Alexandra Sara Grutter

Settlement patterns of juvenile fish shape coral reef communities. During the recruitment process, predation rates are extremely high. However, the role that parental care plays in reducing mortality, especially by cryptic natural enemies such as parasites, remains largely unstudied. We investigated whether parental care in the spiny chromis damselfish ( Acanthochromis polyacanthus ) protects juveniles from parasite-induced mortality by gnathiid isopods ( Gnathia aureamaculosa ). Using laboratory experiments, we found that survival of recently hatched juveniles when exposed to gnathiids was higher when parents were present (77%) than when parents were absent (25%). Investigation of their faeces in the field and laboratory indicates that adults consume gnathiids. Together, our data suggest that parental care plays a key role in reducing parasite-induced mortality of juvenile spiny chromis via parental consumption of gnathiids. This highlights the overlooked role of parasites as a source of high mortality in juvenile coral reef fishes and the composition of coral reef fish communities.

Gnathia antennacrassasp. nov.from seagrass beds off Rottnest Island, Western Australia is the first record of any gnathiid from the entirety of Western Australia; the male can be distinguished from congeners by the stout peduncular articles of the antenna.Gnathia taurussp. nov.is described from two adult specimens reared from praniza larvae found infecting elasmobranch fishes at Heron Island, southern Great Barrier Reef; the males can be distinguished from all congeners by the dorsally strongly elongate mandibles and smoothly rounded mediofrontal process on the anterior part of cephalosome. Gnathia aff. maculosa Ota & Hirose, 2009 is recorded from Australia, together with further records ofG. trimaculataCoetzee, Smit, Grutter & Davies, 2009 andG. grandilarisCoetzee, Smit, Grutter & Davies, 2008, all from elasmobranch fishes.

Corrigendum: Cleaner fish Labroides dimidiatus presence does not indirectly affect demersal zooplankton

Grazing fishes farm algae, and consume algae, detritus and sediment and consequently differentially modify benthic communities. Manipulations of cleaner fish Labroides dimidiatus on reefs show that cleaners affect fish abundance differently according to grazer functional group. Accordingly, whether reefs are grazed differently, with consequences for the benthos (fouling material tile⁻¹), was tested using reefs kept free of L. dimidiatus for 10 years compared with undisturbed control reefs. We recorded on video the grazing density (bites tile⁻¹ h⁻¹ reef⁻¹) on settlement tiles and the natural benthos (roving fishes only), according to territorial algal farmer (Pomacentridae) and roving grazer (Acanthuridae, Labridae, Siganidae) functional groups, and measured the accumulation of fouling material tile⁻¹ after 10 months. Grazing density on tiles (dominated by ‘indeterminate’ farmers, and roving ‘sediment-removing’ detritivore Ctenochaetus striatus) and the natural benthos (dominated by Ct. striatus and other grazers) was not measurably affected by cleaner presence. The composition of fouling material (dominated by detritus > turf algae > sediment > other) and organic and inorganic dry weight of material tile⁻¹ were also not measurably affected by cleaner presence. This points to resilience of the benthic community to loss of cleaners. The likely complex interactions between cleaner fish presence, grazer abundance and mobility, and the often-opposite effects of territorial farmers and roving grazers on the benthos underscore the challenge in determining indirect effects of cleaners on benthic community structure. However, a lack of cleaners has negative ramifications for fish populations and physiology and thus their loss remains problematic for client fishes.

Cleaning symbiosis is critical for maintaining healthy biological communities in tropical marine ecosystems. However, potential negative impacts of mutualism, such as the transmission of pathogens and parasites during cleaning interactions, have rarely been evaluated. Here, we investigated whether the dedicated bluestreak cleaner wrasse, Labroides dimidiatus, is susceptible to and can transmit generalist ectoparasites between client fish. In laboratory experiments, L. dimidiatus were exposed to infective stages of three generalist ectoparasite species with contrasting life histories. Labroides dimidiatus were susceptible to infection by the gnathiid isopod Gnathia aureamaculosa, but were significantly less susceptible to the ciliate protozoan Cryptocaryon irritans and the monogenean flatworm Neobenedenia girellae, compared with control host species (Coris batuensis or Lates calcarifer). The potential for parasite transmission from a client fish to the cleaner fish was simulated using experimentally transplanted mobile adult (i.e. egg-producing) monogenean flatworms on L. dimidiatus. Parasites remained attached to cleaners for an average of 2 days, during which parasite egg production continued, but was reduced compared with that on control fish. Over this timespan, a wild cleaner may engage in several thousand cleaning interactions, providing numerous opportunities for mobile parasites to exploit cleaners as vectors. Our study provides the first experimental evidence that L. dimidiatus exhibits resistance to infective stages of some parasites yet has the potential to temporarily transport adult parasites. We propose that some parasites that evade being eaten by cleaner fish could exploit cleaning interactions as a mechanism for transmission and spread.

