Time of day, age and feeding habits influence coccidian oocyst shedding in wild passerines
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.
Section snippets
Field work
Because of their abundance and diet specificity, European Serins (Serinus serinus, Linnaeus 1766) and Garden Warblers (Sylvia borin, Boddaert 1783) were chosen as models of seed-eater and insectivorous birds, respectively. Birds were trapped during daylight between March and May in 2004 and 2005 in a tree nursery in the city of Seville (37°23′11″N, 5°57′46″W), with mists nets placed amongst bushes. Birds were individually marked with numbered aluminium rings, sexed and aged (as juveniles or
Effects of hour, species and age on coccidian prevalence
Standardized hour was the only variable significantly related to coccidian prevalence in our model (Table 1). No significant differences in prevalence were found either between species or between yearling and adult S. serinus (χ2 = 0.21, d.f. = 1, P = 0.649). The test of mean differences in the minimum squares showed that prevalence was similar and peaked in periods 6, 7, 8 and 9. This means that coccidian elimination in infected individuals takes place mainly between 1/2 and 9/10 of the daylight
Discussion
This research shows that coccidian oocyst shedding in free-living passerines presents clear circadian rhythms, which strongly affect the estimates of both coccidian prevalence and load based on oocyst-counting in chamber. In the wild, these findings are not affected by changes in diet or in the typical activity patterns of birds kept in captivity. We believe this study is the first report of the existence of differences in coccidian load between species with different feeding habits. It also
Acknowledgements
The Spanish Ministerio de Sanidad via its Thematic Research Net ‘EVITAR’ funded our research. Alberto Álvarez, Alicia Cortés, Ángel Mejía, Ara Villegas, Beatriz Fernández, Carmen Gutiérrez, Chari Terceño, Cristina Sánchez, Elena Fierro, Enrique Sánchez, Esteban Serrano, Francisco Miranda, Grego Toral, Inma Cancio, Joaquín Díaz, José Antonio Sánchez, Mari Carmen Roque, Olga Jiménez, Pedro Sáez, Rafael Reina, and Samuel del Río helped with fieldwork. Beatriz Sánchez helped with fieldwork and
References (28)
- et al.
A comparison between IgG antibodies against Eimeria acervulina, E. maxima, and E. tenella and oocyst shedding in broiler-breeders vaccinated with live anticoccidial vaccines
Vaccine
(2003) Diurnal gametic periodicity in avian Isospora
Am. J. Hyg.
(1933)- et al.
Temporal variation in shedding of coccidial oocysts: implications for sexual selection studies
Can. J. Zool.
(1999) - et al.
Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male House Finches
Auk
(2000) - et al.
The periodicity of isosporan oocyst discharge in the greenfinch (Carduelis chloris)
J. Nat. Hist.
(2001) - et al.
Variance partitioning in multilevel logistic models that exhibit overdispersion
J. R. Statist. Soc. A
(2005) Coccidial infection with Eimeria tenella and caecal defaecation in chicks
Br. Poult. Sci.
(1979)- et al.
Protective immunity against Eimeria acervulina following in ovo immunization with a recombinant subunit vaccine and cytokine genes
Infect. Immun.
(2004) Diurnal periodicity of oocysts release of Isospora dilatata (Sporozoa: Eimeriidae) from the common Starling (Sturnus vulgaris) in nature
Parasitologiya
(1999)Diurnal periodicity in appearance of Isospora (Protozoa: Coccidea) oocysts from some passerine birds
Proc. Zool. Inst. RAS
(1999)
Mortality in black siskins (Carduelis atrata) with systemic coccidiosis
J. Wildl. Dis.
A Red Bird in a Brown Bag: The Function and Evolution of Colorful Plumage in the House Finch
How coccidian parasites affect health and appearance of greenfinches
J. Anim. Ecol.
Host resistance and parasite virulence in greenfinch coccidiosis
J. Evol. Biol.
Cited by (50)
Morphological and molecular approaches for identification of murine Eimeria papillata infection
2022, Journal of King Saud University - ScienceCitation Excerpt :Several eimerian species cannot be differentiated by microscopic description due to the similar morphology and the overlapping morphometrics of the oocysts. To describe the identity of Eimeria and complement prior morphological descriptions, molecular techniques are increasingly being applied (López et al., 2007; Power et al., 2009). These techniques have some advantages over previous traditional methods in that they solely use the Eimeria species’ genetic sequence.
The Evolutionary Biology, Ecology and Epidemiology of Coccidia of Passerine Birds
2018, Advances in ParasitologyCitation Excerpt :To our knowledge, in all passerines tested to date, oocyst shedding peaks in the afternoon or evening. In our review of the literature, evidence of a circadian rhythm was found for English house sparrows (P. domesticus; Boughton, 1933), cliff swallows (Petrochelidon pyrrhonota; Stabler and Kitzmiller, 1972), canaries (Serinus canarius; Box, 1977), chaffinches (Fringilla coelebs; Gryczyńska et al., 1999), house finches (Carpodacus mexicanus; Brawner and Hill, 1999), dark-eyed juncos (Junco hyemalis; Hudman et al., 2000), greenfinches (C. chloris; Brown et al., 2001), starlings (Sturnus vulgaris; Dolnik, 2002), scarlet grosbeaks (Carpodacus erythrinus; Dolnik, 2002), reed warblers (Acrocephalus scirpaceus; Dolnik, 2002), willow warblers (Phylloscopus trochilus; Dolnik, 2002), blackbirds (Turdus merula; Misof, 2004), serins (Serinus serinus; López et al., 2007), garden warblers (Sylvia borin; López et al., 2007), regent honeyeaters (Xanthomyza phrygia; Morin-Adeline et al., 2011) and green-winged saltators (Saltator similis; Coelho et al., 2013). In some instances, the difference in oocyst shedding can vary from detection of no oocysts whatsoever shed in the morning to several hundreds of thousands in the afternoon (Brawner and Hill, 1999).
Diurnal fluctuations in nematode egg excretion in naturally and in experimentally infected chickens
2015, Veterinary ParasitologyCitation Excerpt :As shown earlier (Daş et al., 2011a), precision of fecal egg counts is not influenced by consistency or water content of chicken feces samples. However, EPG and AEO might seem to be influenced by host related physiological factors, e.g., feed and water intake and the digesta passage rate through the host gastrointestinal tract, which may alter feces excretion rate and thereby concentration and total numbers of eggs being excreted (Bath-Jacobson et al., 2005; López et al., 2007; Dunkley et al., 2008). Peak feed consumption by laying hens has been reported to be at 8:00–10:00 and 17:00–19:00 (Ezieshi et al., 2003; Choi et al., 2004).
An optimised protocol for molecular identification of Eimeria from chickens
2014, Veterinary ParasitologyCitation Excerpt :However, in a natural setting mixed infections of different Eimeria spp. are commonly encountered and morphological characteristics and pathological changes may overlap, hindering accurate diagnosis and undermining detection of subclinical disease (Long and Joyner, 1984; Rice and Reid, 1973). Thus, it has been suggested that these methods should not be used in isolation for differentiation of Eimeria species (Long and Joyner, 1984; Lopez et al., 2007). Alternatives include molecular or computational approaches such as PCR, qPCR and the software COCCIMORPH.