Friends, foes and followers of fishes

Abstract

Larger fish species are often seen accompanied by smaller species — anything from helpful cleaners, via unobtrusive fellow travellers, through to flesh-eating parasites. Some of these ecological relationships have been studied in detail, but many, especially the more dynamic ones, remain poorly understood. For our understanding of the fate of marine species in a changing oceanic environment, these connections may be of vital importance. Michael Gross reports. Larger fish species are often seen accompanied by smaller species — anything from helpful cleaners, via unobtrusive fellow travellers, through to flesh-eating parasites. Some of these ecological relationships have been studied in detail, but many, especially the more dynamic ones, remain poorly understood. For our understanding of the fate of marine species in a changing oceanic environment, these connections may be of vital importance. Michael Gross reports. Manta rays with their vast wingspan of up to seven metres are among the most charismatic fish species to observe in the warmer parts of the oceans and thus a key attraction in scuba-diving destinations, such as the Maldives or Hawaii. Of the two species now merged into the genus Mobula (together with the devil rays), the smaller, more coastal reef manta ray (Mobula alfredi), in particular, can readily be observed near coral reefs, while the giant ocean manta ray (Mobula birostris) is slightly more elusive. Both species have been listed as Vulnerable on the IUCN Red List, with M. birostris now upgraded to Endangered. Countries such as Indonesia have realised that the long-lived animals are much more economically valuable alive as a tourist attraction rather than dead at the fish market and have protected them accordingly. However, a growing demand for the cartilage of their gill plates is still fuelling an unsustainable level of killing that often happens either illegally or in international waters. The Manta Trust, an international charity based in the UK, is working to improve the protection and appreciation of these animals. Its experts can even identify thousands of individual manta rays. While the rays are mostly black from above (the dorsal side), their ventral side is typically white with a pattern of black spots that is unique in each individual. Working with the dive and snorkel tourism industry in the Maldives, the Manta Trust has established an image database identifying resident individual reef manta rays by their spots, and this database passed 5,000 entries in December 2020. As with the star-like pattern of whale sharks and the whisker spots of lions, the database of fingerprinted individuals enables researchers to better understand the life cycle of the animals, including their social network within their own species and with other species. Manta rays are often observed aggregating in groups of several dozen individuals, and they are often seen accompanied by smaller fish species, including some that attach themselves to the rays. These fellow travellers obviously use the large rays for their own benefits, but are they parasites, mutualists or commensalists (i.e. do they harm, benefit, or have no effect on the rays)? As it is difficult to monitor the contacts of a fast-moving species, surprisingly little is known about the interspecies connections of manta rays. Aimee Nicholson-Jack from the Manta Trust and colleagues recently expanded the scope of knowledge on the manta ray ‘hitchhikers’ with what the authors say is only the second systematic analysis of such species to be published in a peer-reviewed format (PLoS One 16, e0253704). Using the Maldives database and photographic evidence accumulated in three decades’ worth of citizen science engagement, the researchers evaluated the associations observed for 4,901 M. alfredi individuals identified in 353 sites. They found 12 species associated with the reef manta rays, including, for the first time, species that don’t belong to the well-known family Echeneidae (remoras). The most commonly observed companion was the sharksucker remora (Echeneis naucrates), which was observed in 10% of the sightings. These remoras were most likely to be present when the rays were visiting cleaning stations, which are nearshore locations where populations of cleaner fish feed on crustacean parasites present on the rays. Near-term pregnant females were also more likely to be seen with E. naucrates, but this may be causally related to the fact that they spend more time at cleaning stations. Interestingly, juvenile remoras also tended to be found with juvenile rays. In addition to filter-feeding near the surface, manta rays also dive to depths below 200 metres, to hunt there. It is thought that E. naucrates is unable to survive at that depth, so the movement pattern of the ray explains why the hitchhikers aren’t with them at all times. A recent tagging study of M. alfredi diving behaviour found that all tagged individuals went to depths beyond 300 metres, with a maximum recorded depth of 672 metres (PLoS One (2020) 15, e0228815). By contrast, the most common companion of the giant