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

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Behaviour as mitigation mechanism of heat stress As we commented above changes in behaviour is one of the animal responses to mitigate heat stress. Heat stress can be offset by active using the weather-sheltering environment provided by thermal cover, for example forest cover. Cook et al [52], using an experimental design in which elk were exposed to winter and summer conditions under different forest cover envi- ronments, demonstrated that body condition was not affected by reduced wind speed, elevated nocturnal temperature in winter, and shading from solar radiation in summer, but dense for- est cover in winter had a negative effect on deer condition, presumably because of reduction in solar radiation flux. Migratory movement is other behavioural mechanisms to mitigate heat stress. In northern populations of red deer, summer and especially winter habitats increase their suitability to deer because of reducing snow cover in climate warming scenarios [65]. Similarly, in Mediterranean environments, it should be expected a reduction in summer habi- tat suitability because of heat stress increase, under this scenario, altitudinal migration is a plausible strategy of heat stress mitigation. However, for many populations of Iberian red deer this might be a challenge. A large number of Iberian red deer of the southern Spain popula- tions live in fenced hunting estates [66] that precludes long distance and altitudinal move- ments. Besides, most of these populations are under unsustainable management that relies on

food supplementation during mid and late summer, when plants quality and availability is insufficient to maintain high densities of deer [67, 68]. Over-crowded deer populations aimed to hunting eco-tourism have a negative impact on forest renewal, which reduces natural shade availability in these populations. Though no much canopy area is necessary to provide enough shade for a large number of deer, small canopy area concentrates deer on the limited shade spots, increasing aggregation, which promotes diseases [69], and concentrates the impact of herbivory worsening plant regeneration [70]. Reduction in the density of deer in fenced hunt- ing estates could be a solution to achieve sustainable deer populations under climate warming scenarios, but whether this reduction in deer numbers could maintain these hunting estates economically profitable is arguable [71]. Iberian red deer populations from the north of Spain, which almost entirely dwell on open estates and large public grounds, are likely be in the most favourable conditions to cope with climate warming. These deer populations are harvested at sustainable rates and receive no food supplementation year round. Their densities are fitted to the natural resources available, many of them spread across mountain ranges that enable con- siderable altitudinal seasonal migration, so they can adapt their spatial movement to plant resources availability and heat stress. Behavioural response to changes in the physical environment can be fast and flexible. Our

experimental plots were fitted with water sprinklers during summer, showering under water sprinklers was an unusual behaviour in mothers and offspring, mud bathing was frequently observed in calves but less in mothers. Parker and Robbins [18] described that panting is the primary means of heat dissipation in hot environments in mule deer (Odocoileus hemionus) and elk (Cervus elaphus), however, this was not a behaviour that we observed in our experi- mental animals. The most frequent behaviour, to mitigate heat stress observed in mothers and calves in our experiment during the hottest hours of the day, was to reduce activity by lying down under shade. Studies on skin temperature in Odocoileus hemionus suggest that prefer- ence for shadow beds to avoid direct solar radiation may be instrumental to reduce thermal stress at environmental temperatures that exceeded 25˚C [72]. In desert extreme hot summer conditions, Arabian oryx (Oryx leucoryx) laid down in shade in the morning, shortly before air temperature exceeded its core body temperature (38.5˚C), and remained in shadow beds until evening, when body temperature exceeded air temperature [73]. In the same study it has been suggested that body heat accumulation (temporal higher core body temperature than mean PLOS ONE Heat stress and calf growth in red deer PLOS ONE | https://doi.org/10.1371/journal.pone.0233809 June 1, 2020 19 / 26

