Cleaner fish, Labroides dimidiatus, diet preferences for different types of mucus and parasitic gnathiid isopods

Cleaner fish, Labroides dimidiatus, prefer the mucus of the parrotfish, Chlorurus sordidus, to parasitic gnathiid isopods, the main items in their diet, indicating a major conflict between clients and cleaners over what the latter should eat during interactions. We tested whether the conflict varied with client species (and the quality of its mucus) and with the presence of blood in the gnathfids. First, we offered cleaners the choice between mucus of the parrotfish and that of the snapper, Lutjanus fulviflamma. When offered equal amounts of mucus on Plexiglas plates, cleaners readily developed a significant preference for the parrotfish mucus. Reducing the amount of parrotfish mucus by 75% made the preference disappear. In a second test, we offered the cleaners gnathiids that were or were not engorged with client fish blood. Cleaners showed no significant preference for either food item. Our results suggest that the degree of conflict between cleaners and clients may vary between species, depending on whether the latter have a preferred mucus. In contrast, the cleaners' lack of preference for engorged gnathiids benefits clients because it means that cleaners do not hesitate to eat unengorged gnathiids before the gnathiids harm the fish by removing blood or by transmitting blood parasites. (C) 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine

Epaulette sharks Hemiscyllium ocellatum were surveyed on Heron Island, Great Barrier Reef, Australia for gnathiid isopods and protozoan (haemogregarine) parasites to determine the prevalence and intensity of infection and to investigate the potential role of gnathiids as vectors of these haemogregarines, the first such study carried out on elasmobranchs. Juvenile gnathiids were collected and quantified using a novel non-invasive and chemical-free technique and gnathiid squashes were examined for haemogregarine developmental stages. The feeding and reproductive ecology of the Gnathia spp. was investigated to better understand the relationship between gnathiids and haemogregarines. Gnathiids were found on all sharks and intensities ranged between two and 66. Only third-stage gnathiid juveniles were found, which fell into two size groups (A and B). These juveniles remained attached to H. ocellatum for up to 17 days, the longest period of attachment yet recorded for gnathiids. Group A female gnathiids produced broods of 45-187 (median = 120) first stage juveniles from between 54 and 82 days (median = 63 days) after detachment. First stage juveniles survived for an average of 15.8 +/- 0.1 (SEM) days without feeding. The prevalence (6.7%) and parasitaemia (usually

Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods

Variation in the rate at which parasitic gnathiid isopod juveniles emerged from the benthos at Lizard Island, Great Barrier Reef, Australia, was examined (I) every 4 or 8 h throughout the day and night over a 24 h period, (2) over a 12 h period during the day or night, and (3) during different lunar phases (weeks). The number of gnathiids sampled per 4 or 8 h was low, with only 30% of the traps containing gnathiids and the abundance ranging from 0 to 3 gnathiids m(-2). The number of gnathiids that emerged over 12 h, in contrast, ranged from 0 to 36 m(-2). During the third and fifth weeks sampled, more gnathiids emerged during the day than at night. This coincided with the full moon and new moon. Most gnathiids that emerged from the reef during the day (98 %) had not fed, in contrast to those sampled at night (71%). Of the gnathiids with no engorged gut, most (97 %) of those collected during the day were small (II. mm) compared to those collected at night (19%), the latter being mostly >1 mm. Of the gnathiids with an engorged gut, most were sampled at night (83 %) and 97 % were >1 mm in size. These percentages suggest differences in the emergence behaviour among Life stages or species of gnathiids. This study, which shows that gnathiids do emerge during the day and supports other studies showing that gnathiids also attack fishes during the day, has important implications for understanding the role of cleaner fish and their main food source, gnathiids, as it shows there is a constant source of gnathiids emerging from the reef during the day and night in search of hosts.

Cleaning symbioses from the parasites' perspective

Cleaning behaviour has generally been viewed from the cleaner or client's point of view. Few studies, however, have examined cleaning behaviour from the parasites' perspective, yet they are the equally-important third players in such associations. All three players are likely to have had their evolution affected by the association. As cleaner organisms are important predators of parasites, cleaners are likely to have an important effect on their prey. Little, however, is known of how parasites are affected by cleaning associations and the strategies that parasites use in response to cleaners. I examine here what parasites are involved in cleaning interactions, the effect cleaners have on parasites, the potential counter-adaptations that parasites have evolved against the predatory activities of cleaner organisms, the potential influence of cleaners on the life history traits of parasites, and other factors affected by cleaners. I have found that a wide range of ectoparasites from diverse habitats have been reported to interact with a wide range of cleaner organisms. Some of the life history traits of parasites are consistent with the idea that they are in response to cleaner predation. It is clear, however, that although many cleaning systems exist their ecological role is largely unexplored. This has likely been hindered by our lack of information on the parasites involved in cleaning interactions.

