Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis

The preferences exhibited by cleaner fishes for particular client species and the high variability in rates at which various clients visit cleaning stations have remained largely unexplained. In this study, we assessed the relative importance of client ectoparasite load and mucus characteristics for the behaviour of cleaning gobies, Elacatinus spp, and their fish clients on a Barbadian fringing reef. Client species with high ectoparasite loads visited cleaning stations more often than less parasitised species. This effect was independent of body size. Frequency of visits to cleaning stations was not related to client mucus characteristics. These results suggest that the main motivation for clients to interact with cleaners is ectoparasite removal. Cleaners did not preferentially clean clients with higher ectoparasite load or better mucus, nor did they spend more time inspecting such clients. The interests of cleaners and clients therefore appear to be inconsistent. This may be due to the generally low rate of ectoparasitism on Barbadian fish compared to fish of other regions. Cleaning gobies fed at a lower rate on client species with higher loads of gnathiid isopod larvae, which may be explained if cleaners switch from eating ectoparasites to other items, such as mucus, on clients with few ectoparasites. Our estimates of caloric and protein content of fish mucus suggest that it may be as valuable a food source per unit weight as ectoparasites. However, no data are available to compare the value of each item per unit feeding time. The fact that clients with few ectoparasites still visit cleaners, albeit at a low rate, suggests that the cost of mucus removal may be low, compared to the benefit of incidental parasite removal. Thus, the outcome of cleaning interactions may remain positive, even in areas characterised by naturally low parasitism on clients.     

Client preferences by Caribbean cleaning gobies: food,safety or something else?

Predation risk is amongst the most pervasive selective pressures influencing behaviour and animals have been repeatedly shown to trade-off foraging success for safety. We examined the nature of this trade-off in cleaning symbioses amongst Caribbean coral reef fishes. We predicted that cleaning gobies (Elacatinus evelynae and Elacatinus prochilos) should prefer fish clients that pose a low risk of predation (e.g. herbivores) over clients that may have more ectoparasites but pose a higher risk (e.g. piscivores). Our field observations revealed that cleaners did clean preferentially client species with more parasites but predatory and non-predatory clients had similar ectoparasite loads. Despite the lack of a foraging advantage for inspecting predators, cleaners did not avoid risky clients. On the contrary, a larger proportion of visiting predators than non-predators was inspected, gobies initiated more interactions with predatory clients, and predators were attended to immediately upon arrival at cleaning stations. This preferential treatment of dangerous clients may allow the rapid identification of cleaners as non-prey item or may be due to the effect of predators on the rest of the cleaners’ clientele, which avoided cleaning stations whilst predators were present. Dealing with potentially risky clients may allow gobies to regain access to their main food source: non-predatory clients.     

Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus

In fish cleaning associations, the net benefits gained by clients and cleaners from cleaning have still not been clearly evaluated. In particular, the role of ectoparasitism and the importance of client mucus characteristics remain unclear for most cleaner fish species. This paper investigates the cleaning behaviour of the Mediterranean cleaner wrasse Symphodus melanocercus, based on observations, cleaner gut contents, client ectoparasites and mucus characteristics. We showed that this fish is a specialised cleaner fish, similar to some other tropical cleaner species. Gnathiid isopod larvae and caligid copepods represented a large proportion of the items preyed on by S. melanocercus. Although their feeding activity was related to their client ectoparasite load, it was also significantly linked to client mucus load, which would indicate that the cleaning behaviour of S. melanocercus is not purely altruistic. Finally, as client visit to cleaning stations is related to their ectoparasitism, we propose that ectoparasite removal is likely to be a benefit for the client fishes of S. melanocercus. Received: 28 July 2000 / Accepted: 8 November 2000     

Parasitism and a shortage of refuges jointly mediate the strength of density dependence in a reef fish

