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Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system

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Abstract

Sex-biased parasitism highlights potentially divergent approaches to parasite resistance resulting in differing energetic trade-offs for males and females; however, trade-offs between immunity and self-maintenance could also depend on host body condition. We investigated these relationships in the big brown bat, Eptesicus fuscus, to determine if host sex or body condition better predicted parasite resistance, if testosterone levels predicted male parasite burdens, and if immune parameters could predict male testosterone levels. We found that male and female hosts had similar parasite burdens and female bats scored higher than males in only one immunological measure. Top models of helminth burden revealed interactions between body condition index and agglutination score as well as between agglutination score and host sex. Additionally, the strength of the relationships between sex, agglutination, and helminth burden is affected by body condition. Models of male parasite burden provided no support for testosterone predicting helminthiasis. Models that best predicted testosterone levels did not include parasite burden but instead consistently included month of capture and agglutination score. Thus, in our system, body condition was a more important predictor of immunity and worm burden than host sex.

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References

  • Allen DE, Little TJ (2011) Identifying energy constraints to parasite resistance. J Evol Biol 24:224–229

    Article  CAS  PubMed  Google Scholar 

  • Anderson RC, Chabaud AG, Willmott S (2009) Keys to the nematode parasites of vertebrates. Archival Volume. CAB International, Wallingford, UK

    Google Scholar 

  • Barnett CA, Suzuki TN, Sakaluk SK, Thompson CF (2015) Mass-based condition measures and their relationship with fitness: in what condition is condition? J Zool 296:1–5

  • Biard C, Monceau K, Motreuil S, Moreau J (2015) Interpreting immunological indices: the importance of taking parasite community into account. An example in blackbirds Turdus merula. Methods Ecol Evol 6:960–972

    Article  Google Scholar 

  • Blankespoor HD, Ulmer MJ (1970) Helminths from six species of Iowa bats. Proc Iowa Acad Sci 77:200–206

    Google Scholar 

  • Boonekamp JJ, Ros AHF, Verhulst S (2008) Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Lett 4:741–744

    Article  PubMed  PubMed Central  Google Scholar 

  • Bordes F, Ponlet N, de Bellocq JG, Ribas A, Krasnov BR, Morand S (2012) Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecol 170:123–135

    Article  Google Scholar 

  • Boyden SV (1965) Natural antibodies and the immune response. Adv Immunol 5:1–28

    Article  Google Scholar 

  • Bush A, Lafferty K, Lotz J, Shostak A (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Cai XQ, Yang M, Zhong WQ, Wang DH (2009) Humoral immune response suppresses reproductive physiology in male Brandt’s voles (Lasiopodomys brandtii). Zool 112:69–75

    Article  CAS  Google Scholar 

  • Chen J, Crispin JC, Tedder TF, Lucca JD, Tsokos GC (2009) B cells contribute to ischemia/reperfusion-mediated tissue injury. J Autoimmun 32:195–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coggins JR, Tedesco JL, Rupprecht CE (1982) Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte), in a Wisconsin hibernaculum. Am Mid Nat 107:305–315

    Article  Google Scholar 

  • Czaplinski B, Vaucher C (1994) Family Hymenolepididae Ariola, 1899. In: Khalil LF, Jones A, Bray RA (eds) Keys to the cestode parasites of vertebrates. CAB International, Wallingford, UK, pp 595–663

    Google Scholar 

  • Dare OK, Forbes MR (2009) Patterns of infection by lungworms, Rhabdias ranae and Haematoloechus spp., in northern leopard frogs: a relationship between sex and parasitism. J Parasitol 95:275–280

    Article  PubMed  Google Scholar 

  • Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772

    Article  Google Scholar 

  • Degen AA (2006) Effect of macroparasites on the energy budget of small mammals. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites: from evolutionary ecology to management. Springer, Tokyo, pp 372–399

  • Downs CJ, Brown JL, Wone B, Donovan ER, Hunter K, Hayes JP (2013) Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function. Proc Roy Soc B 280

  • Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94

    Article  Google Scholar 

  • Field A (2013) Discovering statistics using IBM SPSS statistics. Sage, New York

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Amer Nat 139:603–622

    Article  Google Scholar 

  • Forbes MR (2007) On sex differences in optimal immunity. Trends Ecol Evol 22:111–113

    Article  PubMed  Google Scholar 

  • Forsman AM, Vogel LA, Sakaluk SK, Grindstaff JL, Thompson CF (2008) Immune-challenged house wren broods differ in the relative strengths of their responses among different axes of the immune system. J Evol Biol 21:873–878

    Article  CAS  PubMed  Google Scholar 

  • Friesen OC, Roth JD, Graham LC (2015) Sex-biased parasitism in monogamous arctic foxes is driven by diet. J Mammal 96:417–424

