Abstract
The theory for thermal plasticity of tropical ectotherms has centered on terrestrial and open-water marine animals which experience reduced variation in diurnal and seasonal temperatures, conditions constraining plasticity selection. Tropical marine intertidal animals, however, experience complex habitat thermal heterogeneity, circumstances encouraging thermal plasticity selection. Using the tropical rocky-intertidal gastropod, Echinolittorina malaccana, we investigated heat tolerance plasticity in terms of laboratory acclimation and natural acclimatization of populations from thermally-dissimilar nearby shorelines. Laboratory treatments yielded similar capacities of snails from either population to acclimate their lethal thermal limit (LT50 variation was ∼2°C). However, the populations differed in the temperature range over which acclimatory adjustments could be made; LT50 plasticity occurred over a higher temperature range in the warm-shore snails compared to the cool-shore snails, giving an overall acclimation capacity for the populations combined of 2.9°C. In addition to confirming significant heat tolerance plasticity in tropical intertidal animals, these findings reveal two plasticity forms, reversible (laboratory acclimation) and non-reversible (population or shoreline specific) plasticity. The plasticity forms should account for different spatiotemporal scales of the environmental temperature variation; reversible plasticity for daily and tidal variations in microhabitat temperature and non-reversible plasticity for lifelong, shoreline temperature conditions. Non-reversible heat tolerance plasticity, likely established after larvae settle on the shore, should be energetically beneficial in preventing heat shock protein overexpression, but also should facilitate widespread colonization of coasts that support thermally-diverse shorelines. This first demonstration of different plasticity forms in benthic intertidal animals supports the hypothesis that habitat heterogeneity (irrespective of latitude) drives thermal plasticity selection. It further suggests that studies not making reference to different spatial scales of thermal heterogeneity, nor seeking how these may drive different thermal plasticity forms, risk misinterpreting ectothermic responses to environmental warming.
Highlights
Thermal plasticity enables ectothermic animals to modify their lifetime responses to environmental temperature
In the three cooler habitats, daily temperatures did not rise above 45◦C, the temperature around which a heat shock response (HSR) is induced (Marshall et al, 2011; Han et al, 2019), whereas peak temperatures in the warmest habitat surpassed 45◦C on 18 days (Figure 2)
Several factors influence long-term temperature variations in these tropical habitats, including seasonal and El Nino effects, our recordings for a narrow timeframe are representative of relative daily thermal regime differences between the habitats and shores
Summary
Thermal plasticity enables ectothermic animals to modify their lifetime responses to environmental temperature. In the context of climate warming, a complex theory for this plasticity has emerged, which considers its energetic benefits, environmental drivers and evolutionary constraints (see the beneficial acclimation hypothesis, and hypotheses for thermal variability, predictability and latitudinal effects; Leroi et al, 1994; Kingsolver and Huey, 1998; Wilson and Franklin, 2002; Angilletta et al, 2006; Deere and Chown, 2006; Gunderson and Stillman, 2015). Studies investigating environmental temperature variation as the primary driver of thermal plasticity selection, commonly consider latitudinal and seasonal effects (Angilletta, 2009) These studies frequently conclude that temperate species, which typically experience greater thermal variation possess a greater capacity for thermal acclimation than tropicallydistributed species, which experience relatively limited thermal variation (Gunderson and Stillman, 2015; Rohr et al, 2018). This may be true for most tropical animals and habitats, tropical marine intertidal habitats often promote extreme and variable temperature conditions, likely to drive thermal plasticity selection (Helmuth et al, 2006a,b; Marshall et al, 2010, 2018; Denny et al, 2011; Gedan et al, 2011)
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