Various predator-prey, host-pathogen, and competitive interactions can combine to cause density dependence in population growth. Despite this possibility, most empirical tests for density-dependent interactions have focused on single mechanisms. Here we tested the hypothesis that two mechanisms of density dependence, parasitism and a shortage of refuges, jointly influence the strength of density-dependent mortality. We used mark-recapture analysis to estimate mortality of the host species, the bridled goby (Coryphopterus glaucofraenum). Sixty-three marked gobies were infected with a copepod gill parasite (Pharodes tortugensis), and 188 were uninfected. We used the spatial scale at which gobies were clustered naturally (approximately 4 m2) as an ecologically relevant neighborhood and measured goby density and the availability of refuges from predators within each goby's neighborhood. Goby survival generally declined with increasing density, and this decline was steeper for gobies with access to few refuges than for gobies in neighborhoods where refuges were common. The negative effects of high density and refuge shortage were also more severe for parasitized gobies than for gobies free of parasites. This parasite has characteristics typical of emerging diseases and appears to have altered the strength of a preexisting density-dependent interaction.     

Cleaning symbiosis in an obligate goby–shrimp association

Shrimps from the genus Alpheidae had never been considered as a cleaner organism. In the present study, we demonstrate for the first time, Alpheus rapax engaging in cleaning symbiosis with its gobiid fish associate Myersina macrostoma. Within 450 min of observation time, 9 instances totalling 546 s of cleaning behaviour were recorded. Cleaning behaviour was always preceded by physical contact between the shrimps and their goby associates. The shrimps initiated all cleaning incidents, but these were always terminated by the gobies. Cleaning sessions were observed to occur mostly in the tail region (60.8 %) and followed by the head region (26.2 %). In one instance, a shrimp was observed to clean the gills of its goby associate. The gobies appear to exert some control as to where they were being cleaned by repositioning themselves during a cleaning session.     

Tracking bioaccumulation in aquatic organisms: A dynamic model integrating life history characteristics and environmental change

We have developed a dynamic model to track the evolution of contaminant concentration in an aquatic organism as a function of season and ontogeny throughout its life cycle. We have focused our analysis on the round goby (Apollonia melanostoma), a globally distributed invasive forage fish. By integrating bioenergetics with a bioaccumulation model, we illustrate how life history characteristics interact to influence contaminant accumulation. We use uncertainty and sensitivity analyses to assess how the model output is affected by uncertainty and variability in model parameters. We then demonstrate the influence of important physiological characteristics on contaminant accumulation with two scenarios. First, we probe the influence of sexual dimorphism by comparing gender-specific accumulation of a standard polychlorinated biphenyl congener, PCB153, in male and female round gobies. We hypothesize that lipid loss in female gobies during spawning season leads to a decrease in the PCB body burden compared to male gobies. Second, we compare PCB accumulation in the round goby and in the mottled sculpin (Cottus bairdi), the native forage fish that the round goby displaced in southern Lake Michigan, to determine whether the invasive species has an intrinsically different bioaccumulation potential than the native one. Our non-intuitive findings from these simulations illustrate how the interaction of growth rate with other life history characteristics lead to unexpected bioaccumulation patterns. The model we present is a flexible tool that integrates complex and dynamic interactions among environmental parameters, thus providing a means to better assess the potential for chemical accumulation in human and wildlife populations, and aiding the development of ecological forecasts.     

The influence of potential reproductive rate and variation in mate quality on male and female choosiness in the sand goby, Pomatoschistus minutus

Recent models of choosiness in mate choice have identified two particularly important factors: the potential reproductive rate (PRR) of the choosing sex relative to that of the chosen sex, and the variation in quality of potential mates. This experimental study tested how these factors affected choosiness in male and female sand gobies, Pomatoschistus minutus. We manipulated relative PRR by means of water temperature, and mate quality by means of body length. The choosing male or female was offered a choice between two mates with either a small or a large difference in body length representing a small or a large variation in mate quality. Choosiness was measured as (1) preference for the larger mate, and (2) as whether or not spawning occurred with the smaller mate, while the larger mate was visible but screened off. We found that females preferred large males, and that their level of choosiness was affected by variation in male quality, but not by their own relative PRR. Males, on the other hand, seemed unselective in all treatments and were in general more likely than females to spawn with their provided partner. This suggests that in the sand goby, variation in male mate quality has a greater influence than relative PRR on facultative changes in female choosiness. However, a general difference in PRR between males and females may be one important factor explaining the observed sex difference in choosiness. Received: 17 April 2000 / Revised: 24 June 2000 / Accepted: 17 July 2000     

