Multiple cleaner species provide simultaneous services to coral reef fish clients

Cleaning symbioses on tropical coral reefs are typically documented between two species: a single client fish and one or more conspecific cleaners. However, multiple cleaner species living sympatrically in the Caribbean have been anecdotally reported to simultaneously clean the same client. Nothing is known about the patterns and processes driving these interactions, which may differ from those involving a single cleaner species. Here, we used remote underwater videography on three reefs in Honduras to record simultaneous cleaning interactions involving Pederson's cleaner shrimp ( Ancylomenes pedersoni ) and cleaner gobies ( Elacatinus spp.). A pilot study on adjacent shrimp and goby stations found interactions were always initiated by shrimp. A larger, multi-year dataset shows cleaner gobies joined 28% of all interactions initiated at A. pedersoni cleaning stations with cleaner gobies residing nearby. Client body size significantly predicted simultaneous cleaning interactions, with 45% of interactions simultaneous for clients greater than 20 cm total body length compared with only 8% for clients less than 20 cm. We also found that simultaneous cleaning interactions lasted over twice as long as shrimp-only interactions. We propose these novel multi-species interactions to be an ideal model system to explore broader questions about coexistence, niche overlap and functional redundancy among sympatric cleaner species.

Mutual visual signalling between the cleaner shrimp Ancylomenes pedersoni and its client fish

Cleaner shrimp and their reef fish clients are an interspecific mutualistic interaction that is thought to be mediated by signals, and a useful system for studying the dynamics of interspecific signalling. To demonstrate signalling, one must show that purported signals at minimum (a) result in a consistent state change in the receiver and (b) contain reliable information about the sender's intrinsic state or future behaviour. Additionally, signals must be perceptible by receivers. Here, we document fundamental attributes of the signalling system between the cleaner shrimp Ancylomenes pedersoni and its clients. First, we use sequential analysis of in situ behavioural interactions to show that cleaner antenna whipping reliably predicts subsequent cleaning. If shrimp do not signal via antenna whipping, clients triple their likelihood of being cleaned by adopting darker coloration over a matter of seconds, consistent with dark colour change signalling that clients want cleaning. Using experimental manipulations, we found that visual stimuli are sufficient to elicit antenna whipping, and that shrimp are more likely to ‘clean' dark than light visual stimuli. Lastly, we show that antenna whipping and colour change are perceptible when accounting for the intended receiver's visual acuity and spectral sensitivity, which differ markedly between cleaners and clients. Our results show that signalling by both cleaners and clients can initiate and mediate their mutualistic interaction.

Dopamine disruption increases cleanerfish cooperative investment in novel client partners

Social familiarization is a process of gaining knowledge that results from direct or indirect participation in social events. Cooperative exchanges are thought to be conditional upon familiarity with others. Indeed, individuals seem to prefer to engage with those that have previously interacted with them, which are more accurate predictors of reward than novel partners. On the other hand, highly social animals do seek novelty. Truth is that the physiological bases underlying how familiarity and novelty may affect cooperative decision-making are still rather obscure. Here, we provide the first experimental evidence that the level of the dopaminergic influence in cooperative exchanges is constrained to mechanisms of social familiarization and novelty in a cleanerfish, Labroides dimidiatus . Cleaners were tested against familiar and novel Ctenochaetus striatus surgeonfish (a common client species) in laboratorial conditions, and were found to spend more time providing physical contact (also referred to as tactile stimulation) to familiar fish clients. Cleaners use tactile stimulation as a way to reduce the risk of a non-rewarding outcome, a behavioural response that is even more pronounced when blocking dopamine (DA) D1 receptors. We discovered that the influence of DA disruption on cleaners' provision of physical contact was dependent on the level of familiarity with its partner, being highly exacerbated whenever the client is novel, and unnoticed when dealing with a familiar one. Our findings demonstrate that DA mediation influences the valuation of partner stimuli and the enhancing investment in novel partners, mechanisms that are similar to other vertebrates, including humans.

Patterns of cleaning behaviour on coral reef fish by the anemoneshrimpAncylomenes pedersoni

Little is known about the cleaning behaviour of shrimps in comparison to that of cleaner fish, and only recently have cleaner shrimps been shown to remove parasites effectively from coral reef fish. Here we describe patterns of cleaning interactions between Pederson shrimpAncylomenes pedersoniand fish clients in St Thomas, US Virgin Islands. Clients observed here were members of at least 16 fish families, including three previously unreported client families. Most cleans lasted <20 seconds; surgeonfish were cleaned most frequently, but lizardfish and groupers received the longest cleans. The shrimp formed social groups of varying sizes on individuals of the host sea anemoneBartholomea annulata, which served as the centres of their cleaning stations. The number and duration of cleans per station increased with the number of resident shrimp, however most anemones hosted small groups of fewer than four individuals, while larger groups of up to nine individuals were relatively rare. Some client fish chased away other fish and competitively excluded them from anemone stations. We conclude that these shrimp clean a wide diversity of clients, vary their clean duration with fish identity, and clean more when in large groups. In addition, clients in part control these patterns of interaction by interfering with access to these stations by other clients.