Non-reversible and Reversible Heat Tolerance Plasticity in Tropical Intertidal Animals: Responding to Habitat Temperature Heterogeneity

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.

Multigenerational experimental simulation of climate change on an economically important insect pest

“…The puzzling finding that fecundity and development survival of 2100 beetles are lower under their home conditions could be explained by the cost of thermal tolerance plasticity. When an organism is being thermally challenged, either by colder, warmer or highly variable temperatures, thermal tolerance plasticity tends to vary whether this organism is adapted to cold, warm, stable or instable temperatures (Angilletta, 2009; Brahim et al., 2019; MacLean et al., 2019). In our study, it is premature to attribute higher thermal tolerance plasticity to the resilience of 2017 insects or to the adaptability of 2100 insect's fecundity and survival when exposed to different conditions.…”

The impact of personality, morphotype and shore height on temperature‐mediated behavioural responses in the beadlet anemone Actinia equina

“…The effects of climate change can be seen particularly in the oceans; since 1971, global average ocean surface temperatures have increased at a rate of 0.11°C per decade (IPCC, 2013), with 2018 having been the hottest year in the oceans since records began (Cheng et al., 2019). Within ocean habitats, the effects of climate change are especially apparent in intertidal zones, as they are already subject to extremely high levels of spatial and temporal heterogeneity (Brahim, Mustapha, & Marshall, 2019). Different heights on the shore vary substantially in their exposure to environmental fluctuation (Bockelmann, Bakker, Neuhaus, & Lage, 2002).…”

“…This leads to highly niche‐specialized intertidal flora and fauna, adapted to live at different shore heights and so under differing levels of heterogeneity in their immediate environment (Allcock, Watts, & Thorpe, 1998; Dias, Christofoletti, Kitazawa, & Jenkins, 2018). Phenotypic differences across the gradient of the shore can also extend within species, and animals adapted to certain shore heights may be more susceptible to potential environmental changes than others (Brahim et al., 2019; Chapperon et al., 2016).…”

“…Actinia equina is highly sedentary, and morphotypes show significant ecological distinction in their distribution across shore heights (although there is some overlap; Allcock et al., 1998). This indicates that they are adapted to live at different heights on the shore (Quicke, Donoghue, & Brace, 1983), which vary in their thermal exposure (Brahim et al., 2019). Actinia equina therefore provides the opportunity not only to investigate differences in temperature‐mediated behavioural shifts at the level of the individual, but to further uncover how these might be linked to population‐level variation brought about by environmental heterogeneity (Monteiro, Solé‐Cava, & Thorpe, 1997).…”

The neritid snails of Brunei Darussalam: their geographical, ecological and conservation significance

“…Ecology and conservation. Inhabiting the upper intertidal zone, extending into the supratidal zone, high shore specialist N. insculpta is able to tolerate highly stressful environmental conditions (such as prolong exposure to extreme ambient air), with the littorinid snail Echinolittorina malaccana (e.g.,Vermeij & Hoeft 2018;Brahim et al 2019). Although several observations of this species have been made, it usually occurs in single numbers.…”