Habitat preferences of coral-associated fishes are altered by short-term exposure to elevated CO2

Rising atmospheric carbon dioxide (CO₂) concentrations are causing additional CO₂ to be absorbed by the oceans. Recent studies show that exposure to elevated CO₂ causes olfactory impairment in reef fishes; however, the ecological consequences of this impairment are largely unknown. This study examined the effects of short-term exposure to elevated CO₂ on habitat preferences of coral-dwelling gobies. Adult gobies collected from the reef at Lizard Island (Great Barrier Reef, Australia) were exposed for 4 days to ambient CO₂ (440 μatm) or elevated CO₂ (880 μatm). Habitat preferences were then tested in laboratory and field experiments at ambient conditions. In olfactory preference tests, Paragobiodon xanthosomus displayed a strong preference for odour cues of their sole host coral Seriatopora hystrix; however, this preference was absent in gobies exposed to elevated CO₂. Habitat choice experiments conducted in the field showed that Gobiodon histrio placed on dead coral colonies located preferred live habitat within 24 h; however, gobies exposed to elevated CO₂ associated with both preferred and non-preferred habitats in approximately equal frequency. Preferred habitats are known to confer fitness advantages to coral-dwelling gobies. Consequently, these results suggest that future elevated CO₂ levels might affect the ability of habitat specialist fishes to select favourable habitats.     

Limitations to colour-based sexual preferences in three-spined sticklebacks (Gasterosteus aculeatus)

Female three-spined sticklebacks (Gasterosteus aculeatus) are suggested to select mates based on their red nuptial coloration, males with a redder display being more preferred. Although there are both laboratory and field data to support this view, there are also published accounts where females do not show a preference for the redder male. Here we report the results of a series of 19 trials where receptive gravid female three-spined sticklebacks were allowed to choose between two size-matched rival males. We used photographic and image analysis techniques to quantify male nuptial coloration to investigate how the magnitude of the colour difference between the two alternative males influenced female preferences. Using the amount of time a female spent oriented towards each male as a measure of his attractiveness to her, females were not always found to select the redder of the two presented males. We did, however, find that that the relative difference in coloration of the two males in each pair was important in determining the level of coloration-based preference, with females only selecting redder males consistently when the difference in coloration was sufficiently large. Received: 26 October 1999 / Received in revised form: 10 January 2000 / Accepted: 13 February 2000     

Validation of otolith growth-increment periodicity in tropical gobies

 We assessed the efficacy of tetracycline, calcein and strontium chloride for validating the periodicity of otolith growth-increments in eight species of tropical marine gobies (family Gobiidae). We compared the number of fishes in which the otoliths were successfully marked when each of these chemicals was administered by intraperitoneal injection or immersion bath at a range of doses and immersion times. All three chemicals could produce a detectable mark in the otoliths of five reef-flat gobies, Asterropteryx semipunctatus, Amblygobius bynoensis, Istigobius goldmanni, Valenciennea muralis and Amblygobius phalaena; however, tetracycline injection at 50 mg kg⁻¹ is recommended because it produced a brighter otolith mark than calcein and is cheaper and quicker to detect than strontium chloride. Calcein immersion treatment of 125 mg l⁻¹ for 24 h was the most successful treatment for two estuarine gobiids, Favonigobius reichei and Glossogobius biocellatus. No treatment produced a detectable mark in the otoliths of the coral-dwelling goby Gobiodon histrio. Adequate care in the preparation of otoliths was found to be essential for detection of the validation mark produced by tetracycline and calcein. Otolith growth-increments were deposited daily in the seven species of goby for which validation was possible. Received: 15 October 1999 / Accepted: 15 June 2000     

