Gastropod Shell Morphology Imparts Functional Constraints on Feeding Performance of Freshwater Pufferfishes

Evolutionary arms races between predators and their prey are responsible for key advancements in phenotypic evolution. The advent of durophagous (shell-crushing) predators during the Mesozoic era spurred large-scale changes in the morphology of marine gastropod shells (i.e., the Mesozoic Marine Revolution; MMR), as sturdier shell forms including closed coiling, more external sculpturing, and high spiring became more common. However, unlike marine environments, freshwater gastropods are severely calcium limited, posing a significant constraint on freshwater gastropod shell sturdiness. For example, freshwater gastropods rarely have external sculpturing, instead relying on manipulating the base coiling pattern of the shell for protection against predation. Major axes of shell variation include whorl expansion rate and whorl translation rate, which describe the rate at which whorls of the shell are growing outwards and down the coiling axis, respectively. In this study, we used three species of freshwater gastropods with common shell morphologies to test the effect of shell morphology on feeding performance of three species of freshwater durophagous pufferfishes. Many pufferfish, including the ones used here, have fused teeth that form a “beak,” which is a major functional innovation that enhances their efficiency and capacity to crush hard-shelled prey. We found significant effects of shell shape and size as well as pufferfish species and size on feeding performance. Extreme shell shapes, both high- and low-spired, results in higher handling time by pufferfishes than mid-spired shells. This is in sharp contrast to marine snails, which exhibit a shift towards high-spired shell morphologies during the MMR. Across all shell morphologies, larger shells resulted in higher handling time by pufferfishes. We also observed several intra- and interspecific behavioral adaptations employed while feeding on snails that may improve performance. In summation, calcium limitation of freshwaters may alter the trajectory of the evolutionary arms race between gastropods and their predators.