body temperature) could be a mechanism of water economy in desert conditions, as body cooling down by evaporation through the skin and respiratory tract requires a considerable amount of water that might compromise survival [73]. This reveals how behavioural response to heat stress can have complex physiological implications. Climate warming implications on deer body size Climatic models suggest with medium confidence that in the Northern Hemisphere the period 1983–2012 was the warmest of the last 1400 years. It is believe that this was the product of an uptake of energy by the climate system due to a positive total radiative forcing, being its largest driver an increase in atmospheric CO2 since 1750 [1]. Under different scenarios climate mod- els predict an increase in land surface temperature of 1–2˚C for the period 2046–2065, and between 1 and 3.7˚C for the period 2081–2100 [1]. This climatic pattern is projected in the form of warmer and/or fewer cold days and nights, and warmer and/or more frequent hot days and nights. A similar warming pattern has been described for the Iberian peninsula, annual mean temperature has increased in 0.10˚C/decade for the period 1850–2005, annual warming was more affected by the increase in autumn and winter temperatures than those in spring and summer, and there were higher rates of change in maximum than in minimum temperatures [74]. Implications of Iberian peninsula warming during this period and that pre- dicted on models at global scale [1], together with results of our study, suggest that body size in

red deer might have been decreasing and will continue to do so. This is, however, a very sim- plistic projection, as climate warming might act on deer body growth in different directions. For example, it has been claimed that increasing atmospheric CO2, because of human GHG emissions, promotes photosynthesis and so plant growth, which in turn increases plant bio- mass for the use of large herbivores. On the other hand, it is argued that plant growth is not constrained by atmospheric CO2 availability but nitrogen input from soil [75], which highlight the complexity of assessing how global warming might affect body size in deer. Our findings have interesting ecological implications on body size geographical clines. Bergmann´s rule establishes that in cold climates large animals benefit by having a lower sur- face area to volume ratio than smaller animals, because they radiate less heat per unit of mass and so spend less energy to maintain homeothermy, the opposite being true in warmer envi- ronments [76]. There is evidence to support this rule in endotherms [77, 78] although there are alternative explanations to this phenomenon [79, 80]. Our results suggest that heat stress in warm environments penalises body growth during lactation. If body growth is not compen- sated for later in life, this could contribute to explain an intra-specific cline in body mass increase from warm to cold environments. Our results indicate that under heat stress conditions, red deer male size is more negatively

affected than female size, whether this would have long-term adaptive consequences in body- size remains unknown, as we commented above, food and other compensatory factors might affect body size [81]. However, we could hypothesise that if warming conditions hamper male´s growth more than female´s growth, this could have implications in polygynous mating systems, which are mainly based on sexual differences in body size [82]. Among the implica- tions are (i) changes in parental investment between sexes [83], (ii) reduction of sexual differ- ences in mortality age-dependent [66], (iii) reduction in spatial sexual segregation [84], and (iv) increase in trophic niche sexual overlap [85, 86]. Implications of heat stress on deer farming Special effort in developing mechanisms to mitigate heat stress has been undertaken in dairy cattle, breeds with high metabolic rate, because heat stress has a negative effect on intake and PLOS ONE Heat stress and calf growth in red deer PLOS ONE | https://doi.org/10.1371/journal.pone.0233809 June 1, 2020 20 / 26

milk production, suppresses their immune and endocrine system, enhancing disease suscepti- bility [87]. Cooling systems based on providing shades, improving ventilation, water sprinklers and evaporation enhancers have been demonstrated to be effective in reducing breath rates by -16 up to -38 breaths/min in cows [33, 34, 35], but less clear is their effect on hormonal stress indices of chronic stress, such as triiodothyronine and cortisol [33]. A simplistic way of assessing the energy costs associated to losses in calf body mass due to heat stress, is by estimating the corresponding energy value of the milk a calf needs to produce changes in body growth associated to values of heat stress index between 0.1 and 0.9 quantiles through the first 143 days of lactation (Fig 2), which is 324 MJ, with a mean of 1126 kJ�d-1 (cal- culated using allometric equation in Robbins et al [88], Energy kcal�d-1 = 226 Wkg0.837). This is an important amount of energy to justify the application of measures to minimize heat stress in captive deer. Spiers and collaborators [58] found in dairy cattle that increasing air tempera- ture 10˚C above thermoneutral conditions (20˚C) increased rectal temperature by 1.5˚C, respi- ration rate from 60 to 90 breath min-1, and across 4 days milk yield dropped from 35 kg�d-1 to 26 kg�d-1 and dry matter intake from 24 kg�d-1 to 12 kg�d-1. Our study indicates that despite the experimental arena offering cooling opportunities they were not enough to completely offset the effects of heat stress in calf growth. The results justify

