The effects of temperature on peripheral neuronal function in eurythermal and stenothermal crustaceans

Abstract

To determine whether neuronal function in Antarctic crustaceans is adapted to the low and narrow range of temperatures at which these animals live, we have compared conduction velocities in the peripheral nervous systems of two temperate species, the decapod Carcinus maenas and the isopod Ligia oceanica, and two Antarctic species, the isopod Glyptonotus antarcticus and the amphipod Paraceradocus gibber. Neuronal conduction velocity differs among the species in the order C. maenas > G. antarcticus > P. gibber > L. oceanica. When measured at the normal environmental temperatures characteristic of each species, conduction velocity of the Antarctic peracarid P. gibber is greater than that of its similar sized temperate relative L. oceanica, demonstrating complete thermal compensation. The temperate decapod C. maenas has a higher thermal dependence of neuronal conduction velocity than either of the Antarctic species, G. antarcticus and P. gibber, but the temperate L. oceanica does not. These data, when collated with published values, indicate that peracarid crustaceans (L. oceanica, G. antarcticus and P. gibber) have lower neuronal conduction velocities and a lower thermal dependence of neuronal conduction velocity than do other arthropods, irrespective of habitat. There is a linear dependence of conduction velocity on temperature down to -1.8 degrees C in all three species. Our data extend by more than 10 degrees the lower range of temperatures at which conduction velocities have been tested systematically in previous studies. The upper thermal block of neuronal conduction is similar in C. maenas, G. antarcticus, P. gibber and L. oceanica at 24.5, 19.5, 21.5 and 19.5 degrees C, respectively. This suggests that failure to conduct action potentials is not what determines the mortality of Antarctic invertebrates at approximately 10 degrees C. The excitability of axons in the leg nerve of G. antarcticus is not affected by temperatures ranging from -1.8 to +18 degrees C. The responses of sensory neurones activated by movements of spines on the leg, however, are strongly modulated by temperature, with maximal responses at 5-10 degrees C; well above the normal environmental temperature range for the species. The responses fail at 20-22 degrees C. The number of large diameter axons (which produce the fast action potentials recorded in this study) is the same in L. oceanica and G. antarcticus, but the median axon diameter is greater in L. oceanica than G. antarcticus. In G. antarcticus, however, there are glial wrappings around some large (>5 microm diameter) axons that may increase their conduction velocity. Such wrappings are not found in L. oceanica.