Section: Infections
Topic: Biology of interactions, Ecology, Evolution

Spring reproductive success influences autumnal malarial load in a passerine bird

10.24072/pcjournal.378 - Peer Community Journal, Volume 4 (2024), article no. e18.

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Although avian haemosporidian parasites are widely used as model organisms to study fundamental questions in evolutionary and behavorial ecology of host-parasite interactions, some of their basic characteristics, such as seasonal variations in within-host density, are still mostly unknown. In addition, their interplay with host reproductive success in the wild seems to depend on the interaction of many factors, starting with host and parasite species and the temporal scale under study. Here, we monitored the parasitemia of two haemosporidian parasites – Plasmodium relictum (lineage SGS1) and P. homonucleophilum (lineage SW2) – in two wild populations of great tits (Parus major) in Switzerland over three years, to characterize their dynamics. We also collected data on birds’ reproductive output – laying date, clutch size, fledging success – to determine whether they were associated with parasitemia before (winter), during (spring) and after (autumn) breeding season. Parasitemia of both species dramatically increased in spring, in a way that was correlated to parasitemia in winter. Parasitemia before and during breeding season did not explain reproductive success. However, the birds which fledged the more chicks had higher parasitemia in autumn, which was not associated with their parasitemia in previous spring. Our results tend to indicate that high haemosporidian parasite loads do not impair reproduction in great tits, but high resource allocation into reproduction can leave birds less able to maintain low parasitemia over the following months.

Published online:
DOI: 10.24072/pcjournal.378
Type: Research article
Keywords: avian malaria, annual variations, relapses, recrudescence, recurrences, parasitemia, life history traits, bird
Pigeault, Romain 1, 2; Cozzarolo, Camille-Sophie 1, 3, 4; Wassef, Jérôme 1; Gremion, Jérémy 1; Bastardot, Marc 1; Glaizot, Olivier 1, 5; Christe, Philippe 1

1 Department of Ecology and Evolution, Université de Lausanne, Biophore, 1015 Lausanne, Switzerland
2 Laboratoire EBI, Equipe EES, UMR CNRS 7267, 86000 Poitiers, France
3 Biogéosciences, UMR 6282 CNRS, université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France
4 Institute of Organismic and Molecular Evolution (iomE), Anthropology, Johannes Gutenberg University, 55128 Mainz, Germany
5 Muséum cantonal des sciences naturelles - Département de zoologie, Palais de Rumine, Place de la Riponne 6, 1005 Lausanne, Switzerland
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Spring reproductive success influences autumnal malarial load in a passerine bird},
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Pigeault, Romain; Cozzarolo, Camille-Sophie; Wassef, Jérôme; Gremion, Jérémy; Bastardot, Marc; Glaizot, Olivier; Christe, Philippe. Spring reproductive success influences autumnal malarial load in a passerine bird. Peer Community Journal, Volume 4 (2024), article  no. e18. doi : 10.24072/pcjournal.378. https://peercommunityjournal.org/articles/10.24072/pcjournal.378/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.infections.100194

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Albery, G.; Watt, K.; Keith, R.; Morris, S.; Morris, A.; Kenyon, F.; Nussey, D.; Pemberton, J. Reproduction has different costs for immunity and parasitism in a wild mammal, Functional Ecology, Volume 34 (2020), pp. 229-239 | DOI

[2] Allander, K.; Bennett, G. F. Retardation of Breeding Onset in Great Tits (Parus major) by Blood Parasites, Functional Ecology, Volume 9 (1995) no. 4 | DOI

[3] Applegate, J. E. Population Changes in Latent Avian Malaria Infections Associated with Season and Corticosterone Treatment, The Journal of Parasitology, Volume 56 (1970) no. 3 | DOI

[4] Applegate, J. Spring relapse of Plasmodium relictum infections in an experimental field population of English sparrows (Passer domesticus), Journal of Wildlife Diseases, Volume 7 (1971), pp. 37-42 | DOI

[5] Applegate, J.; Beaudoin, R. Mechanism of spring relapse in avian malaria: Effect of gonadotropin and corticosterone, Journal of Wildlife Diseases, Volume 6 (1970), pp. 443-447 | DOI

