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Innate immunity and environmental correlates of Haemoproteus prevalence and intensity in an opportunistic breeder

Published online by Cambridge University Press:  21 February 2018

Elizabeth M. Schultz Open the ORCID record for Elizabeth M. Schultz [Opens in a new window] ,
Jamie M. Cornelius ,
Dustin G. Reichard ,
Kirk C. Klasing  and
Thomas P. Hahn
Elizabeth M. Schultz*
Affiliation:
University of California, Davis, One Shields Ave, Davis, California 95616, USA
Jamie M. Cornelius
Affiliation:
Eastern Michigan University, 900 Oakwood St, Ypsilanti, Michigan 48198, USA
Dustin G. Reichard
Affiliation:
Ohio Wesleyan University, 61 S Sandusky St, Delaware, Ohio 43015, USA
Kirk C. Klasing
Affiliation:
University of California, Davis, One Shields Ave, Davis, California 95616, USA
Thomas P. Hahn
Affiliation:
University of California, Davis, One Shields Ave, Davis, California 95616, USA
*
Author for correspondence: Elizabeth M. Schultz, E-mail: [email protected]
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Abstract

While parasite infection can have substantial fitness consequences in organisms, the predictors of parasite prevalence and intensity are often complex and vary depending on the host species. Here, we examined correlates of Haemoproteus (a common malaria parasite) prevalence and intensity in an opportunistically breeding songbird, the red crossbill (Loxia curvirostra). Specifically, we quantified Haemoproteus prevalence and intensity in crossbills caught in the Grand Teton National Park from 2010 to 2013. We found that parasite prevalence varies seasonally and across years, with the highest number of infected individuals occurring in the summer, although there was variation across summers sampled, and that prevalence was positively related to annual mean cone crop sizes (a measure of crossbill food abundance) and daily ambient temperature (a correlate of vector abundance). Parasite intensity was significantly and positively related to one measure of innate immunity, leucocyte counts per blood volume. Finally, neither crossbill age, ecomorph, nor sex had significant effects on parasite infection intensity; however, parasite prevalence did significantly vary among ecomorph and age classes. These results support the interpretation that a combination of physiological (specifically immune activity) and environmental factors affects parasite prevalence and infection intensity in this opportunistically breeding avian species.

Keywords

Avian malariaeco-immunologyhaematozoaHaemoproteusLoxia curvirostraparasitaemiaprevalencered crossbill
Type
Research Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1388 - 1399
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Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