    Article  Google Scholar 

  • Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev 198:185–202

    Article  CAS  PubMed  Google Scholar 

  • Gasque P (2004) Complement: a unique innate immune sensor for danger signals. Mol Immunol 41:1089–1098

    Article  CAS  PubMed  Google Scholar 

  • Giacomin PR, Wang H, Gordon DL, Dent LA (2004) Quantitation of complement and leukocyte binding to a parasitic helminth species. J Immunol Meth 289:201–210

    Article  CAS  Google Scholar 

  • Gooderham K, Schulte-Hostedde A (2011) Macroparasitism influences reproductive success in red squirrels (Tamiasciurus hudsonicus). Behav Ecol 22:1195–1200

    Article  Google Scholar 

  • Grinevitch L, Holroyd SL, Barclay RMR (1995) Sex-differences in the use of daily torpor and foraging time by big brown bats (Eptesicus fuscus) during the reproductive season. J Zool 235:301–309

    Article  Google Scholar 

  • Guerrero R, Martin C, Gardner SL, Bain O (2002) New and known species of Litomosoides (Nematoda: Filarioidea): important adult and larval characters and taxonomic changes. Comp Parasit 69:177–195

    Article  Google Scholar 

  • Hanssen SA, Folstad I, Erikstad KE, Oksanen A (2003) Costs of parasites in common eiders: effects of antiparasite treatment. Oikos 100:105–111

    Article  Google Scholar 

  • Hasu T, Valtonen ET, Jokela J (2006) Costs of parasite resistance for female survival and parental care in a freshwater isopod. Oikos 114:322–328

    Article  Google Scholar 

  • Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. The Guilford Press, New York, NY

    Google Scholar 

  • Hepworth MR, Hardman MJ, Grencis RK (2010) The role of sex hormones in the development of Th2 immunity in a gender-biased model of Trichuris muris infection. Eur J Immunol 40:406–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hillegass MA, Waterman JM, Roth JD (2008) The influence of sex and sociality on parasite loads in an African ground squirrel. Behav Ecol 19:1006–1011

    Article  Google Scholar 

  • Honkavaara J, Rantala MJ, Suhonen J (2009) Mating status, immune defence, and multi-parasite burden in the damselfly Coenagrion armatum. Entomol Exp Appl 132:165–171

    Article  Google Scholar 

  • Khan MN, Sajid MS, Khan MK, Iqbal Z, Hussain A (2010) Gastrointestinal helminthiasis: prevalence and associated determinants in domestic ruminants of district Toba Tek Singh, Punjab, Pakistan. Parasitol Res 107:787–794

    Article  PubMed  Google Scholar 

  • Kiffner C, Stanko M, Morand S, Khoklova IS, Shenbrot GI, Laudisoit A, Leirs H, Hawlena H, Krasnov BR (2013) Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecol 173:1009–1022

    Article  Google Scholar 

  • Krasnov BR, Bordes F, Khokhlova IS, Morand S (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76:1–13

  • Kumar V (1999) Lecithodendriid infections Trematode infections and diseases of man and animals. Kluwer Academic Publishers, Boston, MA, p 363

    Book  Google Scholar 

  • Kunz TH, Anthony ELP (1982) Age estimation and postnatal-growth in the bat Myotis lucifugus. J Mammal 63:23–32

    Article  Google Scholar 

  • Kurta A, Baker R (1990) Eptesicus fuscus. Mamm Species 356:1–10

    Article  Google Scholar 

  • Kurta A, Kunz TH, Nagy KA (1990) Energetics and water flux of free-ranging big brown bats (Eptesicus fuscus) during pregnancy and lactation. J Mammal 71:59–65

    Article  Google Scholar 

  • Lajeunesse MJ, Forbes MR, Smith BP (2004) Species and sex biases in ectoparasitism of dragonflies by mites. Oikos 106:501–508

    Article  Google Scholar 

  • Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC (2008) Constitutive immune defences correlate with life-history variables in tropical birds. J Anim Ecol 77:356–363

    Article  CAS  PubMed  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Lotz JM, Font WF (1983) Review of the Lecithodendriidae (Trematoda) from Eptesicus fuscus in Wisconsin and Minnesota. Proc Helminthol Soc Wash 50:83–102

    Google Scholar 

  • Lotz JM, Font WF (1985) Structure of enteric helminth communities in 2 populations of Eptesicus fuscus (Chiroptera). Can J Zool 63:2969–2978

    Article  Google Scholar 

  • Lotz JM, Font WF (2008) Family Lecithodendriidae. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, 3rd edn. CABI Publishing, Wallingford, UK, pp 527–536

