Fecal sacs attract insects to the nest and provoke an activation of the immune system of nestlings

Frontiers in Zoology - Tập 13 - Trang 1-9 - 2016
Juan Diego Ibáñez-Álamo1,2, Francisco Ruiz-Raya3, Laura Rodríguez3, Manuel Soler3
1Behavioral and Physiological Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands
2Department Wetland Ecology, Estación Biológica de Doñana, C.S.I.C, Sevilla, Spain
3Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Granada, Spain

Tóm tắt

Nest sanitation is a widespread but rarely studied behavior in birds. The most common form of nest sanitation behavior, the removal of nestling feces, has focused the discussion about which selective pressures determine this behavior. The parasitism hypothesis, which states that nestling fecal sacs attract parasites that negatively affect breeding birds, was proposed 40 years ago and is frequently cited as a demonstrated fact. But, to our knowledge, there is no previous experimental test of this hypothesis. We carried out three different experiments to investigate the parasitism hypothesis. First, we used commercial McPhail traps to test for the potential attraction effect of nestling feces alone on flying insects. We found that traps with fecal sacs attracted significantly more flies (Order Diptera), but not ectoparasites, than the two control situations. Second, we used artificial blackbird (Turdus merula) nests to investigate the combined attraction effect of feces and nest materials on arthropods (not only flying insects). Flies, again, were the only group of arthropods significantly attracted by fecal sacs. We did not detect an effect on ectoparasites. Third, we used active blackbird nests to investigate the potential effect of nestling feces in ecto- and endoparasite loads in real nestlings. The presence of fecal sacs near blackbird nestlings did not increase the number of louse flies or chewing lice, and unexpectedly reduced the number of nests infested with mites. The endoparasite prevalence was also not affected. In contrast, feces provoked an activation of the immune system as the H/L ratio of nestlings living near excrements was significantly higher than those kept under the two control treatments. Surprisingly, our findings do not support the parasitism hypothesis, which suggests that parasites are not the main reason for fecal sac removal. In contrast, the attraction of flies to nestling feces, the elevation of the immune response of chicks, and the recently described antimicrobial function of the mucous covering of fecal sacs suggest that microorganisms could be responsible of this important form of parental care behavior (microbial hypothesis).

