The Science of Nature

, 104:21 | Cite as

Immune challenges and visual signalling in tree frogs

  • Julia L. Desprat
  • Thierry Lengagne
  • Nathalie Mondy
Original Paper

Abstract

In animals, mate-choice is often based on sexual signals that carry information and help the receiver make the best choice to improve the receiver’s fitness. Orange visual sexual signals have been hypothesised to carry immune information because they are often due to carotenoid pigments which are also involved in immunity response. Although many studies have focused on the direct relationships between coloration and immunocompetence, few studies have simultaneously studied immunocompetent response and coloration variation after an immune challenge. We tested this hypothesis on starved and ad libitum-fed males of the European tree frog Hyla arborea. Our results show that male coloration is not a reliable indicator of its immune response capacity in this species. However, after an immune challenge induced by a PHA (Phaseolus vulgaris phytohaemagglutinin) injection, starved males presented a significant coloration loss and this alteration was related to the immune response intensity. Taken together, these results suggest that the brighter (lighter) coloration may be used as a cue by female to exclude males with a recent immune challenge, due to diseases or parasites for example.

Keywords

Amphibian Coloration Hyla arborea Immunocompetence Phytohaemagglutinin 

Notes

Acknowledgments

The authors thank Adeline Dumet for the technical assistance and data collection during the experiments and Bernard Kaufmann for the English correction. JLD and NM contributed to the conception, design, data collection, interpretation of experiments, drafting and revision of the article. TL contributed to field work, drafting and revision of the article.

Compliance with ethical standards

Ethical notes

We obtained the European certificate that legally allows us to design and conduct experimental research work using live animals, and all work was performed with the approval of the ethics committee of University of Lyon 1 (BH2012–15). Frogs were housed in the EcoAquatron of University of Lyon, which is a facility approved by Veterinary Services (approval number 692661201). All males were released to the original pond the night after the end of the experiments.