    Google Scholar 

  • MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51:353–364

    Article  PubMed  Google Scholar 

  • Mallon EB, Loosli R, Schmid-Hempel P (2003) Specific versus nonspecific immune defense in the bumblebee, Bombus terrestris L. Evolution 57:1444–1447

    PubMed  Google Scholar 

  • Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299

    Article  Google Scholar 

  • Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans Roy Soc B 363:321–339

    Article  Google Scholar 

  • Marzal A, Reviriego M, de Lope F, Moller AP (2007) Fitness costs of an immune response in the house martin (Delichon urbica). Behav Ecol Sociobiol 61:1573–1580

    Article  Google Scholar 

  • Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286

    Article  CAS  PubMed  Google Scholar 

  • Mazerolle MJ (2006) Improving data analysis in herpetology: using Akaike’s Information Criterion (AIC) to assess the strength of biological hypotheses. Amphib-Reptil 27:169–180

    Article  Google Scholar 

  • McAllister C, Bursey C (2009) New host and geographic distribution records for helminths (Trematoda, Nematoda) in three species of vespertilionid bats (Chiroptera) from the Pine Ridge of Dawes County, Nebraska, USA. Comp Parasitol 76:117–121

    Article  Google Scholar 

  • McCurdy DG, Shutler D, Mullie A, Forbes MR (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82:303–312

    Article  CAS  Google Scholar 

  • Meeusen ENT, Balic A (2000) Do eosinophils have a role in the killing of helminth parasites? Parasitol Today 16:95–101

    Article  CAS  PubMed  Google Scholar 

  • Mendonca MT, Chernetsky SD, Nester KE, Gardner GL (1996) Effects of gonadal sex steroids on sexual behavior in the big brown bat, Eptesicus fuscus, upon arousal from hibernation. Horm Behav 30:153–161

    Article  CAS  PubMed  Google Scholar 

  • Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Amer Nat 173:475–487

    Article  Google Scholar 

  • Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Poikonen T (2010) Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution 64:166–179

    Article  PubMed  Google Scholar 

  • Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Rueda G (2011) Trade-off between immune response and body mass in wintering house sparrows (Passer domesticus). Ecol Res 26:943–947

    Article  Google Scholar 

  • Muehlenbein MP, Hirschtick JL, Bonner JZ, Swartz AM (2010) Toward quantifying the usage costs of human immunity: altered metabolic rates and hormone levels during acute immune activation in men. Am J Human Biol 22:546–556

    Article  Google Scholar 

  • Nakazawa M, Fantappie MR, Freeman GL, Eloi Santos S, Olsen NJ, Kovacs WJ, Secor WE, Colley DG (1997) Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Exp Parasit 85:233–240

    Article  CAS  PubMed  Google Scholar 

  • Nickel PA, Hansen MF (1967) Helminths of bats collected in Kansas, Nebraska, and Oklahoma. Am Mid Nat 78:481–486

    Article  Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Phil Trans Roy Soc 364:61–69

    Article  Google Scholar 

  • Palacios MG, Cunnick JE, Winkler DW, Vleck CM (2012) Interrelations among immune defense indexes reflect major components of the immune system in a free-living vertebrate. Physiol Biochem Zool 85:1–10

    Article  CAS  PubMed  Google Scholar 

  • Pearce RD, O’Shea TJ, Wunder BA (2008) Evaluation of morphological indices and total body electrical conductivity to assess body composition in big brown bats. Acta Chiropter 10:153–159

    Article  Google Scholar 

  • Perkins SE, Ferrari MF, Hudson PJ (2008) The effects of social structure and sex-biased transmission on macroparasite infection. Parasitol 135:1561–1569

    Article  CAS  Google Scholar 

  • Pistole D (1988) A survey of helminth parasites of chiropterans from Indiana. Proc Helminth Soc Wash 55:270–274

    Google Scholar 

  • Porteous IS, Pankhurst SJ (1998) Social structure of the mara (Dolichotis patagonum) as a determinant of gastro-intestinal parasitism. Parasitol 116:269–275

    Article  Google Scholar 

  • Poulin R (1996) Helminth growth in vertebrate hosts: does host sex matter? Int J Parasitol 26:1311–1315

    Article  CAS  PubMed  Google Scholar 

  • Rausch R (1975) Cestodes of the genus Hymenolepis Weinland, 1858 (sensu lato) from bats in North America and Hawaii. Can J Zool 53:1537–1551

    Article  CAS  PubMed  Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239

    Article  Google Scholar 

  • Robinson SA, Forbes MR, Hebert CE, McLaughlin JD (2008) Male-biased parasitism by common helminths is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus. J Avian Biol 39:272–276

