Cleaning symbiosis has been documented extensively in the marine environment over the past 50 years. We estimate global cleaner diversity comprises 208 fish species from 106 genera representing 36 families and 51 shrimp species from 11 genera representing six families. Cleaning symbiosis as originally defined is amended to highlight communication between client and cleaner as the catalyst for cooperation and to separate cleaning symbiosis from incidental cleaning, which is a separate mutualism preceded by no communication. Moreover, we propose the term ‘dedicated’ to replace ‘obligate’ to describe a committed cleaning lifestyle. Marine cleaner fishes have dominated the cleaning symbiosis literature, with comparatively little focus given to shrimp. The engagement of shrimp in cleaning activities has been considered contentious because there is little empirical evidence. Plasticity exists in the use of ‘cleaner shrimp’ in the current literature, with the potential to cause significant confusion. Indeed, this term has been used incorrectly for the shrimp Infraorder Stenopodidea, involving three families, Stenopodidae, Palaemonidae and Hippolytidae, and to represent all members of Lysmata and Stenopus. Caution is expressed in the use of grey literature and anecdotal observations to generate data on cleaning interactions, due to the presence of species complexes. Interest in cleaning organisms as biological controls in aquaculture is increasing due to their value as an alternative to various chemical ectoparasite controls. Reports of the importance of cleaner organisms in maintaining a healthy reef ecosystem has also been increasing and we review the current biological knowledge on cleaner organisms, highlighting areas that are understudied.
The ornamental fish trade provides a pathway for the global translocation of aquatic parasites. We examined a total of 1020 fish imported from Singapore, Malaysia, Thailand, or Sri Lanka to Australia (including freshwater and marine fish species) for monogenean ectoparasites. Fish were received following veterinary certification that they showed no clinical signs of pests and diseases from the exporting country and visual inspection at Australian border control. Australian import conditions require mandatory treatment for goldfish with parasiticides (e.g. trichlorfon, formaldehyde, sodium chloride) for the presence of gill flukes (Dactylogyrus vastator Nybelin, 1924 and Dactylogyrus extensus Mueller and Van Cleave, 1932) prior to export. Over 950 individual parasites were detected in five imported fish species, representing 14 monogenean species. Seven Dactylogyrus spp. including D. vastator and three Gyrodactylus spp. infected goldfish, Carassius auratus Linnaeus, 1758, from Malaysia, Singapore, and Thailand. Dactylogyrus ostraviensis Řehulka, 1988, infected rosy barb, Pethia conchonius Hamilton, 1822, from Singapore, Sri Lanka, and Thailand while two Trianchoratus spp. infected three spot gourami, Trichopodus trichopterus Pallas, 1970 and pearl gourami Trichopodus leerii Bleeker, 1852, from Sri Lanka. Urocleidoides reticulatus Mizelle & Price, 1964, infected guppy, Poecilia reticulata Peters, 1859, from Sri Lanka. The discovery of D. vastator in goldfish, as well as 13 other monogenean species, shows that pre-export health requirements, which include chemical treatment of goldfish, and inspection of all ornamental fish species did not prevent infection by monogeneans. Inspection prior to exportation and at border control must account for the highly cryptic nature of monogenean parasites and consider alternatives to current pre-export conditions and visual inspection at border control.
Two new species, Dendromonocotyle citrosa n. sp. off Dasyatis chrysonota (Smith) from Two Oceans Aquarium in Cape Town and off Himantura gerrardi (Gray) from uShaka Sea World in Durban and D. ukuthena n. sp. off H. gerrardi and H. uarnak (Forsskål) also from uShaka Sea World in Durban, are described. These can be distinguished from previously described Dendromonocotyle species by the morphology of the distal portion of the male copulatory organ and the proximal part of the vagina. Vaginal morphology is proposed as an important diagnostic character for species in the genus. Dendromonocotyle colorni Chisholm, Whittington & Kearn, 2001 which was originally recorded from H. uarnak in Israel, was discovered on H. uarnak sympatrically with D. ukuthena n. sp. and with D. citrosa n. sp. and D. ukuthena n. sp. off H. gerrardi. Minor differences in the number of papillary sclerites, the presence of septal tripartite sclerites and in the number of eyespots were seen between D. colorni collected from H. uarnak and H. gerrardi from uShaka Sea World and those originally described off H. uarnak from Israel. We demonstrate that the position of the marginal hooklets can be used to determine the orientation of the haptor of all representative Dendromonocotyle species with or without hamuli. We conclude that Dendromonocotyle species may not be as host-specific as previously believed and that minor differences in morphology are host or geographically induced.