The basics of acidification: baseline variability of pH on Australian coral reefs

Ocean acidification is one of the key threats facing coral reef ecosystems, but there are few estimates of spatial and temporal variability in pH among reef habitats. The present study documents levels of spatial variability in pH among coral reef habitats (9 to 10), among locations separated by 100’s km of latitude and between east (Great Barrier Reef, GBR) and west (Ningaloo Reef) coasts of Australia. Differences were found in pH between inshore and offshore waters along Ningaloo Reef (means 8.45, 8.53, respectively). Replicate assessments here ranged from 8.22 to 8.64. On the GBR, the range of values over all habitats and replicates was 0.39 pH units (7.98 to 8.37). There were minor but significant differences of 0.05 pH units between 5 consecutive days for habitats on average. Highest pH was recorded in filamentous algal beds maintained by the damselfish Dischistodus perspicillatus. Lowest pH was found in water extracted from sand-dwelling goby holes. While there were marked changes in pH over a 48-h sampling period among 4 habitats at Lizard Island (GBR), there was little evidence of a diel trend. Understanding how pH varies at scales that are relevant to organisms that live on shallow coral reefs is crucial for the design and interpretation of experiments that test the effects on organisms of the changes in water chemistry predicted to affect oceans in the future.     

Behavioral response of fish larvae to low dissolved oxygen concentrations in a stratified water column

Density stratification and respiration lead to vertical gradients in dissolved oxygen in many aquatic habitats. The behavioral responses of fish larvae to low dissolved oxygen in a stratified water column were examined during 1990–1991 with the goal of understanding how vertical gradients in dissolved oxygen may directly affect the distribution and survival of fish larvae in Chesapeake Bay, USA. In addition, the effects of low oxygen on 24-h survival rates were tested so that results of behavior experiments could be interpreted in the context of risk to the larve. Naked goby [Gobiosoma bosc (Lacépède)] and bay anchovy [Anchoa mitchilli (Valenciennes)] larvae strongly avoided dissolved oxygen concentrations <1 mg 1^-1, which were lethal within 24 h at 25 to 27°C. In addition, naked goby larvae, whose behavior was tested at a wider range of dissolved oxygen concentrations, also showed a reduced preference for an oxygen concentration of 2 mg 1^-1, which leads to reduced survival during long-term exposures and to reduced feeding rates. There were no major differences in behavior or survival between the two species, or between the two age classes of naked gobies tested. Results suggest that behavioral responses to oxygen gradients will play a large role in producing marked vertical changes in abundance of feeding-stage larvae in Chesapeake Bay; mortality from direct exposure to low oxygen will likely be much less important in producing vertical patterns of larval abundance.     

Does risk of intraspecific interactions induce shifts in prey-size preference in aquatic predators?

Interactions between foragers may seriously affect individual foraging efficiency. In a laboratory study of handling time, prey value and prey-size preference in northern pike and signal crayfish, we show that risk of intraspecific interactions between predators does not affect handling time or value of prey. However, the presence of agonistic intraspecific interactors shifts prey-size preference in these predators. Neither northern pike nor signal crayfish foraging alone show a prey-size preference, while pike foraging among conspecifics prefer small prey, and crayfish foraging in groups prefer large prey. We ascribe the different outcomes in prey preference to differences in susceptibility to interactions: northern pike under risk avoid large prey to avoid long handling times and the associated risk of interactions, while signal crayfish foraging among conspecifics may defend themselves and their prey during handling, and thus select prey to maximise investment. In addition, the value of pike prey (roach) is low for very small prey, maximises for small prey, and then decreases monotonically for larger prey, while crayfish prey (pond snail) value is low for very small prey, has a maximum at small prey, but does not decrease as much for larger prey. Therefore, a large and easily detected snail prey provides a crayfish with as much value as a small prey. We conclude that interaction risk and predator density affect prey-size preference differently in these aquatic predators, and therefore has different potential effects on prey-size structure and population and community dynamics. Received: 4 October 1999 / Revised: 20 March 2000 / Accepted: 27 May 2000     

