Red, distasteful water mites: did fish make them that way?

Water mites (Acari: Hydrachnida) are unusual among the typically cryptic freshwater fauna in that many species are brightly colored red or orange, and also appear to be distasteful to fish. This apparent aposematism (use of color to warn predators) has been previously explained as the evolutionary end-product of pressure from fish predation. The fish-predation argument has been supported by observations that fish spit out red mites, powder made from red water mites is more distasteful to fish than powder made from non-red mites, and red mites appear to be more abundant than non-red mites in water bodies where fish are present. In this paper, we challenge the hypothesis that fish were the sole driving force behind the evolution of aposematism in water mites. We show that non-red mites actually dominate in water bodies with fish, and that red mites are more abundant in temporary, fishless water bodies. We also demonstrate that powder made from red, terrestrial velvet mites (Trombidiidae) was as distasteful to fish as powder made from red water mites. We suggest that the main role of red and orange carotenoid pigments may be to act as photoprotectants, and hypothesize that redness originated in the terrestrial ancestors of water mites and has been retained in certain lineages of water mites after the invasion of the aquatic habitat. We also suggest that distastefulness evolved subsequent to bright coloration in response to increased conspicuousness to predators. Relaxed selection for redness has occurred when adults and/or larvae are less exposed to sunlight, either through occupying more protected habitats, parasitizing more nocturnal hosts, or parasitizing hosts for a short period of time. Our ability to test this alternative hypothesis is hampered by lack of knowledge of the source and mode of action of distastefulness, and of phylogenetic relationships among the Parasitengona.