Behavioral Ecology and Sociobiology

, Volume 68, Issue 11, pp 1761–1768 | Cite as

The stress of scramble: sex differences in behavior and physiological stress response in a time-constrained mating system

  • Lindsey Swierk
  • Sean P. Graham
  • Tracy Langkilde
Original Paper


Iteroparous species maximize lifetime reproductive fitness by balancing current and future reproductive investments. In order to maximize fitness in the face of social or environmental heterogeneity, individuals of the same species may vary in whether they prioritize current reproductive opportunity or sacrifice immediate reproduction in order to prioritize survival and future reproductive potential. Glucocorticoid (GC) secretion plays an important role in mediating this trade-off by promoting behavioral and physiological responses associated with survival, often at the expense of nonessential (e.g., reproductive) functions. We used wood frogs (Lithobates sylvaticus [Rana sylvatica]) to test whether males and females differed in their (a) physiological response (plasma corticosterone [CORT] concentration) to standardized handling stress—a proxy for predation threat—and (b) performance of reproductive behaviors that may enhance their conspicuousness to predators. We also tested whether levels of male competition influenced sex differences in these factors, as more intense competition may require males to devote more time to risky reproductive behaviors. We found that females had lower baseline CORT but exhibited a significantly greater CORT response to a stressor and spent less time performing potentially risky behavior (surface floating) than did males. These sex differences were consistent across different levels of male mating competition. Our results reveal that during breeding, males and females may differentially respond to stressors and perform risk-prone behaviors, despite facing the same extreme breeding constraints, providing new insight into the survival-reproduction trade-off of explosively breeding species.


Amphibian Corticosterone Life-history trade-off Reproduction Male competition Sex differences 



We thank the Cavener Lab for use of their plate reader. We are grateful to Jennifer Tennessen, Brad Carlson, Vincent Faguliani, Jill Newman, and John Swierk for the field assistance; Courtney Norjen and Tyler Jacobs for the laboratory assistance; Crystal Kelehear Graham for the statistical advice and support; and the Hildebrand family for their support and enthusiasm. We thank B. Chitterlings for the comments on an early draft of this article. This research was funded by the National Science Foundation (DGE-1255832 to LS and IOS-1051367 to TL); any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Ethical standards