Tài liệu tham khảo

Guigueno MF, Sealy SG. Nest sanitation in passerine birds: implications for egg rejection in hosts of brood parasites. J Ornithol. 2012;153:35–52. Herrick FH. Care of nest and young. Auk. 1900;17:100–3. Thomson DF. Some adaptations for the disposal of faeces. The hygiene of the nest in australian birds. Proc Royal Soc B. 1934;46:701–7. Blair RH, Tucker BW. Nest sanitation. Br Birds. 1941;34:206–15. 26–35,50-55. Lang JD, Straight CA, Gowaty PA. Observations of fecal sac disposal by Eastern Bluebirds. Condor. 2002;104:205–7. Gow EA, Wiebe KL, Musgrove A. Nest sanitation in response to short- and long-term changes of brood size: males clean more in a sex-role-reversed species. Anim Behav. 2015;104:137–43. Weatherhead PJ. Fecal sac removal by tree swallows: the cost of cleanliness. Condor. 1984;86:187–91. Petit KE, Petit LJ, Petit DR. Fecal sac removal: do the pattern and distance of dispersal affect the chance of nest predation. Condor. 1989;91:479–82. Ibáñez-Álamo JD, Sanllorente O, Arco L, Soler M. Does nest predation risk induce parent birds to eat nestlings’ fecal sacs? An experimental study. Ann Zool Fenn. 2013;50:71–8. Ibáñez-Álamo JD, Ruiz-Raya F, Roncalli G, Soler M. Is nest predation an important selective pressure determining fecal sac removal? The effect of olfactory cues. J Ornithol. 2014;155:491–6. Petit DR, Petit LJ. Fecal sac dispersal by Prothonotary Warblers: Weatherhead’s hypothesis re-evaluated. Condor. 1987;89:610–3. Skutch AF. Parent birds and their young. Austin: University of Texas Press; 1976. Welty JC. The life of birds. 3rd ed. Philadelphia: CBS College; 1982. Gill FB. Ornithology. New York: WH Freeman; 1990. Bucher EH. Do birds use biological control against nest parasites? Parasitol Today. 1988;4:1–3. Loye JE, Zuk M. Bird-parasite interactions. Ecology, evolution and behaviour. Oxford: Oxford University Press; 1991. Royle NJ, Smiseth PT, Kölliker M. The evolution of parental care. Oxford: Oxford University Press; 2012. Allan SA, Bernier UR, Kline DL. Laboratory evaluation of avian odors for mosquito (Diptera: Culicidae) attraction. J Med Entomol. 2006;3:225–31. Syed Z, Leal WS. Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci U S A. 2009;106:18803–8. Cooperband MF, McElfresh JS, Millar JG, Cardé RT. Attraction of female Culex quinquefasciatus Say (Diptera: Culicidae) to odors from chicken feces. J Insect Physiol. 2008;54:1184–92. Hart BL. Behavioural defence. In: Clayton DH, Moore J, editors. Host-parasite evolution: general principles and avian models. Oxford: Oxford University Press; 1997. p. 59–77. Hurtrez-Boussès S, Renaud F, Blondel J, Perret P, Galan MJ. Effect of ectoparasites of young on parents’ behaviour in a Mediterranean population of Blue tits. J Avian Biol. 2000;31:266–9. Hurd H. Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol. 2003;48:141–61. Ferguson LV, Hillier NK, Smith TG. Influence of Hepatozoon parasites on host-seeking and host-choice behaviour of the mosquitoes Culex territans and Culex pipiens. Int J Parasitol. 2013;2:69–76. Saino N, Calza S, Møller AP. Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos. 1998;81:217–28. Biard C, Monceau K, Motreuil S, Moreau J. Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds Turdus merula. Methods Ecol Evol. 2015;6:960–72. Ibáñez-Álamo JD, Ruiz-Rodríguez M, Soler JJ. The mucous covering of fecal sacs prevents birds from infection with enteric bacteria. J Avian Biol. 2014;45:354–8. Cantarero A, López-Arrabé J, Redondo AJ, Moreno J. Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study. J Avian Biol. 2013;44:591–9. Duffy DC. The ecology of tick parasitism on densely nesting peruvian seabirds. Ecology. 1983;64:110–9. Duffy DC. Ants, ticks and nesting seabirds: dynamic interactions. In: Loye JE, Zuk M, editors. Bird-Parasite Interactions: Ecology, Evolution and Behaviour. Oxford: Oxford University Press; 1991. Dubiec A, Gózdz I, Mazgajski TD. Green plant material in avian nests. Avian Biol Res. 2013;6:133–46. Stanier RY, Ingraham JL, Wheelis ML, Painter PR. The Microbial World. Englewoods Cliffs: Prentice Hall; 1986. Niebuhr CN, Mays SE, Breeden JB, Lambert BD, Kattes DH. Efficacy of chemical repellents against Otobius megnini (Acari: Argasidae) and three species of ixodid ticks. Exp Appl Acarol. 2014;64:99–107. Quan R, Li H, Wang B, Goodale E. The relationship between defecation and feeding in nestling birds: observational and experimental evidence. Front Zool. 2015;12:21. Fallis AM, Desser SS. On species of Leucocytozoon, Haemoproteus and Hepatocystis. In: Kreier JP, editor. Parasitic protozoa, vol. III. London: Academic; 1977. p. 239–66. Hatchwell BJ, Wood MJ, Anwar M, Perrins CM. The prevalence and ecology of the haematozoan parasites of European blackbirds, Turdus merula. Can J Zool. 2000;78:684–7. Krams I, Vrublevska J, Cirule D, Kivleniece I, Krama T, Rantala MJ, et al. Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits (Parus major). Comp Biochem Physiol A. 2012;161:422–8. Lobato E, Moreno J, Merino S, Sanz JJ, Arriero E. Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Ecoscience. 2005;12:27–34. Glidden C. Immune system responses to ectoparasite infections in nestling Barn Swallows Hirundo rustica: an experimental approach. Undergraduate Honors Theses. Boulder: University of Colorado; 2013. Ziprin RL. Heterophil response to intraperitoneal challenge with invasion-deficient Salmonella enteritidis and Salmonella-immune lymphokines. Avian Dis. 1997;41:438–41. Davies AK, Cook KC, Altizer S. Leukocyte profiles in wild house finches with and without mycoplasmal conjuntivitis, a recently emerged bacterial disease. Ecohealth. 