Funding

This work was supported by the French Ministry of Higher Education and Research (to J.L.D., PhD grant 2012–2015).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Can J Zool 79:101–105. doi: 10.1139/z00-190 CrossRefGoogle Scholar
  2. Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659. doi: 10.1086/424971 PubMedGoogle Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Ardia DR (2005) Cross-fostering reveals an effect of spleen size and nest temperatures on immune responses in nestling European starlings. Oecologia 145:327–334. doi: 10.1007/s00442-005-0120-6 CrossRefPubMedGoogle Scholar
  5. Bize P, Piault R, Gasparini J, Roulin A (2010) Indirect costs of parasitism are shaped by variation in the type of immune challenge and food availability. Evol Biol 37:169–176. doi: 10.1007/s11692-010-9092-5 CrossRefGoogle Scholar
  6. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127. doi: 10.1126/science.1082142 CrossRefPubMedGoogle Scholar
  7. Bounous G, Letourneau L, Kongshavn PAL (1983) Influence of dietary-protein type on the immune-system of mice. J Nutr 113:1415–1421. doi: 10.1371/journal.pone.0084039 PubMedGoogle Scholar
  8. Brepson L, Voituron Y, Lengagne T (2013) Condition-dependent ways to manage acoustic signals under energetic constraint in a tree frog. Behav Ecol 24:488–496. doi: 10.1093/beheco/ars189 CrossRefGoogle Scholar
  9. Brinkhof MWG, Heeb P, Kolliker M, Richner H (1999) Immunocompetence of nestling great tits in relation to rearing environment and parentage. P Roy Soc Lond B Bio 266:2315–2322. doi: 10.1098/rspb.1999.0925 CrossRefGoogle Scholar
  10. Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558PubMedGoogle Scholar
  11. Buchanan K, Catchpole C, Lewis J, Lodge A (1999) Song as an indicator of parasitism in the sedge warbler. Anim Behav 57:307–314. doi: 10.1006/anbe.1998.0969 CrossRefPubMedGoogle Scholar
  12. Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257–261Google Scholar
  13. Cichon M, Sendecka J, Gustafsson L (2006) Genetic and environmental variation in immune response of collared flycatcher nestlings. J Evol Biol 19:1701–1706. doi: 10.1111/j.1420-9101.2006.01110.x CrossRefPubMedGoogle Scholar
  14. Davis A, Maney D, Maerz J (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. doi: 10.1111/j.1365-2435.2008.01467.x CrossRefGoogle Scholar
  15. Desprat JL, Lengagne T, Dumet A, Desouhant E, Mondy N (2015) Immunocompetence handicap hypothesis in tree frog: trade-off between sexual signals and immunity? Behav Ecol 26:1138–1146. doi: 10.1093/beheco/arv057 CrossRefGoogle Scholar
  16. Endler JA (1980) Natural-selection on color patterns in Poecilia reticulata. Evolution 34:76–91. doi: 10.2307/2408316
  17. Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103–103. doi: 10.1126/science.1081802 CrossRefPubMedGoogle Scholar
  18. Friedl TWP, Klump GM (2005) Sexual selection in the lek-breeding European treefrog: body size, chorus attendance, random mating and good genes. Anim Behav 70:1141–1154. doi: 10.1016/j.anbehav.2005.01.01 CrossRefGoogle Scholar
  19. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Available from the author upon request at dodogomez@yahoo.fr.Google Scholar
  20. Gomez D, Richardson C, Thery M, Lengagne T, Lena JP, Plenet S, Joly P (2011a) Multimodal signals in male European treefrog (Hyla arborea) and the influence of population isolation on signal expression. Biol J Linn Soc 103:633–647. doi: 10.1111/j.1095-8312.2011.01662.x CrossRefGoogle Scholar
  21. Gomez D, Thery M, Gauthier AL, Lengagne T (2011b) Costly help of audiovisual bimodality for female mate choice in a nocturnal anuran (Hyla arborea). Behav Ecol 22:889–898. doi: 10.1093/beheco/arr039 CrossRefGoogle Scholar
  22. Gomez D, Richardson C, Lengagne T, Derex M, Plenet S, Joly P, Lena JP, Thery M (2010) Support for a role of colour vision in mate choice in the nocturnal European treefrog (Hyla arborea). Behaviour 147:1753–1768. doi: 10.1163/000579510x534227 CrossRefGoogle Scholar
  23. Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Lena JP, Thery M (2009) The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). P Roy Soc Lond B Bio 276:2351–2358. doi: 10.1098/rspb.2009.0168 CrossRefGoogle Scholar
