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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

Published online by Cambridge University Press:  24 November 2021

Clotilde Biard Open the ORCID record for Clotilde Biard [Opens in a new window] ,
Karine Monceau Open the ORCID record for Karine Monceau [Opens in a new window] ,
Maria Teixeira ,
Sébastien Motreuil ,
Soline Bettencourt-Amarante ,
Lucie Develay  and
Jérôme Moreau Open the ORCID record for Jérôme Moreau [Opens in a new window]
Clotilde Biard
Affiliation:
Sorbonne Université, UPEC, Paris 7, CNRS, INRA, IRD, Institut d'Écologie et des Sciences de l'Environnement de Paris, F-75005Paris, France
Karine Monceau
Affiliation:
Centre d'Études Biologiques de Chizé, UMR 7372, CNRS and La Rochelle Université, 79360Villiers-en-bois, France
Maria Teixeira
Affiliation:
UMR CNRS 6282 Biogéosciences, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
Sébastien Motreuil
Affiliation:
UMR CNRS 6282 Biogéosciences, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
Soline Bettencourt-Amarante
Affiliation:
UMR CNRS 6282 Biogéosciences, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
Lucie Develay
Affiliation:
UMR CNRS 6282 Biogéosciences, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
Jérôme Moreau*
Affiliation:
Centre d'Études Biologiques de Chizé, UMR 7372, CNRS and La Rochelle Université, 79360Villiers-en-bois, France UMR CNRS 6282 Biogéosciences, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
*
Author for correspondence: Jérôme Moreau, E-mail: [email protected]
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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.

Keywords

Birdscircadian rhythmscoccidiahost–parasite interactionstemperate foresttropical forest
Type
Research Article
Information
Parasitology , Volume 149 , Issue 4 , April 2022 , pp. 469 - 481
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abd-Al-Aal, Z, Ramadan, NF and Al-Hoot, A (2000) Life-cycle of Isospora mehlhornii sp. nov. (Apicomplexa: Eimeriidae), parasite of the Egyptian swallow Hirundo rubicola savignii. Parasitology Research 86, 270–278.CrossRefGoogle Scholar
Allen, PC and Fetterer, RH (2002) Recent advances in biology and immunobiology of Eimeria species and in diagnosis and control of infection with these coccidian parasites of poultry. Clinical and Microbiology Review 15, 58–65.CrossRefGoogle Scholar
Anderson, MC (1964) Studies of the woodland light climate: II. Seasonal variation in the light climate. Journal of Ecology 52, 643–663.CrossRefGoogle Scholar
Beaudet, M, Messier, C and Leduc, A (2004) Understorey light profiles in temperate deciduous forests: recovery process following selection cutting. Journal of Ecology 92, 328–338.CrossRefGoogle Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B 57, 289–300.Google Scholar
Biard, C, Saulnier, N, Gaillard, M and Moreau, J (2010) Carotenoid-based bill colour is an integrative signal of multiple parasite infection in blackbird. Naturwissenschaften 97, 987–995.CrossRefGoogle ScholarPubMed
Biard, C, Monceau, K, Motreuil, S and Moreau, J (2015) Interpreting immunological indices: the importance of taking parasite community into account. An example in blackbirds Turdus merula. Methods in Ecology and Evolution 6, 960–972.CrossRefGoogle Scholar
Boughton, DC (1933) Diurnal gametic periodicity in avian Isospora. American Journal of Epidemiology 18, 161–184.CrossRefGoogle Scholar
Bourgeron, PS (1983) Spatial aspects of vegetation structure. In Golley, FB (eds), Tropical Rain Forest Ecosystems: Structure and Function. Ecosystems of the World. Amsterdam and New York: Elsevier Scientific Pub. Co., pp. 29–47.Google Scholar
Brawner, WR and Hill, GE (1999) Temporal variation in shedding of coccidial oocysts: implications for sexual-selection studies. Canadian Journal of Zoology 77, 347–350.CrossRefGoogle Scholar