Current Address: Kenyon College, 103 College Rd, Gambier, Ohio 43022, USA

References

Adkisson, C (1996) Red crossbill. The Birds of North America 256, 1–23.Google Scholar
Allander, K (1997) Reproductive investment and parasite susceptibility in the Great Tit. Functional Ecology 11, 358–364.Google Scholar
Allander, K and Bennett, GF (1995) Retardation of breeding onset in great tits (Parus major) by blood parasites. Functional Ecology 9, 677–682.Google Scholar
Andrade, B, Teixeira, C, Barral, A and Barral-Netto, M (2005) Haematophagous arthropod saliva and host defense system: a tale of tear and blood. Anais da Academia Brasileira de Ciências 77, 665–693.Google Scholar
Asghar, M, Hasselquist, D, Hansson, B, Zehtindjiev, P, Westerdahl, H and Bensch, S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436–438.Google Scholar
Atkinson, C and Van Riper, C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Loye, J and Zuk, M (eds). Bird–Parasite Interactions. London: Oxford University Press, pp. 19–48.Google Scholar
Benkman, C (1993) Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecological Monographs 63, 305–325.Google Scholar
Benkman, CW (1987) Food profitability and the foraging ecology of crossbills. Ecological Monographs 57, 251–267.Google Scholar
Benkman, CW (1990) Intake rates and the timing of crossbill reproduction The Auk 107, 376–386.Google Scholar
Benkman, CW (2003) Divergent selection drives the adaptive radiation of crossbills. Evolution 57, 1176–1181.Google Scholar
Bensch, S, Waldenström, J, Jonzén, N, Westerdahl, H, Hansson, B, Sejberg, D and Hasselquist, D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112–122.Google Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach. New York: Springer.Google Scholar
Burns, R and Honkala, B (1990) Silvics of North America. Washington, DC: U.S. Forest Service, Department of Agriculture.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Buttemer, WA and Astheimer, LB (2000) Testosterone does not affect basal metabolic rate or blood parasite load in captive male white-plumed honeyeaters Lichenostomus penicillatus. Journal of Avian Biology 31, 479–488.Google Scholar
Campbell, TW (1995) Avian Hematology and Cytology. Ames, IA: Iowa State University Press.Google Scholar
Casto, JM, Nolan, V Jr and Ketterson, ED (2001) Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist 157, 408–420.Google Scholar
Cellier-Holzem, E, Esparza-Salas, R, Garnier, S and Sorci, G (2010) Effect of repeated exposure to Plasmodium relictum (lineage SGS1) on infection dynamics in domestic canaries. International Journal of Parasitology 40, 1447–1453.Google Scholar
Cornelius, JM, Perfito, N, Zann, RA, Breuner, CW and Hahn, TP (2011) Physiological trade-offs in self-maintenance: plumage molt and stress physiology in birds. Journal of Experimental Biology 214, 2768–2777.Google Scholar
Cornelius, JM, Breuner, CW and Hahn, TP (2012) Coping with the extremes: stress physiology varies between winter and summer in breeding opportunists. Biology Letters 8, 312–315.Google Scholar
Cornelius, JM, Zylberberg, M, Breuner, CW, Gleiss, AC and Hahn, TP (2014) Assessing the role of reproduction and stress in the spring emergence of haematozoan parasites in birds. Journal of Experimental Biology 217, 841–849.Google Scholar
Deviche, P and Parris, J (2006) Testosterone treatment to free-ranging male dark-eyed juncos (Junco hyemalis) exacerbates hemoparasitic infection. The Auk 123, 548.Google Scholar
Deviche, P, Greiner, EC and Manteca, X (2001) Seasonal and age-related changes in blood parasite prevalence in dark-eyed juncos (Junco hyemalis, Aves, Passeriformes). Journal of Experimental Zoology 289, 456–466.Google Scholar
Deviche, P, Fokidis, HB, Lerbour, B and Greiner, E (2010) Blood parasitaemia in a high latitude flexible breeder, the white-winged crossbill, Loxia leucoptera: contribution of seasonal relapse versus new inoculations. Parasitology 137, 261–273.Google Scholar
Fecchio, A, Lima, MR, Silveira, P, Ribas, ACA, Caparroz, R and Marini, MÂ (2015) Age, but not sex and seasonality, influence Haemosporida prevalence in white-banded tanagers (Neothraupis fasciata) from central Brazil. Canadian Journal of Zoology 93, 71–77.Google Scholar
