Cleaner wrasse indirectly affect the cognitive performance of a damselfish through ectoparasite removal

Abstract

Cleaning organisms play a fundamental ecological role by removing ectoparasites and infected tissue from client surfaces. We used the well-studied cleaning mutualisms involving the cleaner wrasse, Labroides dimidiatus, to test how client cognition is affected by ectoparasites and whether these effects are mitigated by cleaners. Ambon damselfish (Pomacentrus amboinensis) collected from experimental reef patches without cleaner wrasse performed worse in a visual discrimination test than conspecifics from patches with cleaners. Endoparasite abundance also negatively influenced success in this test. Visual discrimination performance was also impaired in damselfish experimentally infected with gnathiid (Crustacea: Isopoda) ectoparasites. Neither cleaner absence nor gnathiid infection affected performance in spatial recognition or reversal learning tests. Injection with immune-stimulating lipopolysaccharide did not affect visual discrimination performance relative to saline-injected controls, suggesting that cognitive impairments are not due to an innate immune response. Our results highlight the complex, indirect role of cleaning organisms in promoting the health of their clients via ectoparasite removal and emphasize the negative impact of parasites on host's cognitive abilities.

Keywords: Labridae; Pomacentridae; coral reef fish; learning and memory; mutualism; pathogen infection.

Figure 1.

Diagram of the visual discrimination cognition test protocol viewed laterally. At the beginning of each trial, an opaque barrier separating the holding and the experimental compartments was lifted. In all treatments, the fish was presented with two identical plates separated by a small partition placed lengthwise at the back of the tank. One of the plates consistently had a food reward located at the back of the plate (i.e. invisible from the front). (Online version in colour.)

Figure 2.

The ability of Ambon damsel (P. amboinensis) to successfully complete a visual discrimination task in three different experiments: (a) long-term exposure to ectoparasites in the wild elicited by long-term removal of cleaner wrasse (cleaner present in blue, n = 21; cleaner absent in red, n = 20); (b) short-term exposure to ectoparasites in the laboratory (uninfected in blue, n = 12; infected in red, n = 12); (c) immune stimulation by LPS injection (saline control in blue, n = 16; LPS in red, n = 14). (a) Cumulative percentage completion per trial (inverted survival curve): solid lines are Kaplan–Meier curves (i.e. raw data) and dashed lines are coxph model predictions. (b) Number of trials that fish (individual dots) needed to complete the task; dots above the dashed line represent fish that failed to complete the task in the allotted number of trials. (Online version in colour.)

Figure 3.

The relationship between endoparasite abundance (controlling for fish size) and the ratio of instantaneous success rate for P. amboinensis completing a visual discrimination task. The model predictions indicate that fish with only four endoparasites were twice as likely to complete the task as fish with the mean parasite abundance (21.44, indicated by the red dashed line). The dark and light blue areas represent the 95% and 50% probability interval of the simulations from the Cox PH model (see Materials and methods for details). (Online version in colour.)