Genetic evidence for mixed parentage in nests of the emu (Dromaius novaehollandiae)

Parentage in emus (Dromaius novaehollandiae) was examined by microsatellite analysis using four independent loci. Of 106 chicks sampled in one breeding season from 18 nests, 54 (51%) were not fathered by the nesting male, 12 (11%) were not from the observed mate of the sitting male, and 9 (8%) represented intra-specific brood parasitism, having no alleles in common with either nest parent. Some males (11%) fathered all chicks in their nests, but the majority showed high levels of cuckoldry. Those males commencing incubation earliest in the season tended to have the highest levels of paternity in their own nests. These results reveal a high frequency of extra-pair fertilisations and resultant cuckoldry in a predominantly socially monogamous bird and support recent reports which have described the emu mating system as a complexity of polyandrous, promiscuous and monogamous behaviour. Parentage assignment of chicks resulting from extra-pair fertilisations revealed an evenly scattered pattern of paternity that did not show any particular male dominance in reproductive success. These results lead to a reassessment of behavioural observations of emus, the consequences of parentage distribution, and theories about mating systems and sexual selection. The frequency of extra-pair copulations and intra-specific brood parasitism suggests patterns of descent that differ greatly from those implied by social monogamy. Received: 27 November 1999 / Received in revised form: 8 January 2000 / Accepted: 8 February 2000     

Antipredator responses to invasive lionfish, Pterois volitans: interspecific differences in cue utilization by two coral reef gobies

Understanding prey response to predators and their utilization of sensory cues to assess local predation risk is crucial in determining how predator avoidance strategies affect population demographics. This study examined the antipredator behaviors of two ecologically similar species of Caribbean coral reef fish, Coryphopterus glaucofraenum and Gnatholepis thompsoni, and characterized their responses to different reef predators. In laboratory assays, the two species of gobies were exposed to predator visual cues (native Nassau grouper predator vs. invasive lionfish predator), damage-released chemical cues from gobies, and combinations of these, along with appropriate controls. Behavioral responses indicate that the two prey species differ in their utilization of visual and chemical cues. Visual cues from predators were decisive for both species’ responses, demonstrating their relative importance in the sensory hierarchy, whereas damage-released cues were a source of information only for C. glaucofraenum. Both prey species could distinguish between native and invasive predators and subsequently altered their antipredator responses.     

Mating system and alternative male mating tactics in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae)

 Peculiar fertilization dynamics, with males releasing sperm in mucous trails lasting several hours, characterize some demersal spawning fish. The mating system was investigated in a natural population of one of these species: the grass goby Zosterisessor ophiocephalus (Pallas, 1814), a large coastal goby inhabiting seagrass meadows in shallow brackish water. Adult males ranged in size from 7.4 to 23 cm total length, but only larger ones were observed to dig and defend a burrow, where they performed parental care on eggs laid by one to several females. Field observations together with analyses of age, sperm production, trail sperm content and sperm competition tests indicated the occurrence of alternative male mating tactics, likely the expression of an ontogenetic gradient. Larger males are older than smaller ones, and while the former are territorial, the latter “sneak” territorial male spawns. The ejaculate characteristics indicate that grass goby males have functionally polymorphic spawns: in fact sperm trails of larger males last longer and release fewer sperm than those of smaller males. Sperm production over several days is more constant in larger than in smaller males, but the total number of sperm released is higher in the latter. The influence of seminal fluid in the functional intraspecific variability in sperm release in this species is discussed. Received: 30 December 1999 / Accepted: 31 July 2000     

