BIOTROPIA Vol. 28 No. 2, 2021: 173 - 180 DOI: 10.11598/btb.2021.28.2.1296 173 ENVIRONMENTAL STRESS ON THE REPRODUCTION OF NON-HUMAN PRIMATES MASHITAH SHIKHMAIDIN*,1,2, NUR HAFIZAH MOHAMMED1 AND AHMAD ISMAIL1 1Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia 2Institute of Tropical Agriculture and Food Security (ITAFoS), Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia Received 9 January 2020/Accepted 29 May 2020 ABSTRACT This paper aims to review some highlights on the effects of environmental stresses on the non-human primate population, particularly, climate change and food limitation that may have resulted in their poor reproductive performance. The International Union for Conservation of Nature (IUCN) lists more than a third of the world’s primates as critically endangered or vulnerable. Non-human primates, which are the closest biological relatives of humans, are threatened with extinction from human activities and environmental stress. Deforestation is the main problem that intercalates with climate change. Either, indirectly or directly, those extinction factors could interrupt the physiological basis of reproduction among non-human primates. Researches on other species showed that high ambient temperature causing heat stress had harmed the reproductive performance by interfering with the hypothalamic-pituitary-gonadal axis. Therefore, the survival, conservation and sustainability of nonhuman primates growing in captivity and in the wild, require more works and researches to be done. Keywords: climate change, conservation, heat stress, primate, reproductive INTRODUCTION The non-human primate populations are increasingly endangered as they experienced warnings and threats from abrupt climate changes that slowly result in their population extinction. The Intergovernmental Panel on Climate Change (IPCC) has warned about the impacts of the escalating global temperatures. Moreover, global warming will continue even though it is not regionally uniform and the nations’ potential for adapting to this situation is limited in terms of protecting the natural systems. This situation is more complex than just rising temperature because climate change is an environmental stress causing changes in the body physiological metabolism in a short-term to long-term fight-or-flight response (Schulte 2014). The intense increases in humidity and ambient temperature had resulted in animals and plants being exposed to adverse circumstances that threaten their survival, and ultimately, their biodiversity. Climate change would directly or indirectly cause reduction and shifting of wildlife populations and habitats, including the non- human primates, thereby eventually inhibiting the survivability and sustainability of the species. Most primates are widely distributed throughout the tropical and subtropical regions of Africa, America and Asia. The majority of primates live in tropical areas that are rainfed and rain forested (Reed & Fleagle 1995), but they also exist in tropical dry forests, mangrove vegetation above high-tide levels, savannas, grasslands, inland wetlands and rocky areas (Mittermeier et al. 2013). Habitat for this group of animals is widespread but some of the areas are no longer able to accommodate these primates’ populations, as the areas have been mostly disturbed by human activities. About 80% of the Malaysian rainforests are degraded *Corresponding author, email: mashitah@upm.edu.my BIOTROPIA Vol. 28 No. 2, 2021 174 by logging and largely covered with oil palm plantations (Sophie 2013). Logging had threatened the biodiversity of those areas, including the nonhuman primate populations. Deforestation is also a result of human overpopulation happening in some places in the African and Asian countries. The populations of nonhuman primates are disturbed by human population growth, economic expansion and other human activities, such as those in the agricultural industry. The significant thermal impact that obviously elevated the effects of climate change has led to phenological changes in the wildlife habitats. Extreme irregularities in phenological events have also resulted in shifting food sources that has changed many natural cycles of pollinators and plants, predators and prey, and of