Freezing or supercooling: how does an aquatic subterranean crustacean survive exposures at subzero temperatures?

Abstract

Crystallization temperature (T c ), resistance to inoculative freezing (IF), ice contents, bound water, protein and glycogen body contents were measured in the aquatic subterranean crustacean Niphargus rhenorhodanensis and in the morphologically close surface-dwelling aquatic crustacean Gammarus fossarum, both acclimated at 12°C, 3°C and -2°C. Cold acclimation induced an increase in the T c values in both species but no survival was observed after thawing. However, after inoculation at high sub-zero temperatures, cold-acclimated N. rhenorhodanensis survived whereas all others, including the 3°C and -2°C acclimated G. fossarum died. In its aquatic environment, N. rhenorhodanensis is likely to encounter inoculative freezing before reaching the T c and IF tolerance appears as a highly adaptive trait in this species. Bound water and glycogen were found to increase in the 3°C and -2°C acclimated N. rhenorhodanensis, whereas no variation was observed in G. fossarum. Considering the hydrophilic properties of glycogen, such a rise may be correlated with the increased bound water measured in cold-acclimated N. rhenorhodanensis, and may be linked to the survival of this species when it was inoculated. The ecological significance of the survival of the aquatic subterranean crustacean to inoculative freezing is paradoxical, as temperature is currently highly buffered in its habitat. However, we assume that past geographical distribution and resulting life history traits of N. rhenorhodanensis are key parameters in the current cold-hardiness of the species.

A troglobitic amphipod in the Ice Caves of the Shawangunk Ridge: Behavior and resistance to freezing

“…How can the amphipods survive this event? While the ability to survive in cold environments has been well documented for many taxa, very few cave dwelling organisms have been tested for their ability to seek warmer areas within the caves, or their ability to survive exposure to subzero temperatures (Issartel et al 2006;Novak et al 2014). This is probably because in typical limestone caves, temperature is for the most part constant throughout the year and extreme fluctuations in temperature are not considered one of the limiting factors influencing the life of troglobionts (Lencioni et al 2010).…”

Thermal tolerance breadths among groundwater crustaceans living in a thermally constant environment

“…According to the climatic variability hypothesis and the low seasonal variation of temperature in their environment, groundwater-obligate species should exhibit narrow breadths of thermal tolerance because they should maximize their physiological performance over a very narrow thermal range [stenothermal profile (Huey and Kingsolver, 1989)]. Physiological experiments on the thermal physiology of groundwater invertebrates are scarce, and none of them were specifically designed to test the predictions of the climate variability hypothesis (Pattée, 1965;Ginet and Mathieu, 1968;Mathieu, 1983;Issartel et al, 2005a;Issartel et al, 2005b;Issartel et al, 2006;Colson-Proch et al, 2009;Colson-Proch et al, 2010). Several studies examined the physiological responses of groundwater amphipods to cold temperatures [<3°C (Issartel et al, 2005a;Issartel et al, 2006;Colson-Proch et al, 2009)] or heat shocks (Colson-Proch et al, 2010) but did not attempt to determine their thermal tolerance breadths.…”

“…Physiological experiments on the thermal physiology of groundwater invertebrates are scarce, and none of them were specifically designed to test the predictions of the climate variability hypothesis (Pattée, 1965;Ginet and Mathieu, 1968;Mathieu, 1983;Issartel et al, 2005a;Issartel et al, 2005b;Issartel et al, 2006;Colson-Proch et al, 2009;Colson-Proch et al, 2010). Several studies examined the physiological responses of groundwater amphipods to cold temperatures [<3°C (Issartel et al, 2005a;Issartel et al, 2006;Colson-Proch et al, 2009)] or heat shocks (Colson-Proch et al, 2010) but did not attempt to determine their thermal tolerance breadths. Issartel et al (Issartel et al, 2005b) examined the physiological response of two groundwater amphipods, Niphargus virei and Niphargus rhenorhodanensis, over a wide range of temperatures (−2 to 28°C).…”

New Approaches of Ovarian Tissue Cryopreservation from Domestic Animal Species

“…On the basis of the contribution of DSC in other fields of cryopreservation [vitrification of ovary (Baudot et al, 2007), slow-freezing or vitrification of plants (Volk and Walters, 2006;Skyba et al, 2011), slow-freezing of aquatic crustaceans (Issartel et al, 2006)], our team chose a thermodynamic approach to study slow-freezing solutions for ovarian tissue. In fact, DSC allows the measure of the maximal quantity of ice formed in a solution (Q max ).…”