Is nocturnal activity compensatory in chamois? A study of activity in a cathemeral ungulate

Abstract

Different species exhibit individual daily and annual activity patterns in response to a range of intrinsic and extrinsic drivers. Historically, research on the activity budgets of large wild animals focused on daylight hours due to the logistical difficulties of observing animals at night. Thanks to recent advances in animal-attached technology, however, this research can be extended to a 24-h timeframe. Taking advantage of GPS collars with activity sensors collecting a large amount of data per hour, we separately studied diurnal and nocturnal activity patterns of Alpine chamois (Rupicapra rupicapra), in order to identify the factors affecting them and the correlation between them. From March 2010 to November 2013, we collected data on 17 chamois in the Swiss National Park, a strict Alpine nature reserve where human management was forbidden and human harassment quite rare. Environmental factors were found to significantly influence both diurnal and nocturnal activity rhythms, with temperature and seasonality playing a pivotal role. Surprisingly, we detected a stable peak of activity in the first part of the night, which varied only slightly over the year. In summer, the nocturnal activity of males was inversely correlated to diurnal activity, arguably to compensate for scarce diurnal food intake. Conversely, winter nocturnal activity was positively related to the diurnal activity and served as a cumulative opportunity for energy intake. Chamois showed a weak lunarphilia, with a slight increase in activity levels during moonlit nights, especially during the mating season. In conclusion, our findings denote chamois as a cathemeral species able to adapt its behavioural patterns to match varying environmental conditions.

Introduction

Several animal species exhibit distinct activity rhythms in response to a plethora of intrinsic and extrinsic drivers. The majority of mammal species are nocturnal (Bennie et al., 2014): nocturnal activity is, in fact, considered the ancestral pattern of mammals (Crompton et al., 1978; Heesy and Hall, 2010) having evolved during the Mesozoic era, when eutherian mammals avoided diurnal activity to escape from the dominant taxon of dinosaurs (nocturnal bottleneck hypothesis – Menaker et al., 1997). Thus, one would expect that nocturnal activity would still play an important role, even in species that are not considered strictly nocturnal. As such, it is paramount to study activity budgets throughout the 24 h to understand the relationship between diurnal and nocturnal activities, and how both respond to environmental factors.

Nowadays, human disturbance and the energy balance aimed at avoiding heat stress in an increasingly warm environment are key additional factors affecting activity rhythms: understanding their effects on the distribution of activity between day and night is a new challenge for researchers. Indeed, several wild species have been found to react strongly to human recreational activities, including hunting, by modifying their diurnal activity rhythms and shifting their activity to night hours (Brivio et al., 2017; Enggist-Düblin and Ingold, 2003; Oberosler et al., 2017; Raveh et al., 2012). Research into the effect of global warming on the distribution of activity has only recently been undertaken (Mason et al., 2017). The heat dissipation limit theory predicts that the trade-offs in energy allocation in endothermic organisms are driven more by the animals’ ability to dissipate heat and avoid hyperthermia than by their ability to harvest energy (Speakman and Król, 2010). Since activity (i.e., locomotion and forage intake) entails energy expenditure and increases metabolic heat production (Long et al., 2014), its reduction during the hottest hours may be a strategy to avoid hyperthermia. Indeed, several studies showed that animals reduce activity levels in response to increasing air temperature, so as to buffer themselves from overheating (e.g. Orthoptera: Chappell, 1983; Parker, 1982 – Rodentia: Belovsky, 1984a; Kilpatrick, 2003 – Lafomorpha: Belovsky, 1984b – Cetartiodactyla: Brivio et al., 2017, 2016; Owen-Smith, 1998; Shi et al., 2006 – see Terrien et al., 2011 for a review on this topic). Moreover, animal behaviour and physiology are commonly characterised by seasonal variations, which have evolved as adaptation to match variations in resource availability, and thus maximise resource uptake and individual fitness (Prendergast et al., 2002). In this framework, it might be hypothesised that, during the warmer seasons, heat-sensitive species should modify their distribution of activity in favour of the nocturnal activity to compensate for the reduced energy intake during the warmest part of the day.