Fowells, HA (1968) Silvics of the United States. Washington: USDA Forest Service.Google Scholar
Golding, N, Nunn, MA and Purse, BV (2015) Identifying biotic interactions which drive the spatial distribution of a mosquito community. Parasit Vectors 8, 10.Google Scholar
Granthon, C and Williams, DA (2017) Avian malaria, body condition, and blood parameters in four species of songbirds. The Wilson Journal of Ornithology 129, 492–508.Google Scholar
Greenman, CG, Martin Ii, LB and Hau, M (2005) Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus). Physiological and Biochemical Zoology 78, 60–68.Google Scholar
Grillo, EL, Fithian, RC, Cross, H, Wallace, C, Viverette, C, Reilly, R and Mayer, DCG (2012) Presence of plasmodium and Haemoproteus in breeding prothonotary warblers (Protonotaria citrea: Parulidae): temporal and spatial trends in infection prevalence. Journal of Parasitology 98, 93–102.Google Scholar
Groth, JG (1993) Evolutionary Differentiation in Morphology, Vocalizations, and Allozymes among Nomadic Sibling Species in the North American red Crossbill (Loxia curvirostra) Complex. Berkeley, CA: University of California Press.Google Scholar
Gustafsson, L, Nordling, D, Andersson, MS, Sheldon, BC and Qvarnström, A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions: Biological Sciences 346, 323–331.Google Scholar
Hahn, TP (1995) Integration of photoperiodic and food cues to time changes in reproductive physiology by an opportunistic breeder, the red crossbill, Loxia curvirostra (Aves: Carduelinae). Journal of Experimental Zoology 272, 213–226.Google Scholar
Hahn, TP (1998) Reproductive seasonality in an opportunistic breeder, the red crossbill, Loxia curvirostra. Ecology 79, 2365–2375.Google Scholar
Hasselquist, D (2007) Comparative immunoecology in birds: hypotheses and tests. Journal of Ornithology 148, 571–582.Google Scholar
Ibanez-Justicia, A and Cianci, D (2015) Modelling the spatial distribution of the nuisance mosquito species Anopheles plumbeus (Diptera: Culicidae) in the Netherlands. Parasitology Vectors 8, 258.Google Scholar
Irwin, K (2010) A new and cryptic call type of the red crossbill. Western Birds 41, 10–25.Google Scholar
Janeway, CA, Travers, P, Walport, M and Shlomchik, M (2004) Immunobiology: The Immune System in Health and Disease. New York: Garland.Google Scholar
Kelsey, TR (2008) Foraging Ecology, Biogeography, and Population Dynamics of red Crossbills in North America. Vol. PhD Davis, CA: University of California.Google Scholar
Klasing, KC (2004) The costs of immunity. Acta Zoologica Sinica 50, 961–969.Google Scholar
Knowles, SC, Nakagawa, S and Sheldon, BC (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta regression approach. Functional Ecology 23, 405–415.Google Scholar
Knowles, SCL, Palinauskas, V and Sheldon, BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology 23, 557–569.Google Scholar
Koenig, WD and Knops, JMH (2000) Patterns of annual seed production by northern hemisphere trees: a global perspective. American Naturalist, 155, 59–69.Google Scholar
Latta, SC and Ricklefs, RE (2010) Prevalence patterns of avian haemosporida on Hispaniola. Journal of Avian Biology 41, 25–33.Google Scholar
Lee, KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integrative & Comparative Biology 46, 1000.Google Scholar
Leitner, W, Wali, T and Cotero-Saint Denis, A (2013) Is arthropod saliva the Achilles’ heel of vector-borne diseases? Frontiers in Immunology 4, 255.Google Scholar
Lovett, EL (2016) Population genetic structure and parasite communities in a nomadic songbird, the red crossbill (Loxia curvirostra). In Graduate Program in Biology, Vol. Masters The University of Western Ontario, London, Ontario, pp. 1–68.Google Scholar
Martínez-de la Puente, J, Merino, S, Tomas, G, Moreno, J, Morales, J, Lobato, E, Garcia-Fraile, S and Belda, EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters 6, 663–665.Google Scholar
Martin, LB, Weil, ZM and Nelson, RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 321.Google Scholar
Marzal, A, Bensch, S, Reviriego, M, Balbontin, J and de Lope, F (2008) Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979–987.Google Scholar
Matson, KD, Ricklefs, RE and Klasing, KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Developmental & Comparative Immunology 29, 275–286.Google Scholar
