The deep subterranean environment as a potential model system in ecological, biogeographical and evolutionary research

Sánchez‐Fernández, David; Rizzo, Valeria; Bourdeau, Charles; Cieslak, Alexandra; Comas, Jordi; Faille, Arnaud; Fresneda, Javier; Lleopart, Enric; Millán, Andrés; Montes, Aitor; Pallarés, Susana; Ribera, Ignacio

doi:10.3897/subtbiol.25.23530

Cited by 41 publications

(50 citation statements)

References 28 publications

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“…Our results stress the need of experimental approaches to assess the capability of species to cope with temperatures outside those they currently experience and give rise to further research questions to be explored in subterranean ecosystems, highlighting their potential as natural laboratories to study multiple eco‐evolutionary processes (Mammola, ; Sánchez‐Fernández et al, , ).…”

Section: Discussionmentioning

confidence: 63%

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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Section: Discussionmentioning

confidence: 63%

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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“…Yet, the ecological complexity of most ecosystems and the challenge posed by the geographic scale at which this hypothesis can be tested, have largely prevented ecologists from comprehensively testing the underlying assumptions of Janzen's hypothesis and transferring it to non‐tropical settings (Gill et al, ; McCain, ; Polato et al, ; Scheffers et al, ). Due to their ecological simplicity and environmental stability, subterranean habitats emerge as an ideal model system in which to explore eco‐evolutionary questions in general (Mammola, ; Sánchez‐Fernández et al, ) and hypotheses pertaining to thermal niche breadth in particular (Eme et al, ; Mermillod‐Blondin et al, ; Pallarés et al, ; Raschmanová, Šustr, Kováč, Parimuchová, & Miloslav Devetter, ; Rizzo, Sánchez‐Fernández, Fresneda, Cieslak, & Ribera, ).…”

Section: Discussionmentioning

confidence: 99%

“…For two caves lacking field-collected temperature records (indicated with a superscript a in Table 1), we downloaded annual temperature series from the same period from the nearest thermo-hygro-pluviometric weather station. After correcting the data with the standard environmental lapse rate (0.57°C/100 m; Rubel, Brugger, Haslinger, & Auer, 2017), we calculated the mean annual temperature and used this value as a direct proxy of the cave temperature (Badino, 2010;Sánchez-Fernández et al, 2018).…”

Section: Sampling Protocolmentioning

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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“…Because of their confined nature, subterranean habitats may represent candidate systems for addressing a wide range of similar eco-evolutionary questions (Moldovan et al 2012; but see cautionary arguments in the next section). 1) and are characterized by an extremely reduced environmental variability in the abiotic conditions (Sánchez-Fernández et al 2018). 1) and are characterized by an extremely reduced environmental variability in the abiotic conditions (Sánchez-Fernández et al 2018).…”

Section: Subterranean Habitats As Model Systemsmentioning

confidence: 99%

“…In parallel, subterranean habitats have often clear and predictable environmental gradients from the surface to the subsurface ( Fig. 1) and are characterized by an extremely reduced environmental variability in the abiotic conditions (Sánchez-Fernández et al 2018). Thus, these two factors should facilitate to parameterize the system.…”

Section: Subterranean Habitats As Model Systemsmentioning

confidence: 99%

Finding answers in the dark: caves as models in ecology fifty years after Poulson and White

2018

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The use of semi-isolated habitats such as oceanic islands, lakes and mountain summits as model systems has played a crucial role in the development of evolutionary and ecological theory. Soon after the discovery of life in caves, different pioneering authors similarly recognized the great potential of these peculiar habitats as biological model systems. In their 1969 paper in Science, 'The cave environment', Poulson and White discussed how caves can be used as natural laboratories in which to study the underlying principles governing the dynamics of more complex environments. Together with other seminal syntheses published at the time, this work contributed to establishing the conceptual foundation for expanding the scope and relevance of cave-based studies. Fifty years after, the aim of this review is to show why and how caves and other subterranean habitats can be used as eco-evolutionary laboratories. Recent advances and directions in different areas are provided, encompassing community ecology, trophicwebs and ecological networks, conservation biology, macroecology and climate change biology. Special emphasis is given to discuss how caves are only part of the extended network of fissures and cracks that permeate most substrates and, thus, their ecological role as habitat islands is critically discussed. Numerous studies have quantified the relative contribution of abiotic, biotic and historical factors in driving species distributions and community turnovers in space and time, from local to regional scales. Conversely, knowledge of macroecological patterns of subterranean organisms at a global scale remains largely elusive, due to major geographical and taxonomical biases. Also, knowledge regarding subterranean trophic webs and the effect of anthropogenic climate change on deep subterranean ecosystems is still limited. In these research fields, the extensive use of novel molecular and statistical tools may hold promise for quickly producing relevant information not accessible hitherto.

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The deep subterranean environment as a potential model system in ecological, biogeographical and evolutionary research

Cited by 41 publications

References 28 publications

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

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

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

Finding answers in the dark: caves as models in ecology fifty years after Poulson and White

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