Optimising cleaning behaviour: minimising the costs and maximising ectoparasite removal

Little is known of how client fish minimise the costs of cleaning behaviour while maximising ectoparasite removal by cleaner fish. Previous studies have found that abundance on fish and infestation behaviour of gnathiid isopods, the main parasite eaten by cleaner fish, varies diurnally. We examined whether reduced foraging is a cost of cleaning behaviour in clients and whether the behaviour of the client fish, the thick-lipped wrasse Hemigymnus melapterus, towards the cleaner fish Labroides dimidiatus varied diurnally to maximise ectoparasite removal, possibly in response to the diurnal changes in the abundance and infestation patterns of gnathiids. We found that during the midday and afternoon, client foraging rates were negatively related to the duration and frequency of inspections, suggesting that cleaning may, at some times of the day, be energetically costly to the client in terms of reduced foraging opportunities. Surprisingly, we found that the duration and frequency of inspections of clients by cleaners did not vary among diel time periods. A model of gnathiid dynamics on individual fish is proposed. It shows that the observed diurnal pattern in gnathiid abundance on fish can be generated with the constant duration and frequency of inspections that was observed in this study. Thus clients would not have more gnathiids removed by modifying their cleaning behaviour.

Skin toxins and external parasitism of coral-dwelling gobies

Toxic (Gobiodon spp.) and non-toxic (Paragobiodon xanthosomus) gobies became infected with external parasites (gnathiid isopods) at equal rates in a laboratory experiment. Parasites were evenly distributed over the body of P. xanthosomus but were mostly confined to the fins of Gobiodon spp., where toxin glands are less abundant. Skin toxins were not associated with the rate of infection but their distribution did appear to influence the site of parasite attachment. (C) 2003 The Fisheries Society of the British Isles.

Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions

Recent studies on cleaning behaviour suggest that there are conflicts between cleaners and their clients over what cleaners eat. The diet of cleaners usually contains ectoparasites and some client tissue. It is unclear, however, whether cleaners prefer client tissue over ectoparasites or whether they include client tissue in their diet only when searching for parasites alone is not profitable. To distinguish between these two hypotheses, we trained cleaner fish Labroides dimidiatus to feed from plates and offered them client mucus from the parrotfish Chlorurus sordidus, parasitic monogenean flat-worms, parasitic gnathiid isopods and boiled flour glue as a control. We found that cleaners ate more mucus and monogeneans than gnathiids, with gnathiids eaten slightly more often than the control substance. Because gnathiids are the most abundant ectoparasites, our results suggest a potential for conflict between cleaners and clients over what the cleaner should eat, and support studies emphasizing the importance of partner control in keeping cleaning interactions mutualistic.

Infracommunity structure of parasites of Hemigymnus melapterus (Pisces : Labridae) from Lizard Island, Australia: The importance of habitat and parasite body size

This Study describes the community of all metazoan parasites from 14 individuals of thicklip wrasse, Hemigymnus melapterus, from Lizard Island, Australia. All fish were parasitized, and 4,649 parasite individuals were found. Twenty-six parasite species were identified although only 6 species were abundant and prevalent: gnathiid isopods, the copepod Hatschekia hemigymni, the digenean Callohelmis pichelinae, and 3 morphotypes of tetraphyllidean cestode larvae. We analyzed whether the body size and microhabitat of the parasites and size of the host affected understanding of the structure of the parasite community. We related the abundance, biovolume, and density of parasites with the host body size and analyzed the abundances and volumetric densities of some parasite species within microhabitats. Although the 2 most abundant species comprised 75% of all parasite individuals, 4 species, each in similar proportion, comprised 85% of the total biovolume. Although larger host individuals had higher richness, abundance, and biovolume of parasites than smaller individuals, overall parasite volumetric density actually decreased with the host body size. Moreover. parasites exhibited abundances and densities significantly different among microhabitats; some parasite species depended on the area available, whereas others selected a specific microhabitat. Parasite and habitat size exhibited interesting relationships that should be considered more frequently. Considerations of these parameters improve understanding of parasite community structure and how the parasites use their habitats.

Hematozoa of teleosts from Lizard Island, Australia with some comments on their possible mode of transmission and the description of a new hemogregarine species

Little is known of the blood parasites of coral reef fishes and nothing of how they are transmitted. We examined 497 fishes from 22 families, 47 genera, and 78 species captured at Lizard Island, Australia, between May 1997 and April 2003 for hematozoa and ectoparasites. We also investigated whether gnathiid isopods might serve as potential vectors of fish hemogregarines. Fifty-eight of 124 fishes caught in March 2002 had larval gnathiid isopods, up to 80 per host fish, and these were identified experimentally to be of 2 types, Gnathia sp. A and Gnathia sp. B. Caligid copepods were also recorded but no leeches. Hematozoa, found in 68 teleosts, were broadly hemogregarines of 4 types and an infection resembling Haemohormidium. Mixed infections (hemogregarine with Haemohormidium) were also observed, but no trypanosomes were detected in blood films. The hemogregarines were identified as Haemogregarina balistapi n. sp., Haemogregarina tetraodontis, possibly Haemogregarina bigemina, and an intraleukocytic hemogregarine of uncertain status. Laboratory-reared Gnathia sp. A larvae, fed experimentally on bruslitail tangs, the latter heavily infected with the H. bigemina-like hemogregarine, contained hemogregarine gamonts and possibly young oocysts up to 3 days postfeeding, but no firm evidence that gnathiids transmit hemogregarines at Lizard Island was obtained.