primate and their food sources (Visser 2008; Both et al. 2009; Butt et al. 2015). All these disturbance factors threatening the nonhuman primate species have forced them to move out of their habitat range to get clean water, food, and to raise their offspring. These external factors, such as climate change, demanded an adaptive response from the animals to a new environment (Altmann et al. 2002; Beehner et al. 2006a; Estrada et al. 2017; Fairbanks et al. 2011). The critical challenge facing the global population of nonhuman primates is therefore, survival or extinction, because as animals lose the ability to control their environment (for examples, habitats lost and climate change), their physiological structure ultimately change. Moreover, it could cause adverse effects on their reproduction and development. This paper briefly reviews and discusses the impact of physical disturbances such as feed restriction and climate change on the reproductive physiology as these factors slowly create stress affecting reproduction and eventually, the survival of the nonhuman primates. REVIEW Does Climate Change Affect the Reproductive Performance of Nonhuman Primates? In the last few decades, the effects of environmental stress to animals, mainly climate change, has become a major concern. However, still sparse works are done on the sustainability of wildlife, particularly the nonhuman primates, in this complex stress phenomenon. Many researches showed that continuous increase of the ambient temperature resulting in heat stress had significantly affected the reproductive physiology of animals, including nonhuman primates (Beehner et al. 2006ab; Sharpe, 2010; Rylander et al. 2013; Wang et al. 2014). An acute increase of ambient temperature generally affect the breeding patterns of animals through physiological changes in the brain, the center of the nervous system. Studies among livestock animals showed that extremely high temperatures strongly affected the hypothalamic-pituitary-gonadal axis (Shelton & Huston 1968; Wolfenson et al. 2000; Santolaria et al. 2014). These deleterious effects of heat stress could lead to disruptions in the reproductive performance of nonhuman primates. About 419 primate species, such as lemurs, lorises, tarsiers, monkeys and apes, would experience 10% more warming than the global average (Taylor 2016). Meanwhile, some primates would experience increases of more than 1.5 oC in annual average temperature for every degree in global warming. Therefore, primates that show high sensitivity to little changes on ambient temperature could experience more intense effects in their reproduction as compared to other primates. The consequence of climate change on the reproductive performance of nonhuman primates not only occurs in females but also in males. A 43 ˚C heat stress of about 30 minutes could induce apoptosis of germ cells in the testis of Macaca fascicularis, a non-human primate, (Zhang et al. 2005). This situation was described in studies where suppression of testicular function under heat stress had led to a decrease in fertility in ruminants (Hamilton et al. 2016), and humans (Garolla et al. 2013; Rao et al. 2015). Those testis exposed to high ambient temperature could constantly effect the DNA fragmentation of sperms; thus, reduces the quality of sperms. An elevated surrounding temperature causing a rise in testicular temperature result in a reduction in sperm output, low sperm motility and an increase of morphologically abnormal spermatozoa (Hansen 2009). Germ cell depletion and increase in DNA damage are induced by heat stress (Lue et al. Environmental stress on reproduction of nonhuman primates – ShikhMaidin et al. 175 1999; Paul et al. 2008). Oxidative stress clearly disturbs the functionality of sperm and leads to sperm damage, deformity, and eventually, male infertility (Halliwell & Gutteridge 2007; Mahfouz et al. 2010). Animals vulnerable to environmental changes, particularly heat stress, also exhibited changes in their mating behavior (Deutsch et al. 2008; McFarland et al. 2014). In female, heat stress had significant adverse effects on the reproductive performance particularly, delayed estrus cycle, lower embryo survivability, slow fetus development and early pregnancy