Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae).

BACKGROUND: The progressive deregulation of the immune system with age, termed immunosenescence, has been well studied in mammalian systems, but studies of immune function in long-lived, wild, non-mammalian populations are scarce. In this study we leverage a 38-year mark-recapture study to quantify the relationships among age, sex, survival, reproductive output and the innate immune system in a long-lived reptile, yellow mud turtles (Kinosternon flavescens; Testudines; Kinosternidae). METHODS: We estimated rates of survival and age-specific mortality by sex based on mark-recapture data for 1530 adult females and 860 adult males over 38 years of captures. We analyzed bactericidal competence (BC), and two immune responses to foreign red blood cells - natural antibody-mediated haemagglutination (NAbs), and complement-mediated haemolysis ability (Lys) - in 200 adults (102 females; 98 males) that ranged from 7 to 58 years of age captured in May 2018 during their emergence from brumation, and for which reproductive output and long-term mark-recapture data were available. RESULTS: We found that females are smaller and live longer than males in this population, but the rate of accelerating mortality across adulthood is the same for both sexes. In contrast, males exhibited higher innate immunity than females for all three immune variables we measured. All immune responses also varied inversely with age, indicating immunosenescence. For females that reproduced in the preceding reproductive season, egg mass (and therefore total clutch mass) increased with age,. In addition to immunosenescence of bactericidal competence, females that produced smaller clutches also had lower bactericidal competence. CONCLUSIONS: Contrary to the general vertebrate pattern of lower immune responses in males than females (possibly reflecting the suppressive effects of androgens), we found higher levels of all three immune variables in males. In addition, contrary to previous work that found no evidence of immunosenescence in painted turtles or red-eared slider turtles, we found a decrease in bactericidal competence, lysis ability, and natural antibodies with age in yellow mud turtles.

Over a decade of field physiology reveals life-history specific strategies to drought in garter snakes (Thamnophis legans).

Changing climates and severe weather events can affect population viability. Individuals need to buffer such negative fitness consequences through physiological plasticity. Whether certain life-history strategies are more conducive to surviving changing climates is unknown, but theory predicts that strategies prioritizing maintenance and survival over current reproduction should be better able to withstand such change. We tested this hypothesis in a meta-population of garter snakes having naturally occurring variation in life-history strategies. We tested whether slow pace-of-life (POL) animals, that prioritize survival over reproduction, are more resilient than fast POL animals as measured by several physiological biomarkers. From 2006 to 2019, which included two multi-year droughts, baseline and stress-induced reactivity of plasma corticosterone and glucose varied annually with directionalities consistent with life-history theory. Slow POL animals exhibited higher baseline corticosterone and lower baseline glucose, relative to fast POL animals. These patterns were also observed in stress-induced measures; thus, reactivity was equivalent between ecotypes. However, in drought years, measures of corticosterone did not differ between different life histories. Immune cell distribution showed annual variation independent of drought or life history. These persistent physiological patterns form a backdrop to several extirpations of fast POL populations, suggesting a limited physiological toolkit to surviving periods of extreme drought.

Temperature-dependence of metabolism and fuel selection from cells to whole organisms.

Temperature affects nearly every aspect of how organisms interact with and are constrained by their environment. Measures of organismal energetics, such as metabolic rate, are highly temperature-dependent and governed through temperature effects on rates of biochemical reactions. Characterizing the relationships among levels of biological organization can lend insight into how temperature affects whole-organism function. We tested the temperature dependence of cellular oxygen consumption and its relationship to whole-animal metabolic rate in garter snakes (Thamnophis elegans). Additionally, we tested whether thermal responses were linked to shifts in the fuel source oxidized to support metabolism with the use of carbon stable isotopes. Our results demonstrate temperature dependence of metabolic rates across levels of biological organization. Cellular (basal, adenosine triphosphate-linked) and whole-animal rates of respiration increased with temperature but were not correlated within or among individuals, suggesting that variation in whole-animal metabolic rates is not due simply to variation at the cellular level, but rather other interacting factors across scales of biological organization. Counter to trends observed during fasting, elevated temperature did not alter fuel selection (i.e., natural-abundance stable carbon isotope composition in breath, δ13 Cbreath ). This consistency suggests the maintenance and oxidation of a single fuel source supporting metabolism across a broad range of metabolic demands.

Climate effects on nesting phenology in Nebraska turtles.

A frequent response of organisms to climate change is altering the timing of reproduction, and advancement of reproductive timing has been a common reaction to warming temperatures in temperate regions. We tested whether this pattern applied to two common North American turtle species over the past three decades in Nebraska, USA. The timing of nesting (either first date or average date) of the Common Snapping Turtle (Chelydra serpentina) was negatively correlated with mean December maximum temperatures of the preceding year and mean May minimum and maximum temperatures in the nesting year and positively correlated with precipitation in July of the previous year. Increased temperatures during the late winter and spring likely permit earlier emergence from hibernation, increased metabolic rates and feeding opportunities, and accelerated vitellogenesis, ovulation, and egg shelling, all of which could drive earlier nesting. However, for the Painted Turtle (Chrysemys picta), the timing of nesting was positively correlated with mean minimum temperatures in September, October, December of the previous year, February of the nesting year, and April precipitation. These results suggest warmer fall, and winter temperature may impose an increased metabolic cost to painted turtles that impedes fall vitellogenesis, and April rains may slow the completion of vitellogenesis through decreased basking opportunities. For both species, nest deposition was highly correlated with body size, and larger females nested earlier in the season. Although average annual ambient temperatures have increased over the last four decades of our overall fieldwork at our study site, spring temperatures have not yet increased, and hence, nesting phenology has not advanced at our site for Chelydra. While Chrysemys exhibited a weak trend toward later nesting, this response was likely due to increased recruitment of smaller females into the population due to nest protection and predator control (Procyon lotor) in the early 2000s. Should climate change result in an increase in spring temperatures, nesting phenology would presumably respond accordingly, conditional on body size variation within these populations.