    Article  Google Scholar 

  • Robinson SA, Forbes MR, Hebert CE, McLauglin JD (2010) Male biased parasitism in cormorants and relationships with foraging ecology on Lake Erie, Canada. Waterbirds 33:307–313

    Article  Google Scholar 

  • Rolff J (2002) Bateman’s principle and immunity. Proc Roy Soc B 269:867–872

    Article  Google Scholar 

  • Rossin MA, Malizia AI, Timi JT, Poulin R (2010) Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae). Parasitol 137:1569–1575

    Article  CAS  Google Scholar 

  • Russo J, Madec L (2013) Linking immune patterns and life history shows two distinct defense strategies in land snails (Gastropoda, Pulmonata). Physiol Biochem Zool 86:193–204

    Article  CAS  PubMed  Google Scholar 

  • Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74

    Article  Google Scholar 

  • Schell SC (1985) Handbook of trematodes of North America north of Mexico. Idaho Research Foundation, Moscow, ID

    Google Scholar 

  • Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc Roy Soc B 270:357–366

    Article  Google Scholar 

  • Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

    Article  Google Scholar 

  • Schroderus E, Jokinen I, Koivula M, Koskela E, Mapps T, Mills SC, Oksanen TA, Poikonen T (2010) Intra- and intersexual trade-offs between testosterone and immune system: implications for sexual and sexually antagonistic selection. Amer Nat 176:E90–E97

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Stoehr AM, Kokko H (2006) Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav Ecol 17:751–756

    Article  Google Scholar 

  • Superina M, Sierra R (2008) Hematology and serum chemistry values in captive and wild pichis, Zaedyus pichiy (Mammalia, Dasypodidae). J Wildl Dis 44:902–910

    Article  CAS  PubMed  Google Scholar 

  • Talleklint-Eisen L, Eisen RJ (1999) Abundance of ticks (Acari: Ixodidae) infesting the western fence lizard, Sceloporus occidentalis, in relation to environmental factors. Exp Appl Acarol 23:731–740

    Article  CAS  PubMed  Google Scholar 

  • Tkach VV (2008) Family Plagiorchiidae. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, 3rd edn. CAB International, Wallingford, UK, pp 296–325

    Google Scholar 

  • Tkach VV, Pawlowski J, Sharpilo VP (2000) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Muller, 1780). Syst Parasitol 47:9–22

    Article  CAS  PubMed  Google Scholar 

  • Ujvari B, Madsen T (2006) Age, parasites, and condition affect humoral immune response in tropical pythons. Behav Ecol 17:20–24

    Article  Google Scholar 

  • Waterman JM, Macklin GF, Enright C (2014) Sex-biased parasitism in Richardson’s ground squirrels (Urocitellus richardsonii) depends on the parasite examined. Can J Zool 92:73–79

    Article  Google Scholar 

  • Williams RR (1960) Acanthatrium lunatum n. sp., a parasite of the big brown bat and a key to the described species of Acanthatrium (Trematoda: Lecithodendriidae). Ohio J Sci 60:323–326

    Google Scholar 

  • Zuk M (2009) The sicker sex. PLoS Pathog 5:3

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

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Acknowledgments

The authors would like to thank J.W. Warburton, C.J. Warburton, D.J. Clarke, B.A. Hines, S.M. Warner, D.M. Courtney, B.K. Hubbard, L.M. Vanbladeren, H.E. LaFore, and E.M. Freed for their assistance in the field and in the lab. We appreciate the assistance of F.A. Jiménez in nematode identification. We would also like to thank J. Glatz for creating a map of our sites. Finally, we thank S.L. Kohler, S.A. Gill, and J.M. Lotz as well as two anonymous reviewers for their constructive comments on earlier versions of the manuscript. Funding was provided by the American Society of Mammalogists, the American Society of Parasitologists, the Annual Midwestern Conference of Parasitologists, and Western Michigan University.

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  1. Department of Biological Sciences, Western Michigan University, 1903 West Michigan Avenue, Kalamazoo, MI, 49008-5410, USA

    Elizabeth M. Warburton, Christopher A. Pearl & Maarten J. Vonhof

  2. Environmental and Sustainability Studies Program, Western Michigan University, 1903 West Michigan Avenue, Kalamazoo, MI, 49008-5410, USA

    Maarten J. Vonhof

  3. Present address: Department of Biomedical Sciences, Grand Valley State University, 1 Campus Drive, Allendale, MI, 49401, USA

    Christopher A. Pearl

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Warburton, E.M., Pearl, C.A. & Vonhof, M.J. Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system. Parasitol Res 115, 2155–2164 (2016). https://doi.org/10.1007/s00436-016-4957-x

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