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.

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.

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.

Sediment yield and impacts from river catchments to the Great Barrier Reef lagoon

Land use intensification is estimated to result in an overall increase in sediment delivery to the Great Barrier Reef lagoon by a factor of approximately four. Modelling suggests that, following land use intensification, croplands cause the greatest increase of sediment yield and sediment concentration, whereas erosion of grazing land is the main contemporary source of sediments, primarily owing to the large spatial extent of this land use. The spatial pattern of sediment yield to the coast after land use intensification is strongly correlated with the pattern under natural conditions, although the greatest increase is estimated to have occurred in the wet-dry catchments. Sediment transport and resuspension processes have led to the development of a strongly sediment-partitioned shelf, with modern mud-rich sediments almost exclusively restricted to the inner and inner-middle shelf, northward-facing embayments and in the lee of headlands. Elevated sediment concentrations increase the potential transport rates of nutrients and other pollutants. Whether increased sediment supply to the coastal zone has impacted on reefs remains a point of contention. More sediment load data need to be collected and analysed in order to make detailed estimates of catchment yields and establish the possible sediment impact on the Great Barrier Reef.

Further observations on the Enenteridae Yamaguti, 1958 (Digenea, Lepocreadioidea) of the Indo-West Pacific region, including a new species from Western Australia

Measurements are given for all and full descriptions and illustrations for some of the following enenterid species: Enenterum aureum Linton, 1910 in Kyphosus bigibbus and K. sydneyanus? from Ningaloo Coral Reef, Western Australia, K. vaigiensis from off Heron Island, Queensland and K. vaigiensis from off Moorea, French Polynesia; E. mannarense Hafeezullah, 1980 in K. bigibbus and K. sydneyanus? from Ningaloo Coral Reef; E. elongatum Yamaguti, 1970 in K. vaigiensis from Heron Island, Queensland and K. bigibbus and K. sydneyanus? from Ningaloo Coral Reef; Koseiria alanwilliamsi sp. nov. in Kyphosus cornelii from off Kalbarri, Western Australia; Koseiria xishaense Gu et Shen, 1983 in K. vaigiensis from off Heron Island and K. bigibbus from off Palau, Micronesia; Proenenterum isocotylum Manter, 1954 in Aplodactylus arctidens from off Stanley, Tasmania; R ericotylum Manter, 1954 in A. arctidens from off Stanley; Cadenatella isuzumi Machida, 1993 from Kyphosus bigibbus and K. sydneyanus? from Ningaloo Coral Reef; Cadenatella pacifica (Yamaguti, 1970) from Kyphosus bigibbus from Ningaloo Coral Reef. Two recent cladistic studies of the Enenteridae are discussed and a further analysis has shown that Enenterum and Cadenatella are monophyletic, whilst Koseiria appears polyphyletic. The zoogeography and host-specificity of Kyphosus-inhabiting enenterids is discussed.

The influence of increased line-fishing mortality on the sex ratio and age of sex reversal of the venus tusk fish

The age of sex reversal of the venus tusk fish Choerodon venustus, caught by line fishing at various locations on the southern Great Barrier Reef, indicated that C. venustus is capable of modifying its life cycle in response to increased mortality. The evidence suggests Masthead Reef fish, which experience the highest mortality, underwent sex reversal at a smaller size and younger age than at the other sites. The largest female fish, sexually transitional fish and males were smaller at Masthead Reef than at the Swains Reefs or One Tree Reef at Masthead Reef. There was also considerable overlap in the size of males and females within the exploited populations indicating that sex reversal is not initiated at a particular length but may have a social cause. The sex ratio of fish was essentially the same for fish fully susceptible to line fishing in the Swains and Masthead samples. Circumstantial evidence suggested that the absence of large males in a population may initiate sex reversal, indicating the maintenance of a constant sex ratio may have a social basis. (C) 2002 The Fisheries Society of the British Isles.

