Size-selective predation by the cleaner fish Labroides dimidiatus

A comparison of the size-frequency distribution of parasitic gnathiid isopod larvae in the diet of the cleaner fish Labroides dimidiatus and on six host fish species ( Chlorurus sordidus, Ctenochaetus striatus, Hemigymnus melapterus, Scolopsis bilineatus, Siganus doliatus, Thalassoma lunare ) was made on one occasion. The comparison was repeated with Hemigymnus melapterus on three occasions and between two islands in Australia. L. dimidiatus selected larger gnathiids at all times at Lizard Island but not at Heron Island. Size-selective predation by L. dimidiatus suggests any potential effect of cleaner fish on parasites may vary according to the size of parasite. However, this effect appears to vary spatially.     

A simple molecular technique for identifying marine host fish by sequencing blood-feeding parasites

Gnathiid isopods are common ectoparasites of fish on the Great Barrier Reef, Australia. While screening for appropriate markers for phylogenetic studies of gnathiids, we found that primers for 12S and 16S rDNA preferentially amplified the host fish DNA instead of gnathiid DNA. This amplification occurred even when using gnathiids that were not engorged with host blood and adult gnathiids that do not feed on fish blood. This method could be used in host-parasite studies to identify hosts without having to sample parasites directly from the host (which can be costly and requires considerable skill in a marine environment). Target ribosomal DNA sequences can be amplified from total DNA extracted from parasites that are captured in funnel traps or plankton tows. Sequence data from these can be used to identify the hosts that gnathiids were feeding on before capture.     

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 gnathiids. 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.     

Fish mucous cocoons: the 'mosquito nets' of the sea

Mucus performs numerous protective functions in vertebrates, and in fishes may defend them against harmful organisms, although often the evidence is contradictory. The function of the mucous cocoons that many parrotfishes and wrasses sleep in, while long used as a classical example of antipredator behaviour, remains unresolved. Ectoparasitic gnathiid isopods (Gnathiidae), which feed on the blood of fish, are removed by cleaner fish during the day; however, it is unclear how parrotfish and wrasse avoid gnathiid attacks at night. To test the novel hypothesis that mucous cocoons protect against gnathiids, we exposed the coral reef parrotfish Chlorurus sordidus (Scaridae) with and without cocoons to gnathiids overnight and measured the energetic content of cocoons. Fish without mucous cocoons were attacked more by gnathiids than fish with cocoons. The energetic content of mucous cocoons was estimated as 2.5 per cent of the fish's daily energy budget fish. Therefore, mucous cocoons protected against attacks by gnathiids, acting like mosquito nets in humans, a function of cocoons and an efficient physiological adaptation for preventing parasite infestation that is not used by any other animal.     

Live coral repels a common reef fish ectoparasite

Coral reefs are undergoing rapid changes as living corals give way to dead coral on which other benthic organisms grow. This decline in live coral could influence habitat availability for fish parasites with benthic life stages. Gnathiid isopod larvae live in the substratum and are common blood-feeding parasites of reef fishes. We examined substrate associations and preferences of a common Caribbean gnathiid, Gnathia marleyi. Emergence traps set over predominantly live coral substrata captured significantly fewer gnathiids than traps set over dead coral substrata. In laboratory experiments, gnathiids preferred dead coral and sponge and tended to avoid contact with live coral. When live gnathiids were added to containers with dead or live coral, significantly fewer were recovered from the latter after 24 h. Our data therefore suggest that live coral is not suitable microhabitat for parasitic gnathiid isopods and that a decrease in live coral cover increases available habitat for gnathiids.     

Impact of micropredatory gnathiid isopods on young coral reef fishes

The ecological role of parasites in the early life-history stages of coral reef fish, and whether this varies between fish with and without a pelagic phase, was investigated. The susceptibility to, and effect of reef-based micropredatory gnathiid isopods on larval, recently settled, and juvenile fishes was tested using two damselfishes (Pomacentridae): Neopomacentrus azysron, which has pelagic larvae, and Acanthochromis polyacanthus, which does not. When larval and recently settled stages of N. azysron and very young A. polyacanthus juveniles (smaller than larval N. azysron) were exposed to one or three gnathiids, the proportion of infections did not vary significantly among the three host types or between the number of gnathiids to which the fish were exposed. The overall infection was 35%. Mortality, however, differed among the three gnathiid-exposed host types with most deaths occurring in larval N. azysron; no mortalities occurred for recently settled N. azysron exposed to one or three gnathiids, and A. polyacanthus exposed to one gnathiid. Mortality did not differ significantly between larval N. azysron and A. polyacanthus juveniles, failing to provide support for the hypothesis that reef-based A. polyacanthus juveniles are better adapted to gnathiid attack than fish with a pelagic phase. The study suggests that settling on the reef exposes young fish to potentially deadly micropredators. This supports the idea that the pelagic phase may allow young fish to avoid reef-based parasites.     

