Possession and Loss of Cold Tolerance by Sponge Gemmules: A Comparative Study

Abstract

Gemmules of the freshwater sponges Eunapius fragilis, Ephydatia muelleri, and Spongilla lacustris from southern New England differ in their resistance to exposure to extremely low temperatures. Eunapius fragilis appears to be most tolerant, with greater than 80% of the gemmules surviving exposure to -70? C for one hour. Ephydatia muelleri is slightly less tolerant, and Spongilla lacustris is the least tolerant with no gemmules surviving exposure to temperatures lower than 10? C. Gemmules of both Eunapius fragilis and Ephydatia muelleri lose cold tolerance with storage at 3? to 5? C for more than a few months, most probably due to the loss of cryoprotectants such as sorbitol. Additional key words: Porifera, Eunapius fragilis, Ephydatia muelleri, Spongilla lacustris Most freshwater sponges produce dormant structures called gemmules, each consisting of a dense mass of nutrient-laden cells enclosed by a collagenous capsule that often contains spicules. Some species possess compound gemmules in which each cellular mass is surrounded by its own inner capsule layer but a number of cellular masses share common outer layers. Gemmules may be quiescent, dormancy being imposed by unfavorable environmental conditions, and/ or they may exhibit diapause, in which the dormant state is maintained endogenously (Rasmont 1962; Simpson & Fell 1974; Simpson 1984; Fell 1993). When appropriately tested, the gemmules of freshwater sponges from temperate regions have usually been found to survive exposure to subfreezing temperatures for extended periods of time (Fell 1993). Hydrated gemmules of Ephydatia muelleri in Quebec, Canada survived exposure to 80? C for up to 63 days (Barbeau et al. 1989). Similarly, hydrated gemmules of Eunapius fragilis in Connecticut, USA exhibited more than 80% survival following exposure to -72? C for 30 days (Boutselis et al. 1990); and green gemmules of Spongilla lacustris in Massachusetts, USA showed -80% survival after being frozen in pond water at -20? C for up to 30 days (Fell & Levasseur 1991). Time spent at low temperature has little effect on gemmule survival. However, in some cases, the rate of hatching at 20? C following exposure of gemmules to very low temperatures is markedly slowed compared with that of a Author with whom to correspond. control gemmules which had been maintained at 5? C (Barbeau et al. 1989; Fell & Levasseur 1991). Important factors influencing the cold tolerance of hydrated gemmules of Eunapius fragilis are the rates of cooling and warming. These rates, in turn, affect the rates of ice formation and thawing within the gemmules. Cooling at a rate of 0.1? or 0.5? C/min. and subsequent warming at a rate of 10? C/min. provide optimal conditions for gemmule survival. Under these conditions there was little difference in the survival of gemmules of Eunapius fragilis exposed to -30? -70?, or 100? C (Boutselis et al. 1990). If sponge gemmules are exposed to air during the winter, they may be dehydrated when subjected to subfreezing temperatures (Fell & Bazer 1990). Since little or no ice formation occurs within gemmules under these conditions, it would be expected that cold tolerance should be unaffected by cooling and warming rates. This was found to be the case for dehydrated gemmules of Eunapius fragilis (blotted gemmules were kept in air at 5? C for 24 h before they were tested in air, Boutselis & Fell, unpubl. data). In most cases, the results of earlier studies on the cold tolerances of sponge gemmules cannot be compared directly because each study dealt with a single species and the various studies used different methods. Here we compare the cold tolerances of gemmules of three freshwater sponge species gathered from habitats in southern New England, stored under the same conditions, and then simultaneously exposed to low-temperature conditions. We examined tolerances of the gemmules to different low temperatures over a period This content downloaded from 157.55.39.153 on Mon, 19 Sep 2016 04:42:00 UTC All use subject to http://about.jstor.org/terms Ungemach, Souza, Fell, & Loomis of months in order to ascertain whether changes in cold tolerance occur during maintenance at 4-5? C. Although these sponge gemmules would not be exposed to temperatures as low as -30? or -70? C under natural conditions, we tested the survival of gemmules at these temperatures because we wanted to determine how cold tolerant the gemmules of the different species are. Furthermore, since the amount of extracellular ice formed increases with decreasing temperature, the degree of cold tolerance implies certain physiological conditions within the gemmules.