[6] Asghar, M.; Hasselquist, D.; Bensch, S. Are chronic avian haemosporidian infections costly in wild birds?, Journal of Avian Biology, Volume 42 (2011), pp. 530-537 | DOI

[7] Asghar, M.; Hasselquist, D.; Hansson, B.; Zehtindjiev, P.; Westerdahl, H.; Bensch, S. Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds, Science, Volume 347 (2015), pp. 436-438 | DOI

[8] Asghar, M.; Westerdahl, H.; Zehtindjiev, P.; Ilieva, M.; Hasselquist, D.; Bensch, S. Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers, Parasitology, Volume 139 (2012), pp. 1246-1252 | DOI

[9] Bates, D.; Machler, M.; Bolker, B.; Walker, S. Fitting linear mixed-effects models using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1, pp. 1-48 | DOI

[10] Becker, D. J.; Singh, D.; Pan, Q.; Montoure, J. D.; Talbott, K. M.; Wanamaker, S. M.; Ketterson, E. D. Artificial light at night amplifies seasonal relapse of haemosporidian parasites in a widespread songbird, Proceedings of the Royal Society B: Biological Sciences, Volume 287 (2020) no. 1935 | DOI

[11] Bensch, S.; Hellgren, O.; Pérez‐Tris, J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages, Molecular ecology resources, Volume 9 (2009) no. 5, pp. 1353-1358 | DOI

[12] Cellier-Holzem, E.; Esparza-Salas, R.; Garnier, S.; Sorci, G. Effect of repeated exposure to Plasmodium relictum (lineage SGS1) on infection dynamics in domestic canaries, International Journal for Parasitology, Volume 40 (2010), pp. 1447-1453 | DOI

[13] Christe, P.; Glaizot, O.; Strepparava, N.; Devevey, G.; Fumagalli, L. Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2011) no. 1731, pp. 1142-1149 | DOI

[14] Colangeli, R.; Gupta, A.; Vinhas, S. A.; Chippada Venkata, U. D.; Kim, S.; Grady, C.; Jones-López, E. C.; Soteropoulos, P.; Palaci, M.; Marques-Rodrigues, P.; Salgame, P.; Ellner, J. J.; Dietze, R.; Alland, D. Mycobacterium tuberculosis progresses through two phases of latent infection in humans, Nature Communications, Volume 11 (2020) no. 1 | DOI

[15] Cornet, S.; Bichet, C.; Larcombe, S.; Faivre, B.; Sorci, G. Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system, Journal of Animal Ecology, Volume 83 (2014), pp. 256-265 | DOI

[16] Cornet, S.; Nicot, A.; Rivero, A.; Gandon, S. Evolution of Plastic Transmission Strategies in Avian Malaria, PLoS Pathogens, Volume 10 (2014) no. 9 | DOI

[17] Cosgrove, C.; Wood, M.; Day, K.; Sheldon, B. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus, Journal of Animal Ecology, Volume 77 (2008), pp. 540-548 | DOI

[18] Dawson, R.; Bortolotti, G. Sex-specific associations between reproductive output and hematozoan parasites of American kestrels, Oecologia, Volume 126 (2001), pp. 193-200 | DOI

[19] Delefortrie, Z.; Gante, H. F.; Gordo, O.; Schwab, K. R.; Gonser, R. A. Effects of haemosporidian co-infection and parasitemia on reproductive strategies in a polymorphic species, bioRxiv | DOI

[20] Duffield, K.; Hampton, K.; Houslay, T.; Hunt, J.; Rapkin, J.; Sakaluk, S.; Sadd, B. Age‐dependent variation in the terminal investment threshold in male crickets, Evolution, Volume 72 (2018), pp. 578-589 | DOI

[21] Edler, R.; Klump, G.; Friedl, T. Do blood parasites affect reproductive performance in male red bishops (Euplectes orix)? A test of the Hamilton-Zuk hypothesis, Ethology Ecology and Evolution, Volume 16 (2004), pp. 315-328 | DOI

[22] Garamszegi, L. The evolution of virulence and host specialization in malaria parasites of primates, Ecology Letter, Volume 9 (2006) no. 8, pp. 933-940 | DOI

