Climate change going deep: The effects of global climatic alterations on cave ecosystems

Mammola, Stefano; Piano, Elena; Cardoso, Pedro; Vernon, Philippe; Domínguez‐Villar, David; Culver, David C.; Pipan, Tanja; Isaia, Marco

doi:10.1177/2053019619851594

Cited by 85 publications

(101 citation statements)

References 143 publications

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“…Our study has also important implications for determining the vulnerability of subterranean species to anthropogenic climate change. Climate change is expected to affect deep subterranean habitats (Mammola, Piano, Cardoso, et al, ; Taylor et al, ), especially by increasing ambient temperature and reducing moisture content, although with a certain delay due to the thermal inertia of the rock (Mammola, Piano, Cardoso, et al, ). In this context, the likelihood of evolutionary responses will depend on the magnitude and rates of warming within subterranean habitats.…”

Section: Discussionmentioning

confidence: 99%

Extending Janzen’s hypothesis to temperate regions: A test using subterranean ecosystems

et al. 2019

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Janzen’s hypothesis (1967; American Naturalist) predicts that tropical habitats with reduced thermal seasonality would select for species with narrow thermal tolerance, thereby limiting dispersal among sites of different elevations showing little overlap in temperature. These predictions have so far been tested by confronting tropical and temperate mountain communities, leaving unresolved the question of their generalization to habitats with low thermal seasonality outside the tropics. We provide the first extension of Janzen’s hypothesis to temperate habitats, by testing for differences in thermal tolerance and elevational range among congeneric alpine spiders (Araneae: Linyphiidae: Troglohyphantes) occurring along a steep gradient of decreasing thermal seasonality with increasing cave depth. Using species from the same temperate region rather than from distinct biogeographic regions avoids confounding the effects of short‐ and long‐term climatic variability on thermal tolerance and elevational range extent. Following Jansen’s assumptions, we predicted that cave habitats with low thermal seasonality would select for narrow thermal tolerance. Also, specialized subterranean species would exhibit both narrower elevational range extents and smaller realized thermal niche breadths. Initially, we showed that thermal seasonality and the overlap in temperature across caves were considerably lower in deep than in shallow cave habitats. Then, we measured thermal tolerance and used morphological traits to quantify the degree of specialization to subterranean life of 11 spider species. We found that thermal tolerance decreased with increasing subterranean specialization. Deep subterranean species reached their critical temperature at 1–4°C above their habitat temperature, whereas shallow subterranean species withstood a twofold larger temperature increase. At last, we demonstrated that a species’ elevational range extent and the variation of temperature encountered across its range decreased with increasing specialization to deep subterranean life. Our integrative work, being grounded in organismal and habitat measures, represents the first generalization of Janzen’s framework to caves and provides a conceptual framework to disentangle the effect of long‐term climate variability on subterranean biodiversity patterns. Extending Janzen’s thoughts to a broader range of ecosystems is key to understanding how the ecological specialization–dispersal trade‐off may constrain the response of species to climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Discussionmentioning

confidence: 99%

Extending Janzen’s hypothesis to temperate regions: A test using subterranean ecosystems

et al. 2019

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“…In summer, maximum surface temperatures in the study site exceed or are very close to the ULTs of the species studied here. Although warming will be buffered and delayed in subterranean systems (Domínguez‐Villar, Lojen, Krklec, Baker, & Fairchild, ), these will not escape from the effects of climate change (Mammola, Goodacre, & Isaia, ; Mammola, Piano, Cardoso, et al, ). We show here that subterranean species, even those living under the same climatic and stable conditions, might be differently affected by global warming.…”