abortion (Beehner et al. 2006b; Hansen 2009; Wiederholt et al. 2011). Documented information on the effects of these environmental stressors towards reproduction patterns of the female and male nonhuman primates is still sparse. Hence more studies are needed on understanding the impact of heat stress or climate change particularly on reproductive-physiology and reproductive behavior. Identifying anthropogenic stressors on nonhuman primates is also essential for conservation planning and management of these primates (Graham et al. 2016). Importance of Nutrition and Reproduction The overall functions of the reproductive system are largely controlled by the hormonal interactions of the hypothalamic-pituitary- ovarian axis, but the final output also depends on extrinsic factors such as nutrition. The diet that is easily digested and rich in fibre, carbohydrates and lipid from fruits, leaves, buds and insects, constitute an immense food source for most nonhuman primates (Strier 2007; Lambert 2010; Moges et al. 2014; Kassim et al. 2017). However, habitat fragmentation and climate change could harm food availability. Captive orangutans fed with high-quality feeds have shorter inter-birth intervals as compared to wild orangutans (Kuze et al. 2012). Therefore, with a good quality food sources, the orangutan population will result in an increased reproductive performance and eventually increased population density. Food availability and nutritional composition are also important to the population density of nonhuman primates (Hanya & Chapman 2013). Two factors that contribute to pregnancy failure in females are the inadequate food intake and increased energy expenditure. It is important for pregnant females to meet the basic metabolic requirements mainly during early pregnancy to avoid negative energy balance. Studies done on the nutritional status and reproduction of laboratory and livestock animals recorded that underfed animals experienced delayed puberty period, decreased embryo survival rate, suppressed spermatogenesis and reduced number of sperm motility. Moreover, females that were deprived of food or underfed were less fertile and this reduces the chances of fertilisation; thus, affecting the population birth rate and eventually causing a decrease in population. This probably occurs severely among subordinate females of a nonhuman primate. Dominant females of marmoset monkey produced more offsprings as compared to subordinate females in a healthy environment (Abbot 1987). In the physiological level, dominant females can defeat the reproductive performance of subordinate females. The impact of a threatening activity, such as forest abuse, can damage the individual survival of nonhuman primate species, decrease fertility, and will shrink the population through time. Climate disaster also leads to the extinction of plants and animals. A study on wild baboons documented that pregnancy failure was high if the females conceived after the drought (Beehner et al. 2006b). During the 1990s, the decline in the orangutan population by at least 30% of its total population was caused by fires and drought in the Bornean forests (Gould et al. 1999). In addition, wildfires in Mexico also affected the nonhuman primates, whereby the habitats of New World monkeys were destroyed by drought and El Nino. Reduction of food availability as a result of El Nino event caused the population size reduction of atelines one year after the event (Wiederholt & Post 2010). Extreme temperatures can decrease the food production and drinking water availability of the existing nonhuman primates. High ambient temperature could decrease the concentration of fibre and protein contents of leaves due to high atmospheric carbon dioxide. In addition, a rising level of heat and carbon dioxide could make the leaf or green resources less nutritious (Gray & Brady 2016) and could also affect the plant physiology resulting in changes in the number and size of leaves (Taylor et al. 2003; Dermody et BIOTROPIA Vol. 28 No. 2, 2021 176 al. 2006). Higher temperatures also increased the plant matter toxicity resulting in reduced leaf sizes (Moore et al. 2015). Decreasing food source could also increase the competition within the population. In the long run, this