  24. Graham RI, Deacutis JM, Simpson SJ, Wilson K (2015) Body condition constrains immune function in field populations of female Australian plague locust Chortoicetes terminifera. Parasite Immunol 37:233–241. doi: 10.1111/pim.12179 CrossRefPubMedGoogle Scholar
  25. Griggio M, Zanollo V, Hoi H (2010) UV plumage color is an honest signal of quality in male budgerigars. Ecol Res 25:77–82. doi: 10.1007/s11284-009-0632-3 CrossRefGoogle Scholar
  26. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387. doi: 10.1126/science.7123238 CrossRefPubMedGoogle Scholar
  27. Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. J Avian Biol 31:559–566. doi: 10.1034/j.1600-048X.2000.310415.x CrossRefGoogle Scholar
  28. Ibanez A, Marzal A, Lopez P, Martin J (2013) Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa. Naturwissenschaften 100:1137–1147. doi: 10.1007/s00114-013-1118-2 CrossRefPubMedGoogle Scholar
  29. Ibáñez A, Polo-Cavia N, López P, Martín J (2014) Honest sexual signaling in turtles: experimental evidence of a trade-off between immune response and coloration in red-eared sliders Trachemys scripta elegans. Naturwissenschaften 101:803–811. doi: 10.1007/s00114-014-1219-6 CrossRefPubMedGoogle Scholar
  30. Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78(1):57–66. doi: 10.2307/3545800 CrossRefGoogle Scholar
  31. Josserand R, Troianowski M, Grolet O, Desprat JL, Lengagne T, Mondy N (2015) A phytohaemagglutinin challenge test to assess immune responsiveness of European tree frog Hyla arborea. Amphibia-Reptilia 36:111–118. doi: 10.1163/15685381-00002983 CrossRefGoogle Scholar
  32. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional-status and immunocompetence in northern bobwhite chicks. Auk 110:503–510. doi: 10.2307/4088414 CrossRefGoogle Scholar
  33. McGraw KJ (2007) Dietary mineral content influences the expression of melanin-based ornamental coloration. Behav Ecol 18:137–142. doi: 10.1093/beheco/arl059 CrossRefGoogle Scholar
  34. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712. doi: 10.1086/378904 CrossRefPubMedGoogle Scholar
  35. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159Google Scholar
  36. Mougeot F (2008) Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus. Naturwissenschaften 95:125–132. doi: 10.1007/s00114-007-0303-6 CrossRefPubMedGoogle Scholar
  37. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514. doi: 10.1016/s0169-5347(98)01484-0 CrossRefPubMedGoogle Scholar
  38. Parker TH, Stansberry BM, Becker CD, Gipson PS (2003) Do melanin-or carotenoid-pigmented plumage ornaments signal condition and predict pairing success in the Kentucky Warbler? Condor 105:663–671. doi: 10.1650/7335 CrossRefGoogle Scholar
  39. Perez-Rodriguez L, Mougeot F, Alonso-Alvarez C, Blas J, Vinuela J, Bortolotti GR (2008) Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa). J Exp Biol 211:2155–2161. doi: 10.1242/jeb.017178 CrossRefPubMedGoogle Scholar
  40. Peters A, Delhey K, Denk AG, Kempenaers B (2004) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59. doi: 10.1086/421302 CrossRefPubMedGoogle Scholar
  41. Plasman M, Hugo Reynoso V, Nicolas L, Torres R (2015) Multiple colour traits signal performance and immune response in the Dickerson's collared lizard Crotaphytus dickersonae. Behav Ecol Sociobiol 69:765–775. doi: 10.1007/s00265-015-1892-2 CrossRefGoogle Scholar
  42. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  43. Redpath SM, Appleby BM, Petty SJ (2000) Do male hoots betray parasite loads in tawny owls? J Avian Biol 31:457–462. doi: 10.1034/j.1600-048X.2000.310404.x CrossRefGoogle Scholar
  44. Richardson C, Gomez D, Durieux R, Thery M, Joly P, Lena JP, Plenet S, Lengagne T (2010b) Hearing is not necessarily believing in nocturnal anurans. Biol Lett 6:633–635. doi: 10.1098/rsbl.2010.0038 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Richardson C, Joly P, Lena JP, Plenet S, Lengagne T (2010a) The challenge of finding a high-quality male: a treefrog solution based on female assessment of male calls. Behaviour 147:1737–1752. doi: 10.1163/000579510x530221 CrossRefGoogle Scholar
