Time of day, age and feeding habits influence coccidian oocyst shedding in wild passerines

Abstract

Protozoan coccidia are one of the most common intestinal parasites in birds. Ordinary coccidian detection and quantification techniques have proved to be inaccurate for wild passerines due to the existence of marked oocyst shedding rhythms throughout the day. Previous studies have suggested that these rhythms should be taken into account when analysing coccidian load and prevalence data, but their pattern and magnitude still remain poorly known. In this study we characterised shedding rhythms in the field by means of 406 samples of faeces taken from two species of passerines with different diets: the European Serin (a granivorous species), and the Garden Warbler (an insectivorous species). Both coccidian prevalence and load were two-phased, with maximums occurring in the afternoon. Oocyst elimination remained consistently high during the second half of the day, whereas prevalence peaked during the afternoon, lowering throughout the evening. This pattern was found in both species. We found a high repeatability of prevalence and intensity when differences between the morning and afternoon were statistically controlled. As a result, we suggest that sampling periods used in the analysis of coccidian prevalence and/or load studies should take into account these differences in times of shedding and be limited to the afternoon, otherwise a statistical control of this factor will be required.

Introduction

Parasitism is widespread in nature and its importance in the ecology and evolution of organisms is well known (Thomas et al., 2005). Host-parasite relationships in avian passerine species have become a common focus of research over the last decade. Many studies have centred on ecto- and blood parasites, whereas due to the lack of an accurate quantification method, rather fewer have focused on endoparasites. Coccidian protozoa are intestinal parasites that are found in most vertebrate species and which have been shown to be involved in many ecological avian processes (McGraw and Hill, 2000, Hill, 2002). Most (families Eimeridiidae and Cryptosporidiidae) are monoxenous, the transmission between individuals taking place via infective oocysts released in faeces. The only non-invasive method of determining the presence and burden of these coccidians is to detect and count oocysts in host faeces (Watve and Sukumar, 1995). This is, however, an inaccurate method for field studies, in which only one sample can usually be taken at a time, because circadian variation in oocyst shedding has been observed in many species. For example, variation is known to occur in some species of the genus Eimeria that infect domestic chickens and partridges (Clarke, 1979, Willliams, 1995, Villanúa et al., 2006). Passerines are mainly infected by species belonging to the genus Isospora (reviewed by Giacomo et al., 1997, McGraw and Hill, 2000), in which a host-dependent circadian variation in oocyst shedding has also been observed (Boughton, 1933). Although previous studies with passerines have suggested that oocyst discharge is much greater in the afternoon than in the morning, knowledge of this process is still deficient and indeed many of these studies have only focused on prevalence (Brawner and Hill, 1999, Hudman et al., 2000, Brown et al., 2001). Other studies have assumed, but not tested, the existence of alternative morning/afternoon states (Schwalbach, 1961, Hudman et al., 2000; Misof, 2005 . Eurasian Blackbirds (Turdus merula) and their gastrointestinal parasites: A role for parasites in life-history decisions? ULB, Bonn.), or have been performed on birds kept in captivity for days or weeks at a time (Boughton, 1933, Brawner and Hill, 1999, Dolnik, 1999a). Moreover, the effect that diet and the natural activity rhythms of hosts may have on oocyst shedding rhythms has never been analysed. Since digestive physiology varies with feeding habits (Sturkie, 1986), oocyst shedding may well also be influenced by these variables. Thus, knowledge of patterns occurring in circadian rhythms with different feeding habits will help researchers to collect, analyse, and interpret data correctly. In this paper, we describe coccidian oocyst shedding rhythms in the field over the whole day in two species of passerines with different feeding patterns. Our goal was to achieve an accurate coccidian detection and quantification method in order to establish the best sampling period to use in field studies. We analysed oocyst presence and burden in faeces of both a seed-eater and an insectivorous species of free living passerines.