Coccidial oocyst release: once a day or all day long? Tropical bird hosts shed new light on the adaptive significance of diurnal periodicity in parasite output

Abstract

Many parasites spend part of their life cycle as infectious forms released from an infected host in the external environment, where they may encounter and infect new hosts. The emergence of infectious life stages often occurs once a day to minimize mortality in adverse environments. In bird hosts, intestinal parasites such as coccidia are generally released with feces in the late afternoon. This dynamic is adaptive since it allows avoiding desiccation and ultraviolet (UV) radiation, thus reducing mortality of oocysts in the environment until transmission to the next host. If this circadian rhythm is the result of natural selection to increase oocyst survival, we may hypothesize that oocysts will appear in feces at different times depending on the environment where hosts live. Particularly, in an environment where UV radiation and desiccation are very low, we may expect oocyst circadian release to disappear since the main selective pressure would be relaxed. We sampled different species of birds in tropical and temperate forests in spring and investigated coccidian oocyst output. A strong circadian variation in the prevalence of hosts shedding coccidian oocyst was detected for species caught in the temperate forest with an increase in prevalence in the late afternoon, whereas prevalence of birds shedding oocysts was constant over the course of the day for most species sampled in the tropical rain forest. These results are consistent with the hypothesis that oocysts’ circadian output is maintained by natural selection to increase oocyst survival. We discuss the adaptive significance of diurnal periodicity in parasite output.

Monitoring infection load of oxyurid (nematoda) and Isospora (coccidia) in captive inland bearded dragons (Pogona vitticeps)

“…These patterns seemed to occur in birds living in temperate forests, which had higher oocyst shedding in the afternoons where UV is lower and humidity is higher during that period of the day (Biard et al, 2022). However, bird hosts living in tropical rainforests were observed to have consistent shedding, where UV radiation levels and humidity are more stable throughout the day (Biard et al, 2022). The environment that the dragons were kept in for our study (i.e., constant UV and heat exposure during the day, overall low humidity levels of 35-50%) may encourage consistent shedding of Isospora.…”

“…In particular, some studies show 4->4,000 times higher prevalence of parasites (coccidia) in the afternoons compared to the mornings in bird hosts (e.g., Brown et al, 2001;Morin-Adeline et al, 2011;Coelho et al, 2013). These patterns seemed to occur in birds living in temperate forests, which had higher oocyst shedding in the afternoons where UV is lower and humidity is higher during that period of the day (Biard et al, 2022). However, bird hosts living in tropical rainforests were observed to have consistent shedding, where UV radiation levels and humidity are more stable throughout the day (Biard et al, 2022).…”

“…In general, the shedding of eggs or oocysts has been found to vary depending on the time of day, seasons and behavioural activity in some species (e.g., Hudman et al, 2000;Filipiak et al, 2009;Dolnik et al, 2010;Morin-Adeline et al, 2011;Taylor et al, 2018;Biard et al, 2022). In particular, some studies show 4->4,000 times higher prevalence of parasites (coccidia) in the afternoons compared to the mornings in bird hosts (e.g., Brown et al, 2001;Morin-Adeline et al, 2011;Coelho et al, 2013).…”

“…For example, there is strong evidence of higher shedding of coccidia oocysts in the afternoons compared to the mornings in various bird species hosts (e.g., Brawner & Hill, 1999;Hudman et al, 2000;Misof, 2004;López et al, 2007;Morin-Adeline et al, 2011;Coelho et al, 2013). This higher prevalence of shedding in the afternoon has been attributed to reduced destruction of oocysts due to desiccation and damaging UV radiation, which may increase survivorship of the oocyst in the environment (Martinaud et al, 2009;Biard et al, 2022). Many studies recommended afternoon sampling for parasite checks (López et al, 2007;Filipiak et al, 2009;Morin-Adeline et al, 2011).…”