Gyrodactylus eyipayipi sp. n. is described from the skin, gills, flute and male brood pouch of captive specimens of the greater pipefish Syngnathus acus L., collected for and maintained at the Two Oceans Aquarium in Cape Town, South Africa. It is the first marine Gyrodactylus species reported from the African continent. The new species is compared to the three known Gyrodactylus species affecting syngnathiform hosts (G. pisculentus Williams, Kritsky, Dunnigan, Lash et Klein, 2008, G. shorti Holliman, 1963, and G. syngnathi Appleby, 1996. Although all four species have similar-sized and shaped attachment hooks with some overlap, separation of the species is possible using marginal hook morphology. The marginal hooks of G. eyipayipi measure (mean) 30 µm in total length and are larger than those of the three other species (mean, 24-28 µm). Gyrodactylus eyipayipi can also be discriminated based on differences in the shape of the marginal hook sickle notably by its long sickle point which extends far beyond the toe, its blunt rounded toe and, by the approximate rectangular shape to the base of the sickle. By comparison, the sloping toe regions of G. pisculentus and G. syngnathi give the sickle bases an approximately triangular shape, whilst the short sickle point and open aperture to the sickles of G. shorti allow for their discrimination from G. eyipayipi.
Heterocotyle tokoloshei sp. nov. is described from the gills of a single Short-tail stingray, Dasyatis brevicaudata, kept in captivity at the Two Oceans Aquarium in Cape Town, South Africa. The stingray exhibited laboured gill ventilation and deteriorating health on exhibit and was removed to the quarantine area for parasitological study and treatment. A 12 h bath treatment of praziquantel at 20mg/l, pre-dissolved in ethanol, removed 3084 parasites from the gills of the ray. However, the presence of a large number of eggs 24 h post-treatment indicated that viable egg laying adults remained on the gills and that the treatment was not 100% effective. Praziquantel was subsequently administered orally by intubation to the same ray at 150 mg/kg under anaesthetic (2-phenoxyethanol at 0.15 ml/l for approximately 1 h), which resulted in the removal of approximately 392 000 parasites from the gills 12 h post-oral treatment. Twenty-four h post-oral treatment, 3383 worms, but no eggs were recovered. No worms or eggs were recovered 48 h to 10 days post-oral treatment. The ray died approximately 30 days after the completion of the treatment. Heterocotyle tokoloshei sp. nov. is the first Heterocotyle species described from South Africa and represents the first record of a pathogenic Heterocotyle species. The new species can be distinguished from the other 16 species in the genus by the distal region of the male copulatory organ which has distinct small spines and by the morphology of the male copulatory organ accessory piece. Eggs of H. tokoloshei sp. nov. are laid singly and hatch spontaneously between 5 and 8 days at 18°C.
The monogenean family, Hexabothriidae Price, 1942 (1908), currently consists of 15 valid genera parasitic on the gills ofchondrichthyan fishes. The hexabothriid literature is littered with inconsistencies, ambiguity and editorial errors whichhampers the progress and the development of investigations after the significant treatment of the family by Boeger &Kritsky (1989). A lack of consistency in the measurement protocol for the haptoral armature of hexabothriids is highlight-ed and discussed. The preliminary results of a new measurement protocol incorporating existing and novel parameterswere explored for the first time using statistical analyses. Character variables were investigated for their utility as poten-tially useful discriminators using univariate and multivariate analyses. The elimination of age-associated variance in suck-er sclerites was performed by ratio-transformation of the data to an age-dependant variable. Character variables with ahigh coefficient of variance after accounting for age were disqualified for use in the subsequent analyses. A coefficient ofvariance exceeding a conservative 10% limit was considered the result of measurement error resulting from the small sizesof these variables and therefore may also reflect the limitations of hardware and software in making small but accuratemeasurements. The proposed protocol is tested on representatives of Callorhynchocotyle and a Rajonchocotyle species totest the utility of character variables in separating species. Principle Component Analysis of the combination of the sucker-sclerites and the hamulus provided a preliminary level of robustness in separating Callorhynchocotyle species with theexception of Callorhynchocotyle hydrolagi for which there were insufficient data. Results confirm the importance of thehamulus in providing valuable diagnostic significance but the shape of the sucker sclerites as a function of total length anddiameter may also provide significant potential. Callorhynchocotyle is revisited with the addition of new specimens for 3of the species. The new data resulting from the measurement protocol are included in the redescription of Callorhynchoc-otyle marplatensis, Callorhynchocotyle callorhynchi and Callorhynchocotyle amatoi. Supplemental information is provided for C. hydrolagi and Callorhynchocotyle sagamiensis.
Chemical use is widespread in aquaculture to treat parasitic diseases in farmed fish. Cleaner fish biocontrols are increasingly used in fish farming as an alternative to medicines. However, cleaner fish are susceptible to some of their clients’ parasites and their supply is largely dependent on wild harvest. In comparison, cleaner shrimp are not susceptible to fish ectoparasites and they can be reliably bred in captivity. The effectiveness of shrimp in reducing parasites on farmed fish remained unexplored until now. We tested four cleaner shrimp species for their ability to reduce three harmful parasites (a monogenean fluke, a ciliate protozoan, and a leech) on a farmed grouper. All shrimp reduced parasites on fish and most reduced the free-living early-life environmental stages – a function not provided by cleaner fish. Cleaner shrimp are sustainable biocontrol candidates against parasites of farmed fish, with the peppermint cleaner shrimp reducing parasites by up to 98%.
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