applying management measures to minimise heat stress in red deer, such as providing shades, good ventilation, baths and water sprinklers, as it is recommended in cattle dairy farms [59]. This is especially advisable in deer farms located in hot environments and where animals do not have free access to waterbodies for bathing, nor plenty of tree cover or enough ground that offers deer a variety of physical environments across which thermal stress could be minimised. Actual climatic data and projections of mean maximum temperature into 2100 in Spain (www.aemet.es) suggest that, north-west areas are those that rarely reach heat stress conditions at present and also less chance of reaching those in the future. Under this scenario it seems advisable to locate deer farms in those areas, which has the additional benefit of having some of the best grazing conditions in Spain [89], and so having to rely less on feed supplementation making deer production more sustainable. It is advisable to deer managers to consider the provision of thermal cover to reduce ther- mal stress in deer, which also depends on habitat quality and food availability [14]. Moen [90] pointed out that in fawns and does of white-tailed deer (Odocoileus virginianus) under the thermal stress conditions of his experiment, the energy balance predicted should not cause a negative balance as long as food supply was sufficient and the deer could seek shelter. Similarly, it has been highlighted in wild red deer the importance of appropriate food supply and the use

of behaviour as means to compensate for potential heat stress [91]. This highlights the impor- tance that food energy supply has when assessing the impact of heat stress on the animal’s energy budget and consequently in the animal performance. Supporting information S1 Fig. Frequency distribution of monitoring events across 143 days of lactation in the study period (2000–2018); mean: Continuous vertical line; median = dashed vertical line. (JPEG) S2 Fig. Frequency distribution of days between monitoring events across the study (2000– 2018); mean: Vertical line. (JPEG) S3 Fig. Supplementary material. Actual calf weight (kg) versus calf age (d) across the first 143 days of life in males and females of Iberian red deer. Grey triangle: male calf; magenta circle: PLOS ONE Heat stress and calf growth in red deer PLOS ONE | https://doi.org/10.1371/journal.pone.0233809 June 1, 2020 21 / 26

female calf. (JPEG) S4 Fig. Supplementary material. Response of mother body weight through lactation (from birth to forced weaning day 143) to mother age (years) and calf age (days) of the final model in Table 5, all other variables in the model fixed at their mean values. Dashed line: ± standard error. Response variable has been centred by subtraction of the mean value. (JPG) Acknowledgments Jose´ Marı´a Luja´n Go´mez attended the animals on a daily basis. David Walker, Andrew McWil- liam and two anonymous reviewers revised a version of this paper. Author Contributions Conceptualization: F. J. Pe´rez-Barberı´a. Data curation: F. J. Pe´rez-Barberı´a, J. Cappelli. Formal analysis: F. J. Pe´rez-Barberı´a. Funding acquisition: A. J. Garcı´a, T. Landete-Castillejos, M. P. Serrano, L. Gallego. Investigation: F. J. Pe´rez-Barberı´a. Methodology: F. J. Pe´rez-Barberı´a. Project administration: T. Landete-Castillejos, L. Gallego. Resources: A. J. Garcı´a, T. Landete-Castillejos, M. P. Serrano. Software: F. J. Pe´rez-Barberı´a. Supervision: F. J. Pe´rez-Barberı´a. Validation: F. J. Pe´rez-Barberı´a. Visualization: F. J. Pe´rez-Barberı´a. Writing – original draft: F. J. Pe´rez-Barberı´a. Writing – review & editing: F. J. Pe´rez-Barberı´a, T. Landete-Castillejos, M. P. Serrano. References 1. Stocker T.F., Qin D., Plattner G.K., Tignor M., Allen S.K., Boschung J., et al, 2013. Climate Change 2013: The Physical Science Basis. Cambridge University Press, Cambridge, United Kingdom. 2. Rojas-Downing M.M., Nejadhashemi A.P., Harrigan T., Woznicki S.A., 2017. Climate change and live-

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