Mammals are usually classified as diurnal, nocturnal or crepuscular species based on anecdotal information. Research has only started taking into account the concept of cathemeral species in recent years (Hetem et al., 2012; Tattersall, 2006; Wu et al., 2018). The term “cathemerality” was defined for primates: it describes activity patterns distributed almost evenly throughout the 24 h of the daily cycle, or patterns with significant amounts of activity occurring within both the nocturnal and the diurnal periods (Tattersall, 2006, 1987). Curtis and Rasmussen (2006) expanded the concept of cathemerality to include the transfer of activity between diurnal and nocturnal periods, or viceversa, in response to chrono-ecological factors (temperature, moonlight, competition for resources, predation-risk). In this regard, analyses of the activity rhythms of the most widespread large herbivores suggested that they may potentially adopt cathemeral patterns, modifying the periodicity of their activity rhythms. For instance, wild boar (Sus scrofa), one of the most widespread ungulates in Europe, was reported by different studies to be, in turn, monophasic, biphasic and polyphasic (Brivio et al., 2017; Caley, 1997; Keuling et al., 2008; Russo et al., 1997), likely because this species may switch from predominantly diurnal to predominantly nocturnal activity in response to anthropogenic disturbance (Keuling et al., 2008; Ohashi et al., 2013; Podgórski et al., 2013). Similarly, chamois (Rupicapra rupicapra), the most ubiquitous ungulate in the Alps (Apollonio et al., 2010), has been defined as a diurnal species with unimodal (Šprem et al., 2015) or bimodal patterns (Darmon et al., 2014; Mason et al., 2014; Pachlatko and Nievergelt, 1985), even though others found it to be active also at night (Carnevali et al., 2016; Ingold et al., 1998). More recently, Brivio et al. (2016) showed that the daily activity of chamois was mainly diurnal and the pattern changed during the year from unimodal to bimodal and trimodal. Overall, these studies suggested that these species may modify their distribution of the activity across diurnal and nocturnal periods. Cathemerality may be a worthwhile strategy through which animals can respond to environmental drivers – i.e. thermal stressors, intense precipitation, moon cycle, and human harassment – by increasing nocturnal activity in order to compensate for the forced inactivity during the daylight period. If we exclude research on primates, however, studies on this topic are very rare. The Arabian oryx (Oryx leucoryx) has been shown to re-schedule its daily activity pattern in response to extreme environmental temperatures (Hetem et al., 2012). Similarly, Jetz et al. (2003) showed that nocturnal birds (nightjars: Macrodipteryx longipennis and Caprimulgus climacurus) increased twilight foraging activity during moonlit nights to compensate for the shorter nocturnal foraging window. In general for large mammals, the effect of moonlight on activity budgets has been mainly analysed in terms of predation risk and foraging efficiency, for prey and predator species, respectively. Additionally, moonlight could have opposing potential effects on activity. On the one hand, moonlight is expected to have a suppressive effect on the activity levels of primary consumers feeding in open areas, since the risk of detection by predators is higher during the brightest moonlit nights (Prugh and Golden, 2014). On the other hand, moonlight is expected to increase foraging efficiency and detection of predators and thus to have a positive effect on prey activity (Prugh and Golden, 2014).

We analysed chamois activity records collected in a strict nature reserve in the Swiss Alps, where predation is negligible, hunting is forbidden and any human management and harassment are avoided. Most significantly, predation risk and human disturbance in the selected study area are likely the lowest across the whole of this species’ range and we can therefore exclude a major role of predation on chamois activity rhythms. In this context, we tested whether chamois are a cathemeral species or not, and whether their activity patterns are affected by ecological factors, or driven mainly by their internal timing system. In this framework, we formulated the following predictions:

• Since predation risk is low in our study area, we predicted that most of chamois activity would be carried out during the day and, consequently, only diurnal activity would be affected by extrinsic factors. Therefore, we separately analysed the effects of environmental factors on diurnal mean activity (DMA) and nocturnal mean activity (NMA). We expected significant effects only on DMA.

• Conversely, we hypothesised that nocturnal activity played a compensatory role for the forced inactivity during the daylight period. Specifically, we predicted that:

  • NMA would be affected by the amount of DMA more than by external factors;

  • this effect would be more relevant during the more energy-demanding periods, i.e. summer, winter, and mating season;

  • there would be no periodicity in the distribution of acrophase – i.e., the time when the rhythm peaks – of the nocturnal activity throughout the year.

• Given our hypothesis of the compensatory role of nocturnal activity and taking into account the low levels of predation risk and human harassment in our study area, we predicted a positive effect of moonlight on NMA throughout the year, particularly during summer (when increasing forage intake allows chamois to prepare for winter), and during the mating season to increase the reproductive opportunities.