This work adhered to the national and international standards on animal welfare, the legal requirements of the USA, and the Institutional Guidelines of Penn State University (IACUC #33346). This work was approved by the Pennsylvania Fish and Boat Commission (Permit #483, Type 1) and the Pennsylvania Game Commission (Permit #NC-028-2012, NC-027-2011, NC-019-2010).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Arak A (1988) Callers and satellites in the natterjack toad: evolutionarily stable decision rules. Anim Behav 36:416–432CrossRefGoogle Scholar
  2. Aubret F, Bonnet X, Shine R, Lourdais O (2002) Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis). Horm Behav 42:135–147PubMedCrossRefGoogle Scholar
  3. Baldwin RF, Demaynadier PG, Calhoun AJK (2007) Rana sylvatica (wood frog) predation. Herpetol Rev 38:194–195Google Scholar
  4. Balm PHM (1999) Stress physiology in animals. Sheffield Academic, SheffieldGoogle Scholar
  5. Banta AM (1914) Sex recognition and the mating behavior of the wood frog, Rana sylvatica. Biol Bull 26:171–183CrossRefGoogle Scholar
  6. Berven KA (1981) Mate choice in the wood frog, Rana sylvatica. Evolution 35:707–722CrossRefGoogle Scholar
  7. Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599–1608CrossRefGoogle Scholar
  8. Cease AJ, Lutterschmidt DI, Mason RT (2007) Corticosterone and the transition from courtship behavior to dispersal in male red-sided garter snakes (Thamnophis sirtalis parietalis). Gen Comp Endocrinol 150:124–131PubMedCrossRefGoogle Scholar
  9. Chuang M-F, Bee MA, Kam Y-C (2013) Short amplexus duration in a territorial anuran: a possible adaptation in response to male-male competition. PLoS ONE 8:e83116PubMedCrossRefPubMedCentralGoogle Scholar
  10. Cockrem JF, Silverin B (2002) Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen Comp Endocrinol 125:248–255PubMedCrossRefGoogle Scholar
  11. Conant R, Collins JT (1998) A field guide to reptiles and amphibians of eastern and central North America. Houghton Mifflin Company, BostonGoogle Scholar
  12. Dunbar RIM, Dunbar EP (1977) Dominance and reproductive success among female gelada baboons. Nature 266:351–352PubMedCrossRefGoogle Scholar
  13. French SS, McLemore R, Vernon B, Johnston GIH, Moore MC (2007) Corticosterone modulation of reproductive and immune systems trade-offs in female tree lizards: long-term corticosterone manipulations via injectable gelling material. J Exp Biol 210:2859–2865PubMedCrossRefGoogle Scholar
  14. Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1–24CrossRefGoogle Scholar
  15. Greenberg NT, Wingfield JC (1987) Stress and reproduction: reciprocal relationships. In: Norris DO, Jones RE (eds) Hormones and reproduction in fishes, amphibians and reptiles. Plenum, New York, pp 461–503CrossRefGoogle Scholar
  16. Gross MR (2005) The evolution of parental care. Q Rev Biol 80:37–45PubMedCrossRefGoogle Scholar
  17. Guillette LJ Jr, Cree A, Rooney AA (1995) Biology of stress: interactions with reproduction, immunology and intermediary metabolism. In: Warwick C, Frye FL, Murphy JB (eds) Health and welfare of captive reptiles. Chapman and Hall, London, pp 32–81CrossRefGoogle Scholar
  18. Hadley ME (1996) Endocrinology. Prentice Hall, New JerseyGoogle Scholar
  19. Harvey LA, Propper CR, Woodley SK, Moore MC (1997) Reproductive endocrinology of the explosively breeding desert spadefoot toad, Scaphiopus couchii. Gen Comp Endocrinol 105:102–113PubMedCrossRefGoogle Scholar
  20. Higham JP, Heistermann M, Maestripieri D (2013) The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67:19–30PubMedCrossRefPubMedCentralGoogle Scholar
  21. Höbel G, Kolodziej RC (2013) Wood frogs (Lithobates sylvaticus) use water surface waves in their reproductive behaviour. Behaviour 150:471–483Google Scholar
  22. Howard RD (1980) Mating behaviour and mating success in woodfrogs Rana sylvatica. Anim Behav 28:705–716CrossRefGoogle Scholar
  23. Howard RD, Kluge AG (1985) Proximate mechanisms of sexual selection in wood frogs. Evolution 39:260–277CrossRefGoogle Scholar
  24. Jasnow AM, Drazen DL, Huhman KL, Nelson RJ, Demas GE (2001) Acute and chronic social defeat suppresses humoral immunity of male Syrian hamsters (Mesocricetus auratus). Horm Behav 40:428–433PubMedCrossRefGoogle Scholar
  25. Jørgensen CB (1981) Ovarian cycle in a temperate zone frog, Rana temporaria, with special reference to factors determining number and size of eggs. J Zool 195:449–458CrossRefGoogle Scholar
  26. Jørgensen CB (1982) Factors controlling the ovarian cycle in a temperate zone anuran, the toad Bufo bufo: food uptake, nutritional state, and gonadotropin. J Exp Zool 224:437–443PubMedCrossRefGoogle Scholar
