Abstract

Stress experienced during prenatal development—either applied to reproducing females (maternal stress), directly to developing offspring (embryonic stress) or in combination—is associated with a range of post-natal behavioral effects in numerous organisms. We conducted an experiment to discern if maternal and embryonic stressors affect the behavior of hatchlings of the cuttlefish Sepia officinalis, a species with features that allow for the examination of these stress types in isolation. Separating the impact of stress transmitted through the mother vs. stress experienced by the embryo itself will help clarify the behavioral findings in viviparous species for which it is impossible to disentangle these effects. We also compared the effect of a naturally-occurring (predator cue) and an “artificial” (bright, randomly-occurring LED light) embryonic stressor. This allowed us to test the hypothesis that a threat commonly faced by a species (natural threat) would be met with a genetically-programmed and adaptive response while a novel one would confound innate defense mechanisms and lead to maladaptive effects. We found that the maternal stressor was associated with significant differences in body patterning and activity patterns. By contrast, embryonic exposure to stressors increased the proportion of individuals that pursued prey. From these results, it appears that in cuttlefish, maternal and embryonic stressors affect different post-natal behavior in offspring. In addition, the effect of the artificial stressor suggests that organisms can sometimes react adaptively to a stressor even if it is not one that has been encountered during the evolutionary history of the species.

Highlights

  • Stress responses occur in reaction to any external or anticipated threat

  • We found that the maternal stressor was associated with significant differences in body patterning and activity patterns

  • Pairwise post hoc comparisons showed that mean heterogeneity index (HI) values are lower in unstressed mother controls (UM-C) eggs than in Wild mother eggs (WM) eggs (p < 0.001) and Stressed Mother offspring (SM) eggs (p = 0.034)

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Summary

Introduction

In response to a predator, for instance, an animal may increase its metabolism and divert resources to its muscles and away from less critical functions like digestion and foraging behavior—the “fight or flight” stress response (Cannon, 1939). In response to food scarcity, for instance, an animal may have the opposite reaction, prioritizing digestive processes to extract the maximum amount of energy from food items and even undertaking risky foraging behavior (Wang et al, 2006). While stress responses have presumably evolved to increase survival in the face of an immediate stressor, there is an increasing awareness that stress responses come with a host of negative fitness consequences. This often depends on whether the stressor causing

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