indirect effect might impact the evolutionary and ecological processes of a certain population. Obviously, several factors contribute to food limitation in nonhuman primate habitats, such as forest exploitation, forest clearing for agriculture and climate change. As mentioned earlier, nutritional restriction can interrupt the breeding pattern, fertility, puberty development, embryo growth and development, and can increase susceptibility to disease and predation, intensify mortality of infants and mothers, and can delay reproductive maturity to a much later age (Korstjens & Hillyer 2016; Chaves et al. 2019; Laver et al. 2020). The synchronization of reproductive events of primate to fit the availability of the resources was also affected (Van Schaik et al. 1993; Post 2013). Climate change occuring in the African regions has cause significant changes in fruit production, as it was lower between 1988 and 1993 than between 1994 and 2003 (Erhart and Overdorff 2008). This event negatively affected the red-fronted lemurs (Eulemur fulvus rufus), specifically their reproductive patterns, sex ratio, group sizes and population density. Early embryo wastage, one of the key factors towards species extinction, is a particularly critical issue for nonhuman primates,. The nonhuman primates in captive management may need to refine the feed intake that would satisfy the dietary needs and take into account to have an optimal reproductive functions. Reproductive and Stress Hormones on Reproduction It is well-known that progesterone is the main reproductive hormone that is essential to maintain pregnancy in animals, including in nonhuman primates and humans. Meanwhile, testosterone is important in mating behaviour and confounded with dominance rank in male primates (Dixson 1998; Wallen & Zehr 2004). Expressions of reproductive hormones depend on maternal responsiveness with the environments and differ between young and experienced female primates (Rangel‐Negrín et al. 2009; Saltzman & Maestripieri 2011). The understanding of neuroendocrine and primate maternal behaviour has increased, but of the physiology mechanism underlying the effects is still limited. During early pregnancy in nonhuman primates, progesterone secretion is solely from corpus luteum and it is replaced by the placenta during mid-pregnancy (Beehner et al. 2006a). An in vitro study on Macaque recorded the direct actions of progesterone and oestradiol on primate pre-antral follicle development (Ting et al. 2015). Androgens appeared to be a survival factor but hindered antral follicle differentiation; oestradiol appeared to be a survival and growth factor at the pre-antral and early antral stages, whereas progesterone may not be essential during early folliculogenesis in primates. Macaque and baboon are nonhuman primate models used for studies related to human reproductive health, such as contraception, reproductive aging, infertility, ovarian function, and reproductive tract disorder (Wandji et al. 1997; D'Hooghe et al. 2004; Ting et al. 2015). Maternal stress during pregnancy that is controlled by the hypothalamus–pituitary– adrenal (HPA) axes could produce disruptive effects on embryo and fetal growth and development (Del Giudice 2012; Laver et al. 2020). Among wild baboons, food limitation due to drought contributed to fetal loss in the Amboseli population (Beehner et al. 2006b). A study on orangutans in Southeast Asian tropical forests showed that solitary lifestyle is relative to late weaning which is a consequence of their ecological environment (Vogel et al. 2015). Faecal glucocorticoid (fGC) is a survival probability indicator of many nonhuman primates, such as ring-tailed lemurs and red- bellied lemurs. It shows high mortality rate due to habitat degradation that would cause reduction in fruit availability (Pride 2005; Tecot 2013; Balestri et al. 2014). The non-invasive technique was used to measure reproductive hormones and cortisol through urine and faeces during a normal reproductive cycle (Rangel-Negrín et al. 2009). Chaves et al. (2019) used non-invasive biomarkers, fecal glucocorticoid metabolites to assess the physiological stress of adult wild brown howlers and the food availability in Brazilian Atlantic Forest fragments, and found