Within and between day variability in coral reef fish assemblages: Implications for fish community surveys

Coral reef ecosystems are under increasing anthropogenic pressures making it ever more important to monitor changes in fish communities to implement appropriate management. In contrast to long-term spatial and temporal variation which has been extensively documented, little work has been carried out to identify variability in fish assemblages on short time scales, with few studies testing patterns of fish assemblages between and within days. Here we investigated the diurnal changes in species richness, relative abundance and assemblage composition in a shallow coral reef fish community in Egypt. To do so, a section of coral reef was filmed during the morning (0600 h), midday (1000 and 1400 h) and afternoon (1800 h) over eleven days. Dusk (0600 h) and dawn samples (1800 h) showed higher species richness compared to late morning (1000 h) and mid-day samples (1400 h) and borderline significantly higher numbers of total individuals, likely associated with feeding activity and predator avoidance. Assemblage composition varied across days and time-of-day, showing greater variability during dusk and dawn associated with a transition between day-time and night-time assemblages. Our results have implications for designing coral reef fish surveys, emphasising that short-term changes in fish communities should be considered when designing experiments to monitor fish assemblages over time. Where possible, we suggest increasing replication within sites and time scales or randomising data within a specific time window at all sites, looking to exclude dusk and dawn.     

Low Susceptibility of Invasive Red Lionfish (Pterois volitans) to a Generalist Ectoparasite in Both Its Introduced and Native Ranges

Escape from parasites in their native range is one of many mechanisms that can contribute to the success of an invasive species. Gnathiid isopods are blood-feeding ectoparasites that infest a wide range of fish hosts, mostly in coral reef habitats. They are ecologically similar to terrestrial ticks, with the ability to transmit blood-borne parasites and cause damage or even death to heavily infected hosts. Therefore, being highly resistant or highly susceptible to gnathiids can have significant fitness consequences for reef-associated fishes. Indo-Pacific red lionfish (Pterois volitans) have invaded coastal habitats of the western tropical and subtropical Atlantic and Caribbean regions. We assessed the susceptibility of red lionfish to parasitic gnathiid isopods in both their native Pacific and introduced Atlantic ranges via experimental field studies during which lionfish and other, ecologically-similar reef fishes were caged and exposed to gnathiid infestation on shallow coral reefs. Lionfish in both ranges had very few gnathiids when compared with other species, suggesting that lionfish are not highly susceptible to infestation by generalist ectoparasitic gnathiids. While this pattern implies that release from gnathiid infestation is unlikely to contribute to the success of lionfish as invaders, it does suggest that in environments with high gnathiid densities, lionfish may have an advantage over species that are more susceptible to gnathiids. Also, because lionfish are not completely resistant to gnathiids, our results suggest that lionfish could possibly have transported blood parasites between their native Pacific and invaded Atlantic ranges.     

Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs

Ontogenetic niche shifts are characteristic of organisms with complex life cycles such as many marine invertebrates. Research has focused primarily on changes in habitat or diet. However, ontogenetic changes can also occur in the temporal pattern of foraging. Gnathiid isopods feed on fish blood throughout their larval stages and are the primary food item for cleaning organisms on coral reefs. At sites in Australia and the Caribbean, gnathiid larvae exhibit size-related differences in diel activity. However, it is unclear whether this is due to interspecific or intraspecific variation in behavior. Fish were deployed in cages near sunset on shallow reefs off St. John, U.S. Virgin Islands and allowed to be infected with larval gnathiids. Larvae collected from fish retrieved near midnight developed into adults, with most developing into females. In contrast, approximately 80% of gnathiids collected after first light developed into second or third stage larvae, and nearly all of the remaining, large, individuals developed into males. Comparison of ITS2 gene regions from individuals collected in emergence traps from the same reefs during the day versus during the night revealed no differences in this highly variable region. Thus, gnathiid larvae at this locality shift their time of activity as they develop, and larvae developing into males remain active over a longer time period than those developing into females.     