Brawner, WR, Hill, GE and Sundermann, CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male House finches. The Auk 117, 952–963.CrossRefGoogle Scholar
Brinkmann, WLF (1971) Light environment in a tropical rain forest of central Amazonia. Acta Amazonica 1, 37–49.CrossRefGoogle Scholar
Brown, M, Ball, S and Holman, D (2001) The periodicity of isosporan oocyst discharge in the greenfinch (Carduelis chloris). Journal of Natural History 35, 945–948.CrossRefGoogle Scholar
Bruno, RD, Rocha, HR, Freitas, HC, Goulden, ML and Miller, SD (2006) Soil moisture dynamics in an eastern Amazonian tropical forest. Hydrology Processes 20, 2477–2489.CrossRefGoogle Scholar
Buckley, GP (1992) Ecology and Management of Coppice Woodlands. London, UK: Chapman and Hall.CrossRefGoogle Scholar
Bush, AO, Fernández, JC, Esch, GW and Seed, JR (2001) Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge, UK: Cambridge University Press.Google Scholar
Canham, CD and Marks, PL (1985) The response of woody plants to disturbance: patterns of establishment and growth. In Pickett, STA and White, PS (eds), The Ecology of Natural Disturbance and Patch Dynamics. New York, USA: Academic Press, pp. 197–216.Google Scholar
Chazdon, RL and Fetcher, N (1984) Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. Journal of Ecology 72, 553–564.CrossRefGoogle Scholar
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. London, UK: University of Chicago Press and London.Google Scholar
Combes, C, Fournier, A, Moné, H and Théron, A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.CrossRefGoogle ScholarPubMed
Dolnik, OV (1999 a) Diurnal periodicity of oocysts release of Isospora dilatata (Sporozoa: Eimeriidae) from the common Starling (Sturnus vulgaris) in nature. Parasitologia 33, 74–80.Google Scholar
Dolnik, OV (1999 b) Diurnal periodicity in appearance of Isospora (Protozoa: Coccidea) oocysts from some passerine birds. Proceedings of the Zoological Institute RAS 281, 113–118.Google Scholar
Dolnik, OV, Dolnik, VR and Bairlein, F (2010) The effect of host foraging ecology on the prevalence and intensity of coccidian infection in wild passerine birds. Ardea 98, 97–103.CrossRefGoogle Scholar
Dolnik, OV, Metzger, BJ and Loonen, MJJE (2011) Keeping the clock set under the midnight sun: diurnal periodicity and synchrony of avian Isospora parasites cycle in the High Arctic. Parasitology 138, 1077–1081.CrossRefGoogle ScholarPubMed
Durrant, KL, Beadell, JS, Ishtiaq, F, Graves, GR, Olson, SL, Gering, E, Peirce, MA, Milensky, CM, Schmidt, BK, Gebhard, C and Fleischer, RC (2006) Avian hematozoa in South America: a comparison of temperate and tropical zones. Ornithological Monographs 60, 98–111.CrossRefGoogle Scholar
Filipiak, L, Mathieu, F and Moreau, J (2009) Caution on the assessment of intestinal parasitic load in studying parasite-mediated sexual selection: the case of blackbirds coccidiosis. International Journal for Parasitology 39, 741–746.CrossRefGoogle ScholarPubMed
Freiberg, M (1997) Spatial and temporal pattern of temperature and humidity of a tropical premontane rain forest tree in Costa Rica. Selbyana 18, 77–84.Google Scholar
Hilty, S (2002) Birds of Venezuela, 2nd Edn, Princeton, USA: Princeton University Press.Google Scholar
Hõrak, P, Saks, L, Karu, U, Ots, I, Surai, PF and McGraw, KJ (2004) How coccidian parasites affect health and appearance of greenfinches. Journal of Animal Ecology 73, 935–947.CrossRefGoogle Scholar
Hudman, SP, Ketterson, ED and Nolan, V (2000) Effects of time of sampling on oocyst detection and effects of age and experimentally elevated testosterone on prevalence of coccidia in male dark-eyed juncos. The Auk 117, 1048–1051.CrossRefGoogle Scholar
