Abstract

Thermal extremes alter population processes, which can result in part from temperature-induced movement at different spatial and temporal scales. Thermal thresholds for animal movement likely change based on underlying thermal physiology and life-history stage, a topic that requires greater study. The intertidal porcelain crab Petrolisthes cinctipes currently experiences temperatures that can reach near-lethal levels in the high-intertidal zone at low tide. However, the thermal thresholds that trigger migration to cooler microhabitats, and the extent to which crabs move in response to temperature, remain unknown. Moreover, the influence of reproductive status on these thresholds is rarely investigated. We integrated demographic, molecular, behavioral, and physiological measurements to determine if behavioral thermal limits varied due to reproductive state. Demographic data showed a trend for gravid, egg bearing, crabs to appear more often under rocks in the cooler intertidal zone where crab density is highest. In situ expression of 31 genes related to stress, metabolism, and growth in the field differed significantly based on intertidal elevation, with mid-intertidal crabs expressing the gene for the reproductive yolk protein vitellogenin (vg) earlier in the season. Furthermore, VG protein levels were shown to increase with density for female hemolymph. Testing for temperatures that elicit movement revealed that gravid females engage in heat avoidance behavior at lower temperatures (i.e., have a lower voluntary thermal maximum, VTmax) than non-gravid females. VTmax was positively correlated with the temperature of peak firing rate for distal afferent nerve fibers in the walking leg, a physiological relationship that could correspond to the mechanistic underpinning for temperature dependent movement. The vulnerability of marine organisms to global change is predicated by their ability to utilize and integrate physiological and behavioral strategies in response to temperature to maximize survival and reproduction. Interactions between fine-scale temperature variation and reproductive biology can have important consequences for the ecology of species, and is likely to influence how populations respond to ongoing climate change.

Highlights

  • There is an increasing need to understand the effects of temperature on biota given ongoing global change

  • There were more rocks in the midintertidal zone (MIZ) with gravid females under them than in the high-intertidal zone (HIZ) (48 vs. 24%, respectively; Chi square test, X2 = 3.73, p = 0.054), but the proportion of females that were gravid did not differ between the MIZ and HIZ (0.49 vs. 0.43, respectively; Chi square test, X2 = 0.22, p = 0.637)

  • There was a significant sex × date interaction associated with expression PC2, where PC2 increased in females on average from July to December in both the HIZ and MIZ but remained relatively constant for males; PC2 had higher expression in females compared to males (Table 2B and Figure 4B; model explains 66% of the variation in PC2)

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Summary

Introduction

There is an increasing need to understand the effects of temperature on biota given ongoing global change. One major life-history stage that influences temperature-dependent behavior in females is gravidity or egg bearing (Cree and Hare, 2016). When given the choice within a laboratory thermal gradient, female alpine newts prefer a narrow range of temperatures for oviposition (Dvorák and Gvoždík, 2009), and thermal oviposition site selection is likely an adaptive behavior that promotes optimal temperatures for offspring survival and development in the butterfly Pyrgus armoricanus (Eilers et al, 2013). Some organisms, such as the crabs that are the focus of this study, carry their broods. There is a high cost of reproduction in marine invertebrates (Fernandez et al, 2000) and females must consider temperatures that maximize their own performance (Scheirs et al, 2000)

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