[23] Garcia-Longoria, L.; Magallanes, S.; Huang, X.; Drews, A.; Råberg, L.; Marzal, A.; Bensch, S.; Westerdahl, H. Reciprocal positive effects on parasitemia between coinfecting haemosporidian parasites in house sparrows, BMC Ecology and Evolution, Volume 22 (2022) no. 1 | DOI

[24] Gooderham, K.; Schulte-Hostedde, A. Macroparasitism influences reproductive success in red squirrels (Tamiasciurus hudsonicus), Behavioral Ecology, Volume 22 (2011) no. 6, pp. 1195-1200 | DOI

[25] Grzędzicka, E. Immune challenge of female great tits at nests affects provisioning and body conditions of their offspring, Acta Ethologica, Volume 20 (2017), pp. 223-233 | DOI

[26] Hamilton, W. D.; Zuk, M. Heritable True Fitness and Bright Birds: A Role for Parasites?, Science, Volume 218 (1982) no. 4570, pp. 384-387 | DOI

[27] Hanssen, S. A.; Hasselquist, D.; Folstad, I.; Erikstad, K. E. Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction, Proceedings of the Royal Society B: Biological Sciences, Volume 272 (2005) no. 1567, pp. 1039-1046 | DOI

[28] Harrison, X.; Blount, J.; Inger, R.; Norris, D.; Bearhop, S. Carry-over effects as drivers of fitness differences in animals: Carry-over effects in animal populations, Journal of Animal Ecology, Volume 80 (2011), pp. 4-18 | DOI

[29] Hasik, A. Z.; Siepielski, A. M. Parasitism shapes selection by drastically reducing host fitness and increasing host fitness variation, Biology Letters, Volume 18 (2022) no. 11 | DOI

[30] Hasker, E.; Kansal, S.; Malaviya, P.; Gidwani, K.; Picado, A.; Singh, R. P.; Chourasia, A.; Singh, A. K.; Shankar, R.; Menten, J.; Wilson, M. E.; Boelaert, M.; Sundar, S. Latent Infection with Leishmania donovani in Highly Endemic Villages in Bihar, India, PLoS Neglected Tropical Diseases, Volume 7 (2013) no. 2 | DOI

[31] Hellgren, O.; Pérez-Tris, J.; Bensch, S. A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites, Ecology, Volume 90 (2009), pp. 2840-2849 | DOI

[32] Hellgren, O.; Wood, M.; Waldenström, J.; Hasselquist, D.; Ottosson, U.; Stervander, M.; Bensch, S. Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the garden warbler, Journal of Evolutionary Biology, Volume 26 (2013), pp. 1047-1059 | DOI

[33] Hicks, O.; Green, J. A.; Daunt, F.; Cunningham, E. J. A.; Newell, M.; Butler, A.; Burthe, S. J. Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population, Ecology, Volume 100 (2019) no. 8 | DOI

[34] Ishtiaq, F.; Bowden, C.; Jhala, Y. Seasonal dynamics in mosquito abundance and temperature do not influence avian malaria prevalence in the Himalayan foothills, Ecology and Evolution, Volume 7 (2017), pp. 8040-8057 | DOI

[35] Rooyen, J. v.; Lalubin, F.; Glaizot, O.; Christe, P. Avian haemosporidian persistence and co-infection in great tits at the individual level, Malaria Journal, Volume 12 (2013) no. 1 | DOI

[36] Knowles, S.; Nakagawa, S.; Sheldon, B. Elevated reproductive effort increases blood parasitemia and decreases immune function in birds: A meta-regression approach, Functional Ecology, Volume 23 (2009), pp. 405-415 | DOI

[37] Knowles, S.; Palinauskas, V.; Sheldon, B. Chronic malaria infections increase family inequalities and reduce parental fitness: Experimental evidence from a wild bird population, Journal of Evolutionary Biology, Volume 23 (2010), pp. 557-569 | DOI

[38] Kubacka, J.; Cichoń, M. An immune challenge of female great tits decreases offspring survival and has sex-specific effects on offspring body size, Acta ethologica, Volume 23 (2020), pp. 173-181 | DOI

[39] Kulma, K.; Low, M.; Bensch, S.; Qvarnström, A. Malaria-Infected Female Collared Flycatchers (Ficedula albicollis) Do Not Pay the Cost of Late Breeding, PLoS ONE, Volume 9 (2014) no. 1 | DOI