Cleaner fish Labroides dimidiatus reduce 'temporary" parasitic corallanid isopods on the coral reef fish Hemigymnus melapterus

To determine if cleaners affect 'temporary' parasitic corallanid isopods (Argathona macronema) on fish, we used caged fish Hemigymnus meldpterus (Labridae) on 5 patch reefs on Lizard Island, Great Barrier Reef, and removed all cleaner fish Labroides dimidiatus (Labridae) from 3 of the reefs, In a short-term experiment, fish were sampled after 12 or 24 h, at dawn and sunset respectively, and in a long-term experiment they were sampled after 12 d at sunset. Isopod prevalence, abundance and size were measured. In the short-term experiment, on reefs without cleaners the prevalence of A. macronema was higher after 24 h than after 12 h while on reefs with cleaners, prevalence was low at all times, Although the abundance of A, macronema did not vary after 12 and 24 h, when combined over the 24 h, the effect of cleaners was significant with only 2 % of all the A. macronema found on reefs with cleaners. Cleaners had no effect on the size frequency distribution of A. macronema in the short-term experiment, most likely because fish had so few isopods on reef with cleaners. In the longer-term experiment, the effects of cleaners on isopod prevalence and abundance were less clear. Their effect on isopod size was, however, significant with smaller parasites on reefs without cleaners. The reduction of isopod prevalence and abundance by cleaner fish over a period of hours may explain why these A, macronema are rare on wild fish. Our findings support the idea that cleaning is beneficial to clients and has important implications for the control of parasites of fish farmed in cages,

Diversity and population characteristics of terrestrial isopods (Crustacea, Oniscidea) across three forest environments in southern Brazil

Terrestrial isopods are important and dominant component of meso and macrodecomposer soil communities. The present study investigates the diversity and species composition of terrestrial isopods on three forests on the Serra Geral of the state of Rio Grande do Sul, Brazil. The area has two natural formations (Primary Woodland and Secondary Woodland) and one plantation of introduced Pinus. The pitfall traps operated from March 2001 to May 2002, with two summer periods and one winter. There were 14 sampling dates overall. Of the five species found: Alboscia silveirensis Araujo, 1999, Atlantoscia floridana (van Name, 1940), Benthana araucariana Araujo & Lopes, 2003 (Philoscidae), Balloniscus glaber Araujo & Zardo, 1995 (Balloniscidae) and Styloniscus otakensis (Chilton, 1901) (Styloniscidae); only A. floridana is abundant on all environments and B. glaber is nearly exclusive for the native forests. The obtained data made it possible to infer about population characteristics of this species. The Similarity Analysis showed a quantitative difference among the Secondary forest and Pinus plantation, but not a qualitative one. The operational sex ratio (OSR) analysis for A. floridana does not reveal significant differences in male and female proportions among environments. The reproductive period identified in the present study for A. floridana was from spring to autumn in the primary forest and Pinus plantation and during all year for the secondary forest. The OSR analysis for B. glaber reveals no significant differences in abundance between males and females for secondary forest, but the primary forest was a significant difference. The reproductive period for B. glaber extended from summer to autumn (for primary and secondary forest). This is the first record for Brazil of an established terrestrial isopod population in a Pinus sp. plantation area, evidenced by the presence of young, adults and ovigerous females, balanced sex ratio, expected fecundity and reproduction pattern, as compared to populations from native vegetation areas.

Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef

Captive Hemigymnus melapterus exposed to large numbers of cultured juvenile parasitic isopods (Gnathia sp.) had significantly lower haematocrit (median 27-62% +/- 5-83% inter-quartile range) than uninfected, control fish (median 32-73% +/- 4-90%). This study is the first to show that juvenile Gnathia sp. reduce total blood volume in H. melapterus. The low haematocrit in infected fish was most likely due to plasma replacing erythrocytes lost as a result of isopods feeding on fish blood. (c) 2005 The Fisheries Society of the British Isles.

TABLE 2. - Number of Asellota isopods collected in the Beagle Channel

The shallow-water Asellota from the Beagle Channel were investigated, based on material collected at four localities in 2001-2002. A total of 3,124 asellotes were sorted, and three new species and 12 new records of distribution were reported. The Paramunnidae showed the highest species diversity and abundance (11 species and 1,463 specimens). The present research raises the number of species known from the Beagle Channel to 23; of these, 16 were previously reported from the Magellan Straits, representing 69% of similarity. Based on the present results and published data, the faunistic affinities for the shallow-water Asellota was 30% between the Magellan region and the Scotia Arc, and 26% between the Magellan region and the Antarctic Peninsula.