skip to main content

Title: Diminished warming tolerance and plasticity in low-latitude populations of a marine gastropod
Abstract Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from native Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance − habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest more » climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations. « less
; ;
Cooke, Steve
Award ID(s):
Publication Date:
Journal Name:
Conservation Physiology
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Analyses of heat tolerance in insects often suggest that this trait is relatively invariant, leading to the use of fixed thermal maxima in models predicting future distribution of species in a warming world. Seasonal environments expose populations to a wide annual temperature variation. To evaluate the simplifying assumption of invariant thermal maxima, we quantified heat tolerance of 26 ant species across three seasons that vary two‐fold in mean temperature. Our ultimate goal was to test the hypothesis that heat tolerance tracks monthly temperature. Ant foragers tested at the end of the summer, in September, had higher average critical thermal maximum (CTmax) compared to those in March and December. Four out of five seasonal generalists, species actively foraging in all three focal months, had, on average, 6°C higher CTmaxin September. The invasive fire ant,Solenopsis invicta, was among the thermally plastic species, but the native thermal specialists still maintained higher CTmaxthanS. invicta. Our study shows that heat tolerance can be plastic, and this should be considered when examining species‐level adaptations. Moreover, the plasticity of thermal traits, while potentially costly, may also generate a competitive advantage over species with fixed traits and promote resilience to climate change.

  2. Abstract

    Capacity to cope with warming temperatures is a key determining factor of species' persistence under global climate change. Many successful invasive species have heightened thermal tolerance relative to their native counterparts, which may provide competitive advantages for habitat utilization and resource acquisition under warming scenarios, ultimately contributing to radically altered community composition. Enhanced transcriptional plasticity may be an important factor conferring superior abilities to cope with environmental stress, but the molecular mechanisms driving key differences of organismal traits in invasive versus native species are not well known. Although it is predicted that established invaders will evolve canalized phenotypes well‐adapted to new environments, it is not clear whether the same expectations are true for invaders of variable thermal environments or under climate warming scenarios where abilities to cope with fluctuating and increasing temperatures may provide fitness advantages. Here, we compare a highly successful invasive fish and a sympatric endangered native fish living in a dynamic estuarine environment that is projected to warm under climate change. We linked organismal physiological limits with global transcriptional responses at multiple common relative and absolute temperature thresholds and determined that heightened thermal tolerance of invasive Inland Silversides (Menidia beryllina) is associated with transcriptional changes thatmore »are greater both in the number of genes and the magnitude of response relative to native Delta Smelt (Hypomesus transpacificus). Modulated genes contributed to the enrichment of biological processes that differed between species and generally increased with temperature. These results are in concordance with the hypothesis that transcriptional plasticity may play a key role in determining population persistence, species interactions, and shaping community assemblages under climate change. Future studies encompassing a wider range of species and taxa are needed to determine whether this is a general pattern found between native and invasive species more broadly.

    « less
  3. Abstract

    Cities are rapidly expanding, and global warming is intensified in urban environments due to the urban heat island effect. Therefore, urban animals may be particularly susceptible to warming associated with ongoing climate change. We used a comparative and manipulative approach to test three related hypotheses about the determinants of heat tolerance or critical thermal maximum (CTmax) in urban ants—specifically, that (a) body size, (b) hydration status, and (c) chosen microenvironments influenceCTmax. We further tested a fourth hypothesis that native species are particularly physiologically vulnerable in urban environments. We manipulated water access and determinedCTmaxfor 11 species common to cities in California's Central Valley that exhibit nearly 300‐fold variation in body size. There was a moderate phylogenetic signal influencingCTmax, and inter (but not intra) specific variation in body size influencedCTmaxwhere larger species had higherCTmax. The sensitivity of ants’CTmaxto water availability exhibited species‐specific thresholds where short‐term water limitation (8 hr) reducedCTmaxand body water content in some species while longer‐term water limitation (32 hr) was required to reduce these traits in other species. However,CTmaxwas not related to the temperatures chosen by ants during activity. Further, we found support for our fourth hypothesis becauseCTmaxand estimates of thermal safety margin in native species were more sensitive tomore »water availability relative to non‐native species. In sum, we provide evidence of links between heat tolerance and water availability, which will become critically important in an increasingly warm, dry, and urbanized world that others have shown may be selecting for smaller (not larger) body size.

    « less
  4. Abstract

    Anthropogenic changes are often studied in isolation but may interact to affect biodiversity. For example, climate change could exacerbate the impacts of biological invasions if climate change differentially affects invasive and native species. Behavioural plasticity may mitigate some of the impacts of climate change, but species vary in their degree of behavioural plasticity. In particular, invasive species may have greater behavioural plasticity than native species since plasticity helps invasive species establish and spread in new environments. This plasticity could make invasives better able to cope with climate change.

    Here our goal was to examine whether reproductive behaviours and behavioural plasticity vary between an introduced and a nativeOnthophagusdung beetle species in response to warming temperatures and how differences in behaviour influence offspring survival.

    Using a repeated measures design, we exposed small colonies of introducedO. taurusand nativeO. hecateto three temperature treatments, including a control, low warming and high warming treatment, and then measured reproductive behaviours, including the number, size and burial depth of brood balls. We reared offspring in their brood balls in developmental temperatures that matched those of the brood ball burial depth to quantify survival.

    We found that the introducedO. taurusproduced more brood balls and larger brood balls, and buried brood ballsmore »deeper than the nativeO. hecatein all treatments. However, the two species did not vary in the degree of behavioural plasticity in response to warming. Differences in reproductive behaviours did affect survival such that warming temperatures had a greater effect on survival of offspring of nativeO. hecatecompared to introducedO. taurus.

    Overall, our results suggest that differences in behaviour between native and introduced species are one mechanism through which climate change may exacerbate negative impacts of biological invasions.

    « less
  5. Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.