Testing the applicability of molecular genetic markers to population analyses of scleratinian corals

The abundance of coral reefs worldwide is in decline, and despite the ecological importance of reefs, only a limited number of DNA markers have been identified for scleractinian coral genetic studies. This paper addresses the search for new coral molecular markers and investigates the applicability of the cytochrome c oxidase subunit I (COI), the internal transcribed spacer region 1 (ITS1), and the pocilloporin gene to the question of intraspecific variation in the scleractinian coral Pocillopora verrucosa along the southeast African coastline. The COI fragment was 710 bp long and was identical for P. verrucosa (n = 10) and P. damicornis (n = 3). Only two different ITS1 sequences were found (differing by 13 bp insertion), but more importantly, 24% of the sequences were heterogenous indicating that different multiple copies of the sequence exist. Pocilloporin is an intronless gene that was absolutely conserved throughout all P. verrucosa populations (n = 50). Thus, the three DNA regions studied appear unsuitable for the population genetic analyses of P. verrucosa.

DMSP in corals and benthic algae from the Great Barrier Reef

In this study the first measurements of DMSP in six species of corals and ten species of benthic algae collected from four coral reefs in the Great Barrier Reef are reported, together with DMSP measurements made on cultured zooxanthellae. Concentrations ranged from 21 to 3831 (mean=743) fmol DMSP zooxanthellae(-1) in corals, 0.16 to 2.96 nmol DMSP cm(-2) (mean=90) for benthic macroalgae, and 48-285 fmol DMSP zooxanthellae(-1) (mean=153) for cultured zooxanthellae. The highest concentrations of DMSP in corals occurred in Acropora formosa (mean= 371 fmol DMSP zooxanthellae(-1)) and Acropora palifera (mean=3341 fmol DMSP zooxanthellae(-1)) with concentrations in A. palifera the highest DMSP concentrations reported in corals examined to date. As well as inter-specific differences in DMSP, intra-specific variation was also observed. Adjacent colonies of A. formosa that are known to have different thermal bleaching thresholds and morphologically distinct zooxanthellae, were also observed to have different DMSP concentrations, with the zooxanthellae in the colony that bleached containing DMSP at an average concentration of 436 finol zooxanthellae(-1), whilst the non-bleaching colony contained DMSP at an average concentration of 171 finol zooxanthellae(-1). The results of the present study have been used to calculate the area normalized DMSP concentrations in benthic algae (mean=0.015 mmol m(-2)) and corals (mean=2.22 mmol m(-2)) from the GBR. This data indicates that benthic algae and corals are a significant reservoir of DMSP in GBR waters. (C) 2002 Published by Elsevier Science Ltd.

Ecological criteria for evaluating candidate sites for marine reserves

Several schemes have been developed to help select the locations of marine reserves. All of them combine social, economic, and biological criteria, and few offer any guidance as to how to prioritize among the criteria identified. This can imply that the relative weights given to different criteria are unimportant. Where two sites are of equal value ecologically; then socioeconomic criteria should dominate the choice of which should be protected. However, in many cases, socioeconomic criteria are given equal or greater weight than ecological considerations in the choice of sites. This can lead to selection of reserves with little biological value that fail to meet many of the desired objectives. To avoid such a possibility, we develop a series of criteria that allow preliminary evaluation of candidate sites according to their relative biological values in advance of the application of socioeconomic criteria. We include criteria that,. while not strictly biological, have a strong influence on the species present or ecological processes. Out scheme enables sites to be assessed according to their biodiversity, the processes which underpin that diversity, and the processes that support fisheries and provide a spectrum of other services important to people. Criteria that capture biodiversity values include biogeographic representation, habitat representation and heterogeneity, and presence of species or populations of special interest (e.g., threatened species). Criteria that capture sustainability of biodiversity and fishery values include the size of reserves necessary to protect viable habitats, presence of exploitable species, vulnerable life stages, connectivity among reserves, links among ecosystems, and provision of ecosystem services to people. Criteria measuring human and natural threats enable candidate sites to be eliminated from consideration if risks are too great, but also help prioritize among sites where threats can be mitigated by protection. While our criteria can be applied to the design of reserve networks, they also enable choice of single reserves to be made in the context of the attributes of existing protected areas. The overall goal of our scheme is to promote the development of reserve networks that will maintain biodiversity and ecosystem functioning at large scales. The values of eco-system goods and services for people ultimately depend on meeting this objective.

