Regional differences in the architecture and size of lateral line canals and neuromasts were measured in an Antarctic fish, Trematomus bernacchii, and the data were used in models of canal and cupular mechanics to predict the frequency response of these two peripheral structures. These modeled predictions were then compared to frequency response functions measured with single unit recording techniques from anterior and posterior lateral line fibers innervating different canals on the head and trunk of fish of various sizes. Despite large variations in the peripheral morphology of head and trunk canals in fish of different sizes, lateral line fibers were relatively homogeneous in their frequency response properties. In response to stimuli of equal pk-pk acceleration levels, all canal neuromast fibers responded with equal and maximum responsiveness in the 10-45 Hz range, after which responsiveness fell off at about 18 dB/octave. Whereas the biomechanical models of cupular and canal responsiveness predicted the region of equal and maximum responsiveness in the 10-45 Hz range, they did not predict the high frequency cutoff nor the slope. Rather, these models predicted responsiveness out to at least 540 Hz, and a high frequency slope of 12 dB/octave. In terms of the frequency response of peripheral fibers, we conclude that (1) there can be considerable morphological variability, with little consequence for function, as long as some minimum standards for maintaining constant acceleration responsiveness in the 10-45 Hz range are met, and (2) there must be additional filters between the cupula and primary afferent fibers.