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

Swierk, Lindsey; Graham, Sean P.; Langkilde, Tracy

doi:10.1007/s00265-014-1784-x

Cited by 13 publications

(13 citation statements)

References 45 publications

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“…Frogs receiving the ACTH-injections had significantly higher plasma levels of corticosterone than those sampled at rest (resting mean (SE) = 19.86 (1.18) ng/mL, ATCH-induced mean (SE) = 43.65 (1.20) ng/mL; β Injection = 0.342 ± 0.108, t 35.99 = 3.15, P = 0.003). The overnight housing of frogs did not cause a physiological stress response, as the resting values we measured were either similar to or below those collected from frogs within 2-3 min of capture (Swierk et al, 2014). While there was not a main effect of pond type on plasma corticosterone concentrations (β Interaction = 0.295 ± 0.229, t 32 = 1.291, P = 0.206; β Roadside = − 0.304 ± 0.154, t 32 = − 1.969, P = 0.058), there was a significant interaction between injection treatment and body mass residuals (β Interaction = − 0.223 ± 0.089, t 32 = − 2.508, P = 0.017; β Mass residuals = − 0.192 ± 0.054, t 32 = 3.575, P = 0.001, Fig.…”

Section: Adult Male Physiologysupporting

confidence: 53%

Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults

Hall

Brady

Mattheus

et al. 2017

Biological Conservation

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Aquatic organisms living adjacent to roads face many challenges posed by exposure to toxic runoff. The use of deicing road salt across northern latitudes has salinized nearby freshwater habitats. Freshwater amphibians exposed to road salt at early life stages typically experience reduced survival; however, few studies address laterlife effects. One study investigating whether populations can adapt to roadside ponds found survival in wood frog embryos raised in roadside environments was lowest in individuals with parents from roadside ponds. We investigated whether this negative response is also exhibited in late larval stages in reciprocally transplanted individuals from roadside populations and those located away from roads ('woodland' populations). We found reduced growth rates and more variable developmental rates in larvae raised in roadside ponds relative to woodland ponds regardless of origin, but no difference in survival between rearing environments. Laboratory exposure to road salt at relevant concentrations (0.6 ppt salinity) reduced larval activity and foraging behaviors, which may explain slower growth observed in the transplant experiment. Physiological assays of adult males migrating to breed revealed increased water retention in roadside populations. Further, these bloated males exhibited elevated resting plasma corticosterone levels and reduced capacity to secrete corticosterone when stimulated. Potential fitness consequences, such as reduced longevity and fecundity post metamorphosis through adulthood, of the roadside habitat could affect wood frog demography. Taken together, we provide evidence that the conditions experienced in the roadside environment pose challenges across life stages that have implications for persistence if populations are challenged with further stressors.

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Section: Adult Male Physiologysupporting

confidence: 53%

Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults

Hall

Brady

Mattheus

et al. 2017

Biological Conservation

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“…Wrestling can be intense, wounding or drowning females in the process (Trauth et al., ; Verrell & McCabe, ). Although female wood frogs maintain a somewhat higher physiological stress response to human handling and manipulation during breeding than do males (Swierk et al., ), it is unknown if females mount a physiological stress response when at the center of one of these “mating balls”. Due to the pervasiveness and inescapability of this risk, selection may favor any mechanism preventing the transfer of negative effects to offspring in response to forceful disengagement of amplexus.…”

Section: Discussionmentioning

confidence: 99%

“…Although it is widely understood that parental stress can negatively affect offspring (e.g., Meaney, Szyf, & Seckl, 2007;Robert, Vleck, & Bronikowski, 2009;Sheriff, Krebs, & Boonstra, 2009;Sheriff & Love, 2013) and that even brief handling or disturbance of parents (Bertin et al, 2008;Schreck, Contreras-Sanchez, & Fitzpatrick, 2001) or short-term exposure of unfertilized eggs to glucocorticoids (Sloman, 2010) can elicit these negative effects, whether investigator handling and manipulation of parents affect offspring in species that have modulated stress responses during breeding is largely untested. These species are frequently used in reproductive ecology research because their suppressed breeding-season responses to perceived threats, such as humans, permit close monitoring and manipulation of apparently natural reproductive behavior (e.g., garter snakes, wood frogs, Swierk, Graham, & Langkilde, 2014;sea turtles, Valverde, 1999 (Conant & Collins, 1998), have a time-constrained, highly synchronized breeding season of only a few days (2-6 days at our study sites). Wood frogs reproduce in vernal (temporary) pools soon after ice melts in early spring, and breeding is characterized by a male-biased sex ratio and scramble competition for females (Banta, 1914;Berven, 1981;Howard & Kluge, 1985).…”

