Freeze-tolerant frogs accumulate cryoprotectants using photoperiod: A potential ecological trap.

Abstract

Climate change is disrupting the reliability of photoperiod as a cue signalling seasonal changes in temperature. Temperate and Arctic species are especially vulnerable to this mismatch between photoperiod and temperature because winters are warming more rapidly in these areas relative to the rest of the world. Organisms relying on autumn photoperiods to trigger physiological adaptations to survive winter may incorrectly time the onset of winter and exhibit maladaptive responses. We exposed a freeze-tolerant amphibian, the eastern gray treefrog (Hyla versicolor), to variation in photoperiod and measured its cryoprotectant reserves (glycogen stored in the liver), thermal tolerance and post-metamorphic growth. We raised treefrogs under three photoperiods starting at egg development through the juvenile stage in the context of a warm growing environment. By the end of the experiment, juveniles were under photoperiods simulating late June, late September and early November (early, average and late, respectively). We show that gray treefrogs under the late-season photoperiod accumulated large reserves of cryoprotectants (i.e. 'antifreeze') and exhibited greater cold tolerance. Treefrogs raised under the late-season photoperiod had both higher concentrations of glycogen in liver tissue and larger livers compared to individuals from the other photoperiods. This resulted in treefrogs from the late-season photoperiod exhibiting 13.8 times more total liver glycogen compared to treefrogs in the early-season photoperiod and 8.2 times more reserves than treefrogs in the average-season photoperiod. Treefrogs under a late-season photoperiod also exhibited a lower critical thermal minimum but not critical thermal maximum compared to treefrogs from the early-season photoperiod. However, treefrogs in the late-season photoperiod also had reduced size-specific growth rates during the juvenile stage, indicating a potential cost to these physiological overwintering strategies. Photoperiod alone, without decreases in temperature, induced all of these physiological changes. Our results highlight the importance of photoperiod as a cue for overwintering preparation in a widespread North American amphibian. However, as climate change continues to expand the growing season, organisms relying on photoperiod to prepare for overwintering may therefore enter an ecological trap where photoperiod no longer accurately signals seasonal changes in temperature.