McAlpine, JF (1981) Manual of Neartic Diptera. Hull (Quebec), Canada: Agriculture Canada.Google Scholar
Merino, S, Moreno, J, Sanz, JJ and Arriero, E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society B 267, 2507–2510.Google Scholar
Millet, S, Bennett, J, Lee, KA, Hau, M and Klasing, KC (2007) Quantifying and comparing constitutive immunity across avian species. Developmental & Comparative Immunology 31, 188–201.Google Scholar
Monaghan, P and Nager, RG (1997) Why don't birds lay more eggs? Trends in Ecology & Evolution 12, 270–274.Google Scholar
Norte, AC, Araujo, PM, Sampaio, HL, Sousa, JP and Ramos, JA (2009) Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis 151, 677–688.Google Scholar
Pérez-Tris, J, Hasselquist, D, Hellgren, O, Krizanauskiene, A and Wald- enstro m̈, J and S, B (2005) What are malaria parasites? Trends in Parasitology 21, 209–211.Google Scholar
Podmokła, E, Dubiec, A, Drobniak, SM, Arct, A, Gustafsson, L and Cichoń, M (2014) Determinants of prevalence and intensity of infection with malaria parasites in the blue Tit. Journal of Ornithology 155, 721–727.Google Scholar
Podmokla, E, Dubiec, A, Drobniak, SM, Sudyka, J, Krupski, A, Arct, A, Gustafsson, L and Cichon, M (2017) Effect of haemosporidian infections on host survival and recapture rate in the blue tit. Journal of Avian Biology 48, 796–803.Google Scholar
Pyle, P (1997) Identification Guide to North American Birds. Part I. Columbidae to Ploceidae. Bolinas, CA, USA: Slate Creek Press.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Raberg, L, Sim, D and Read, A (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812–814.Google Scholar
Richards, SA (2005) Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86, 2805–2814.Google Scholar
Ricklefs, RE, Swanson, BL, Fallon, SM, Martínez-Abraín, A, Scheuerlein, A, Gray, J and Latta, SC (2005) Community relationships of avian malaria parasites in southern Missouri. Ecologiocal Monographs 75, 543–559.Google Scholar
Schmid-Hempel, P and Ebert, D (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 27–32.Google Scholar
Schultz, EM (2015) Seasonality and Environmental Regulation of Immunity and Parasitemia in the red Crossbill (Loxia curvirostraI). Vol. Ph.D., Davis, CA: University of California.Google Scholar
Schultz, EM, Hahn, TP and Klasing, KC (2017) Photoperiod but not food restriction modulates innate immunity in an opportunistic breeder, Loxia curvirostra. Journal of Experimental Biology 220, 722–730.Google Scholar
Sorci, G (2013) Immunity, resistance and tolerance in bird-parasite interactions. Parasite Immunology 35, 350–361.Google Scholar
Super, PE and van Riper, C III (1995) A comparison of avian hematozoan epizootiology in two California coastal scrub communities. Journal of Wildlife Diseases 31, 447–461.Google Scholar
Szollosi, E, Garamszegi, LZ, Hegyi, G, Laczi, M, Rosivall, B and Torok, J (2016) Haemoproteus infection status of collared flycatcher males changes within a breeding season. Parasitology Research 115, 4663–4672.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida: CRC Press.Google Scholar
Valkiunas, G, Bairlein, F, Iezhova, TA and Dolnik, OV (2004) Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla. Parasitology Research 93, 218–222.Google Scholar
Waite, J, Henry, A, Owen, J and Clayton, D (2014) An experimental test of the effects of behavioral and immunological defenses against vectors: do they interact to protect birds from blood parasites? Parasite & Vectors 7, 1–11.Google Scholar
Worms, M (1972) Circadian and seasonal rhythms in blood parasites In Canning, E and Wright, C (eds). Behavioural Aspects of Parasite Transmission. London: Academic Press, pp. 53–67.Google Scholar
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.Google Scholar
Zylberberg, M (2015) Common measures of immune function vary with time of day and sampling protocol in five passerine species. Journal of Experimental Biology 218, 757–766.Google Scholar
Zylberberg, M, Derryberry, EP, Breuner, CW, Macdougall-Shackleton, EA, Cornelius, JM and Hahn, TP (2015) Haemoproteus infected birds have increased lifetime reproductive success. Parasitology 142, 1033–1043.Google Scholar