Seamounts are widely regarded as hotspots of biodiversity due to the unique oceanographic conditions that they generate and have been identified as important staging areas for migrant marine megafauna. While the ecological mechanisms that attract elasmobranchs to seamounts are poorly understood, it has been suggested that they provide refuge, represent social convergence points, act as navigational waypoints, and function as mating, feeding, and nursery grounds for a variety of pelagic species. The Giant Manta Ray, Mobula birostris, is one of two recognised Manta Ray species. Reaching 6.70 m in total (disc) width, the Ray is popular among tourists for its size and approachable behaviour. Recognised from fisheries and by-catch to frequent tropical and subtropical offshore waters circumglobally, Giant Manta Rays mature late, have low fecundity, and are classified as Vulnerable to Extinction by the International Union for the Conservation of Nature and Natural Resources’ Red List of Species. For the past two decades, Giant Manta Rays have been observed by SCUBA divers on Monad Shoal, which is a shallow coastal seamount in the Central Visayas of the Philippines, where they interact with Blue Streaked Cleaner Wrass, Labroides dimidiatus, and Moon Wrasse, Thalassoma lunare. Rays, including Giant Manta Rays, are known to host Metazoan parasites, and it is proposed that they visit a cleaning station at this site to control infection.
Batoid rays infected with parasites suffer a variety of health consequences. These include skin lesions, necrosis, anaemia, respiratory disease, and chronic Bacterial and Viral infections that have been reported as lethal in some species. Ectoparasitic infections in captive Elasmobranchs cause behavioural modifications such as rubbing against the structures of enclosures and interacting with Cleaner Fish.
The cleaning system is a classic model of cooperative behaviour among species in which Cleaner Fish remove ectoparasites and dead or infected tissue from the surface, gills, and sometimes the mouth of client Fish. Interactions with Cleaner Fish appear to improve the health of teleost clients by reducing their ectoparasite loads, but the benefit of these interactions is less understood amongst Elasmobranchs. Clients will often ‘pose’ near cleaning stations to solicit ‘services’ from Cleaner Fish. There are approximately 130 species of marine cleaners, with ectoparasitic infection being the most likely proximate cue for clients seeking their services. The Blue Streaked Cleaner Wrasse, Labroides dimidiatus, is an obligate cleaner that preferentially feeds on Gnathiid Isopod larvae that are known to infect the gills of Reef Manta Rays. Labroides dimidiatus prefer large clients and interact with Manta Rays at spatially diverse locations across the globe. The Moon Wrasse, Thalassoma lunare, which is less understood as a cleaner species, also provides cleaning services for Manta Rays. Moon Wrasse are facultative cleaners wherein only juveniles clean whilst contemporaneously exploiting alternative food sources.
Cleaners may maximize the profitability of their energy return by selectively foraging on areas of clients where specific types of parasites can be found. When investigating how cleaners forage on Elasmobranchs, it has been shown that Labroides dimidiatus and Thalassoma lunare spent more time inspecting areas of Thresher Sharks, Alopias pelagicus, that were infected by ectoparasitic Digeneans, Paronatrema spp., compared to areas that are known to harbour other types of parasites. They concluded that cleaners may optimise their foraging by selecting areas of a client’s body that are most likely to produce the highest energy reward per unit effort. A cleaner’s foraging behaviour is, therefore, likely to be driven by the quality of the food patch in relation to the ease with which food may be obtained there. Since specific types of parasites infect specific patches of an Elasmobranch’s body, it can be predicted that cleaners will show preferences for foraging in some patches over others.
A Moon Wrasse, Thalassoma lunare, on the Great Barrier Reef, Australia. Leonard Low/Flikr/Wikimedia Commons.
Murie et al. quantified behavioural interactions between Giant Manta Rays and Cleaner Wrasse from remote video observations to address the following hypotheses: (1) the dynamics of the Cleaner–Manta system are driven by environmental factors; and (2) Cleaner Wrasse preferentially forage on specific areas of a Manta Ray’s body. The Cleaner–Manta association is discussed in relation to other known cleaner–client systems in the marine environment.
