MARINE ECOLOGY PROGRESS SERIES Vol. 164: 263-271,1998 Published April 9 Mar Ecol Prog Ser Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes Alexandra S. Grutter 'l*, Robert poulin2 'Department of Parasitology, The University of Queensland. Brisbane, Queensland 4072, Australia 'Department of Zoology, University of Otago. PO Box 56. Dunedin. New Zealand ABSTRACT: Parasitic gnathud isopod larvae on coral reef teleosts and elasmobranchs were quantified at Lizard and Heron Islands (Great Barrier Reef), and Moreton Bay, Australia. The relationship between gnathlid abundance and host size was examined across and within species. Of the 56 species examined. 70 % had gnathiids, with counts ranging from 1 to 200 per fish and the elasmobranchs hav- ing the highest numbers. Pomacentrids rarely had gnathiids. In contrast, most labrids had gnathiids. Gnathiid abundance was positively correlated with host size in the species Chlorurus sordidus, Ctenochaetus stnatus, Hernigyrnnus melapterus, Siganus dollatus, and Thalassorna lunare, but not for Scolopsis b~lineatus.Mean gnathlid abundance per host species also correlated with host size across species, even after controlling for the potential confounding effects of uneven sampling effort and host phylogeny Thus host size explains much of the intraspecific and interspecific variation In gnathiid abundance on fish. KEY WORDS: Gnathiidae . Ectoparasites . Coral reef fish . Host-parasite interactions . Fish size . Great Barrier Reef INTRODUCTION gnathiids on fish (Grutter 1996a). When present in 'large' numbers (Paperna & Por 1977) and when fish Until recently, there was little evidence that para- have 'around a hundred' (Mugridge & Stallybrass sites were important in fish cleaning behavior (Losey 1983),gnathiids can cause fish mortality in captive fish 1987), however, current studies on the Great Barrier (Paperna & Por 1977). Gnathiids, in 'numerous num- Reef, Australia, show that parasites, in particular bers', also affect stingrays in the wild, causing destruc- gnathiid isopod larvae, play a significant role in clean- tion and inflammation of the mucosal tissues and a ing interactions. Ninety percent of the items in the propagation of bacilli (Honma & Chiba 1991). That diet of the cleaner wrasse Labroides dimidiatus are cleaner fish may control these potentially deleterious gnathiids (Grutter 1997a) and each of these cleaner parasites has important implications for understanding fish eats on average 1200 parasites per day (Grutter the ecological significance of cleaning, as studies to 1996a).Larger gnathiids are also selectively preyed on date have been unable to experimentally demonstrate by this cleaner fish (Grutter 1997b). Most importantly, any benefit of cleaning to the host (Youngbluth 1968, the high predation rate, relative to the number of Losey 1972, Gorlick et al. 1987, Grutter 1996b, 1997~). gnathiids on fish and their infection rate, suggests that Information on gnathiids, therefore, is needed to L. dimidiatus have an effect on the abundance of understand their role in cleaning. Research on gnathiids has likely been hindered by their complicated life history. Gnathiids are only para- sitic as larvae, feeding on host blood and other fluids, O Inter-Research 1998 Resale of full article not permitted 264 lMar Ecol Prog Ser 164: 263-271, 1998 and return to the benthos to moult after each of the 3 Elasmobranchs were collected on the reef flat (0.5 to larval stages (blonod 1926, Upton 1987, Klitgaard 2 m depth) at Heron Island by herding rays and sharks 1991). Adults are benthjc and do not feed. Because lnto a net. Sharks and rays at Heron Island were held adult males and females are so different from each In a 4.5 x 4.5 m pool for 1 to 5 wk prior to the removal other, species descriptions are based on males. About of gnathiids. Rays from hloreton Bay were collected one fourth of the 155 gnathiid species described world- with a commercial twin-otter board trawl. Lengths of wide are from Australia (Cohen & Poore 1994 and ref- sharks are measured as total length. The size of rays erences therein). Of these, 5 have been described from was measured along the widest (wings) part of the the Great Barrier Reef. Despite the richness of gnathiid body. These measurement methods and the one above specles in Australia, 1ittl.e is known of their ecology, were chosen because they best estimated the relative particularly of the parasi.tic stages. sizes of the hosts. Although ~nformation on what fish species are Gnathiid removal. To remove gnathiids, larger fish cleaned by Labroides dimidiatus is available (Grutter (>60 mm) (except those collected at Heron Island in & Poulin 1998),it is not known from which fish species March 1996, see below) were soaked in the anaes- these cleaners obtain gnathiids. On the Great Barrier thetic chloretone for 30 to 60 min and all Liquids were Reef, few fish species have been examined for gnathi- filtered at 57 pm (except