[40] Lecomte, V.; Sorci, G.; Cornet, S.; Jaeger, A.; Faivre, B.; Arnoux, E.; Gaillard, M.; Trouvé, C.; Besson, D.; Chastel, O.; Weimerskirch, H. Patterns of aging in the long-lived wandering albatross, Proceedings of the National Academy of Sciences, Volume 107 (2010), pp. 6370-6375 | DOI

[41] Leggett, H.; Buckling, A.; Long, G.; Boots, M. Generalism and the evolution of parasite virulence, Trends in Ecology & Evolution, Volume 28 (2013) no. 10, pp. 592-596 | DOI

[42] Leivesley, J. A.; Bussière, L. F.; Pemberton, J. M.; Pilkington, J. G.; Wilson, K.; Hayward, A. D. Survival costs of reproduction are mediated by parasite infection in wild Soay sheep, Ecology Letters, Volume 22 (2019) no. 8, pp. 1203-1213 | DOI

[43] Loiseau, C. Avian Plasmodium parasitaemia as an indicator of reproduction investment, Peer Community In Infections (2024) | DOI

[44] Lynton-Jenkins, J.; Bründl, A.; Cauchoix, M.; Lejeune, L.; Sallé, L.; Thiney, A.; Russell, A.; Chaine, A.; Bonneaud, C. Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co-occurring host species, Ecology and Evolution, Volume 10 (2020), pp. 6097-6111 | DOI

[45] Madsen, T.; Ujvari, B.; Olsson, M. Old pythons stay fit; effects of haematozoan infections on life history traits of a large tropical predator, Oecologia, Volume 142 (2004) no. 3, pp. 407-412 | DOI

[46] Martinez-Bakker, M.; Helm, B. The influence of biological rhythms on host–parasite interactions, Trends in Ecology & Evolution, Volume 30 (2015), pp. 314-326 | DOI

[47] Marzal, A.; Lope, F.; Navarro, C.; Møller, A. Malarial parasites decrease reproductive success: An experimental study in a passerine bird, Oecologia, Volume 142 (2005), pp. 541-545 | DOI

[48] Marzal, A.; Reviriego, M.; Hermosell, I.; Balbontín, J.; Bensch, S.; Relinque, C.; Rodríguez, L.; Garcia-Longoria, L.; Lope, F. Malaria infection and feather growth rate predict reproductive success in house martins, Oecologia, Volume 171 (2013), pp. 853-861 | DOI

[49] Merino, S.; Moreno, J.; José Sanz, J.; Arriero, E. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus), Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1461, pp. 2507-2510 | DOI

[50] Methling, C.; Douda, K.; Reichard, M. Intensity-dependent energetic costs in a reciprocal parasitic relationship, Oecologia, Volume 191 (2019) no. 2, pp. 285-294 | DOI

[51] Neto, J.; Mellinger, S.; Halupka, L.; Marzal, A.; Zehtindjiev, P.; Westerdahl, H. Seasonal dynamics of haemosporidian (Apicomplexa, Haemosporida) parasites in house sparrows Passer domesticus at four European sites: comparison between lineages and the importance of screening methods, International Journal for Parasitology, Volume 50 (2020), pp. 523-532 | DOI

[52] Nilsson, J.-Å.; Råberg, L. The resting metabolic cost of egg laying and nestling feeding in great tits, Oecologia, Volume 128 (2001), pp. 187-192 | DOI

[53] Nordling, D.; Andersson, M.; Zohari, S.; Lars, G. Reproductive effort reduces specific immune response and parasite resistance, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 265 (1998) no. 1403, pp. 1291-1298 | DOI

[54] Norte, A.; Araújo, P.; Sampaio, H.; Sousa, J.; Ramos, J. Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health: Haematozoa infections in Great Tits from Central Portugal, Ibis, Volume 151 (2009), pp. 677-688 | DOI

[55] Oppliger, A.; Christe, P.; Richner, H. Clutch size and malarial parasites in female great tits, Behavioral Ecology, Volume 8 (1997), pp. 148-152 | DOI

