Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population

Abstract

Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.

Context‐dependent costs and benefits of tuberculosis resistance traits in a wild mammalian host

“…after 51 days of gestation (Karen et al, 2011) and has been validated in this study herd (Beechler et al, 2017). The presence of a calf at heel was detected visually or by evidence of lactation (manual milking of all four teats; Jolles et al, 2005), and calves were aged by body size and horn shape.…”

“…Conversely, if bTB force of infection is low and infection resistance mechanisms do not confer resistance to other virulent pathogens, we would expect the condition costs of infection resistance to impact long‐term reproductive rates and survival, resulting in directional selection away from this trait. Interestingly, bTB was only recently detected in the African buffalo of Kruger National Park in 1990 (Rodwell et al, ), therefore representing a “novel” pathogen and coevolutionary partner relative to other endemic pathogens in the region including Rift Valley fever (Beechler, et al, ), brucellosis (Gorsich et al, ), and schistosomes (Beechler et al, ). The high phenotypic variation observed in these resistance traits could also result from plasticity or other physiological or environmental factors not addressed in this study.…”

“…Pathogen virulence has been shown to drive the evolution and maintenance of resistance phenotypes in many wild systems (Ferrandon, 2009;Little, Shuker, Colegrave, Day, & Graham, 2010). Theory suggests that for infection resistance to evolve in a system, pathogen virulence must be high such that the costs of resisting are less than the negative fitness effects of succumbing to infection over the lifetime of the animal (Boots & Haraguchi, 1999 (Rodwell et al, 2001), therefore representing a "novel" pathogen and coevolutionary partner relative to other endemic pathogens in the region including Rift Valley fever (Beechler, et al, 2015), brucellosis (Gorsich et al, 2015), and schistosomes (Beechler et al, 2017). The high phenotypic variation observed in these resistance traits could also result from plasticity or other physiological or environmental factors not addressed in this study.…”

“…Pregnancy status and stage were determined by rectal palpation done by a wildlife veterinarian. This method shows 100% sensitivity in Egyptian buffalo ( Bos bubalis ) after 51 days of gestation (Karen et al, ) and has been validated in this study herd (Beechler et al, ). The presence of a calf at heel was detected visually or by evidence of lactation (manual milking of all four teats; Jolles et al, ), and calves were aged by body size and horn shape.…”

Why did the buffalo cross the park? Resource shortages, but not infections, drive dispersal in female African buffalo (Syncerus caffer)

“…Previous work has shown GI nematode infections in this buffalo population commonly include, Cooperia fuelleborni , Haemonchus placei , Haemonchus bedfordi , and an undescribed Parabronema species and that fecal egg counts accurately reflect GI helminth burdens (Budischak, Hoberg, Abrams, Jolles, & Ezenwa, ). A lateral flow assay to detect a specific schistosome antigen, circulating anodic antigen (CAA) in serum (Corstjens et al, ), was validated for use in buffalo (Beechler et al, ) and used to determine schistosome infection. TB was diagnosed using a whole‐blood gamma interferon assay (BOVIGAM, Prionics), optimized for African buffalo with a sensitivity of 86% and a specificity of 92% (Michel, Cooper, Jooste, Klerk, & Jolles, ).…”