Knight, A, Ewen, JG, Brekke, P and Santure, AW (2018) Chapter two – The evolutionary biology, ecology and epidemiology of coccidia of passerine birds. In Rollinson, D and Stothard, JR (eds), Advances in Parasitology. London, UK: Academic Press, pp. 35–60.Google Scholar
Koizumi, H and Oshima, Y (1985) Seasonal changes in photosynthesis of four understory herbs in deciduous forests. Botanical Magazine 98, 1–13.CrossRefGoogle Scholar
Kruszewicz, AG (1995) The occurrence of Isospora lacazei (Coccidia: Eimeriidae) and its influence on nestling growth in house sparrows (Passer domesticus) and tree sparrows (Passer montanus). In Pinowski, J, Kavanagh, BP and Pinowska, B (eds), Nestling Mortality of Granivorous Birds Due to Microorganisms and Toxic Substances: Synthesis. Warszawa, Poland: Polish Scientific Publishers, pp. 291–305.Google Scholar
Lopez, G, Figuerola, J and Soriguer, R (2007) Time of day, age and feeding habits influence coccidian oocyst shedding in wild passerines. International Journal for Parasitology 37, 559–564.CrossRefGoogle ScholarPubMed
Marks, R and Plewig, G (1991) The Environmental Threat to the Skin. London, UK: Taylor and Francis Ltd.Google Scholar
Martinaud, G, Billaudelle, M and Moreau, J (2009) Circadian variation in shedding of the oocysts of Isospora turdi (Apicomplexa) in blackbirds (Turdus merula): an adaptative trait against desiccation and ultraviolet radiation. International Journal for Parasitology 39, 735–739.CrossRefGoogle ScholarPubMed
McElrone, AJ, Choat, B, Gambetta, GA and Brodersen, CR (2013) Water uptake and transport in vascular plants. Nature Education Knowledge 4, 6.Google Scholar
Merino, S, Moreno, J, Vásquez, RA, Martínez, J, Sánchez-Monsálvez, I, Estades, CF, Ippi, S, Sabat, P, Rozzi, R and Mcgehee, S (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.CrossRefGoogle Scholar
Misof, K (2004) Diurnal cycle of Isospora spp. oocyst shedding in Eurasian blackbirds (Turdus merula). Canadian Journal of Zoology 82, 764–768.CrossRefGoogle Scholar
Olsen, OW (1974) Animal Parasites: Their Life Cycles and Ecology. Baltimore, USA: University Park Press.Google Scholar
R Core Team (2021) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Reece, SE, Prior, KF and Mideo, N (2017) The life and times of parasites: rhythms in strategies for within-host survival and between-host transmission. Journal of Biological Rhythms 32, 516–533.CrossRefGoogle ScholarPubMed
Restall, R, Rodner, C and Lentino, M (2006 a) Birds of Northern South America: An Identification Guide. Species Accounts, vol. 1, 1st Edn. London, UK: Helm Field Guides.Google Scholar
Restall, R, Rodner, C and Lentino, M (2006 b) Birds of Northern South America: An Identification Guide. Plates and Maps, vol. 2, 1st Edn. London, UK: Helm Field Guides.Google Scholar
Ricklefs, RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences 89, 4722–4725.CrossRefGoogle ScholarPubMed
Ricklefs, RE and Sheldon, KS (2007) Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush. The Auk 124, 1254–1266.CrossRefGoogle Scholar
Svensson-Coelho, M, Ellis, VA, Loiselle, BA, Blake, JG and Ricklefs, RE (2014) Reciprocal specialization in multihost malaria parasite communities of birds: a temperate-tropical comparison. American Naturalist 184, 624–635.CrossRefGoogle ScholarPubMed
Szwagrzyk, J, Szewczyk, J and Bodziarczyk, J (2001) Dynamics of seedling banks in beech forest: results of a 10-year study on germination, growth and survival. Forest Ecology and Management 141, 237–250.CrossRefGoogle Scholar
Théron, A (1984) Early and late shedding patterns of Schistosoma mansoni Cercariae: ecological significance in transmission to human and murine hosts. Journal of Parasitology 70, 652–655.CrossRefGoogle ScholarPubMed
Vazquez-Yanes, C, Orozco-Segovia, A, Rincon, E, Sanchez-Coronado, ME, Huante, P, Toledo, JR and Barradas, VL (1990) Light beneath the litter in a tropical forest: effect on seed germination. Ecology 71, 1952–1958.CrossRefGoogle Scholar