Can non-cleaners replace dedicated cleaners?
Dedicated cleaner fishes are considered amongst the most functionally critical and most vulnerable organism groups on coral reefs (Wolfe et al. 2020). However, this assessment is based solely on studies on Indo-Pacific cleaners. The reputation of cleaners as the major consumers of gnathiids is based on extensive gut content studies aimed at determining what cleaners are removing from clients (Losey 1974, Soares et al. 2010, Whiteman and Côté 2002). However, such studies have almost completely ignored the myriad of other fishes that could potentially consume as many or more gnathiids during their free-living stages, and that could therefore have greater impacts on gnathiid populations. While many feeding studies have been conducted on coral reef fishes (Choat et al. 2004, Hobson 1975, Randall 1967, Russell 1983) gnathiids appear to be overlooked and characterized as “unidentified crustaceans”. This is because very few individuals are trained to detect and identify them and genetic barcodes which would allow for DNA metabarcoding approaches to gut content analysis (Matley et al. 2018) have been almost completely lacking. Within each of the 10 non-cleaner functional groups was at least one individual fish that consumed at least a single gnathiid. Although some herbivores will on occasion supplement their diet with invertebrates (Ceccarelli 2007), this result was surprising because the species within the scraper and herbivore groups are not considered to be major consumers of invertebrates, let alone parasitic species. Given the infrequent occurrence of gnathiids in the gut contents of herbivores and scrapers, it seems likely that these were cases of incidental consumption where the gnathiid was consumed along with the targeted benthic algal matter. The various invertivores sampled here also consumed gnathiids quite infrequently, regardless of the microhabitat they occupied. In fact, dedicated cleaners, which comprise less than 1% of fish biomass, consumed 18 times more gnathiids per gut relative to the highest invertivore group (the planktivores) and 100 times more than the next highest group (the benthic invertivores, Table 1). This suggests that gnathiids are not a key prey item for non-cleaner invertivores. This is likely due to low habitat mediated availability (such as in the case of sand invertivores) or no preference relative to the many other available invertebrates.
Nicholson et al. (2020) showed that gnathiids sometimes travel above the benthos (upwards of 3.5m) into the water column to attach to a fish host. Planktivorous fishes in this study were the non-cleaner group most likely to consume a gnathiid (33%, Table 1) and ate gnathiids more often than the nocturnal consumers examined from one of the same study sites from Artim et al. (2017). This suggests that either gnathiids are spending time swimming above the reef during post-dawn morning times, or, more likely that they are being eaten by planktivores feeding closer to the reef substrate during dawn emergence from, or dusk entrance to, nocturnal refuges. The low-level of consumption by demersal feeding invertivores further suggests that when gnathiids are on the benthos, they are most often hiding in crevices and rubble (Artim and Sikkel 2013, Santos and Sikkel 2017).
Our data included many instances where no gnathiids were detected in fish gut samples. In cases where at least one gnathiid was consumed, non-cleaner gut contents still typically only contained the remnants of one or two gnathiids, and never more than 5 (Fig. 2B). This eliminates the possibility that there may be some intraspecific variation among non-cleaners, where some individuals have an increased likelihood to consume gnathiids. Furthermore, the consistently low levels of gnathiid consumption by non-cleaners means it would take, for nearly all non-cleaner functional groups, nearly 100 or more individuals to compensate for the loss of a single cleaner goby (Fig. 3). These results are in line with previous studies on gnathiid consumption by nocturnal microcarnivores (Artim et al. 2017) and show that while many species and functional groups are capable of consuming gnathiids, there is not sufficient functional redundancy of gnathiid consumption by non-cleaner fishes to replace dedicated cleaners.