Thermoregulatory plasticity in free-ranging vervet monkeys (Chlorocebus pygerythrus)

Abstract

Future climate change scenarios predict that many species will be faced with natural habitats which progressively fail to meet their niche requirements. For a species to persist in a stochastic environment, it must either adapt, move to a more suitable location, or risk becoming locally extinct. For vervet monkeys and other long-lived, slowly reproducing species, phenotypic plasticity (including phenology, morphology, behaviour, and physiology) is proposed to be the first and most robust response to rapidly changing environmental conditions. It is therefore crucial to understand the degree of behavioural and physiological plasticity employed by species in their natural environments in order to better understand the impacts of future climate change on their survival. My study is the first phase of data collection for a long-term project which aims to investigate the physiological and behavioural mechanisms employed by free-ranging vervet monkeys (Chlorocebus pygerythrus) in response to environmental stress. To my knowledge, my study is the first to use miniature data loggers to obtain simultaneous and continuous measurements of body temperature and activity for a free-ranging non-human primate. Data were collected from 12 vervet monkeys over a ten month period at Samara Private Game Reserve, Eastern Cape, South Africa. Samara represents a highly seasonal environment in terms of environmental temperature and photoperiod. In winter, vervet monkeys were subjected to short day lengths (~ 10 h) and low environmental temperatures (mean ± SD 24-h minimum black-globe temperature = 2.3 ± 3.8 ºC), whereas in summer day lengths were longer (~ 14 h) and the primary thermal stressor was high environmental temperatures (mean ± SD 24-h maximum black-globe temperature = 45.2 ± 6.3 ºC). Uncharacteristically for the Nama Karoo region, Samara experienced high rainfall (450 mm) over the duration of my study period; approximately double the average annual rainfall for the region over the previous ten years. In seasonal environments such as the Nama Karoo, individuals face the challenge of maintaining body temperature within a narrow range (i.e. homeothermy) whilst exposed to a thermally dynamic environment. Maintaining homeothermy is primarily expensive in terms of body water at high environmental temperatures, and metabolic energy at low environmental temperatures. Over the duration of my study period, mean (± SD) 24-h body temperature for individual monkeys was 37.9 ± 0.1 ºC. Despite being exposed to mean 24-h variations in black-globe temperature of 30.0 °C, the mean (± SD) 24-h amplitude of body temperature rhythm exhibited by individual monkeys for the duration of my study was 2.9 ± 0.1 °C, more or less within the traditionally defined limits of homeothermy (± 2 °C). However, vervet monkeys did display significant thermoregulatory plasticity (as indexed by variations in the 24-h amplitude of the body temperature rhythm) between seasons. In summer, when the primary thermoregulatory requirement was heat dissipation at high environmental temperatures, monkeys had ad libitum access to free-standing water, relatively high food availability (as indexed using the sum of monthly rainfall as a proxy for food availability), and long day lengths. Vervet monkeys were limited to diurnal activity and thus long day lengths allowed for a flexible activity schedule over the diurnal period. Total time active over the diurnal period was negatively correlated with mean diurnal black-globe temperature (r2 = 0.26, n = 91, p < 0.0001), indicating that high environmental temperatures inhibited activity. Periods of inactivity during the diurnal period coincided with the warmest part of the day when monkeys generally sought out cooler, shady microclimates. Reduced activity and cool micro-climate selection at high environmental temperatures are common behavioural responses amongst primates, serving to reduce thermal stress and conserve body water by reducing evaporative cooling requirements. Vervet monkeys at Samara were able to effectively maintain homeothermy, largely independent of environmental temperature in summer. This is most likely achieved through a combination of autonomic (e.g. evaporative cooling) and behavioural (e.g. shade-seeking) mechanisms. Conversely, in winter, 24-h variations in body temperature of more than twice the traditionally defined limit of homeothermy (i.e. > 4 ºC) were frequently recorded for individual monkeys and the highest recorded 24-h amplitude of the body temperature rhythm was 5.6 °C. Indeed, vervet monkeys displayed a significantly larger mean 24-h amplitude of the body temperature