Monad Shoal is a seamount in the Central Visayan Sea, near Malapascua Island, Cebu, the Philippines. The top of the mount (15–25 m) is formed by a shallow plateau of low-profile Acropora that is fringed on all sides by a Coral Reef which crests and sheers down 250 m to the valley below. An array of cleaning stations lines the southern face of the mount, one of which (Station A) is frequented by Giant Manta Rays.
SCUBA divers initially deployed remote video cameras at five cleaning stations (A–E) on Monad Shoal during a pilot study which ascertained that Station A was the only location on the seamount where Giant Manta Rays could be observed interacting with Cleaner Fish. A total of 1171.45 h of video observations were subsequently recorded from a fixed point on Station A between April 2011 and June 2013, during three field expeditions spanning 262 days over 20 months. A
Sony Handycam® HDR-SR8, housed in an Amphibico Elite housing and fitted with a 120° wide-angle lens, with focal range locked to 0.3 m, was pre-set to record for 360 continuous minutes for all camera deployments. The camera was retrieved at the end of each deployment period, and the video data downloaded for analysis.
Environmental data including tidal conditions, water temperature, and the in situ current strength were documented for each camera deployment. Temperature was measured in situ to the nearest degree Celsius using the readouts of a dive computer at the time of the camera deployment. Current strength was measured from a submerged windsock that was fixed to the substrate in the camera’s field of view. Tides were estimated from
Admiralty predictions for Bogo Bay, the Philippines.
Murie et al. took still images of the video recordings when a Manta Ray was positioned directly above the camera to capture its ventral surface. They then entered the still images into a photo bank that considered patterning in the manta’s ventral markings to identify a new individual, or a match to an individual that had been previously observed at Station A. Due to the camera’s field of view, it was not always possible to capture the entire ventral surface for each Manta Ray so some mantas could not be individually identified.
To investigate whether cleaners forage selectively on Giant Manta Rays, it was assumed that different areas of a client’s bodyscape host different types of parasites and that some areas represent higher quality food patches for cleaners than others. Eight food patches were outlined on a sketch of a Giant Manta Ray and categorised as ‘gills’, ‘pelvis’, ‘dorsal head’, ‘ventral head’, ‘pectoral’, ‘ventral body’, ‘dorsal body’, and tail. These were then used to document cleaner interactions for each event. The pelvic and tail patches included the cloaca and tail, respectively, the pectoral patch incorporated both pectoral fins, the gill patch included both sets of gill openings, and the head patch consisted of the cephalic lobes, the eyes, and the mouth. The Ray’s dorsal surface was split into two patches, the boundary of which followed the underside of the Ray’s superbranchial region.
The food patches onto which locations of cleaning interactions were mapped during the analysis of the video recordings. Murie et al. (2020).
Cleaning interactions were characterised by a cleaner’s mouth making discernible physical contact with a Manta Ray and were termed ’bites’. Bite locations were individually mapped onto the sketch according to their associated cleaner species, Labroides dimidiatus or Thalassoma lunare, and treated separately in the analyses. Bites were used as a proxy for parasite removal. The number of cleaning inspections may be underestimated because Cleaner Fish activity behind a Manta Ray could not be observed on the video recordings.
Nine Mantas (M2–M10) were first recorded in 2011, four of which were observed revisiting the site in 2012 (M5, M7, M8, M9). Six Mantas (M11–M16) were first observed in 2012, two of which (M12, M13) were observed revisiting the site in 2013. One Manta (M9) was observed every year (2011–2013). Across all observations four Manta Rays were only seen on a single occasion. The remaining eleven had an average return rate of 5.64 across the three observation years.
Comparisons between models of Giant Manta Ray visits showed that the minutes observed, and the minutes after the high tide explanatory variables should be omitted from the final model. Manta Ray visits to the cleaning station varied throughout the year, occurring most frequently between April and September, with visits rare during March and July. Visits were most likely to occur during warmer temperatures and in the afternoon. Visits were also most likely to occur when the current was strong (over 1.5 metres per second) or weak (about 0.2–0.4 metres per second), but they were rare when the current was mild (about 1 metres per second).
