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

Mammola, Stefano

doi:10.1111/ecog.03905

Cited by 131 publications

(135 citation statements)

References 324 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, 2018;Sánchez-Fernández et al, 2016.…”

Section: Ta B L E 1 Results Of Glm Andmentioning

confidence: 67%

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: Ta B L E 1 Results Of Glm Andmentioning

confidence: 67%

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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“…We conclude that both neutral dynamics and differentiation along a trophic niche axis are likely contributing to species co‐occurrences on a local scale (Gravel et al ) and that these processes are reflected over different geographic scales. Our study shows how the species rich and highly diversified group of interstitial Niphargus may offer an interesting model system to evaluate niche differentiation at continental scales, with local communities and respective conditions being naturally highly replicated (Mammola ). Communities in a long‐term stable environment, such as groundwater, caves, deep sea or deep lakes, seem to be a promising model system for testing the contrasting effects of environmental filtering and interaction processes, driving species differentiation and co‐occurrence.…”

Section: Discussionmentioning

confidence: 96%

Niches within a niche: ecological differentiation of subterranean amphipods across Europe's interstitial waters

et al. 2019

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Species that successfully colonized subterranean environments are subject to two opposing selection processes. Stringent abiotic factors select for convergent adaptations, such as loss of eyes and pigments, while interspecific competition drives between‐species divergence. Subterranean species can resolve opposing selection by adaptation to physically different microhabitats. Yet, species frequently co‐occur in physically homogeneous subterranean habitats, like interstitial. These co‐occurrences in such a narrow ecological context can be explained either by equalizing mechanisms, in which neither of the co‐occurring species has a competitive advantage, or by more complex niche models that include species’ differentiation along a trophic niche axis. We tested these hypotheses using the amphipod genus Niphargus. We analysed Europe‐wide co‐occurrence records of Niphargus species from interstitial habitats, split into six independent large‐scale regions. Firstly, we addressed whether species’ pairwise co‐occurrences are random using a probabilistic model. Secondly, we tested whether species cluster into distinct functional–morphological groups and whether ecologically or phylogenetically distinct species are more likely to co‐occur. We found that 68% of species co‐occurrences were not different from random expectation, indicating that most species had access to most sites within each region. The remaining 32% co‐occurred either significantly more or less often than expected by chance. Cluster analysis of functional morphological characters showed that interstitial species belong to two feeding types, micro‐ and macrofeeders, likely representing two peaks of the interstitial adaptive landscape, and hinting that niche divergence, as a mechanism allowing coexistence, is favoured. Finally, we found that the number of co‐occurrences increases with increasing differentiation of functional morphology, but not phylogenetic differences. We conclude that ecological differentiation may be important in shaping such interstitial communities.

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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%

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

Cited by 131 publications

References 324 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

Niches within a niche: ecological differentiation of subterranean amphipods across Europe's interstitial waters

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

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