fig. 1.

Measurements used to represent size in (A) Canadian Lynx (Lynx canadensis) and (B) American Marten (Martes americana). Skull length was measured in 2 ways: greatest total length of the skull (GTL, defined as the maximum distance from the anterior margin of the premaxilla to the posterior margin of the lambdoidal ridge) and condylopremaxillary length (CPL, defined as the maximum distance from the anterior margin of the premaxilla to the posterior margin of the occipital condyle). The other measurements are greatest skull width (i.e., zygomatic breadth, ZB, defined as the maximum width of the skull), interorbital width (i.e., interorbital constriction, IO, defined as the minimum distance between the orbits, lynx only), upper canine width (CAN, defined as anteroposterior width of the upper canine tooth closest to the socket, or when the tooth is absent, the inner width of the socket itself), and fourth upper premolar width (PM4, defined as the anteroposterior width of the fourth upper premolar, martens only). Lynx and marten skull diagrams are not to scale with respect to each other.

Fig. 2.

Nonlinear increase in select skull measurements with age. With increasing age, both male and female Canadian Lynx (Lynx canadensis) increase significantly in skull length (A, C), skull width (E), and size PC1 (G), while male American Marten (Martes americana) increase significantly in skull length (B, D) but both sexes increase significantly in skull width (F) and size PC1 (H). All models are corrected for latitude, longitude, year, and relevant conditions (predicted harvest for lynx, climate PC1 for martens). Shaded areas represent the 95% confidence interval, with the lighter color denoting males and the darker color females. PhyloPic images by Gabriela Palomo-Munoz (https://creativecommons.org/licenses/by-nc/3.0/).

Fig. 3.

Nonlinear change in mean size PC1 over time in (A) Canadian Lynx (Lynx canadensis; significant decrease) and (B) American Marten (Martes americana; significant increase). The measure of time (year of collection for lynx, year of birth for martens) included in the GAM is based on the best-fitting linear model structure. All models also include latitude, longitude, age, and relevant conditions (predicted harvest for lynx, climate PC1 for martens). Shaded areas represent the 95% confidence interval, with the lighter color denoting males and the darker color females. PhyloPic images by Gabriela Palomo-Munoz (https://creativecommons.org/licenses/by-nc/3.0/).

Fig. 4.

Temporal shifts in age structure in (A) Canadian Lynx (Lynx canadensis) and (B) American Marten (Martes americana). The proportion of the population comprising younger individuals is represented by lighter shading, and older individuals by darker shading. Significant differences (based on chi-square tests) are marked by *. PhyloPic images by Gabriela Palomo-Munoz (https://creativecommons.org/licenses/by-nc/3.0/).