Seasonal Patterns of Hormones, Macroparasites, and Microparasites in Wild African Ungulates: The Interplay among Stress, Reproduction, and Disease

Abstract

Sex hormones, reproductive status, and pathogen load all affect stress. Together with stress, these factors can modulate the immune system and affect disease incidence. Thus, it is important to concurrently measure these factors, along with their seasonal fluctuations, to better understand their complex interactions. Using steroid hormone metabolites from fecal samples, we examined seasonal correlations among zebra and springbok stress, reproduction, gastrointestinal (GI) parasite infections, and anthrax infection signatures in zebra and springbok in Etosha National Park (ENP), Namibia, and found strong seasonal effects. Infection intensities of all three GI macroparasites examined (strongyle helminths, Strongyloides helminths, and Eimeria coccidia) were highest in the wet season, concurrent with the timing of anthrax outbreaks. Parasites also declined with increased acquired immune responses. We found hormonal evidence that both mares and ewes are overwhelmingly seasonal breeders in ENP, and that reproductive hormones are correlated with immunosuppression and higher susceptibility to GI parasite infections. Stress hormones largely peak in the dry season, particularly in zebra, when parasite infection intensities are lowest, and are most strongly correlated with host mid-gestation rather than with parasite infection intensity. Given the evidence that GI parasites can cause host pathology, immunomodulation, and immunosuppression, their persistence in ENP hosts without inducing chronic stress responses supports the hypothesis that hosts are tolerant of their parasites. Such tolerance would help to explain the ubiquity of these organisms in ENP herbivores, even in the face of their potential immunomodulatory trade-offs with anti-anthrax immunity.

Digging for answers: contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal

“…Thus our data provide evidence for frequency-dependent parasite transmission as would be expected in directly transmitted ectoparasites as those considered in the current study (Côté and Poulin 1995;Rifkin et al 2012;Patterson and Ruckstuhl 2013). Seasonal variation in parasite burden is an ubiqous feature of parasite populations including those of social mammals Ezenwa 2004b;Altizer et al 2006;Huffman et al 2009;Viljoen et al 2011;Cizauskas et al 2015;Klompen et al 2015;Lutermann et al 2015). Consequently, our understanding of the prevalence of density vs. frequency-dependent drivers of host-parasite interactions might be improved by considering seasonal changes in both host and parasite traits.…”

Parasites, stress and reindeer: infection with abomasal nematodes is not associated with elevated glucocorticoid levels in hair or faeces

“…Some found a positive but often context-dependent association, whereas others found no relationships at all (Fleming, 1997, 1998; Chapman et al ., 2006; Pedersen and Greives, 2008; Monello et al ., 2010; St Juliana et al ., 2014). The few studies that have looked at natural infections in ungulates showed that parasite burdens are not associated with increased faecal GC metabolite levels (Goldstein et al ., 2005; Cizauskas et al ., 2015). In fact, our results echo findings presented by Cizauskas et al .…”

“…By definition, a parasite affects its host negatively (Zelmer, 1998), and parasite infection can, as such, be considered a ‘stressor’, which we would expect to elicit a stress response. In spite of the ubiquitous presence of parasites in wildlife (Poulin, 2014) and their demonstrated influence on, and importance for, individual and population health (Irvine, 2006; Gómez and Nichols, 2013), very few studies have examined the relationship between stress and parasitism (Goldstein et al ., 2005; Chapman et al ., 2006; Monello et al ., 2010; Cizauskas et al ., 2015), and none has looked at these relationships in Rangifer .…”

Influences of the stress endocrine system on the reproductive endocrine axis in sheep (Ovis aries)

“…A stressor is a stimulus that disrupts homeostasis (Smith & Dobson 2002) and activates a variety of chemical and specific physiological processes and behavioural coping mechanisms to restore homeostasis and promote survival (Cizauskas et al 2015). Acute stress is caused by a short-term negative situation, whereby the individual is able to quickly and completely recover (Trevisi & Bertoni 2009;Papargiris et al 2011).…”