  27. Juszczyk W (1959) The development of reproductive organs of the female common frog (Rana temporaria) in the yearly cycle. Annales UMCS 14:169–231Google Scholar
  28. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating in guppies (Poecilia reticulata). Behav Ecol 16:294–300CrossRefGoogle Scholar
  29. Martínez-Rivera CC, Gerhardt HC (2008) Advertisement-call modification, male competition, and female preference in the bird-voiced treefrog Hyla avivoca. Behav Ecol Sociobiol 63:195–208PubMedCrossRefPubMedCentralGoogle Scholar
  30. McGrady AV (1984) Effects of psychological stress on male reproduction: a review. Syst Biol Reprod Med 13:1–7CrossRefGoogle Scholar
  31. Mendonça MT, Licht P, Ryan MJ, Barnes R (1985) Changes in hormone levels in relation to breeding behavior in male bullfrogs (Rana catesbeiana) at the individual and population levels. Gen Comp Endocrinol 58:270–279PubMedCrossRefGoogle Scholar
  32. Moore FL, Miller LJ (1984) Stress-induced inhibition of sexual behavior: corticosterone inhibits courtship behaviors of a male amphibian (Taricha granulosa). Horm Behav 18:400–410PubMedCrossRefGoogle Scholar
  33. Moore FL, Orchinik M (1994) Membranes receptors for corticosterone: a mechanism for rapid behavioral responses in an amphibian. Horm Behav 28:512–519PubMedCrossRefGoogle Scholar
  34. Moore IT, Greene MJ, Mason RT (2001) Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male garter snake, Thamnophis sirtalis. J Exp Zool 289:99–108PubMedCrossRefGoogle Scholar
  35. Moore IT, Jessop TS (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39–47PubMedCrossRefGoogle Scholar
  36. Noble GK, Farris EJ (1929) The method of sex recognition in the wood frog Rana sylvatica Le Conte. Am Mus Novit 363:1–17Google Scholar
  37. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  38. Rittenhouse TAG, Semlitsch RD, Thompson FR III (2009) Survival costs associated with wood frog breeding migration: effects of timber harvest and drought. Ecology 90:1620–1630PubMedCrossRefGoogle Scholar
  39. Romero MJ (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255PubMedCrossRefGoogle Scholar
  40. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Phys A 140:73–79CrossRefGoogle Scholar
  41. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, and preparative actions. Endocr Rev 21:55–89PubMedGoogle Scholar
  42. Schwarzkopf L (1993) Costs of reproduction in water skinks. Ecology 74:1970–1981CrossRefGoogle Scholar
  43. Silverin B, Wingfield JC (1998) Adrenocortical responses to stress in breed pied flycatchers, Ficedula hypoleuca: relation to latitude, sex, and mating status. J Avian Biol 29:228–234CrossRefGoogle Scholar
  44. Sirinathsinghji DJS, Rees LH, Rivier J, Vale W (1983) Corticotropin-releasing factor is a potent inhibitor of sexual receptivity in the female rat. Nature 305:232–235PubMedCrossRefGoogle Scholar
  45. Skjæraasen JE, Nash RDM, Korsbrekke K, Fonn M, Nilsen T et al (2012) Frequent skipped spawning in the world’s largest cod population. Proc Natl Acad Sci U S A 109:8995–8999PubMedCrossRefPubMedCentralGoogle Scholar
  46. Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51:3–47PubMedCrossRefGoogle Scholar
  47. Tavecchia G, Pradel R, Boy V, Johnson AR, Cézilly F (2001) Sex- and age-related variation in survival and cost of first reproduction in greater flamingos. Ecology 82:165–174CrossRefGoogle Scholar
  48. Tedesco PA, Benito J, García-Berthou E (2008) Size-independent age effects on reproductive effort in a small, short-lived fish. Freshwater Biol 53:865–871CrossRefGoogle Scholar
  49. Thaker M, Vanak AT, Lima SL, Hews DK (2010) Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat 175:50–60PubMedCrossRefGoogle Scholar
  50. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871-1971. Aldine Publishing, Chicago, pp 136–179Google Scholar
  51. Tully T, Ferrière R (2008) Reproductive flexibility: genetic variation, genetic costs and long-term evolution in a collembola. PLoS ONE 3:e3207PubMedCrossRefPubMedCentralGoogle Scholar
  52. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690CrossRefGoogle Scholar
  53. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage.”. Am Zool 38:191–206Google Scholar
  54. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Endocrinol 15:711–724Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lindsey Swierk
    • 1
    • 3
  • Sean P. Graham
    • 1
    • 2
  • Tracy Langkilde
    • 1
  1. 1.Department of Biology, Intercollege Graduate Degree Program in Ecology, and the Center for Brain, Behavior, and CognitionThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.College of ScienceUniversity of FindlayFindlayUSA
  3. 3.University ParkUSA

Personalised recommendations