Heat stress reduces growth rate of red deer calf: Climate warming implications

account for about 25% of methane emissions worldwide [1]. Heat stress on ruminants has received a great deal of attention, probably because it is the immediate animal response to changes in its thermal environment. There is a range of ambient temperatures within which an animal experiences no regulatory changes in metabolic heat production or evaporative heat loss, and it is known as thermo-neutral zone TNZ [5, 6]. TNZ condition implies an animal´s energy expenditure is at its minimum, for a specific behavioural activity and physiological state, and it varies across species and individuals. Heat stress takes place when an animal is in a physical environment above its TNZ [7, 8]. An animal responds to heat stress with adaptive mechanisms, some of them are fast responses, such as behavioural (changes in body position, activity budget, foraging), physiological (respiratory rate, core temperature, heart beating, sweating), neuro-endocrine, blood biochemical, metabolic, cellular and molecular; while other responses require long-term changes, such as morphological adaptations (size, coat insulation, changes in allometric size relations between body parts) [9]. When an animal is exposed to temperatures upper its lethal thermal maximum, even for short periods of time, adaptive mechanisms are no longer effective and the animal dies [10]. Any adaptive mechanism an ani- mal uses to acclimatise to the new thermal environment implies energy costs [11]. If the cost is such that it can be offset using body reserves, it will not affect animal´s fitness [9], otherwise,

food nutrient utilization, intake, animal production, reproduction, health and mortality will be affected by heat stress [2]. Red deer is the most widely distributed deer species in the world. Its natural range covers Europe, south western Asia and North Africa, and it has been successfully extended via intro- duction of populations to Australia, New Zealand and Argentina [12]. Red deer live under a wide range of physical environment conditions, from cold and windy exposure in mountain ranges, to hot and dry in Mediterranean habitats. Despite its good adaptation to a variety of cli- matic conditions [13], deer stresses under critical combinations of wind speed, solar radiation, air temperature and humidity [14]. There are numerous studies that have assessed the perfor- mance of ungulate populations in response to climatic variables, especially those associated with climate change [15, 16]. Less effort has been dedicated to assess short term effects of heat on individual traits in wild species, because of the logistical problems involved in collecting this data [17, 18, 8]. Red deer is an economically important species in Europe [19, 20], as it provides a sustain- able resource of meat and income via hunting and eco-tourism to economically depressed and depopulated rural areas [21]. Spain has probably the largest red deer population in Europe [19, 4], the higher numbers are concentrated in the west between 38–40˚ latitude, where maximum temperatures during the first few months of a calf´s life can reach 45˚C (www.aemet.es).

In highly polygynous species, such as the red deer, males are larger than females [22, 23]. This sexual dimorphism starts from birth and increases rapidly during the first months of life [24, 25]. Calves of the sex more expensive to produce, ie. males, are more sensitive to limita- tions in energy supply than female calves [26, 27, 28], so it is expected that under heat stress conditions males´ growth suffered more than females´ growth. Lactation in red deer hinds is energetically demanding, it can double the energy requirements of advance pregnancy [29], which might made body condition of lactating hinds more susceptible to heat stress than body condition of dry hinds. Using longitudinal data of body weight of mother and offspring during lactation in a cap- tive population of Iberian red deer, together with physical environment variables and heat stress indices, we aimed to assess if heat stress in a hot environment affects calves´ growth and mothers´ condition across lactation. The predictions are: (1) heat stress has a negative effect on calf growth rate, stronger on males, as they are energetically more expensive to produce than females; (2) mother´s body condition, expressed as body weight, decreases through PLOS ONE Heat stress and calf growth in red deer PLOS ONE | https://doi.org/10.1371/journal.pone.0233809 June 1, 2020 2 / 26 Competing interests: The authors have declared that no competing interests exist.