Kinematics of waterfall climbing in Hawaiian freshwater fishes (Gobiidae): vertical propulsion at the aquatic–terrestrial interface

Abstract

To reach adult habitats, juveniles of three species of Hawaiian gobies (fishes under 3 cm long) climb waterfalls up to 350 m high, over 10 000 times their body length. The demands of moving through such an extreme environment could constrain the range of viable locomotor mechanisms that these fishes use. Previous qualitative observations indicated that Lentipes concolor and Awaous guamensis use ‘powerbursts’ of axial undulation to climb, whereas Sicyopterus stimpsoni ‘inches up’ vertical surfaces by alternately attaching oral and pelvic suckers to the substrate. To compare these propulsive mechanisms and their physiological requirements, high-speed video footage of climbing by juveniles from these three species on an artificial waterfall were collected, and climbing kinematics and performance for the two climbing styles were quantified. Bouts of powerburst climbing by L. concolor and A. guamensis typically begin in or near direct water flow and are initiated by a single, rapid adduction of the pectoral fins. Powerburst climbing bouts are rapid (12.4±1.0 body lengths (BL) s⁻¹), but short in duration (0.07±0.02 s) with few continuous locomotor cycles (3.8±1.3 cycles bout⁻¹). Powerburst climbers use high amplitude undulations along the entire body, but minimum resultant velocities of these undulations are high (>6 BL s⁻¹). This suggests that these species may hybridize terrestrial propulsive mechanisms with aquatic mechanisms. In contrast, climbing by inching in S. stimpsoni involves little axial undulation or fin movement. Sicyopterus stimpsoni typically exit the water outside of direct flow and seem to use terrestrial propulsive mechanisms. As the oral disc attaches to the substrate, it expands to almost twice its resting area, after which the posterior body is pulled upwards; once the pelvic disc attaches, the oral disc releases and the anterior body advances. Climbing bouts include several continuous cycles of disc attachment (11.0±1.4 cycles bout⁻¹) and last several seconds at velocities of 0.21±0.01 BL s⁻¹. Before climbing waterfalls during migration to adult habitats, S. stimpsoni undergo a non-feeding metamorphosis that leads to the development of the mouth as a secondary locomotor organ. The unusual behaviour and ontogenetic strategy of S. stimpsoni seem to be evolutionary novelties, rather than ancestral retentions, suggesting that the evolution of these features may have been closely correlated. The substantial performance and kinematic distinctions between powerburst and inching climbing indicate that considerable locomotor diversity can evolve even in the context of extreme environmental demands.