Sushi, fish and parasites

Farming yellowtail in Japan is big business and cultivation of the closely related kingfish in South Australia is rapidly emerging as a local industry. But when it comes to parasites, farming the sea is no different from farming on land. Parasites can affect productivity, and solving parasite problems is important in this rapidly growing industry.

Experimental susceptibility of some reef fish species to Benedenia lutjani (Monogenea : Capsalidae), a parasite of Lutjanus carponotatus (Pisces : Lutjanidae)

The susceptibility of species of lutjanid, lethrinid and serranid fish to infection by either larval or post-larval (juvenile and adult) specimens of the capsalid monogenean Benedenia lutjani Whittington and Kearn (1993) was examined experimentally. Four species of lutjanids became infected when exposed to larvae of B. lutjani, but three species of lethrinids and four species of serranids were not susceptible to larvae under the same conditions. Variability in the intensity of infection by larvae occurred within and between lutjanid species. Few post-larval specimens of B. lutjani transferred between individuals of the specific host Lutjanus carponotatus (Richardson 1842) in 60-l aquaria and none transferred between specimens of L. carponotatus in a 7,500-l concrete tank. These results indicate that transfer of post-larval B. lutjani between individuals of the specific host is unlikely to occur in the wild. Other lutjanid species did not become infected when exposed to specimens of L. carponotatus infected heavily by post-larval B. lutjani, but two lethrinid species were susceptible to infection under the same conditions. These data indicate that different factors may mediate host-specificity for larval and post-larval B. lutjani.

Stenotherms at sub-zero temperatures: thermal dependence of swimming performance in Antarctic fish

We examined the burst swimming performance of two Antarctic fishes, Trematomus bernacchii and T. centronotus, at five temperatures between -1 degreesC and 10 degreesC. As Antarctic fishes are considered one of the most cold specialised and stenothermal of all ectotherms, we predicted they would possess a narrow thermal performance breadth for burst swimming and a correlative decrease in performance at high temperatures. Burst swimming was assessed by videotaping swimming sequences with a 50-Hz video camera and analysing the sequences frame-by-frame to determine maximum velocity, the distance moved throughout the initial 200 ms, and the time taken to reach maximum velocity. In contrast to our prediction, we found both species possessed a wide thermal performance breadth for burst swimming. Although maximum swimming velocity for both T. bernacchii and T. centronotus was significantly highest at 6 degreesC, maximum velocity at ah other test temperatures was less than 20% lower. Thus, it appears that specialisation to a highly stable and cold environment is not necessarily associated with a narrow thermal performance breadth for burst swimming in Antarctic fish. We also examined the ability of the Antarctic fish Pagothenia borchgrevinki to acclimate their burst-swimming performance to different temperatures. We exposed P, borchgrevinki to either -1 degreesC or 4 degreesC for 4 weeks and tested their burst-swimming performance at four temperatures between -1 degreesC and 10 degreesC. Burst-swimming performance of Pagothenia borchgrevinki was unaffected by exposure to either -1 degreesC or 4 degreesC for 4 weeks. Maximum swimming velocity of both acclimation groups was thermally independent over the total temperature range of -1 degreesC to 10 degreesC. Therefore, the loss of any capacity to restructure the phenotype and an inability to thermally acclimate swimming performance appears to be associated with inhabiting a highly stable thermal environment.

Foraging by the endangered black-breasted button-quail (Turnix melanogaster) within fragmented rainforest of an agricultural landscape

We studied the foraging habitat of the endangered black-breasted button-quail (Turnix melanogaster) in 13 rainforest patches of an agricultural landscape (23.4 km(2)) in eastern Australia to assess its use of fragmented habitats outside conservation reserves. The species foraged only in the three largest patches (17.4, 40.0, 63.8 ha in size), all of which were connected to open eucalypt forest, and in intact rainforest. Occurrence of birds was greatest in the largest patch. The maximum number of individuals within the study area was estimated to be 22. Radio-tracking of nine birds revealed that three were resident in the largest patch for periods of over 100 days; no movements between patches were detected. Three radio-tagged birds were taken by avian and mammalian predators. Our results indicated that the long-term future of the species in agricultural landscapes is bleak and that management action is urgently needed to arrest its decline in these ecosystems, (C) 2001 Elsevier Science Ltd. All rights reserved.

Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish

Cleaning behavior is a popular example of non-kin cooperation. However, quantitative support for this is generally sparse and the alternative, that cleaners are parasitic: has also been proposed. Although the behaviour involves some of the most complex and highly developed interspecific communication signals known, the proximate causal factors for why clients Seek cleaners are controversial. However, this information is essential to understanding the evolution of cleaning. I tested whether clients seek cleaners in response to parasite infection or whether clients seek cleaners for tactile stimulation regardless of parasite load. Parasite loads oil client fish were manipulated and clients exposed to cleaner fish and control fish hehind glass. I found that parasitized client fish spent more time than unparasitized fish next to a cleaner fish. In addition; parasitized clients spent more rime next to cleaners than next to control fish whereas unparasitized fish were not attracted to cleaners. This study shows, I believe for the first time, which is somewhat surprising, that parasite infection alone causes clients to seek cleaning by cleaners and provides insight into how this behaviour evolved.

Turning up the heat on subzero fish: thermal dependence of sustained swimming in an Antarctic notothenioid

We determined the maximum sustained swimming speed (U-crit), and resting and maximum ventilation rates of the Antarctic fish Pagothenia borchgrevinki at five temperatures between -1degreesC and 8degreesC. We also determined resting metabolic rate (VO2) at -1degreesC, 2degreesC, and 4degreesC. U-crit of P. borchgrevinki was highest at -1degreesC (2.7+/-0.1 BL s(-1)) and rapidly decreased with temperature, representing a thermal performance breadth of only 5degreesC. This narrow thermal performance supports our prediction that specialisation to the subzero Antarctic marine environment is associated with a physiological trade-off in performance at high temperatures. Resting oxygen consumption and ventilation rate increased by more than 200% across the temperature range, which most likely contribute to the decrease in aerobic swimming capabilities at higher temperatures. (C) 2002 Published by Elsevier Science Ltd.

Asymmetric cheating opportunities and partner control in a cleaner fish mutualism

How can cooperation persist if, for one partner, cheating is more profitable than cooperation in each round, while the other partner has no option to cheat? Our laboratory experiments suggest that such a situation exists between the cleaner fish Labroides dimidiatus and its nonpredatory client reef fish species, which actively seek cleaners to have their ectoparasites removed. Clients Ctenochaetus striatus regularly jolted in response to cleaner mouth contact, and these jolts were not linked to the removal of parasites. In addition, cleaners did not search for parasites but fed on mucus when exposed to anaesthetized clients, which could not control the cleaners' behaviour. Field data showed that clients often terminated an interaction immediately after a jolt. Client species with access to only one cleaning station, owing to their small territories or home ranges, terminated interactions mainly by chasing cleaners while clients with access to two or more cleaning stations mainly swam away. Thus, the chasing of cleaners appeared to be a form of punishment, imposing costs on the cleaner at the client's (momentary) expense. Chasing yields future benefits, as jolts were on average less frequent during interactions between cleaners and individuals that had terminated their previous interaction by aggressive chasing. 2002 The Association for the Study of Animal Behaviour.

Cleaner fish Labroides dimidiatus recognise familiar clients

Individual recognition has been attributed a crucial role in the evolution of complex social systems such as helping behaviour and cooperation. A classical example for interspecific cooperation is the mutualism between the cleaner fish Labroides dimidiatus and its client reef fish species. For stable cooperation to evolve, it is generally assumed that partners interact repeatedly and remember each other's past behaviour. Repeated interactions may be achieved by site fidelity or individual recognition. However, as some cleaner fish have more than 2,300 interactions per day with various individuals per species and various species of clients, basic assumptions of cooperation theory might be violated in this mutualism. We tested the cleaner L. dimidiatus and its herbivorous client, the surgeon fish Ctenochaetus striatus, for their ability to distinguish between a familiar and an unfamiliar partner in a choice experiment. Under natural conditions, cleaners and clients have to build up their relationship, which is probably costly for both. We therefore predicted that both clients and cleaners should prefer the familiar partner in our choice experiment. We found that cleaners spent significantly more time near the familiar than the unfamiliar clients in the first 2 minutes of the experiment. This indicates the ability for individual recognition in cleaners. In contrast, the client C. striatus showed no significant preference. This could be due to a sampling artefact, possibly due to a lack of sufficient motivation. Alternatively, clients may not need to recognise their cleaners but instead remember the defined territories of L. dimidiatus to achieve repeated interactions with the same individual.