for some species collected ids (7 species in Grutter 1994, and 2 recorded in Lester prior to June 1996 for which a 57 pm or a 200 pm filter h Sewell 1989).Elsewhere they have been found on a was used; see Grutter 1994 for species and filters wide variety of fish, ranging from large ela.smobranchs used). Th.ese methods were modified for some of the In Japan (Honma et al. 1991) to small blennies in Eng- species due to high mucus loads (Scaridae: the whole land (Davies 1981). fish and gills were scanned using a dissecting micro- There is evidence that gnathiid abundance is corre- scope) or difficulties In removing all parasites from gills lated with host size within the labrid species Hemi- (Hemigymnus melapterus: gills were removed and gymnus melapterus (Grutter 1996a) and among 6 other examined separately) (see Grutter 1994, 199513 for fish species (Grutter 1994). Larger fish with more para- modifications). Relatively small fish species (<60 mm) sites are cleaned more often and longer (Grutter were fixed whole and scanned under a microscope for 1995a). Understanding the relationship between host parasites following Grutter (1996b). Parasites and size and gnathiid abundance may explain variation in small fish were fixed in 5 % Formalin in seawater. gnathi1.d abundance among fish and provide insight To reduce processing time when removing gnathlids into the role of gnathiids in cleaning behavior. This from fish, gnathiid removal without an anaesthetic study quantified the abundance of gnathiids on a wide bath was tested. Fish collected in March 1996 were range of fish species collected at Lizard Island, Heron rinsed and all fins and gills scraped with the tip of a Island, and Moreton Bay, Australia, and examined the squirt bottle. All liquids were filtered at 57 pm. A sub- relationship between gnathiid abundance and host set of fish (38 individuals from 19 species) was exam- size both within and among species. ined under a microscope after the rinse to determine if any gnathiids remained. Only 1 gnathiid was found remaining compared to 31 gnathiids removed, indicat- MATERIALS AND METHODS ing a 3 % loss. To remove gnathiids from elasmobranchs, flsh tvere Fish collection. Fish were collected from shallow pithed and their gills exclsed and examined for gnathi- reefs (2 to 7 m) at Lizard Island (14" 40' S, 145" 26' E) in ids with a stereo microscope. The buccal and gill cavi- October 1991, June and August 1992, January 1993 ties and surface of the fish were also examined. and October 1994, at Heron Island (23"27'S, Gnathiids were gently pulled off using forceps. 151°55'E) in June 1993, March and April 1996, and Gnathiid abundances greater than 50 are likely mini- July and August 1996, and at Moreton Bay (Brisbane, mum estimates as gnathiids tvere observed in the bot- Queensland) in May and June 1996. Teleost fish were tom of the pool in which the elasmobranchs were held collected by herding one flsh at a time into a net and indicating that some gnathiids had left their hosts. capturing it with a handnet following Grutter (1994, Statistical analysis. The relationship between 1995b). Fish were sealed in plastic bags to avold gnathiid abundance and host size was assessed both gnathiid loss during handling and transport. Fish spe- within and among flsh species. For the withln-species cies were selected based on their ease of collection and analyses, data on fishes of the 6 most common species availability and from as wide a range of families as collected at all times were used (Acanthochromispoly- possible and are therefore not a random sample. Stan- acanthus was omitted because it was rarely infected). dard length was used as the measure of teleost host To determine whether or not to pool data from both size. locations, the effect of location on abundance was Grutter & Poulin: Host slze an1cl abundance of parasitic isopods 265 tested using analysis of covariance (ANCOVA) with (1994). Relationships among contrasts were assessed fish standard length as the covariable. Additional spec- using correlations and regressions forced through the imens of Hemigymnus rnelapterus (n = 7) collected origin (see Garland et al. 1992 for details and justifica- from similar sites at Lizard Island were included in the tion). Estimates of gnathiid abundance corrected for analyses to increase the sample size but were not sample size were obtained by using the residuals of a included in other analyses due to their small sample regression of contrasts in gnathiid abundance on con- size at each collection time Simple linear correlation trasts in sample size. coefficients between host size and gnathiid abundance The comparative analyses described above were were computed within each species. Uninfected and repeated after the exclusion of fish species on which no infected fish were included in correlation analyses and gnathiids were found. These may be either true cases when calculating mean abundances per species.