Environmental stress on reproduction of nonhuman primates – ShikhMaidin et al. 177 that nursing females are highly nutrition demanding for their pregnancy and lactation It shows that hormones obsess and affect the appetite throughout pregnancy, explaining the consistent association between undernutrition and reproductive failure. Studies on brain activity via hypothalamic-pituitary-ovarian axis and stress hormones on embryo and fetal losses are still scarce. We suggest that researches need to focus on this because as observed, maternal hormonal patterns and external factors are important in sustaining embryo survivability. CONCLUSION AND FUTURE PERSPECTIVES This article has focused on how environmental stress, mainly climate change and poor dietary intake, can lead to reproductive stress and failure among nonhuman primates. These factors, known to be either directly or indirectly link to the hypothalamic-ovarian axis, harm the reproductive sites. Furthermore, the anthropogenic stressors on primate populations also contribute towards species extinctions, particularly in animals with slow reproductive rates. All these factors are closely related to the extinction of this vulnerable species. Primates are a flagship species for entire ecosystems, so its conservation also present important consequences for many other species. The success of its conservation and preservation programs are dependent on the ability of the species to reproduce successfully and to minimize offspring loss. Thus, important information on the fitness and success of its reproduction provides an understanding of the physiological-environment interactions of the nonhuman primates reproduction. Moreover, the successful reproduction is fundamental to the survival and evolution of all species. Hence, further studies are needed to understand the impact of environmental stress on their physiological changes mainly the reproductive performance and endocrine reproduction of nonhuman primates. It would probably help researchers or governments to properly manage this species by investing on resources to safeguard the animals from the threats of habitat destruction, and, to monitor their reproductive performance through hormonal control for sustainable primate populations. ACKNOWLEDGEMENTS The authors would like to thank the Reprophysio Team from the Department of Biology, Faculty of Science, Universiti Putra Malaysia and Putra Grant GP/2018/9619600 for generously supporting this publication. REFERENCES Abbott DH. 1987. Behaviourally mediated suppression of reproduction in female primates. J Zool 213:455- 70. Altmann J, Alberts SC, Altmann SA, Roy SB. 2002. Dramatic change in local climate patterns in the Amboseli Basin, Kenya. Afr J Ecol 40:248-51. Balestri M, Barresi M, Campera M, Serra V, Ramanamanjato JB, Heistermann M, Donati G. 2014. Habitat degradation and seasonality affect physiological stress levels of Eulemur collaris in littoral forest fragments. PloS one 9(9): e107698. Beehner JC, Nguyen N, Wango EO, Alberts SC, Altmann J. 2006a. The endocrinology of pregnancy and fetal loss in Wild Baboons. Horm Behav 49(5):688-99. Beehner JC, Onderdonk DA, Alberts SC, Altmann J. 2006b. The ecology of conception and pregnancy failure in Wild Baboons. Behav Ecol 17(5):741-50. Both C, Van Asch M, Bijlsma RG, Van Den Burg AB, Visser ME. 2009. Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?. J Ani Ecol 78(1):73-83. Butt N, Seabrook L, Maron M, Law BS, Dawson TP, Syktus J, McAlpine CA. 2015. Cascading effects of climate extremes on vertebrate fauna through changes to low‐latitude tree flowering and fruiting phenology. Glob Chang Biol 21(9):3267-77. Chaves ÓM, Fernandes FA, Oliveira GT, Bicca-Marques JC. 2019. Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic forest fragments. Sci Total Environ 690:705-16. Del Giudice M. 2012. Fetal programming by maternal stress: Insights from a conflict perspective. Psychoneuroendocrinology 37(10):1614-29. Dermody O, Long SP, DeLucia EH. 2006. How does elevated CO2 or ozone affect the leaf‐area index of soybean when applied independently?. New Phytol 169(1):145-55. BIOTROPIA Vol. 28 No. 2, 2021 178 Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. In: Proc Natl Acad Sci USA. 105(18):6668-72. D'Hooghe TM, Mwenda JM, Hill JA. 2004. A critical review of the use and application of the baboon as a model for research in women's reproductive health. Gynecol Obstet Invest 57(1):1-60. Dixson A. 1998. The international encyclopedia of human sexuality: Primate sexuality. NY(US): John Wiley & Sons, Ltd. p.861-1042. Erhart EM, Overdorff DJ. 2008. Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists 136(2):183-93. Estrada A, Garber PA, Rylands AB, Roos C, Fernandez- Duque E, Di Fiore A, … , Li B. 2017. Impending extinction crisis of the world’s primates: Why primates matter. Sci Adv 3(1): e1600946. Fairbanks LA, Bailey JN, Breidenthal SE, Laudenslager ML, Kaplan JR, Jorgensen MJ. 2011. Environmental stress alters genetic regulation of novelty seeking in Vervet monkeys. Genes Brain Behav 10(6):683-8. Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, Foresta C. 2013. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod 28(4):877-85. Gould L, Sussman RW, Sauther ML. 1999. Natural disasters and primate populations: the effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in southwestern Madagascar. Int J Primatol 20(1):69-84. Graham TL, Matthews HD, Turner SE. 2016. A global- scale evaluation of primate exposure and vulnerability to climate change. Int J Primatol 37(2):158-74. Gray SB, Brady SM. 2016. Plant developmental responses to climate change. Dev Biol 419(1):64-77. Halliwell B, Gutteridge JMC. 2007. Cellular responses to oxidative stress: adaptation, damage, repair, senescence and death. Free Radical Bio Med 4: 187-267. Hamilton TRDS, Mendes CM, Castro LSD, Assis PMD, Siqueira AFP, Delgado JDC, … , Visintin JA. 2016. Evaluation of lasting effects of heat stress on sperm profile and oxidative status of ram semen and epididymal sperm. Oxid Med Cell Longev:1- 12. Hanya G, Chapman CA. 2013. Linking feeding ecology and population abundance: A review of food resource limitation on primates. Ecol Res 28(2): 183-90. Hansen PJ. 2009. Effects of heat stress on mammalian reproduction. Philosophical Transactions of the Royal Society B: Biological Sciences 364(1534): 3341-50. Kassim N, Hambali K, Amir A. 2017. Nutritional composition of fruits selected by long-tailed macaques (Macaca fascicularis) in Kuala Selangor, Malaysia. Trop Life Sci Res 28(1):91. Kamilar JM, Beaudrot L. 2018. Effects of environmental stress on primate populations. Annu Re Anthropol 47:417-34. Kuze N, Dellatore D, Banes GL, Pratje P, Tajima T, Russon AE. 2012. Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval. Primates 53(2): 181-92. Korstjens AH, Hillyer AP. 2016. Primates and climate change: A review of current knowledge. In: An Introduction to Primate Conservation. Oxford (GB): Oxford University Press. p. 175-92. Lambert JE. 2010. Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. Primates in perspective. Oxford (GB): Oxford University Press. Laver PN, Ganswindt A, Ganswindt SB, Alexander KA. 2020. Effect of food limitation and reproductive activity on fecal glucocorticoid metabolite levels in banded mongooses. BMC Ecol 20(1):1-24. Lue YH, Sinha Hikim AP, Swerdloff RS, Im P, Taing KS, Bui T, Leung A, Wang C. 1999. Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinol 140(4):1709-17. Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A. 2010. Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril 94(6):2141-6. McFarland R, Barrett L, Boner R, Freeman NJ, Henzi SP. 2014. Behavioral flexibility of Vervet monkeys in response to climatic and social variability. Am J Phys Anthropol 154(3):357-64. Mittermeier RA, Wilson DE, Rylands AB. 2013. Handbook of the mammals of the world: primates. Lynx Edicions. Moges E, Balakrishnan M. 2014. Nutritional composition of food plants of geladas (Theropithecus gelada) in Guassa Community Protected Area, Ethiopia. J Biol Agri Healthc 4(23):38-44. Moore BD, Wiggins NL, Marsh KJ, Dearing MD, Foley WJ. 2015. Translating physiological signals to changes in feeding behaviour in mammals and the future effects of global climate change. Anim Prod Sci 55(3):272-83. Environmental stress on reproduction of nonhuman primates – ShikhMaidin et al. 179 Paul C, Murray AA, Spears N, Saunders PT. 2008. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reprod 136(1):73-84. Post E. 2013. Ecology of climate change: the importance of biotic interactions (Vol. 68). Princeton (US): Princeton University Press. Pride ER. 2005. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol Lett 1:60–3. Rangel‐Negrín A, Alfaro JL, Valdez RA, Romano MC, Serio‐Silva JC. 2009. Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild and captive populations. Ani Conserv 12(5):496-502. Rao M, Zhao XL, Yang J, Hu SF, Lei H, Xia W, Zhu CH. 2015. Effect of transient scrotal hyperthermia on sperm parameters, seminal plasma biochemical markers, and oxidative stress in men. Asian J Androl 17(4):668. Reed K, Fleagle J. 1995. Geographic and climatic control of primate diversity. Proc Natl Acad Sci USA. 92(17):7874-6. Rylander C, Odland JØ, Sandanger TM. 2013. Climate change and the potential effects on maternal and pregnancy outcomes: an assessment of the most vulnerable – the mother, fetus, and newborn child. Global Health Action 6(1):19538. Saltzman W, Maestripieri D. 2011. The neuroendocrinology of primate maternal behavior. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35(5):1192-204. Santolaria P, Yániz J, Fantova E, Vicente-Fiel S. Palacín I. 2014. Climate factors affecting fertility after cervical insemination during the first months of the breeding season in Rasa Aragonesa ewes. Int J Biometeorol 58(7):1651-5. Schulte PM. 2014. What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217(1):23-34. Sharpe RM. 2010. Review: Environmental/lifestyle effects on spermatogenesis. Philosophical Transactions of Royal Society B 365:1697-712. Shelton M. Huston JE. 1968. Effects of high temperature stress during gestation on certain aspects of reproduction in the ewe. J Anim Sci 27(1):153-8. Sophie Y. 2013. 80% of Malaysian Borneo’s rainforests destroyed by logging. Climate Home News Ltd. In press Strier K. 2007. Primate Behavioral Ecology (3rd ed.). Boston (US): Allyn & Bacon. Taylor A. 2016. Press: Impact of Climate Change on Primates. Taylor G, Tricker PJ, Zhang FZ, Alston VJ, Miglietta F, Kuzminsky E. 2003. Spatial and temporal effects of free-air CO2 enrichment (POPFACE) on leaf growth, cell expansion, and cell production in a closed canopy of poplar. Plant Physiol 131(1):177- 85. Tecot SR. 2013. Variable energetic strategies in disturbed and undisturbed rain forest: Eulemur rubiventer fecal cortisol levels in South-Eastern Madagascar. In: Masters J, Gamba M, Génin F, eds. Leaping Ahead: Advances in Prosimian Biology. NY (US): Springer. p. 185-95. Ting AY, Xu J, Stouffer RL. 2015. Differential effects of estrogen and progesterone on development of primate secondary follicles in a steroid-depleted milieu in vitro. Hum Reprod 30(8):1907-17. Van Schaik CP, Terborgh JW, Wright SJ. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24(1):353-77. Visser ME. 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc Biol Sci 275(1635):649-59. Vogel ER, Harrison ME, Zulfa A, Bransford TD, Alavi SE, Husson S, … , Farida WR. 2015. Nutritional differences between two orangutan habitats: Implications for population density. PloS One 10(10): e0138612. Wallen K, Zehr JL. 2004. Hormones and history: The evolution and development of primate female sexuality. J Sex Res 41(1):101-12. Wandji SA, Srsen V, Nathanielsz PW, Eppig JJ, Fortune JE. 1997. Initiation of growth of baboon primordial follicles in vitro. Hum Reprod 12(9):1993-2001. Wang, H., Wang, B., Normoyle, K.P., Jackson, K., Spitler, K., Sharrock, M.F., Miller, C.M., Best, C., Llano, D. and Du, R., 2014. Brain temperature and its fundamental properties: a review for clinical neuroscientists. Front Neurosci 8:307. Wiederholt R, Post E. 2011. Birth seasonality and offspring production in threatened neotropical primates related to climate. Glob Chang Biol 17(10):3035-45. Wiederholt R, Post E. 2010. Tropical warming and the dynamics of endangered primates. Biol Lett 6(2): 257-60. Wolfenson D, Roth Z, Meidan R. 2000. Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim Reprod Sci 60:535-47. Zhang XS, Lue YH, Guo SH, Yuan JX, Hu ZY, Han CS, Hikim AP, Swerdloff RS, Wang C, Liu YX. 2005. Expression of HSP105 and HSP60 during germ cell apoptosis in the heat-treated testes of adult cynomolgus monkeys (Macaca fascicularis). Front Biosci 10(1):3110-21. BIOTROPIA Vol. 28 No. 2, 2021 180