There were 32 recorded cleaning events by 11 identifiable Mantas for which all data was available. These events lasted between 41 and 2976 seconds and involved between 1 and 22 discernible cleaning interactions. Comparisons between single-term deletions of the model for cleaning interactions indicated that all of the explanatory variables should remain in the final model.
The rate of interactions varied between individual Manta Rays, with some (for example M8) receiving much more attention from cleaners than others. The current strength was found to constrain the number of interactions a Manta Ray received, and higher water temperatures had a weakly positive effect, The minute after 05:00 had a weak negative effect, and the day of the year had a weakly positive effect.
Single-term deletions of the model for patch preferences by cleaner species indicated that the interaction between the patch and species should be omitted from the final fitted model.
After controlling for differences in patch area and comparing each patch to the ‘dorsal head’, cleaners showed preferences for certain patches. Both species targeted the gills, which received the largest absolute number of cleaning interactions, with both cleaner species also showing a preference for the pelvis. The pectoral fins received large absolute numbers of cleaning interactions by Labroides dimidiatus, which resulted in a slight preference for this patch by this species despite its large value for patch proportion. Thalassoma lunare’s preference for the ventral body could not be estimated since no cleaning interactions were recorded in this patch for this species, even though this parameter was structurally identifiable in the analysis.
While the cleaner–client system amongst reef Teleosts has received considerable attention, the spatially and taxonomically diverse associations between cleaners and Elasmobranchs are less understood. This study represents the first attempt to quantify interactions between Giant Manta Rays
and cleaner wrasse in the natural environment and supports knowledge of the importance of cleaning stations to marine ecosystems.
Our observations of giant manta rays were most likely to occur in the afternoon on a seasonal basis between the months of April and September. Giant Manta Rays’ large body size and planktivorous diet make ocean productivity a key factor in determining their movements and seasonal shifts in food availability encourage them to undertake substantial migrations. Giant Manta Rays are known to frequent cleaning stations in Mozambique, Ecuador, and Indonesia during the austral winter, and their seasonal fidelity to these sites has largely been attributed to increases in local productivity that is driven by oceanographic processes, including currents. It is possible that Giant Manta Rays have limited movements on a regional scale in Murie et al.'s study area and that they are only in the vicinity of Monad Shoal when seasonal oceanographic processes promote shifts in productivity and the consequent availability of food. They may partition their time to converge on Station A during the afternoon when food is scarce and/or when hydrodynamic conditions facilitate cleaning. Similar temporal trends for Giant Manta rays visiting cleaning stations have been observed in Indonesia where they are known to move offshore to forage nocturnally in deep waters after they clean. Mantas’ movements and use of our study area may be part of a strategy that considers both temporal variations in food availability and cleaner services without being mutually exclusive.
The overall occurrence of Giant Manta Ray cleaning events was strongly influenced by the state of the current on the seamount. Certain hydrodynamic conditions may generate sufficient water flow and lift for Giant Mantas to ‘hover’ over specific topographical features. In Mozambique, Reef Manta Rays are known to clean during moderate strength currents because these conditions are favourable for hovering over cleaning stations. Hovering may facilitate Giant Mantas’ interactions with cleaners since cleaning typically occurs near spatially finite structures that are known as ‘focal points’. Hovering is also likely to be an energetically efficient strategy that makes Giant Manta Rays more accessible to cleaners and, therefore, more attractive as clients. However, even though hydrodynamic flow may provide lift and facilitate a Giant Manta’s hovering behaviour over a cleaning station, cleaning events were not observed on Monad Shoal when the current was strong. Cleaners are known to seek refuge and conserve their energy during strong currents, which stalls the provision of cleaning services for their clients. The reduced availability of cleaners may have decreased the likelihood of a Giant Manta Ray visiting the site during these periods in spite of the energetic benefits provided by strong currents.