Effect of the removal of cleaner fish on the abundance and species composition of reef fish

The ecological significance of cleaner fish on coral reefs was investigated. I removed all cleaner fish, Labroides dimidiatus, from eight small reefs, measured the subsequent effect on the abundance and species composition of all reef fish after 3 and 6 months, and compared it with eight control reefs with cleaner fish. The removal of cleaner fish had no detectable effect on the total abundance of fish on reefs and the total number of fish species at both times. Multivariate analysis by non-metric multidimensional scaling and ANOSIM pairwise tests based on 191 fish species revealed no effect of cleaners on the community structure of fish. Similar results were obtained using principal components analysis on subsets of the data using the 33 most common fish species and the 15 most abundant species (≥5 individuals per reef ) with both log10 (x + 1) transformed data and with fish numbers standardized for abundance. This study demonstrates that the removal of cleaner fish for 6 months did not result in fish suffering increased mortality nor in fish leaving reefs to seek cleaning elsewhere. Received: 28 October 1996 / Accepted: 7 February 1997     

Interactions between gnathiid isopods,cleaner fish and other fishes on Lizard Island,Great Barrier Reef

The rate of emergence of micropredatory gnathiid isopods from the benthos, the proportion of emerging gnathiids potentially eaten by Labroides dimidiatus, and the volume of blood that gnathiids potentially remove from fishes (using gnathiid gut volume) were determined. The abundance (mean ±s.e .) of emerging gnathiids was 41·7 ± 6·9 m^?2 day^?1 and 4552 ± 2632 reef^?1 day^?1 (reefs 91–125 m²). The abundance of emerging gnathiids per fish on the reef was 4·9 ± 0·8 day^?1; but excluding the rarely infested pomacentrid fishes, it was 20·9 ± 3·8 day^?1. The abundance of emerging gnathiids per patch reef was 66 ± 17% of the number of gnathiids that all adult L. dimidiatus per reef eat daily while engaged in cleaning behaviour. If all infesting gnathiids subsequently fed on fish blood, their total gut volume per reef area would be 17·4 ± 5·6 mm³ m^?2 day^?1; and per fish on the reefs, it would be 2·3 ± 0·5 mm^?3 fish^?1 day^?1 and 10·3 ± 3·1 mm³ fish^?1 day^?1 (excluding pomacentrids). The total gut volume of gnathiids infesting caged (137 mm standard length, L_S) and removed from wild (100–150 mm L_S) Hemigymnus melapterus by L. dimidiatus was 26·4 ± 24·6 mm³ day^?1 and 53·0 ± 9·6 mm³ day^?1, respectively. Using H. melapterus (137 mm L_S, 83 g) as a model, gnathiids had the potential to remove, 0·07, 0·32, 0·82 and 1·63% of the total blood volume per day of each fish, excluding pomacentrids, caged H. melapterus and wild H. melapterus, respectively. In contrast, emerging gnathiids had the potential of removing 155% of the total blood volume of Acanthochromis polyacanthus (10·7 mm L_S, 0·038 g) juveniles. That L. dimidiatus eat more gnathiids per reef daily than were sampled with emergence traps suggests that cleaner fishes are an important source of mortality for gnathiids. Although the proportion of the total blood volume of fishes potentially removed by blood‐feeding gnathiids on a daily basis appeared to be low for fishes weighing 83 g, the cumulative effects of repeated infections on the health of such fish remains unknown; attacks on small juvenile fishes, may result in possibly lethal levels of blood loss.     

Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish

Infestation dynamics of parasitic gnathiid isopods on Caribbean reefs were studied throughout the 24-h diel cycle. Gnathiid infestation on caged longfin damselfish (Stegastes diencaeus) peaked strongly at dawn, remained low during the remainder of the day, and increased again at night until about midnight. Gnathiids were less abundant during the pre-dawn period. Peak loads on fish retrieved at dawn were the highest reported in any study thus far. The dawn peak consisted almost exclusively of individuals from the smallest size class, whereas nocturnal activity consisted almost exclusively of individuals of the largest size class. Because of the high rates of infestation at night and dawn, and the high variation in parasite loads on fish collected during that time, reduction of parasite infestation may play an important role in the selection of nocturnal and crepuscular shelter holes and settlement sites by reef fishes.     