Section: Discussionmentioning

confidence: 99%

Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions

Pallarés

Colado

Pérez‐Fernández³

et al. 2019

Ecology and Evolution

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Cave‐dwelling ectotherms, which have evolved for millions of years under stable thermal conditions, could be expected to have adjusted their physiological limits to the narrow range of temperatures they experience and to be highly vulnerable to global warming. However, most of the few existing studies on thermal tolerance in subterranean invertebrates highlight that despite the fact that they show lower heat tolerance than most surface‐dwelling species, their upper thermal limits are generally not adjusted to ambient temperature. The question remains to what extent this pattern is common across subterranean invertebrates. We studied basal heat tolerance and its plasticity in four species of distant arthropod groups (Coleoptera, Diplopoda, and Collembola) with different evolutionary histories but under similar selection pressures, as they have been exposed to the same constant environmental conditions for a long time. Adults were exposed at different temperatures for 1 week to determine upper lethal temperatures. Then, individuals from previous sublethal treatments were transferred to a higher temperature to determine acclimation capacity. Upper lethal temperatures of three of the studied species were similar to those reported for other subterranean species (between 20 and 25°C) and widely exceeded the cave temperature (13–14°C). The diplopod species showed the highest long‐term heat tolerance detected so far for a troglobiont (i.e., obligate subterranean) species (median lethal temperature after 7 days exposure: 28°C) and a positive acclimation response. Our results agree with previous studies showing that heat tolerance in subterranean species is not determined by environmental conditions. Thus, subterranean species, even those living under similar climatic conditions, might be differently affected by global warming.

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“…It is worth noting that climate change will also determine substantial environmental changes in the subterranean habitats that this species uses as breeding sites (Figure S1). While the effects of climate change are largely studied in surface habitats, the impacts on subterranean habitats are still poorly explored (Mammola, Cardoso, et al, ; Mammola, Piano, et al, ). Andrias davidianus primarily exploits habitats at the surface/subterranean interface for breeding (Liang et al, ; Luo et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Andrias davidianus primarily exploits habitats at the surface/subterranean interface for breeding (Liang et al, ; Luo et al, ). The temperature increment in these transitional subterranean habitats is expected to parallel the external one almost synchronically (Mammola, Piano, et al, ). Furthermore, climate change is expected to determine drops in relative humidity and even desiccation of subterranean habitats (Mammola, Piano, et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…As one of the most serious global environmental concerns, climate change poses multiple threats to terrestrial (Burrows et al, ), freshwater (Mantyka‐Pringle, Martin, Moffatt, Linke, & Rhodes, ), marine (Burrows et al, ; Dulvy et al, ), and subterranean ecosystems (Mammola, Piano, et al, ), encompassing habitat change, biodiversity loss, alterations in species interactions, and shifts in species phenology (Bellard, Bertelsmeier, Leadley, Thuiller, & Courchamp, ; Parmesan, ). For instance, previous studies have demonstrated that in response to global warming, terrestrial species are shifting their distribution towards higher altitudes or latitudes (Chen, Hill, Ohlemüller, Roy, & Thomas, ) and marine species are even migrating to deeper waters (Dulvy et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Future climate change will severely reduce habitat suitability of the Critically Endangered Chinese giant salamander

Zhang

Mammola

Liang³

et al. 2020

Freshwater Biology

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Being the largest extant amphibian in the world, the IUCN Critically Endangered Chinese giant salamander Andrias davidianus is a charismatic species with great international public interest. While threats such as commercial overexploitation and habitat degradation have been extensively documented to affect natural populations of A. davidianus, still no information is available about the species sensitivity to climate change. Here, we develop an ensemble of species distribution models (SDMs) for A. davidianus and projected its habitat suitability under present‐day and future climate change scenarios. We based our SDMs on bioclimatic and topographic predictors, and recent (2012–2018) field‐collected occurrence data across the whole distribution range of the species. The ensemble SDMs exhibited good predictive capacity and suggested that slope, maximum temperature of warmest month, precipitation of driest month, and isothermality are the most influential predictors in determining distribution patterns in this species. The projections of our models point to a pronounced impact of climate changes over A. davidianus, with more than two‐thirds of its suitable range expected to be lost in all scenarios of future climates tested. In concert with the numerous other threats that are affecting this species, climate change poses a serious hindrance to the long‐term survival of A. davidianus. We emphasise the urgent need of undertaking strict measures to manage this species and safeguard the few remaining available suitable habitats. We suggest that adaptive management strategies including designation of new reserves should be considered to mitigate the impacts of climate change on A. davidianus.

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Climate change going deep: The effects of global climatic alterations on cave ecosystems

Cited by 85 publications

References 143 publications

Extending Janzen’s hypothesis to temperate regions: A test using subterranean ecosystems

Extending Janzen’s hypothesis to temperate regions: A test using subterranean ecosystems

Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions

Future climate change will severely reduce habitat suitability of the Critically Endangered Chinese giant salamander

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