[56] Oppliger, A.; Christe, P.; Richner, H. Clutch size and malaria resistance, Nature, Volume 381 (1996) no. 6583, p. 565-565 | DOI

[57] Ots, I.; Hõrak, P. Health impact of blood parasites in breeding great tits, Oecologia, Volume 116 (1998), pp. 441-448 | DOI

[58] Palinauskas, V.; Valkiūnas, G.; Bolshakov, C.; Bensch, S. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co-infection on experimentally infected passerine birds, Experimental Parasitology, Volume 127 (2011), pp. 527-533 | DOI

[59] Palinauskas, V.; Žiegytė, R.; Šengaut, J.; Bernotienė, R. Different paths – the same virulence: experimental study on avian single and co-infections with Plasmodium relictum and Plasmodium elongatum, International Journal for Parasitology, Volume 48 (2018), pp. 1089-1096 | DOI

[60] Peig, J.; Green, A. New perspectives for estimating body condition from mass/length data: The scaled mass index as an alternative method, Oikos, Volume 118 (2009), pp. 1883-1891 | DOI

[61] Pigeault, R.; Caudron, Q.; Nicot, A.; Rivero, A.; Gandon, S. Timing malaria transmission with mosquito fluctuations, Evolution Letters, Volume 2 (2018), pp. 378-389 | DOI

[62] Pigeault, R.; Cozzarolo, C.-S.; Choquet, R.; Strehler, M.; Jenkins, T.; Delhaye, J.; Bovet, L.; Wassef, J.; Glaizot, O.; Christe, P. Haemosporidian infection and co-infection affect host survival and reproduction in wild populations of great tits, International Journal for Parasitology, Volume 48 (2018), pp. 1079-1087 | DOI

[63] Pigeault, R.; Cozzarolo, C.; Wassef, J.; Bastardot, M.; Glaizot, O.; Christe, P. Data and script of “Spring reproductive success influences autumnal malarial load in wild birds, Figshare, 2023 | DOI

[64] Pigeault, R.; Cozzarolo, C.-S.; Wassef, J.; Gremion, J.; Bastardot, M.; Glaizot, O.; Christe, P. Spring reproductive success influences autumnal malarial load in a passerine bird, bioRxiv, 2023 | DOI

[65] Pigeault, R.; Ruiz De Paz, A.; Baur, M.; Isaïa, J.; Glaizot, O.; Christe, P. Impact of host stress on the replication rate of Plasmodium: take it easy to avoid malaria recurrences, Frontiers in Ecology and Evolution, Volume 11 (2023) | DOI

[66] Pigeault, R.; Vézilier, J.; Cornet, S.; Zélé, F.; Nicot, A.; Perret, P.; Gandon, S.; Rivero, A. Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 370 (2015) no. 1675 | DOI

[67] Podmokła, E.; Dubiec, A.; Drobniak, S.; Arct, A.; Gustafsson, L.; Cichoń, M. Avian malaria is associated with increased reproductive investment in the blue tit, Journal of Avian Biology, Volume 45 (2014), pp. 219-224 | DOI

[68] Prior, K.; Rijo-Ferreira, F.; Assis, P.; Hirako, I.; Weaver, D.; Gazzinelli, R.; Reece, S. Periodic parasites and daily host rhythms, Cell Host & Microbe, Volume 27 (2020), pp. 176-187 | DOI

[69] Pulgarín-R, P.; Gómez, C.; Bayly, N.; Bensch, S.; FitzGerald, A.; Starkloff, N.; Kirchman, J.; González-Prieto, A.; Hobson, K.; Ungvari-Martin, J.; Skeen, H.; Castaño, M.; Cadena, C. Migratory birds as vehicles for parasite dispersal? Infection by avian haemosporidians over the year and throughout the range of a long-distance migrant, Journal of Biogeography, Volume 46 (2019), pp. 83-96 | DOI

[70] Raveh, S.; Heg, D.; Dobson, F.; Coltman, D.; Gorrell, J.; Balmer, A.; Röösli, S.; Neuhaus, P. No experimental effects of parasite load on male mating behaviour and reproductive success, Animal Behaviour, Volume 82 (2011), pp. 673-682 | DOI

