Water deprivation compromises maternal physiology and reproductive success in a cold and wet adapted snake Vipera berus

Abstract

Droughts are becoming more intense and frequent with climate change. These extreme weather events can lead to mass mortality and reproduction failure, and therefore cause population declines. Understanding how the reproductive physiology of organisms is affected by water shortages will help clarify whether females can adjust their reproductive strategy to dry conditions or may fail to reproduce and survive. In this study, we investigated the consequences of a short period of water deprivation (2 weeks) during early pregnancy on the physiology and behaviour of a cold- and wet-adapted ectotherm (Vipera berus). We also examined water allocation to developing embryos and embryonic survival. Water-deprived females exhibited significant dehydration, physiological stress and loss of muscle mass. These effects of water deprivation on water balance and muscle loss were correlated with the number of developing embryos. While water-deprived females maintained water transfer to embryos at the expense of their own maintenance, water deprivation also led to embryonic mortality. Overall, water deprivation amplifies the reproductive costs of water allocation to support embryonic development. The deleterious impacts of water deprivation on female current reproductive performance and on potential survival and future reproduction could lead to severe population declines in this species.

Behavioural hydroregulation protects against acute effects of drought in a dry-skinned ectotherm

“…Second, dehydration should induce compensatory physiological responses to mitigate water constraints. We predict, in particular, patterns of structural muscle catabolism to release bound water (Brusch et al, 2018) and a greater thirst reaction (Dezetter et al, 2021;Dupoué et al, 2014). Third, behavioural selection of wet microclimates should mitigate these effects by reducing evaporative water loss, especially when the simulated air is drier.…”

Reproducing in a changing world: combined effects of thermal conditions by day and night and of water constraints during pregnancy in a cold‐adapted ectotherm

“…Interestingly, within temperature treatments, females in wet or dry conditions gained similar relative mass per day, suggesting that females in wet conditions either drank less or females in dry conditions were able to reduce evaporative water loss. Temperatures were imposed by climatic chambers to eliminate the possibility of behavioral thermoregulation, but differences in transcutaneous or ocular water loss rates may have occurred due to changes in behavioral hydroregulation or plasticity of the skin barrier to transepidermal water loss (Dupoué et al 2015, Refsnider et al 2019, Dezetter et al 2021).…”

“…Second, all females experienced muscle loss during the experiment and losses were highest in females in dry conditions, especially if they had limited access to preferred temperatures during the daytime. Muscle wasting during pregnancy is common in reptiles (Lourdais et al 2004, 2013, Lorioux et al 2016) and skeletal muscle has been shown to be an important substrate for the reallocation of hydric resources when demands are high and intake is limited (Brusch et al 2019, 2020, Dezetter et al 2021). Because proteins are a much lower energetic source compared to lipids and their oxidation provides five times more water (Jenni and Jenni‐Eiermann 1998), increased muscle catabolism likely supported the hydric costs of reproduction in our study.…”

“…Thus, our full models included fixed effects of day and night temperatures, water availability and all interactions, additive effects of relative body size (RBS) and fecundity, and two‐way interactions between water availability and fecundity and between water availability and RBS. These interactions were included because allocation tradeoffs between mothers and embryos may change with differences in water availability (Dezetter et al 2021). Starting with these initial models, we used stepwise removal of insignificant coefficients as recommended for null hypothesis testing in manipulative studies (Arnold 2010, Zuur et al 2010).…”

Response of farmland reptiles to agricultural intensification: Collapse of the common adder Vipera berus and the western green lizard Lacerta bilineata in a hedgerow landscape

“…The adder has several life‐history traits (limited movement, low frequency of reproduction, high costs of reproduction) that make it vulnerable to perturbation. The species is also particularly sensitive to microclimatic conditions and vulnerable to water loss (Guillon et al ., 2014; Dezetter et al ., 2021). There are important declines of adders elsewhere, notably in small isolated populations (Gardner et al ., 2019; Graitson, Barbraud, & Bonnet, 2019).…”