1- Introduction

2- Materials and methods

3- Results

4- Discussion

References

Abstract

Physiological stress markers may provide valuable insight for our understanding of costs of given life-history strategies or of wildlife health condition, most importantly in case of threatened species. In the last decade, there has been growing interest in the ecological relevance of cellular oxidative stress, which would provide complimentary information to that obtained by the classic analyses of glucocorticoid hormones. In this study, we analysed the sex and species variation of five blood-based markers of oxidative status, both molecular oxidative damage and antioxidant protection, in sympatric cheetahs (Acinonyx jubatus) and leopards (Panthera pardus) living on Namibian farmlands. Both these terrestrial carnivores are classified as vulnerable by the International Union for Conservation of Nature. We found that female cheetahs had significantly higher serum reactive oxygen metabolites of non-protein origin and lower glutathione peroxidase activity in whole blood than both male and female leopards and male cheetahs. We also found that cheetahs and leopards differed in the association between the two antioxidant enzymes glutathione peroxidase and superoxide dismutase. Correlations among oxidative status markers were stronger in female cheetahs than leopards or male cheetahs. Our results suggest that female cheetahs are more sensitive to local sources of stress. Our work did not corroborate the assumption that two species with different life histories consistently differ in key physiological traits.

Introduction

Measures of physiological stress are commonly used to assess the costs of given life-history events and the health status of free-living animals. Glucocorticoids are valuable biomarkers to assess the stress response of individuals (Romero, 2004; Angelier and Wingfield, 2013; Dantzer et al., 2014) and the population health in ecological and conservation studies (Busch and Hayward, 2009; Dantzer et al., 2014). However, glucocorticoids do not provide a direct quantification of actual physiological costs (e.g., cellular damage) an organism accrues when being exposed to a stressor or demanding activity. Thus, in the last decade, there has been a burgeoning of studies that tested the connections between oxidative stress and environmental stressors or key life-history functions in free-ranging animals (reviewed in Costantini, 2014). Body functions like aerobic metabolism and activity of immune cells are responsible for the production of several reactive oxygen chemicals (e.g. free radical or non-free radical chemicals such as superoxide anion, hydrogen peroxide, hypochlorous acid or peroxynitrite). While these reactive oxygen chemicals are counteracted by the antioxidant system (enzymatic and non-enzymatic), they cause oxidation of proteins, lipids and nucleic acids (Halliwell and Gutteridge, 2015). The resulting chemical modifications of biomolecules caused by the reactive chemicals are referred as molecular oxidative damage, which is classically being used as an endpoint to estimate the oxidative stress level (Halliwell and Gutteridge, 2015). Eco- and conservation physiologists have become interested in oxidative stress, recognizing that the mechanisms needed to keep oxidative damage under control may underlie adaptability of species to environmental stressors and many life-history trade-offs (Costantini, 2008, 2014; Isaksson et al., 2011; Stier et al., 2012; Beaulieu and Costantini, 2014; Speakman et al., 2015; Alonso-Alvarez et al., 2017).

The 7000+ islands of Philippine archipelago hosts over 70 bat species belonging to seven families (Ingle and Heaney, 1992; Heaney et al., 2010) (Fig. 1). Ingle and Heaney (1992) pioneered a comprehensive assessment of bats in the Philippines and developed the first taxonomic key, which has become fundamental to most bat studies in the country. Approximately 32% bat species in the Philippines are frugivorous or nectarivorous and the remainder is predominantly insectivorous (Fig. 1). Insectivorous species include Vespertilionidae (33%, n= 26), Rhinolophidae (13%, n=10), Hipposideridae (11%, n=9), and other insectivorous species (Mollosidae (6%, n=5), Megadermatidae (1%, n=1), and Emballonuridae (4%, n=3) (Heaney et al., 2010). In terms of endemism, 35% (n=27) of species are known to be endemic to the country, with the highest described endemism in the Old-world fruit bats (Pteropodidae), with 60% endemic in the country, and often restricted to Islands or single localities. In contrast to this, insectivorous families have relatively low described endemism (12%), though this is likely due to under-description of species present and large numbers of ‘cryptic’ species i.e., the case of Hipposideros groups (Esselstyn et al., 2012; Murray et al., 2012). A high proportion of Philippine bats rely on primary forests (Heaney et al., 2006; Sedlock et al., 2008). Flying foxes (bats of the genus Acerodon and Pteropus), for example, selectively roost, and forage, in primary to secondary forests (Van Weerd et al., 2003; Mildenstein et al., 2005; Stier and Mildenstein, 2005). While, around thirty species roost in caves and underground habitats (Ingle et al., 2011; Sedlock et al., 2014). However, unprecedented environmental change poses a threat to many bat populations and their habitats (Posa et al., 2008; Wiles et al., 2010). Intensification of agriculture and other land-use changes have also meant ever-increasing pressure on native habitats. The increasing conversion of natural habitats into agricultural areas has driven extensive loss and fragmentation of natural habitats and frequently the degradation of remaining habitats in the Philippines (Carandang, 2005; Posa et al., 2008; Apan et al., 2017). Additionally, land-use change combined with climate change is projected to significantly alter species richness and range of most Southeast Asian bats in the future and have an important implication in the Philippine bat biodiversity (Hughes et al., 2012). Thus, to facilitate future conservation and management, bat research in the Philippines should clearly set its national-level priorities according to gaps and best knowledge available to provide a clear understanding of (1) species diversity, population patterns, and tolerance to varying habitat conditions (2) accurate taxonomy and systematics (3) the role of bats in providing ecosystem services, (4) effects of current environmental changes to design effective conservation measures in the future and avoid mismatch of priorities. Heaney et al. (2002) emphasized that though basic information on the diversity and distribution of Philippine mammals has been collated further information is needed to develop effective priorities and action plans (i.e., species ecology, the extent of distributional range). The most recent and comprehensive review of Philippine bats was detailed in the ‘Synopsis of the Philippine Mammals’ by Heaney et al. (1998) which was updated in 2010. In addition, Ingle et al. (2011) reviewed the status of cave bats including known roosting cave and karst ecosystems. Their reviews have provided essential information on conservation status and threats; however, the reviews largely focus the distribution of species and diversity patterns, and further reviews are needed to identify conservation gaps in Philippine bat biodiversity. The synthesis from this review aims to assess recent bat research directions in the Philippines in order to match priorities according to gaps and guide future bat research and conservation efforts in the Philippines.