Learning competence of the temperate facultative cleaner wrasse Thalassoma pavo (Labridae).

Cleaner fishes remove parasites from other fishes called "clients," thereby contributing to a healthier ecosystem. Although the behavior and learning abilities of dedicated and tropical cleaner fishes have been broadly studied, a limited number of studies investigated the behavior of facultative and temperate cleaner fishes and, to the best of our knowledge, none focused on their cognitive abilities. Here, we tested the learning abilities of a species of temperate facultative cleaner, the ornate wrasse Thalassoma pavo in laboratory conditions, based on two problems. These two problems, or tasks, are relevant in two different contexts: the first one, deemed as mutualistically relevant, the cue-based discrimination task, and the second one, the spatial-based discrimination task, which is relevant in a non-cleaning context, when fish navigate through their environment to find food and return to their territories. We found that T. pavo individuals were able to solve these two tasks but excelled at the spatial task rather than with the cue discrimination. The same individuals were also challenged to learn the reverse protocol of these tasks and were again most successful in learning the reverse spatial discrimination problem, but not the cue. Contrary to the dedicated cleaner wrasse Labroides dimidiatus, this temperate facultative cleaner wrasse is slower to learn mutualistic relevant problems but competent in solving spatially derived problems. This may be due to the specific demands of their socio-ecological environment, with facultative cleaners having a greater component of non-mutualistic skills (spatial component), which prepares them to search for alternative food sources if necessary (e.g., feeding on the substrate) or even to expand territories more easily and less prepared to deal with mutualistic exchanges compared to dedicated cleaners that specialize to become increasingly socially competent.

Cleaner fish are potential super-spreaders.

Cleaning symbiosis is critical for maintaining healthy biological communities in tropical marine ecosystems. However, potential negative impacts of mutualism, such as the transmission of pathogens and parasites during cleaning interactions, have rarely been evaluated. Here, we investigated whether the dedicated bluestreak cleaner wrasse, Labroides dimidiatus, is susceptible to and can transmit generalist ectoparasites between client fish. In laboratory experiments, L. dimidiatus were exposed to infective stages of three generalist ectoparasite species with contrasting life histories. Labroides dimidiatus were susceptible to infection by the gnathiid isopod Gnathia aureamaculosa, but were significantly less susceptible to the ciliate protozoan Cryptocaryon irritans and the monogenean flatworm Neobenedenia girellae, compared with control host species (Coris batuensis or Lates calcarifer). The potential for parasite transmission from a client fish to the cleaner fish was simulated using experimentally transplanted mobile adult (i.e. egg-producing) monogenean flatworms on L. dimidiatus. Parasites remained attached to cleaners for an average of 2 days, during which parasite egg production continued, but was reduced compared with that on control fish. Over this timespan, a wild cleaner may engage in several thousand cleaning interactions, providing numerous opportunities for mobile parasites to exploit cleaners as vectors. Our study provides the first experimental evidence that L. dimidiatus exhibits resistance to infective stages of some parasites yet has the potential to temporarily transport adult parasites. We propose that some parasites that evade being eaten by cleaner fish could exploit cleaning interactions as a mechanism for transmission and spread.

Parasite infection directly impacts escape response and stress levels in fish.

Parasites can account for a substantial proportion of the biomass in marine communities. As such, parasites play a significant ecological role in ecosystem functioning via host interactions. Unlike macropredators, such as large piscivores, micropredators, such as parasites, rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via sublethal effects. Recent research suggests that infection by gnathiid isopods (Crustacea) causes significant physiological stress and increased mortality rates. However, it is unclear whether infection causes changes in the behaviours that underpin escape responses or changes in routine activity levels. Moreover, it is poorly understood whether the cost of gnathiid infection manifests as an increase in cortisol. To investigate this, we examined the effect of experimental gnathiid infection on the swimming and escape performance of a newly settled coral reef fish and whether infection led to increased cortisol levels. We found that micropredation by a single gnathiid caused fast-start escape performance and swimming behaviour to significantly decrease and cortisol levels to double. Fast-start escape performance is an important predictor of recruit survival in the wild. As such, altered fitness-related traits and short-term stress, perhaps especially during early life stages, may result in large scale changes in the number of fish that successfully recruit to adult populations.

Practical methods for culturing parasitic gnathiid isopods.

The reliance of parasites on their hosts makes host-parasite interactions ideal models for exploring ecological and evolutionary processes. By providing a consistent supply of parasites, in vivo monocultures offer the opportunity to conduct experiments on a scale that is generally not otherwise possible. Gnathiid isopods are common ectoparasites of marine fishes, and are becoming an increasing focus of research attention due to their experimental amenability and ecological importance as ubiquitous, harmful, blood-feeding "mosquito-like" organisms. They feed on hosts once during each of their three juvenile stages, and after each feeding event they return to the benthos to digest and moult to the next stage. Adults do not feed and remain in the benthos, where they reproduce and give birth. Here, we provide methods of culturing gnathiids, and highlight ways in which gnathiids can be used to examine parasite-host-environment interactions. Captive-raised gnathiid juveniles are increasingly being used in parasitological research; however, the methodology for establishing gnathiid monocultures is still not widely known. Information to obtain in vivo monocultures on teleost fish is detailed for a Great Barrier Reef (Australia) and a Caribbean Sea (US Virgin Islands) gnathiid species, and gnathiid information gained over two decades of successfully maintaining continuous cultures is summarised. Providing a suitable benthic habitat for the predominantly benthic free-living stage of this parasite is paramount. Maintenance comprises provision of adequate benthic shelter, managing parasite populations, and sustaining host health. For the first time, we also measured gnathiids' apparent attack speed (maximum 24.5 cm sec-1; 6.9, 4.9/17.0, median, 25th/75th quantiles) and illustrate how to collect such fast moving ectoparasites in captivity for experiments. In addition to providing details pertaining to culture maintenance, we review research using gnathiid cultures that have enabled detailed scientific understanding of host and parasite biology, behaviour and ecology on coral reefs.