oceanic manta ray, the giant remora (Remora remora), seems to stay with the ray for longer periods of time, and often attaches itself to the ray. Based on records of 663 identified M. birostris individuals, R. remora was present in just over half the sightings. While the remoras provide some benefits to the manta ray host, including removal of crustacean parasites, the habit of attaching to the ray can also come with a fitness cost to the ray. The researchers have observed examples of scars due to remora attachment and of remoras attached in unsuitable places, such as inside the gills or the anus. A third remora species, the white suckerfish (Remora albescens), was only rarely seen on the images analysed, but has been discovered within the mouths of rays examined more closely, which leads the authors to suggest that these remoras are more commonly associated with rays than the observation data suggest. New hitchhiker species from outside the echeneid family identified for the first time included black, bluefin, and giant trevallies (Caranx lugubris, C. melampygus and C. ignobilis, respectively), rainbow runner (Elagatis bipinnulata), cobia (Rachycentron canadum), red snapper (Lutjanus bohar), and Chinese trumpetfish (Aulostomus chinensis). These species are generally more loosely associated with the rays and not thought to harm them, so their relationship would be classified as commensalism. They benefit from the presence of the larger species in terms of shelter from predators (shown for juvenile golden trevally) and availability of food leftovers and may also save energy due to drag reduction. Some, including adult trevally, snapper and trumpetfish, use the body of the manta ray to get closer to their prey and launch their predation attack from this shelter. Considering that the habitat of manta rays is already changing rapidly due to climate change and other anthropogenic factors, the authors call for a more comprehensive assessment of the ecological network around these charismatic and vulnerable species. The study of the Maldives population, backed by the unique tool of the image database identifying individual animals, is laying a foundation. “Further research of hitchhikers in different manta ray populations is warranted to evaluate whether the associations found within the Maldives apply to other locations”, Nicholson-Jack comments. “Further research on the ecology of the individual hitchhiker species is essential to understand the drivers of the association more holistically.” One other recent study of manta rays and their companions focused on observations of M. birostris and its symbiont R. remora in a marine protected area near the Pacific coast of Mexico. Edgar Becerril-García from the Instituto Politécnico Nacional at La Paz, Mexico, and colleagues analysed 271 images taken by researchers and amateur divers and documented a mean of 1.6 remoras per manta ray (Mar. Freshwater Res. (2019) 71, 414–417). Among the hitchhiking species, the remoras have attracted attention for the efficiency of the reversible suction mechanism that they use to attach to their hosts, which apart from rays also include other marine megafauna, from sharks to whales. The attachment survives remarkable drag forces on fast-swimming animals, but can be fastened or released in a fraction of a second. The remoras achieve this with an adhesive disc that evolved from dorsal fin elements and consists of a series of parallel lamellae surrounded by a fleshy lip. When the lip makes contact, the lamellae rotate to expand the enclosed space and thus reduce the pressure. The group of Brooke Flammang at New Jersey Institute of Technology at Newark, USA, has studied the suction apparatus for clues towards remora behaviour, especially when, where and why they attach or let go. Investigating the anatomy of the lip in E. naucrates, the researchers discovered densely innervated structures, which they propose to be push-rod mechanoreceptors that allow the remoras to sense when they have made contact with a host and quickly trigger attachment (R. Soc. Open Sci. (2020) 7, 190990). Once attached, the mechanism would enable them to sense shear forces and ensure they remain fixed. While entirely plausible in terms of what the remoras need to hitch a ride, this was a sensational discovery because it is unprecedented among fishes. The only other comparable mechanism the researchers could find in the literature is in monotremes (platypus and echidnae). “One of the wildest things about this work was not only finding a mechanoreceptor complex not previously known to fishes, but that the only other organisms known to possess them are monotremes,” Flammang said. “This is exciting because it shows how much we as integrative comparative biologists still have to learn about the sensory world of organisms.” Regarding the question of where remoras attach and how they behave on their host surface, Flammang had a lucky break when she saw a conference talk from whale researcher Jeremy Goldbogen of Stanford University, USA, who had tagged blue whales with video cameras and “inadvertently gotten hundreds of hours of remora