The Visual Ecology of the Cleaner Shrimp-Client Fish Mutualism

Cleaner shrimp are small, brightly-colored tropical crustaceans that attract reef fish clients to set locations on a reef called cleaning stations and then "clean" them by removing ectoparasites from their scales, gills, and mouths. Because clients benefit from the removal of potentially harmful parasites, and shrimp benefit from a meal, this interaction is considered mutualistic. The evolution of cleaner-client relationships is especially paradoxical, however, given that crustaceans make an easy meal for many reef fish. How did such an interaction arise and evolve? Additionally, how do cleaner shrimp and clients find and recognize each other, and why doesn't the client eat the cleaner? One hypothesis is that mutualistic partners evolve signals that identify them as beneficial partners. For the cleaner shrimp-client fish mutualism, it has been suggested that these signals are visual, and function to identify cleaners as helpers, rather than food, and perhaps to identify clients as seeking cleaning rather than a meal.

The broad goal of this dissertation was to examine the cleaner shrimp-client fish mutualism by combining visual physiology, visual ecology, and animal behavior. Throughout, I focus on visual acuity-the ability to perceive detail-an underexplored aspect of visual capability which should represent an important selective force on signals, as it determines what visual information can and cannot be resolved. To begin, in Chapter 2, I characterized the visual capabilities of cleaner shrimp for the first time, in particular examining spectral sensitivity, visual acuity, and temporal resolution of three species from the three primary genera where cleaning has arisen. This revealed that these cleaner shrimp have monochromatic, coarse vision, and thus that their color patterns likely do not serve an intraspecific signaling purpose, but rather may be part of signals directed at client fish. Thus, Chapter 3 examined visual acuity in fish by performing a literature synthesis of known visual acuity values across fishes and examining how acuity relates to certain aspects of morphology and ecology. Here, I found that acuity is higher in fish with larger eyes and in fish that live in spatially complex habitats.

Having examined the visual capabilities of both parties in the cleaner-client mutualism, I then explored signaling between cleaners and clients. In chapter (4), I used sequential analysis to demonstrate that certain stereotyped motions by cleaner shrimp are signals directed at clients, and provide the first evidence of potential signals on the part of client fish as well. Additionally, I developed an R package, AcuityView (Appendix A) which displays images with only the spatial information available to a receiver of given acuity from a given distance, and used it to show that cleaner and client signals are visible to their intended receivers. Lastly, in Chapter (5), I outlined what we know about acuity across species, provide primers on the anatomical basis for acuity and what factors can make acuity higher, and put forward specific predictions and hypotheses about how receiver acuity may influence signal form.