Oceanic interchange and nonequilibrium population structure in the estuarine dependent Indo-Pacific tasselfish, Polynemus sheridani

We assayed mtDNA haplotype [300 base pairs (bp) control region] geography and genealogy in the Indo-Pacific tasselfish, Polynemus sheridani from its contiguous estuarine distribution across northern Australia (n = 169). Eight estuaries were sampled from three oceanographic regions (Timor Sea, Gulf of Carpentaria and the Coral Sea) to assess the impact of Pleistocene sea level changes on the historical connectivity among P. sheridani populations. Specifically, we investigated the genetic consequences of disruption to Indian-Pacific Ocean connectivity brought about by the closure of the Torres Strait. Overall there was significant population subdivision among estuaries (F-ST = 0.161, (Phi(ST) = 0.187). Despite a linear distribution, P. sheridani did not show isolation by distance over the entire sampled range because of genetic similarity of estuaries greater than 3000 km apart. However, significant isolation by distance was detected between estuaries separated by less than 3000 km of coastline. Unlike many genetic studies of Indo-Pacific marine species, there was no evidence for an historical division between eastern and western populations. Instead, phylogeographical patterns were dominated by a starlike intraspecific phylogeny coupled with evidence for population expansion in both the Gulf of Carpentaria and the Coral Sea but not the Timor Sea. This was interpreted as evidence for recent west to east recolonization across of northern Australia following the last postglacial marine advance. We argue that although sufficient time has elapsed postcolonization for populations to approach gene flow-drift equilibrium over smaller spatial scales (< 3000 km), the signal of historical colonization persists to obscure the expected equilibrium pattern of isolation by distance over large spatial scales (> 3000 km).

Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia

In response to recent reports of contamination of the nearshore marine environment along the Queensland coast by herbicides (including areas inside the Great Barrier Reef Marine Park), an ecotoxicological assessment was conducted of the impact of the herbicides diuron and atrazine on scleractinian corals. Pulse-amplitude modulated (PAM) chlorophyll fluorescence techniques were used to assess the herbicide effects on the symbiotic dinoflagellates within the tissues (in hospite) of 4 species of coral (Acropora formosa, Montipora digitata, Porites cylindrica, Seriatopora hystrix) in static toxicity tests, and in freshly isolated symbiotic dinoflagellates from Stylophora pistillata. Using change in the effective quantum yield (DeltaF/F-m') as an effect criterion, diuron (no observable effect concentration, NOEC = 0.3 mug 1(-1); lowest observable effect concentration, LOEC = 1 mug 1(-1); median effective concentration, EC50 4 to 6 mug 1(-1)) was found to be more toxic than atrazine (NOEC = 1 mug 1(-1), LOEC = 3 mug 1(-1), EC50 40 to 90 mug 1(-1)) in short-term (10 h) toxicity tests. In the tests with isolated algae, significant reductions in DeltaF/F-m' were recorded as low as 0.25 mug 1(-1) diuron (LOEC, EC50 = 5 mug 1(-1)). Time-course experiments indicated that the effects of diuron were rapid and reversible. At 10 mug 1(-1) diuron, DeltaF/F-m' was reduced by 25% in 20 to 30 min, and by 50% in 60 to 90 min. Recovery of DeltaF/F-m' in corals exposed to 10 mug 1(-1) diuron and then transferred to running seawater was slower, returning to within 10% of control values inside 1 to 7 h. The effect of a reduction in salinity (35 to 27%) on diuron toxicity (at 1 and 3 mug 1(-1) diuron) was tested to examine the potential consequences of contaminated coastal flood plumes inundating inshore reefs. DeltaF/F-m' was reduced in the diuron-exposed corals, but there was no significant interaction between diuron and reduced salinity seawater within the 10 h duration of the test. Exposure to higher (100 and 1000 mug 1(-1)) diuron concentrations for 96 h caused a reduction in DeltaF/F-m' the ratio variable to maximal fluorescence (F,1F.), significant loss of symbiotic dinoflagellates and pronounced tissue retraction, causing the corals to pale or bleach. The significance of the results in relation to diuron contamination of the coastal marine environment from terrestrial sources (mainly agricultural) and marine sources (antifouling paints) are discussed.