[71] Reinoso-Pérez, M.; Dhondt, K.; Sydenstricker, A.; Heylen, D.; Dhondt, A. Complex interactions between bacteria and haemosporidia in coinfected hosts: An experiment, Ecology and Evolution, Volume 10 (2020), pp. 5801-5814 | DOI

[72] Richner, H.; Christe, P.; Oppliger, A. Paternal investment affects prevalence of malaria, Proceedings of the National Academy of Sciences, Volume 92 (1995), pp. 1192-1194 | DOI

[73] Risely, A.; Klaassen, M.; Hoye, B. Migratory animals feel the cost of getting sick: A meta-analysis across species, Journal of Animal Ecology, Volume 87 (2018), pp. 301-314 | DOI

[74] Rivero, A.; Gandon, S. Evolutionary ecology of avian malaria: Past to present, Trends in Parasitology, Volume 34 (2018), pp. 712-726 | DOI

[75] Sanz, J.; Arriero, E.; Moreno, J.; Merino, S. Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers, Oecologia, Volume 126 (2001), pp. 339-344 | DOI

[76] Saraux, C.; Chiaradia, A. Age‐related breeding success in little penguins: a result of selection and ontogenetic changes in foraging and phenology, Ecological Monographs, Volume 92 (2021) no. 1 | DOI

[77] Schoepf, I.; Olson, S.; Moore, I. T.; Bonier, F. Experimental reduction of haemosporidian infection affects maternal reproductive investment, parental behaviour and offspring condition, Proceedings of the Royal Society B: Biological Sciences, Volume 289 (2022) no. 1987 | DOI

[78] Sheldon, B.; Verhulst, S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology, Trends in Ecology & Evolution, Volume 11 (1996) no. 8, pp. 317-321 | DOI

[79] Siikamäki, P.; Rätti, O.; Hovi, M.; Bennett, G. Association between haematozoan infections and reproduction in the Pied Flycatcher, Functional Ecology, Volume 11 (1997), pp. 176-183 | DOI

[80] Stahlschmidt, Z.; Rollinson, N.; Acker, M.; Adamo, S. Are all eggs created equal? Food availability and the fitness trade-off between reproduction and immunity, Functional Ecology, Volume 27 (2013), pp. 800-806 | DOI

[81] Stearns, S. Trade-offs in life-history evolution, Ecology, Volume 3 (1989), pp. 259-268 | DOI

[82] Stjernman, M.; Råberg, L.; Nilsson, J.-Å. Maximum Host Survival at Intermediate Parasite Infection Intensities, PLoS ONE, Volume 3 (2008) no. 6 | DOI

[83] Sundberg, J. Parasites, Plumage Coloration and Reproductive Success in the Yellowhammer, Emberiza citrinella, Oikos, Volume 74 (1995) no. 2 | DOI

[84] Sánchez, C.; Becker, D.; Teitelbaum, C.; Barriga, P.; Brown, L.; Majewska, A.; Hall, R.; Altizer, S. On the relationship between body condition and parasite infection in wildlife: a review and meta‐analysis, Ecology Letters, Volume 21 (2018), pp. 1869-1884 | DOI

[85] Valkiūnas, G. Avian malaria parasites and other haemosporidia, CRC Press, Boca Raton, 2005 | DOI

[86] Velando, A.; Drummond, H.; Torres, R. Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1593, pp. 1443-1448 | DOI

[87] Visser, M. E.; Lessells, C. M. The costs of egg production and incubation in great tits (Parus major), Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 268 (2001) no. 1473, pp. 1271-1277 | DOI

[88] Williams, G. Natural selection, the cost of reproduction, and a refinement of Lack’s Principle, The American Naturalist, Volume 100 (1966) no. 916, pp. 687-690 | DOI

[89] Zylberberg, M.; Derryberry, E.; Breuner, C.; Macdougall-Shackleton, E.; Cornelius, J.; Hahn, T. Haemoproteus infected birds have increased lifetime reproductive success, Parasitology, Volume 142 (2015), pp. 1033-1043 | DOI

[90] Šujanová, A.; Špitalská, E.; Václav, R. Seasonal Dynamics and Diversity of Haemosporidians in a Natural Woodland Bird Community in Slovakia, Diversity, Volume 13 (2021) no. 9 | DOI

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