Coral reef mutualisms involve complex trophic ecological relationships that produce indirect effects. Excluding mutualistic cleaner fish Labroides dimidiatus from reefs indirectly increases the abundance of many fishes and reduces demersal stages of their ectoparasitic prey (gnathiid isopods). Whether cleaners affect populations of planktivorous fishes that consume demersal zooplankton, and consequently indirectly affect the rest of the demersal zooplankton community — via presumed changes in planktivory — is unknown. Therefore, using a long-term cleaner fish manipulation on patch reefs (July 2000 to December 2012, Great Barrier Reef), we tested whether cleaner treatment (removal or control) affects planktivorous fish abundance and diversity, and demersal zooplankton biomass, abundance, and diversity. Fish surveys, 9 and 12 years after removing cleaners revealed fewer fish on removal compared to control reefs for one of the three most abundant planktivores, but not total abundance (Pomacentridae, 26 species), diversity, and composition. Emerging zooplankton were sampled during the day and night over nine sampling trips across 12 years. There was no effect of cleaner treatment on post-removal values, compared with pre-removal values in July 2000, for zooplankton biomass, abundance, diversity, and composition (34 taxa). Zooplankton abundance showed no diel differences, but diversity, and occasionally biomass, were higher at night. Zooplankton composition also showed diel differences, with three taxa contributing the most to this dissimilarity [Cirripeda nauplii, Facetotecta (Arthopoda), Oikopleuridae (Chordata)]. Zooplankton diversity did not differ among times, abundance was higher in January 2002 relative to July 2000, and composition differed among all times. The lack of detectable indirect effects of cleaner fish presence on zooplankton (non-gnathiid) may partly be due to cleaners’ variable effect on planktivorous fish abundance, but also the result of invertebrate planktivory and other processes that affect zooplankton populations not investigated here. Nevertheless, the pronounced diel and temporal changes in zooplankton observed likely influence coral reef trophic interactions.

Aim: Several drivers explain the global distribution of all reef fish. However, whether these drivers also explain the distribution and traits of a functional subgroup involving cleaner fishes remain unclear. Here we examine the variation in traits of cleaner fishes and test whether historical, environmental, ecological and geographical drivers are correlated with cleaner species richness and abundance at global reefs.Location: Tropical and subtropical reefs.Taxon: Actinopterygii.Methods: We tested whether species traits and trait space vary between facultative (i.e. species that clean only during the juvenile stages or sporadically) and dedicated (i.e. species that clean during their whole lives) cleaner types. We compiled data from local checklists (relative richness) and belt transects (standardized richness and abundance). We built four models to test whether past and current isolation (i.e. distance from Quaternary refugia and biodiversity centres), sea temperature, primary productivity, local species pool and abundance of potential clients influenced the relative richness and abundance of cleaners.Results: Facultative cleaners had high trait variability that contributed disproportionally to the trait space, whereas dedicated cleaners exhibited low trait variability. Cleaner species richness was higher in the Indo‐Pacific and Caribbean provinces, but the relative richness and standardized abundance of cleaners were higher in the Atlantic (i.e. North Eastern and Southwestern) and Eastern Pacific. Isolation influenced the relative richness of facultative cleaners, whereas the distance to Quaternary refugia, sea temperature and isolation influenced the relative richness of dedicated cleaners. Local species richness and standardized abundance of cleaner fish exhibited a strong relationship with regional diversity. The standardized abundance of both facultative and dedicated cleaners was influenced by the abundance of potential clients and the local species pool.Main conclusions: The small trait space occupied by cleaner fishes may reflect their restricted origin among lineages of reef fishes. Differences in the relative richness and standardized abundance of cleaner fishes across marine realms suggest a strong influence on biogeographical history. Our results also indicate that cleaner fishes originated mostly in peripheral areas in high latitudes due to the absence of dedicated cleaners. Our results imply that cleaner fishes do not follow the pattern of main centres of origin described for reef fishes due to opportunistic cleaning behaviour that originated with higher frequency at locations with low species richness.