2004;1:362–73. Lombardo MP, Thorpe PA, Cichéwicz R, Henshaw M, Millard C, Steen C, et al. Communities of cloacal bacteria in tree swallow families. Condor. 1996;98:167–72. Brandl HB, van Dongen WFD, Drolová A, Kristofik J, Majtan J, Hoi H. Composition of bacterial assemblages in different components of reed warbler nests and a possible role of egg incubation in pathogen regulation. Plos One. 2014;9:e114861. Zurek L, Denning SS, Schal C, Watson DW. Vector competence of Musca domestica (Diptera: Muscidae) for Yersinia pseudotuberculosis. Med Entomol. 2001;38:333–5. Alam MJ, Zurek L. Association of Escherichia coli O157:H7 with houseflies on a cattle farm. Appl Environ Microbiol. 2004;70:7578–80. Gross WB, Siegel HS. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 1983;27:972–9. Davies AK, Maney AK, Maerz JC. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol. 2008;22:760–72. Amo L, Galván I, Tomás G, Sanz JJ. Predator odour recognition and avoidance in a songbird. Funct Ecol. 2008;22:289–93. Parejo D, Amo L, Rodríguez J, Avilés JM. Rollers smell the fear of nestlings. Biol Lett. 2012;8:502–4. Soler JJ, Pérez-Contreras T, De Neve L, Macías-Sánchez E, Møller AP, Soler M. Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism. J Evol Biol. 2014;27:1265–70. Soler JJ, de Neve L, Pérez-Contreras T, Soler M, Sorci G. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B. 2003;270:241–8. Mauck RA, Matson KD, Philipsborn J, Ricklefs RE. Increase in the constitutive innate humoral immune system in Leach’s Strom-Petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct Ecol. 2005;19:1001–7. Brzęk P, Konarzewski M. Relationship between avian growth rate and immune response depends on food availability. J Exp Biol. 2007;210:2361–7. Ibáñez-Álamo JD, Soler M. Does urbanization affect selective pressures and life-history strategies in common blackbirds (Turdus merula L.)? Biol J Linn Soc. 2010;101:759–66. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ. Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett. 2003;8:532–7. Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M. Antibiotic-producing bacteria as a possible defense of birds against pathogenic microorganisms. Open Ornithol J. 2010;3:93–100. Martín-Vivaldi M, Soler JJ, Peralta-Sánchez JM, Arco L, Martín-Platero AM, Martínez-Bueno M, et al. Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increases hatching success. J Anim Ecol. 2014;83:1289–301. Misof K. Diurnal cycle of Isospora spp. oocyst shedding in Eurasian blackbirds (Turdus merula). Can J Zool. 2004;82:764–8. Brooke M. Vertical transmission of feather lice between adult blackbirds Turdus merula and their nestlings: A lousy perspective. J Parasitol. 2010;96:1076–80. Bƚoszyk J, Bajerlein D, Gwiazdowicz DJ, Halliday RB, Dylewska M. Uropodine mite communities (Acari: Mesostigmata) in birds’ nest in Poland. Belg J Zool. 2006;136:145–53. Steyskal GC. History and use of the McPhail trap. Florida Entomol. 1977;60:11–7. Ricketts TH, Daily GC, Ehrlich PR. Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales. Biol Conserv. 2002;103:361–70. Various authors. Dimethyl 2,2-dichlorovinyl phosphate Hazard Assesment Report. Tokyo: Chemicals Evaluation and Research Institute; 2007. Barrientos JA. Curso práctico de entomología. Barcelona: Universitat Autònoma de Barcelona; 2004. Singh KK, Kotwaliwale N, Singh R. Effect of temperature and time on thermal disinfestation of green gram. J Agric Eng. 2009;46:14–7. Lodjak J, Mägi M, Tilgar V. Insulin-like growth factor 1 and growth rate in nestlings of a wild passerine bird. Funct Ecol. 2014;28:159–166. Clayton DH, Walther BA. Collection and quantification of arthropod parasites of birds. In: Clayton DH, Moore J, editors. Host-parasite evolution: General principles and avian models. Oxford: Oxford University Press; 1997. p. 419–40. Valkiunas G. Avian malaria parasites and other haemosporidia. New York: CRC Press; 2005. Merino S, Potti J, Fargallo JA. Blood parasites of passerine birds from Central Spain. J Wild Dis. 1997;33:638–41. Cirule D, Krama T, Vrublevska J, Rantala M, Krams I. A rapid effect of handling on counts of white blood cells in a wintering passerine bird: a mmore practical measure of stress? J Ornithol. 2012;153:161–6. Tuyttens FAM, de Graaf S, Heerkens JLT, Jacobs L, Nalon E, Ott S, et al. Observer bias in animal behaviour research: can we believe what we score, if we score what we believe? Anim Behav. 2014;90:273–80. Holman L, Head ML, Lanfear R, Jennions MD. Evidence of experimental bias in the life sciences: why we need blind data recording. PLoS Biol. 2015;13:e1002190. Kardish M, Mueller UG, Amador-Vargas S, Dietrich EI, Ma R, Barrett B, et al. Blind trust in unblinded observation in ecology, evolution, and behavior. Front Ecol Evol. 2015;3:51. Møller AP. Ectoparasites increase the cost of reproduction in their hosts. J Anim Ecol. 1993;62:309–22. Richner H, Heeb P. Are clutch and brood size patterns in birds shaped by ectoparasites? Oikos. 1995;73:435–41. Lee PLM, Clayton DH. Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success. Ecol Entomol. 1995;20:43–50.