Climatic stability, not average habitat temperature, determines thermal tolerance of subterranean beetles

Colado, Raquel; Pallarés, Susana; Fresneda, Javier; Mammola, Stefano; Rizzo, Valeria; Sánchez‐Fernández, David

doi:10.1002/ecy.3629

Cited by 14 publications

(10 citation statements)

References 73 publications

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“…To date, conservation of subterranean ecosystems has been dominated by problem‐based studies focused on identifying the main drivers associated with subterranean biodiversity decline (Mammola et al ., 2019a; Gerovasileiou & Bianchi, 2021). For example, we have elucidated the ecological impacts of polluted surface waters percolating underground (Di Lorenzo et al ., 2015, 2021; Manenti et al ., 2021), the long‐term consequences of climate change on specialised subterranean organisms adapted to thermally stable conditions (Mammola et al ., 2019c; Pallarés et al ., 2020a,b; Colado et al ., 2022), and some of the negative impacts that pathogens and alien species can cause to subterranean ecosystems (Howarth et al ., 2007; Wynne et al ., 2014; Howarth & Stone, 2020; Hoyt, Kilpatrick & Langwig, 2021).…”

Section: Introductionmentioning

confidence: 99%

Towards evidence‐based conservation of subterranean ecosystems

et al. 2022

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Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate metaanalytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.

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Section: Introductionmentioning

confidence: 99%

Towards evidence‐based conservation of subterranean ecosystems

et al. 2022

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“…As a result, small variations in temperature would have severe consequences for the survival and fitness of tropical species (Deutsch et al, 2008;Ghalambor, 2006). However, other studies have shown that some temperate species may be equally vulnerable to climate change (Colado et al, 2022;Johansson et al, 2020;Mi et al, 2022). For example, temperate species with short activity periods may only experience narrow ranges in temperature (Johansson et al, 2020) and may be selected for low thermal tolerance in a similar way to tropical species (Colado et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Thermoregulatory ability and mechanism do not differ consistently between neotropical and temperate butterflies

Laird‐Hopkins

Ashe-Jepson

Basset

et al. 2023

Global Change Biology

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Climate change is a major threat to species worldwide, yet it remains uncertain whether tropical or temperate species are more vulnerable to changing temperatures. To further our understanding of this, we used a standardised field protocol to (1) study the buffering ability (ability to regulate body temperature relative to surrounding air temperature) of neotropical (Panama) and temperate (the United Kingdom, Czech Republic and Austria) butterflies at the assemblage and family level, (2) determine if any differences in buffering ability were driven by morphological characteristics and (3) used ecologically relevant temperature measurements to investigate how butterflies use microclimates and behaviour to thermoregulate. We hypothesised that temperate butterflies would be better at buffering than neotropical butterflies as temperate species naturally experience a wider range of temperatures than their tropical counterparts. Contrary to our hypothesis, at the assemblage level, neotropical species (especially Nymphalidae) were better at buffering than temperate species, driven primarily by neotropical individuals cooling themselves more at higher air temperatures. Morphology was the main driver of differences in buffering ability between neotropical and temperate species as opposed to the thermal environment butterflies experienced. Temperate butterflies used postural thermoregulation to raise their body temperature more than neotropical butterflies, probably as an adaptation to temperate climates, but the selection of microclimates did not differ between regions. Our findings demonstrate that butterfly species have unique thermoregulatory strategies driven by behaviour and morphology, and that neotropical species are not likely to be more inherently vulnerable to warming than temperate species.

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“…Knowledge of the HSR in organisms from thermally stable subterranean habitats, including their associated inducible HSPs and at which temperatures this response might be activated, is scarce, with only a few studies devoted to invertebrate taxa 14 , 19 – 25 . However, invertebrates overwhelmingly contribute to the biodiversity of subterranean habitats compared to vertebrates 26 , 27 .…”

Section: Introductionmentioning

confidence: 99%

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2022

Sci Rep

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Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38 °C cf. 42–46 °C), but the genetic basis of this physiological difference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35 °C), as determined by comparative transcriptomics. However, genes involved in these responses differ between species and a far greater number were differentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only differentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular findings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

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Climatic stability, not average habitat temperature, determines thermal tolerance of subterranean beetles

Cited by 14 publications

References 73 publications

Towards evidence‐based conservation of subterranean ecosystems

Towards evidence‐based conservation of subterranean ecosystems

Thermoregulatory ability and mechanism do not differ consistently between neotropical and temperate butterflies

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

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