rhythm in winter (3.2 ± 0.4 ºC) compared to summer (2.5 ± 0.1 ºC; t = 5.47, n = 6, p < 0.01). Furthermore, the ability of vervet monkeys to maintain homeothermy was significantly compromised at low environmental temperatures; reflected by the negative correlation between 24-h amplitude of the body temperature rhythm and 24-h minimum black-globe temperature (r2 = 0.58, n = 92, p < 0.0001). Due to their strictly diurnal activity scheduling, time available to complete all fundamental activities (i.e. energetic, social, and biological) was compromised by short day lengths in winter. Confounding the influence of short day lengths, the thermoregulatory challenges imposed by low environmental temperatures further reduced the time available for activity. In contrast to summer, total time active over the diurnal period was positively correlated with mean diurnal black-globe temperature (r2 = 0.32, n = 92, p < 0.0001), indicating that low environmental temperatures inhibited activity. Whilst thermoregulatory challenges at low environmental temperatures promote inactive behaviours such as sunbasking and huddling to conserve energy, the coinciding mating season likely increased the requirement for monkeys to be active in order to maintain their social hierarchy and secure mating opportunities. These conflicting requirements likely resulted in a trade-off for monkeys between maintaining homeothermy and completing fundamental activities at a time when both thermoregulatory and social requirements were high. These confounding environmental (i.e. photoperiod and temperature) and social (i.e. mating season) factors are therefore likely to infer significant energetic challenges for vervet monkeys in winter, as indexed by an increase in the 24-h amplitude of the body temperature rhythm compared to summer. After accounting for the influence of environmental temperature and photoperiod on the expression of the body temperature rhythm for vervet monkeys, I found that, over the duration of my study, periods of reduced food availability also were associated with an increase in the 24-h amplitude of the body temperature rhythm (Z = -7.71, p < 0.0001). When food availability was reduced, the energetic balance of vervet monkeys was presumably compromised by reduced food intake, so less energy was available to maintain all biological functions. The significant thermoregulatory plasticity in response to proximal environmental stressors suggests that, for vervet monkeys, maintaining strict homeothermy may be a luxury rather than a predefined norm. When environmental conditions were “good” (i.e. access to water and high food availability), monkeys were able to allocate sufficient resources towards maintaining homeothermy, which is presumably beneficial in terms of optimizing performance. In contrast, when environmental conditions were “bad” (i.e. low environmental temperatures and periods of low food availability), vervet monkeys displayed an increase in the 24-h amplitude of the body temperature rhythm. The expression of the 24-h amplitude of the body temperature rhythm may therefore provide a proxy for environmental stress experienced by an animal in its natural habitat. My study has contributed towards a better understanding of the influence of environmental stressors on the expression of vervet monkey activity and body temperature patterns. An important future line of inquiry will be to determine the energetic implications, and ultimately the fitness consequences, of observed thermoregulatory plasticity in response to environmental stressors in order to better understand the ecological implications of climate change. Due to the marked behavioural inflexibility in activity scheduling between the diurnal and nocturnal periods, it is likely that any environmental stressors which confound the influence of short day lengths in winter may impose a significant bottleneck on survival for vervet monkeys in the Nama Karoo. Low environmental temperatures and food availability are therefore likely to be the primary environmental determinants of habitat suitability for vervet monkeys and other diurnal primates living in similar seasonal habitats. As low environmental temperatures appear to pose the primary thermoregulatory challenge for vervet monkeys under conditions during my study, the predicted increase in mean environmental temperature under future climate change scenarios may actually alleviate, to a degree, the energetic requirements of thermoregulation in winter. More pertinent to the survival of vervet monkeys occupying marginal habitat such as Samara is likely to be the frequency and duration of extreme weather events (e.g. drought, heat waves, and severe cold snaps) associated with climate change.