Section: Introductionmentioning

confidence: 99%

“…Natural threats are substantial during the short breeding season (Trauth, McCallum, & Cartwright, 2000) and include predation during Seasonal alteration of behavioral and physiological stress responses may be a vital adaptation permitting wood frogs (and species with similar reproductive constraints) to successfully reproduce despite these risks (e.g., Moore, Lemaster, & Mason, 2000). Wood frogs suppress their physiological (as quantified by plasma corticosterone concentration) and behavioral (as quantified by time spent engaging in risky behavior) stress responses during the mating season (Swierk et al, 2014). In addition, there is strong evidence that maternal effects, including consequences of maternal environmental stress, influence offspring development and survival in wood frogs and other anuran amphibians (Berven, 1982;Kaplan & Phillips, 2006;Laurila, Karttunen, & Merila, 2002;Räsänen, Laurila, & Merilä, 2003, 2005Shu, Laurila, Suter, & Räsänen, 2016;Warne, Kardon, & Crespi, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Does repeated human handling of study animals during the mating season affect their offspring?

Swierk

Langkilde

2018

J Exp Zool Pt A

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Minimizing disturbance of study animals is a major consideration in ethological and ecological research design. One nearly universal type of disturbance is the handling of study animals as a component of trial setup. Even low to moderate levels of handling can be a substantial stressor to study animals, which may negatively affect their offspring via maternal effects. Understanding how routine human handling and manipulation may affect the outcome of research studies is therefore critical for interpreting study outcomes. We tested whether repeatedly handling and manipulating (i.e., manually disengaging) amplexed pairs of wood frogs (Rana sylvatica [Lithobates sylvaticus]), which have an explosive breeding season, would affect their reproductive output and offspring fitness. Handling and manipulation did not alter any parameter that we measured: reproductive timing, hatching success, and offspring larval duration, survival, and size at metamorphosis. These results suggest that handling and manipulation by researchers may have a negligible effect on wood frog reproduction and offspring fitness. It is possible that many species that are commonly used in reproductive studies because they suppress behavioral and physiological responses during the mating season are likewise unaffected by human handling. Nevertheless, researchers should examine possible consequences of methodological interventions on their study species in order to determine any potential influence on their results. Having a broad understanding of these effects on species that have robust or dampened stress responsiveness during the breeding season would be useful for making generalizations about potential effects.

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“…Males of many species are now known to carefully optimize and conserve their reproductive investments (Wedell, Gage & Parker, ). Courtship, mate competition, and mating are energetically costly and carry the risk of injury (Plaistow, Bollache & Cézilly, ; Kasumovic et al ., ; Swierk, Graham & Langkilde, ). It is also becoming more widely recognized that sperm and components of ejaculates are limited and constrain a male's mating frequency, copulation duration, and fertilization success (Dewsbury, ; Pitnick, ; Olsson, ; Hughes et al ., ; Preston et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Sperm depletion may not limit male reproduction in a capital breeder

Swierk

Tennessen

Langkilde

2015

Biol. J. Linn. Soc.

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Male reproduction is not only constrained by the number of encountered females but also by physiological limitations, including sperm production and the ability to sustain courtship and mating. Over a breeding season, sperm stores may drop in tandem with male energetic reserves or motivation, confounding the constraints imposed by sperm quantity with other correlated physiological limitations. We used wood frogs (Lithobates sylvaticus) to test whether explosive capital breeders are functionally limited by sperm depletion. We paired males with four conspecific females in succession and counted all of the fertilized and unfertilized eggs that each pair produced. In general, males did not experience a progressive decrease in fertilization rates with each mating (which is characteristic of sperm depletion). Instead, a few males experienced complete fertilization failure during their third and/or fourth mating, perhaps as a result of physical exhaustion, loss of motivation or hormonal changes. This pattern suggests that, even if male wood frogs do become increasingly sperm depleted over a breeding season, they are not necessarily limited by sperm. Understanding how and why fertilization rates change over multiple matings (i.e. incremental decrease vs. all-or-nothing) will help clarify the role of sperm depletion in limiting reproduction.

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

Cited by 13 publications

References 45 publications

Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults

Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults

Does repeated human handling of study animals during the mating season affect their offspring?

Sperm depletion may not limit male reproduction in a capital breeder

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