  46. Richardson C, Popovici J, Bellvert F, Lengagne T (2009) Conspicuous colouration of the vocal sac of a nocturnal chorusing treefrog: carotenoid-based? Amphibia-Reptilia 30:576–580. doi: 10.1163/156853809789647095 CrossRefGoogle Scholar
  47. Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110CrossRefGoogle Scholar
  48. Saino N, Ninni P, Calza S, Martinelli R, De Bernardi F, Moller AP (2000) Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. P Roy Soc B-Biol Sci 267:57–61. doi: 10.1098/rspb.2000.0966 CrossRefGoogle Scholar
  49. Saks L, Ots I, Horak P (2003) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307. doi: 10.1007/s00442-002-1125-z CrossRefPubMedGoogle Scholar
  50. Simons MJP, Cohen AA, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds-a meta-analysis. PLoS One 7:14. doi: 10.1371/journal.pone.0043088 Google Scholar
  51. Singer MS, Mason PA, Smilanich AM (2014) Ecological immunology mediated by diet in herbivorous insects. Integr Comp Biol 54:913–921. doi: 10.1093/icb/icu089 CrossRefPubMedGoogle Scholar
  52. Smith HG, Raberg L, Ohlsson T, Granbom M, Hasselquist D (2007) Carotenoid and protein supplementation have differential effects on pheasant ornamentation and immunity. J Evol Biol 20:310–319. doi: 10.1111/j.1420-9101.2006.01203.x CrossRefPubMedGoogle Scholar
  53. Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189. doi: 10.1163/000579510x548673 CrossRefGoogle Scholar
  54. Szuroczki D, Koprivnikar J, Baker RL (2016) Dietary antioxidants enhance immunocompetence in larval amphibians. Comp Biochem Phys A 201:182–188. doi: 10.1016/j.cbpa.2016.07.014 CrossRefGoogle Scholar
  55. Toomey MB, Butler MW, McGraw KJ (2010) Immune-system activation depletes retinal carotenoids in house finches (Carpodacus mexicanus). J Exp Biol 213:1709–1716. doi: 10.1242/jeb.041004 CrossRefPubMedGoogle Scholar
  56. Vinkler M, Albrecht T (2010) Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health. Naturwissenschaften 97:19–28. doi: 10.1007/s00114-009-0595-9 CrossRefPubMedGoogle Scholar
  57. Vinkler M, Albrecht T (2011) Handling immunocompetence' in ecological studies: do we operate with confused terms? J Avian Biol 42:490–493. doi: 10.1111/j.1600-048X.2011.05499.x CrossRefGoogle Scholar
  58. Vinkler M, Bainova H, Albrecht T (2010) Functional analysis of the skin-swelling response to phytohaemagglutinin. Funct Ecol 24:1081–1086. doi: 10.1111/j.1365-2435.2010.01711.x CrossRefGoogle Scholar
  59. Voituron Y, Brepson L, Richardson C, Joly P, Lengagne T (2012) Energetics of calling in the male treefrog Hyla arborea: when being large means being sexy at low cost. Behaviour 149:775–793. doi: 10.1163/1568539x-00003004 CrossRefGoogle Scholar
  60. Weatherhead PJ, Metz KJ, Bennett GF, Irwin RE (1993) Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 33:13–23. doi: 10.1007/BF00164342 CrossRefGoogle Scholar
  61. Xu D-L, Liu X-Y, Wang D-H (2011) Food restriction and refeeding have no effect on cellular and humoral immunity in mongolian gerbils (Meriones unguiculatus). Physiol Biochem Zool 84:87–98. doi: 10.1086/657687 CrossRefPubMedGoogle Scholar
  62. Yeum K-J, Aldini G, Russell RM, Krinsky NI (2009) Antioxidant/pro-oxidant actions of carotenoids. In: Britton G, Pfander H, Liaaen-Jensen S (eds) Carotenoids: volume 5: nutrition and health. Birkhäuser Basel, Basel, pp 235–268. doi: 10.1007/978-3-7643-7501-0_12 Google Scholar
  63. Zahavi A (1975) Mate selection -selection for a handicap. J Theor Biol 53:205–214. doi: 10.1016/0022-5193(75)90111-3 CrossRefPubMedGoogle Scholar
  64. Zahavi A (1977) Cost of honesty - (further remarks on handicap principle). J Theor Biol 67:603–605. doi: 10.1016/0022-5193(77)90061-3 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Julia L. Desprat
    • 1
  • Thierry Lengagne
    • 1
  • Nathalie Mondy
    • 1
  1. 1.UMR 5023 LEHNA Écologie des Hydrosystèmes Naturels et AnthropisésUnivLyon, Université Claude Bernard Lyon 1, CNRS, ENTPEVilleurbanneFrance

Personalised recommendations