Reef Teleost clients are known to show preferences for specific services that are offered by specific cleaners at specific stations. A client’s fidelity to individual cleaners may be driven by the type and quality of service on offer (parasite removal, wound healing, tactile stimulation), or other clients competing for the same resources. Many of the individual mantas that we observed on Station A had open wounds from bite marks and dismembered cephalic lobes, presumably from encounters with predators and/or fishing gear. Giant Manta Rays’ fidelity to this site may be indicative of a lack of competition from other Elasmobranch clients, and/or specialist wound healing and parasite removal services that are on offer at this particular location.
Higher temperatures were found to influence the frequency with which Giant Manta Rays visited Station A and were also associated with an increase in the frequency of their interactions with cleaners. Digenean Flatworms (Phylum Platyhelminthes) that are known to infect the cloacas of Elasmobranchs on Monad Shoal are typically dioxenous, parasitising two hosts during their life cycle. During reproduction, oviparous Digeneans release their fertilised eggs into the water column where they hatch to produce miracidia. The miracidia swim to find an intermediate Mollusc host where they grow through several life stages until they eventually emerge as cercaria larvae. Larvae live freely in the water column before they attach to their terminal host, which they locate from host-derived chemical or mechanical cues, or shadows. Attachment typically occurs during seasonal epizootic events, which are characterised by cool (roughly 25 °C) or warm (roughly 32 °C) water conditions and may coincide with a time when hosts are particularly vulnerable to infection.
Murie et al.'s conjecture for further study that the seasonality with which Giant Manta Rays visit Monad Shoal might coincide with ectoparasite attachment events in the area, leading to heightened parasitism and a greater need for interacting with cleaners.
Since Cleaner Fish tend to modify their foraging patterns in response to variations in the quantity and quality of a food resource, Giant Manta Rays with the highest parasite loads are more likely to be attractive clients. Labroides dimidiatus typically favours larger clients with high ectoparasite infections, and a client’s body size has been positively correlated with ectoparasite abundance. The number of cleaning interactions (per unit time) varied substantially among individual Mantas across our observations. Although Murie et al were not able to quantify body size, it is possible that larger Mantas received more attention from cleaners than smaller ones.
Cleaning interactions were patch-specific, suggesting that the cleaners forage selectively across a Giant Manta Ray’s bodyscape. Ectoparasites that attach to Elasmobranchs are site specific and typically infect the same sites across different host species. Platyhelminthes parasitise most Elasmobranchs, and Paronatrema spp. found in and around the cloaca of pelagic Thresher Sharks, Alopias pelagicus, that regularly visit our study site are thought to be the primary driver for cleaners preferentially foraging on their pelvis. Monogenean Flatworms are similarly known to infect the cloaca of Manta Rays in Mozambique, and Gnathiid Isopods, which are a primary food source for the Blue Streaked Cleaner Wrasse, infect their buccal cavities. While it was not possible to verify whether Manta Rays visiting Monad Shoal are infected by Gnathiids, Digeneans, or Monogeneans, Murie et al.'s observations suggest that either parasitic abundance is highest in and around the cloaca and gills, or that Cleaner Fish are selecting parasites, mucus, and/or dead tissue there because they are accessible.
Many large marine organisms visit cleaning stations to have parasites removed and giant manta rays appear to regularly visit cleaning stations on inshore reefs. The Rays may visit cleaning stations to benefit from feeding opportunities nearby or they may migrate inshore to clean after they forage in deep-water. Giant Manta Rays are thought to have limited regional connectivity and so the low number of absolute visits that we recorded either suggests that the habitat no longer supports their requirements, or that they are in regional decline. Cleaning interactions are both spatially and taxonomically diverse and cleaners’ selective foraging on Giant Manta Ray clients demonstrates a level of preference for areas of a Manta’s body where specific types of parasites might be found. Future identification and quantification of parasite loads on Giant Manta Rays would offer further evidence that Elasmobranch clients provide high-quality food patches for cleaners at seamounts. Cleaning stations are key points of convergence for Giant Manta Rays and they may only frequent specific cleaning stations so these spatially finite habitats should be carefully managed.
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