footage.” After seeing the movies of remoras skating around on the surface of the whales, Flammang set out to analyse their behaviour. Until then, the only information available was based on photos or short-term observations. Working with experts on fluid dynamics, and the Barcelona Supercomputing Centre in Spain, Flammang and colleagues obtained models of the flow conditions around the whale (J. Exp. Biol. (2020) 223, jeb226654). They identified various areas where the anatomy of the whale reduces the drag forces and makes it easier to remain attached, such as behind the blowhole and behind the fins. In these areas, the drag force on a whale swimming at 1.5 metres per second is reduced by up to 80%. Sure enough, the videos show the remoras preferentially settling in these areas, thus saving energy. Calculations showed, however, that they could maintain attachment anywhere on the whale, even on the highly agile tail fluke. While the remoras had their favourite spots, they didn’t always stay in one place. Footage shows them gliding across the surface, to get from one sweet spot to another, or to meet with fellow passengers. “The skimming and surfing behaviour is amazing for many reasons, especially because we think that by staying about a centimetre off the whale body, they are taking advantage of the Venturi effect and using suction forces to maintain their close proximity,” Flammang explained. “In this narrow space between the remora and whale, when fluid is funnelled into a narrow space it moves at a higher velocity but has lower pressure, so it is not going to push the remora away but can actually suck it toward the host.” Knowing the best spot to attach to animals like whales, rays and sharks will also prove helpful to conservation research, as it can facilitate tagging the animals. With applications like tagging in mind, Flammang’s group has also developed biomimetic suction devices based on the remora studies (Bioinspir. Biomim. (2019) 14, 056014). Most recently, the group of Wen Li at Beihang University, China have further studied the structure and function of the mechanism with a view towards creating similar biomimetic structures (Matter (2020) 2, 1207–1221; Bioinspir. Biomim. (2020) 15, 056018). One ecological connection between fish species that has been studied extensively is that between cleaner fish, such as cleaner wrasses (genus Labroides), and their clients, which is a mutualistic one because the cleaners feed by ridding their clients of crustacean parasites. Manta rays and other large fish species visit cleaning stations, environments where cleaner fish are abundant, so this interaction is readily observed at specific locations. Many other interactions remain to be explored. Some involve parasitic species hiding inside a fish’s body cavities, such as the tongue biters, crustaceans of the isopod family Cymothoidae that attach themselves to the host’s tongue and often end up eating it and taking its place. These can often remain hidden, as demonstrated by the surprising discovery of a rare species found in a museum specimen almost antipodal to the place where the only other examples were found. The cymothoid Elthusa splendida was first described in 1981 on the basis of five specimens recovered from a Cuban dogfish, a deep-sea shark, that had been caught in the western South Atlantic, off southern Brazil. Among cymothoids settling in the mouth of their host, it is an unusual species as it attaches to the palate. No other representatives of this species were reported until November 2020, when Ryota Kawanishi and Shinpei Ohashi from Hokkaido University identified one they discovered in a museum specimen of another deep-sea shark, a Japanese spurdog, caught in the East China Sea, very nearly on the other side of the planet compared with the original discovery (Species Divers. (2020) 25, 343–348). This surprising discovery appears to suggest that the species is, or at least has been, present around the globe, but managed to remain hidden from the eyes of scientists. The authors also suggest a more generalised scrutiny of fish specimens kept in museums, in case other examples are still awaiting their discovery. Other connections between species remain elusive because they are fleeting and dynamic. Thus, large fish species like whale sharks (Rhincodon typus) are often observed in the company of numerous smaller species, including blackfin tuna (Thunnus atlanticus), which in a survey conducted in the Gulf of Mexico was the most commonly seen companion among more than a dozen species identified. A detailed analysis of the precise nature of these interactions remains to be accomplished. The typical Pleistocene megafauna has so far survived much better in the marine environment than on land (Curr. Biol. (2015) 25, R209–R212) although several whale species had a close encounter with extinction (Curr. Biol. (2021) 31, R215–R218). As the impact of anthropogenic change continues to increase, efforts to save these species will require, among other things, a better understanding of the complex network of interactions that links the charismatic big beasts to the other fish in the oceans.