The energetic and oxidative costs of reproduction in a free-ranging rodent

Abstract

Summary 1.As understanding of the energetic costs of reproduction in birds and mammals continues to improve, oxidative stress is an increasingly cited example of a non-energetic cost of reproduction that may serve as a proximal physiological link underlying life-history trade-offs. 2. Here, we provide the first study to measure daily energy expenditure (DEE) and oxidative damage in a wild population. We measured both traits on eastern chipmunks (Tamias striatus) and assessed their relationships with age, reproductive status, litter size and environmental conditions. 3. We found that both physiological traits were correlated with environmental characteristics (e.g. temperature, seasons). DEE tended to increase with decreasing temperature, while oxidative damage was lower in spring, after a winter of torpor expression, than in autumn. We also found that DEE decreased with age, while oxidative damage was elevated in young individuals, reduced in animals of intermediate age and tended to increase at older age. 4. After controlling for age and environmental variables, we found that both female DEE and oxidative damage increased with litter size, although the latter increased weakly. 5. Our results corroborate findings from laboratory studies but highlight the importance of considering environmental conditions, age and reproductive status in broader analyses of the causes and consequences of physiological costs of reproduction in wild animals.

Context-dependent correlation between resting metabolic rate and daily energy expenditure in wild chipmunks

“…However, both traits are also known to be related to body mass (M b ) (e.g. Fletcher et al, 2012;Speakman et al, 2003;Speakman et al, 2004), reproductive status (Bergeron et al, 2011a;Speakman, 2008), and age (Bergeron et al, 2011a;Bouwhuis et al, 2011;Broggi et al, 2010;Das et al, 2001;Even et al, 2001), meaning that the correlation could arise from covariation with one or more of these individual traits at the whole-animal level. Previous studies examining intra-specific correlations between DEE and BMR (or RMR) had a limited ability to assess potential environmental and individual drivers of the correlation (but see Speakman et al, 2003), and studies assessing multiple drivers have generally focused on a single metabolic trait (e.g.…”

Limits to sustained energy intake. XIV. Heritability of reproductive performance in mice

“…The period of late lactation in small rodents has been intensively studied when investigating limits to SusEI as it is one of the most demanding periods in a small mammal's life (Bergeron et al, 2011;Gittleman and Thompson, 1988;McNab, 2002;Speakman, 2008;Thompson and Nicoll, 1986). During early lactation, food intake increases sharply to meet the increasing demands of the pups; however, during late lactation a plateau is reached (Johnson et al, 2001a;Speakman and Król, 2005a;Speakman, 2008).…”

Oxidative damage and antioxidant defense are assay and tissue‐dependent both in captive and wild‐caught bank voles (Myodes glareolus) before and after reproduction

“…We are aware of only five studies that have examined oxidative stress in breeding free‐living mammals and all of them reported oxidative damage to blood plasma. Eastern chipmunk ( Tamias striatus ) females showed a weak positive effect of litter size on the TBARS level (Bergeron et al., 2011). Females of Soay sheep ( Ovies aries ) which produced two surviving offspring in the previous spring, had a lower concentration of TBARS than females with one or no surviving offspring (Nussey et al., 2009).…”

“…The idea that oxidative damage (to lipids, proteins, and DNA) is a consequence of reproductive effort has been extensively studied in recent years, but has received mixed support (Blount, Vitikainen, Stott, & Cant, 2016; Metcalfe & Monaghan, 2013; Monaghan, Metcalfe, & Torres, 2009; Selman, Blount, Nussey, & Speakman, 2012; Speakman & Garratt, 2013; Speakman et al., 2015). The general picture from studies on various species is very diverse: from an increase in the oxidative stress during reproduction (Alonso‐Alvarez et al., 2004; Bergeron et al., 2011; Fletcher et al., 2013) through the lack of significant differences between breeders and nonbreeders (Nussey, Pemberton, Pilkington, & Blount, 2009; Vitikainen et al., 2016), to the decrease in oxidative stress in breeding individuals (Costantini, Casasole, & Eens, 2014; Garratt, Pichaud, King, & Brooks, 2013; Garratt et al., 2011; Ołdakowski, Wasiluk, Sadowska, Koteja, & Taylor, 2015; Ołdakowski et al., 2012). …”

“…An important question is whether this situation adequately mimics the situation in the field with respect to the factors that generate oxidative stress. However, studies conducted on wild animals in their natural environment, especially on mammals, that provide important information about their real costs of living, are still scarce (Bergeron et al., 2011; Christensen et al., 2015; Fletcher et al., 2013; Nussey et al., 2009; Sharick, Vazquez‐Medina, Ortiz, & Crocker, 2015). …”