Evolutionary divergence in common marine ectoparasites Gnathia spp. (Isopoda: Gnathiidae) on the Great Barrier Reef: phylogeography, morphology, and behaviour

The blood‐feeding juvenile stages of gnathiid isopods are important ectoparasites of marine fishes on the Great Barrier Reef (GBR), and are a major component of the diet of cleaner fishes. We report here that these gnathiids have undergone evolutionary diversification, both geographically and temporally (into diurnally and nocturnally active taxa), which has been accompanied by changes in their morphology and behaviour. To perform this analysis, we sequenced a portion of the nuclear ribosomal ITS2 for 47 gnathiids collected from 29 host fishes of 11 species at three locales spanning 2000 km on the GBR. Maximum parsimony and Bayesian phylogenetic analyses both revealed four major clades. There was some degree of geographical structuring in these clades, but there was no evidence supporting host fish specialization, as gnathiids collected from the skin of different teleost taxa did not resolve into distinct clades. The topology of the phylogeny also implied some structuring that was dependent upon collection time (day or night), so we investigated whether there were also behavioural and morphological differences between taxa active at these different times. Nocturnal gnathiids had significantly longer antennules and larger eyes than diurnal gnathiids – two traits presumably adaptive for nocturnal activity. Behavioural tests showed that both nocturnal and diurnal gnathiids use olfaction and vision while foraging, but that nocturnal gnathiids used olfaction more often in dark conditions, and that they were able to perceive movement under extremely low levels of light. Diurnal gnathiids used vision more effectively when there was some ambient light. Our results thus suggest that both phenotypic and genotypic divergence in gnathiids may be influenced by natural selection acting on ecological traits, such as predator avoidance and host detection. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 569–587.     

The thermoregulatory function of diel vertical migration for a juvenile fish,Cottus extensus

Juvenile sculpin (Cottus extensus) less than 30 mm long exhibit a diel vertical migration in the limnetic zone of Bear Lake (Utah-Idaho). Using mid-water and bottom trawls we found that these fish inhabit the bottom of the lake (5° C) during the day but migrate 30–40 m into the water column at night where they reside in the metalimnion or epilimnion at temperatures near 13–16°C. Larger fish do not migrate into the water column. Stomach analyses demonstrated that the young-of-the-year fish do not migrate into the water column to feed: from July to October their diet is 70–93% benthic ostracods and copepods, and pelagic prey are rarely consumed. Furthermore, gut fullness of the sculpin increases through the daylight period and decreases through the night, reaching minimum levels just before the dawn descent. Laboratory experiments demonstrated that the diel migration would increase digestion rate from 3%/h at profundal temperatures, to 22%/h in the warmer surface water, thus allowing the fish to empty their guts overnight and permit feeding the following day. Additionally, sculpin held in a temperature and feeding regime that mimicked that experienced by migrating fish grew 300% faster than those reared at 5° C. Given the overwhelming importance of fast growth for juvenile fishes, a post-feeding thermotaxs that increases digestion may be a common phenomenon increasing growth, and affecting the distribution and bioenergetic relationships of fish.     

In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish

Although cleaning interactions are deemed a textbook example of mutualism, there is limited evidence that clients benefit from cleaning in terms of reduced ectoparasite loads. The proximate causes of cleaning behaviour are also contentious. We examined the effect of ectoparasite load (i.e. the number of larval gnathiid isopods) on client behaviour under natural conditions. Diel variation in gnathiid loads of longfin damselfish, Stegastes diencaeus, a common coral reef fish client of cleaning gobies (Elacatinus spp.), was correlated with variation in gnathiid emergence from the substratum at sites in both Puerto Rico and St John, northeastern Caribbean. Both benthic emergence of gnathiids and their infestation on damselfish peaked in the morning. Concomitantly, clients spent significantly more time posing for and being inspected by cleaners in the morning than at other times of day. Our results corroborate recent experimental results on captive clients and are consistent with the mutualistic interpretation of cleaning symbioses.     

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 <0.1% infected erythrocytes) of infections of the haemogregarine Haemogregarina hemiscyllii were relatively low and most stages were immature gamonts. Two undescribed Gnathia spp. were identified by examining adult male gnathiids that metamorphosed from juveniles from each of the two size groups. Our hypothesis that Gnathia spp. transmit H. hemiscyllii is neither supported or refuted, as although intact H. hemiscyllii gamonts were detected in squashes of gnathiids that had engorged on haemogregarine-positive H. ocellatum 24-57 days previously, no further developmental stages were detected.     

Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes

A gnathiid species (Crustacea: Isopoda; one of the most common ectoparasites of coral reef fishes) from the Great Barrier Reef, Australia, was allowed to choose among fishes from three different families to feed on (using two species of fishes per family). Gnathiids showed a strong preference for labrids, rarely feeding on pomacentrids or apogonids. In a separate experiment, gnathiid host preference did not vary among three labrid fish species. Gnathiids that fed on labrids had higher survival than those that fed on apogonids. Male gnathiids that fed on labrids also moulted to the adult stage more quickly. This suggests that host specialization and local adaptation might be occurring between these ectoparasites and their host fishes at the host fish family level.     

Movement in a large predatory fish: coral trout, Plectropomus leopardus (Pisces: Serranidae), on Heron Reef, Australia

 Movement by the larger more mobile species of coral reef fish plays a significant role in determining patterns in abundance and population structure. Fish movement is also relevant to the use and effectiveness of marine reserves in managing fish populations. Coral trout are large piscivorous serranids supporting major fisheries on the Great Barrier Reef (GBR). This study reports on the within-reef movement of the common coral trout, Plectropomus leopardus, at Heron Reef, southern GBR, over a twelve month period, investigated by tagging and underwater tracking. Tracking of coral trout revealed no apparent relationship between the area moved and stage of tide or time of day. However, movement areas were affected by the size of fish: in spring a linear relationship between fish size and area of movement was measured, but in summer the largest (male) fish moved over significantly smaller areas than medium-sized fish. Movement of males may be related to cleaning behaviour and spawning. Fifty nine percent (n=101) of the tagged fish were resighted over periods of 4–5 months, in “home sites” measuring ∼2000 m². Coral trout were not restricted to home sites, but moved on average 2 km along the reef slope; maximum distances of 7–7.5 km were measured. Coral trout appear to range as mobile, opportunistic predators, but also maintain home sites for access to shelter and cleaning stations. Accepted: 1 August 1996     

Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals

Host specificity data for gnathiid isopods are scarce because the parasitic stages are difficult to identify and host-parasite contact is often brief. We examined two common nocturnal species, Gnathia falcipenis and Gnathia sp. C, collected in light traps from two locations at Lizard Island on the Great Barrier Reef, Australia. Engorged third stage gnathiids were photographed and permitted to moult into adults to allow identification. We compared approximately 580 bp sequences of 16S mtDNA from blood meals with host sequences available on GenBank using BLASTn. Where homology was <98%, familial identity was investigated with neighbour-joining trees. All blood meal sequences (n=60) and homologous fish sequences (n=87) from GenBank were used in a Bayesian analysis, which identified all but three sequences to family. The host frequency distributions used by each species were significantly different; only four host families were shared. No gnathiids fed on elasmobranchs, blennies or apogonids, and most fed on host families whose representatives are typically large. Gnathia sp. C showed a distinct predilection for nemipterids. Gnathia falcipenis often parasitised sand-dwelling families, and unlike sympatric diurnal gnathiid species, it also frequently parasitised pomacentrids. We conclude that G. falcipenis and Gnathia sp. C operate as generalist micropredators with preferences.     

Sinusoidal swimming in fishes: the role of season,density of large zooplankton,fish length,time of the day,weather condition and solar radiation

The sinusoidal swimming of fish, previously interpreted as foraging behaviour, was studied with respect to season, density of large zooplankton, fish length, time of the day, weather condition and solar radiation in Římov Reservoir, Czech Republic, using a bottom-mounted, split-beam transducer (7°, nominal angle; frequency 120 kHz). The proportion of sinusoidally swimming fish increased from April to August while this behaviour was absent in October. The occurrence of sinusoidal swimming showed an apparent pattern throughout the day; it increased sharply around sunrise, was highest within 5–6 h around solar noon, and sharply decreased around sunset. Significantly less frequent occurrence of sinusoidal swimming was recorded during cloudy days compared to sunny days. The vast majority of records came from fish of standard length ranging from 100 to 400 mm, which represents the typical size range of common bream Abramis brama and roach Rutilus rutilus of age >1+, the main zooplanktivores in the reservoir. The presence of these larger fish in the open water of the reservoir, as well as the presence of sinusoidal swimming, apparently correlates with the presence of large zooplankton (Daphnia, Leptodora and Cyclops vicinus) in the epilimnion. The increase of sinusoidal swimming between April, June and finally August resulted in an increase of zooplankton component in fish guts. It appears that high values of solar radiation, and stable calm weather during high pressure periods, result in optimal optical conditions for sinusoidal swimming, making this foraging behaviour more efficient and widely used in fishes exploiting the zooplankton production in the reservoir.