To determine which physiological properties contribute to temperature adaptation in the squid giant axon, action potentials were recorded from four species of squid whose habitats span a temperature range of 20 degrees C. The environments of these species can be ranked from coldest to warmest as follows: Loligo opalescens>Loligo pealei>Loligo plei>Sepioteuthis sepioidea. Action potential conduction velocities and rise times, recorded at many temperatures, were equivalent for all Loligo species, but significantly slower in S. sepioidea. By contrast, the action potential's fall time differed among species and correlated well with the thermal environment of the species ('warmer' species had slower decay times). The biophysical underpinnings of these differences were examined in voltage-clamped axons. Surprisingly, no differences were found between the activation kinetics or voltage-dependence of Na(+) and K(+) currents. Conductance levels, however, did vary. Maximum Na(+) conductance (g(Na)) in S. sepiodea was significantly less than in the Loligo species. K(+) conductance (gK) was highest in L. pealei, intermediate in L. plei and smallest in S. sepiodea. The time course and magnitude of g(K) and g(Na) were measured directly during membrane action potentials. These data reveal clear species-dependent differences in the amount of g(K) and g(Na) recruited during an action potential.