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,

Experimental evidence that partner choice is a driving force in the payoff distribution among cooperators or mutualists: the cleaner fish case

Supply and demand largely determine the price of goods on human markets. It has been proposed that in animals, similar forces influence the payoff distribution between trading partners in Sexual selection, intraspecific cooperation and interspecific mutualism. Here we present the first experimental evidence supporting biological market theory in it study on cleaner fish, Labroides dimidiatus. Cleaners interact with two classes of clients: choosy client species with access to several cleaners usually do not queue for service and do not return if ignored, while resident client species with access to only one cleaning station do queue or return. We used plexiglas plates with equal amounts of food to stimulate these behaviours of the two client classes. Cleaners soon inspected 'choosy' plates before 'resident' plates. This supports previous field observations that suggest that client species with access to several cleaners exert choice to receive better(immediate) service.

Geographic variation in the behaviour of the cleaner fish Labroides dimidiatus (Labridae)

Geographical variation in the outcome of interspecific interactions has a range of proximate ecological causes. For instance, cleaning interactions between coral reef fishes can result in benefits for both the cleaner and its clients. However, because both parties can cheat and because the rewards of cheating may depend on the local abundance of ectoparasites on clients, the interaction might range from exploitative to mutualistic. In a comparative analysis of behavioural measures of the association between the cleaner fish Labroides dimidiatus and all its client species, we compared cleaning interactions between two sites on the Great Barrier Reef that differ with respect to mean ectoparasite abundance. At Heron Island, where client fish consistently harbour fewer ectoparasites, client species that tended to pose for cleaners were more likely to receive feeding bites by cleaners than client species that did not pose for cleaners. This was not the case at Lizard Island, where ectoparasites are significantly more abundant. Client fish generally spent more time posing for cleaners at Lizard Island than their conspecifics at Heron Island. However, fish at Heron Island were inspected longer on average by cleaners than conspecifics at Lizard Island, and they incurred more bites and swipes at their sides per unit time from cleaners. These and other differences between the two sites suggest that the local availability of ectoparasites as a food source for cleaners may determine whether clients will seek cleaning, and whether cleaners will feed on parasites or attempt to feed on client mucus. The results suggest that cleaning symbiosis is a mosaic of different outcomes driven by geographical differences in the benefits for both participants.

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.

The effect of the cleaner fish Labroides dimidiatus on the capsalid monogenean Benedenia lolo parasite of the labrid fish Hemigymnus melapterus

The cleaner fish Labroides dimidiatus affected the pigmented monogenean parasite Benedenia lolo on the fish Hemigymnus melapterus (Labridae) held in aquaria. The effect of cleaner fish varied with the size class of fish; only small fish [a posteriori size class < 11-5 cm standard length (L-S)] exposed to cleaner fish had fewer monogeneans compared with fish not exposed to cleaner fish. The abundance of monogeneans on large fish (a posteriori size class > 11-5 cut L-S) was not affected by cleaner fish. The size-frequency distributions of monogeneans on both size-classes of H. melapterus were affected by cleaner fish. Fish exposed to cleaner fish had fewer large (> 3 mm) and more small (< 1 mm) monogeneans than fish not exposed to cleaner fish, suggesting cleaner fish selectively removed larger monogeneans. This difference was more pronounced on large fish. In the absence of cleaner fish, small fish had almost as many monogeneans as large fish; they also had more small monogeneans than the large fish, suggesting small fish were more vulnerable to infection by monogeneans than larger fish. This suggests that the cleaner fish L. dimidiatus has the potential to control benedeniine monogeneans on captive fish and highlights the importance of taking into account fish size in studies of the effect of cleaner fish on ectoparasites. (C) 2002 The Fisheries Society of the British Isles. Published by Elsevier Science Ltd. All rights reserved.