Settlement patterns and presettlement behavior of the naked goby,Gobiosoma bosci,a temperate oyster reef fish

Dispersion, distribution, development and feeding incidence of larvae of the naked goby,Gobiosoma bosci (Lacepéde), were examined for linkages between larval behavior while near the reef surface and later patterns of settlement and recruitment. Field sampling and experiments were conducted during the summers of 1988 and 1989 in the Flag Pond oyster reef along the western shore of the Chesapeake Bay near Camp Conoy, Maryland, USA. Results indicated that prior to settlement most demersal larvae aggregate in shoals and exhibit distinct microhabitat preferences on the reef. In a field experiment, larvae settled both during the day and at night. Dispersion at settlement was aggregated, suggesting that demersal shoaling influences settlement patterns in this species. The distribution of demersal larvae also indicated that larval swimming behavior is sufficiently strong to permit active control of position on reefs. Large demersal larvae settled rapidly when brought to the laboratory, but small larvae in demersal shoals appeared to require additional growth and morphological development prior to settlement. Development of the pelvic fins, used by juveniles and adults for perching on the substrate, may be a good indicator of competence to settle in this species. The adaptive significance of demersal shoaling by small larvae of the naked goby, and the fate of these larvae, remains perplexing because the low feeding rates found for larvae shoaling near the reef surface should slow or prevent the growth and development required prior to settlement. Observations made by other authors indicate that demersal shoaling and the use of water directly overlying reefs may be common behaviors of temperate and tropical reef fishes.     

The benefit of obligate versus facultative strategies in a shrimp–goby mutualism

Obligate mutualists are predicted to benefit more from mutualism than facultative mutualists and harbor traits that help derive this extra benefit. I tested these predictions with a shrimp–goby mutualism. Individual shrimp (Alpheus floridanus) construct burrows that are shared with individual gobiid fishes that warn shrimp when emergence from burrows is unsafe. The benefit to gobies is refuge from predation. I compared predator avoidance performance of obligate (Nes longus) and facultative (Ctenogobius saepepallens) shrimp-associated gobies with access to a shell, a shrimp burrow, or no shelter. The two gobies performed similarly with shells and no shelter, but N. longus outperformed C. saepepallens with shrimp burrows. Thus, N. longus benefits more from mutualism than C. saepepallens. Also, N. longus has four behavioral traits that likely allow it to benefit from mutualism more than does C. saepepallens: (1) diving into the nearest shrimp burrow when confronted with predators, (2) long flight initiation distance, (3) long time-until-re-emergence after taking refuge, and (4) remaining close to shelter. The latter three likely come with a cost to foraging or mate acquisition as they limit searching range outside the burrow and detract from time spent outside burrows. Thus, N. longus likely harbors traits that allow it to deal with these costs. I discuss a framework for determining whether traits crucial to obligate association with shrimp (both for reaping benefits and dealing with costs) are pre-adaptations or are created through coevolution with shrimp.     

Strategic male signalling effort in a desert-dwelling fish

Males often use elaborate courtship displays to attract females for mating. Much attention, in this regard, has been focused on trying to understand the causes and consequences of signal variation among males. Far less, by contrast, is known about within-individual variation in signal expression and, in particular, the extent to which males may be able to strategically adjust their signalling output to try to maximise their reproductive returns. Here, we experimentally investigated male courtship effort in a fish, the Australian desert goby, Chlamydogobius eremius. When offered a simultaneous choice between a large and a small female, male gobies spent significantly more time associating with, and courting, the former, probably because larger females are also more fecund. Male signalling patterns were also investigated under a sequential choice scenario, with females presented one at a time. When first offered a female, male courtship was not affected by female size. However, males adjusted their courtship effort towards a second female depending on the size of the female encountered previously. In particular, males that were first offered a large female significantly reduced their courtship effort when presented with a subsequent, smaller, female. Our findings suggest that males may be able to respond adaptively to differences in female quality, and strategically adjust their signalling effort accordingly.     

Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998