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.