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

Abstract

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.

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

“…These results are in agreement with previous work showing that many subterranean species can withstand temperatures up to 20°C with no apparent signs of stress (e.g., Issartel et al, ; Mermillod‐Blondin et al, ; Rizzo et al, ). Although narrower thermal limits have been reported for some cave terrestrial invertebrates (e.g., Mammola, Piano, Malard, et al, ), it seems that such limits are generally not adjusted to ambient temperature in subterranean ectotherms, in contrast with taxa from other thermally stable (but also much colder) environments such as polar waters (Peck, Webb, & Bailey, ; Somero & DeVries, ). Such higher thermal sensitivity of polar species might be related to the different mechanisms for thermoregulation in aquatic species or the role of oxygen in setting thermal tolerance, which is particularly relevant for aquatic organisms (Verberk et al, ).…”

“…Such relationship was also consistent across a set of 37 phylogenetically distant invertebrate species (Novak et al, ). Within troglobionts, species confined to the internal parts of the caves show also higher thermal sensitivity than closely related ones found closer to cave entrances, where thermal conditions are more fluctuating (Latella, Bernabò, & Lencioni, ; Mammola, Piano, Malard, et al, ). Our small set of unrelated species and the lack of phylogenetic information of the studied lineages prevent us to test this relationship between the degree of subterranean specialization and thermal tolerance within an appropriate phylogenetic context.…”

“…As an extreme example, some Antarctic cold‐stenothermal species (e.g., Clark, Fraser, Burns, & Peck, ; Clark Fraser & Peck, ; La Terza, Papa, Miceli, & Luporini, ; Rinehart et al, ; Somero, ) as well as warm stenothermal coral reef fishes (Kassahn et al, ; Nilsson, Östlund‐Nilsson, & Munday, ) have lost the ability to activate a heat shock response via the expression of heat shock proteins, which makes them especially vulnerable to global change (Kellermann & van Heerwaarden, ; Patarnello, Verde, Prisco, Bargelloni, & Zane, ; Somero, ). These questions remain poorly explored in other extremely thermally stable habitats, such as subterranean environments, although some recent studies have found support for the climatic variability hypotheses for cave springtails (Raschmanová, Šustr, Kováč, Parimuchová, & Devetter, ) and spiders (Mammola, Piano, Malard, Vernon, & Isaia, ). However, the generality of such patterns remains controversial (see Gunderson & Stillman, ; Rohr et al, ), as other studies have found weak support for a correlation between some thermal tolerance traits and the magnitude or predictability of thermal variability (e.g., Kellermann et al, ; Overgaard, Kearney, & Hoffmann, ; Seebacher, White, & Franklin, ).…”

“…The relatively scarce, more recent studies that have specifically measured thermal breadth and plasticity in subterranean species show contrasting results for different taxa. Some species present the typical characteristics of stenothermal organisms, that is, low physiological plasticity (e.g., Di Lorenzo & Galassi, ) and narrow thermal breadths for survival (e.g., some deep subterranean spiders – Mammola, Piano, Malard, et al, ), locomotion or respiration (e.g., Issartel, Hervant, Voituron, Renault, & Vernon, ; Mermillod‐Blondin et al, ), being sensitive to changes of only a few grades below or above their habitat temperature. In contrast, other subterranean species have shown much wider thermal ranges for performance and survival (Issartel et al, ; Mammola, Piano, Malard, et al, ; Mermillod‐Blondin et al, ).…”

“…Some species present the typical characteristics of stenothermal organisms, that is, low physiological plasticity (e.g., Di Lorenzo & Galassi, ) and narrow thermal breadths for survival (e.g., some deep subterranean spiders – Mammola, Piano, Malard, et al, ), locomotion or respiration (e.g., Issartel, Hervant, Voituron, Renault, & Vernon, ; Mermillod‐Blondin et al, ), being sensitive to changes of only a few grades below or above their habitat temperature. In contrast, other subterranean species have shown much wider thermal ranges for performance and survival (Issartel et al, ; Mammola, Piano, Malard, et al, ; Mermillod‐Blondin et al, ). Studies on subterranean leiodid beetles have reported similar thermal tolerance ranges (between 0 and 20–23°C) among different species irrespective of the climatic conditions of the caves where they live (Glaçon, ; Juberthie et al, ; Rizzo, Sánchez‐Fernández, Fresneda, Cieslak, & Ribera, ), suggesting a lack of adjustment of thermal limits to environmental conditions in this group.…”