Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis

The ecological role of parasites in the early life-history stages of coral reef fish is far from clear. Parasitism in larval, recently settled and juvenile stages of a coral reef fish damselfish (Pomacentridae) was therefore investigated by quantifying the ontogenetic change in parasite load and comparing the growth rates of parasitized juvenile fish to those of unparasitized ones. Parasite prevalence in two lunar pulses of Pomacentrus moluccensis was 4 and 0% for larval stage fish, 34 and 56% for recently settled fish and 42 and 49% for juveniles. A significant increase in parasite prevalence with age group was found; the most marked increase occurred immediately after larval fish had settled. Standard length did not model prevalence well; as length is a proxy for age, this indicates that the higher prevalence in recently settled and juvenile fish compared with larvae was not a simple result of parasites accumulating with age. In one of three cohorts, there was some evidence that parasitism affected the growth rate of juveniles, as measured by otolith width. The study suggests that settling on the reef exposes young fish to potentially harmful parasites. This supports the idea that the pelagic phase may have the effect of reducing the exposure of young fish to the debilitating effects of parasites.     

Modelling larval dispersal and behaviour of coral reef fishes

Coral reef fish spend their first few weeks developing in the open ocean, where eggs and larvae appear merciless to tides and currents, before attempting to leave the pelagic zone and settle on a suitable reef. This pelagic dispersal phase is the process that determines population connectivity and allows replenishment of harvested populations across multiple coral reef habitats. Until recently this pelagic larval dispersal phase has been poorly understood and has often been referred to as the ‘black-box’ in the life-history of coral reef fishes. In this perspective article we highlight three areas where mathematical and computational approaches have been used to aid our understanding of this important ecological process. We discuss models that provide insights into the evolution of the pelagic larval phase in coral reef fish, an unresolved question which lends itself well to a modelling approach due to the difficulty in obtaining empirical data on this life history strategy. We describe how studies of fish hearing and physical sound propagation models can be used to predict the detection distance of reefs for settling larval fish, and the potential impact of anthropogenic noise. We explain how random walk models can be used to explore individual- and group-level behaviour in larval fish during the dispersal and settlement stage of their life-history. Finally, we discuss the mutual benefits that mathematical and computational approaches have brought to and gained from the field of larval behaviour and dispersal of reef fishes.     

Experimental test of the influence of the size of shoals and density of fish on parasite infections

There is an increasing interest in the relationship between adult coral reef fishes and their parasites; however, there is almost no information concerning post larvae (i.e. newly recruited) fish and their parasites. Newly recruited and juvenile fish are highly sensitive to their environment and they have a very low survival rate. Fish grouping behavior has been studied in several ways and many studies have shown that increasing group size might be a way to share a cost linked to parasitism, via a dilution effect. To my knowledge, this hypothesis has never been tested for juveniles of fish. The potential influence of school size and density of a juvenile coral reef fish, Haemulon flavolineatum (Haemulidae), on the success of a monogenean fish parasite, Haliotrema sp., was studied. First, the fish acquired their monogeneans when they were more than 40 mm long, size corresponding also to a change in their foraging behavior. Second, there was a positive effect of fish density on the success of the establishment of the parasite on the host population. Finally, although the parasite success was not directly related to fish group size, the parasite abundance was higher for intermediate shoal size. These results are discussed in terms of the consequence parasitism may have on a fish's shoaling and to a larger extent on the fish population.     

Parasites of recruiting coral reef fish larvae in New Caledonia

Recruiting coral reef fish larvae from 38 species and 19 families from New Caledonia were examined for parasites. We found 13 parasite species (Platyhelminthes: Monogenea, Cestoda and Trematoda) but no acanthocephalan, crustacean or nematode parasites. Over 23% of individual fish were infected. Didymozoid metacercariae were the most abundant parasites. We conclude that most of the parasites are pelagic species that become ‘lost’ once the fish larvae have recruited to the reef. Larval coral reef fish probably contribute little to the dispersal of the parasites of the adult fish so that parasite dispersal is more difficult than that of the fish themselves.     

Auditory sensitivity in settlement-stage larvae of coral reef fishes

The larval phase of most species of coral reef fishes is spent away from the reef in the pelagic environment. At the time of settlement, these larvae need to locate a reef, and recent research indicates that sound emanating from reefs may act as a cue to guide them. Here, the auditory abilities of settlement-stage larvae of four species of coral reef fishes (families Pomacentridae, Lutjanidae and Serranidae) and similar-sized individuals of two pelagic species (Carangidae) were tested using an electrophysiological technique, auditory brainstem response (ABR). Five of the six species heard frequencies in the 100–2,000 Hz range, whilst one carangid species did not detect frequencies higher than 800 Hz. The audiograms of the six species were of similar shape, with best hearing at lower frequencies between 100 and 300 Hz. Strong within-species differences were found in hearing sensitivity both among the coral reef species and among the pelagic species. Larvae of the coral reef species had significantly more sensitive hearing than the larvae of the pelagic species. The results suggest that settlement-stage larval reef fishes may be able to detect reef sounds at distances of a few 100 m. If true hearing thresholds are lower than ABR estimates, as indicated in some comparisons of ABR and behavioural methods, the detection distances would be much larger.     

An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish

ABSTRACT: BACKGROUND: Coral reefs are areas of maximum biodiversity, but the parasites of coral reef fishes, and especially their species richness, are not well known. Over an 8-year period, parasites were collected from 24 species of Lutjanidae, Nemipteridae and Caesionidae off New Caledonia, South Pacific. RESULTS: Host-parasite and parasite-host lists are provided, with a total of 207 host-parasite combinations and 58 parasite species identified at the species level, with 27 new host records. Results are presented for isopods, copepods, monogeneans, digeneans, cestodes and nematodes. When results are restricted to well-sampled reef fish species (sample size[THIN SPACE]>[THIN SPACE]30), the number of host-parasite combinations is 20[EN DASH]25 per fish species, and the number of parasites identified at the species level is 9[EN DASH]13 per fish species. Lutjanids include reef-associated fish and deeper sea fish from the outer slopes of the coral reef: fish from both milieus were compared. Surprisingly, parasite biodiversity was higher in deeper sea fish than in reef fish (host-parasite combinations: 12.50 vs 10.13, number of species per fish 3.75 vs 3.00); however, we identified four biases which diminish the validity of this comparison. Finally, these results and previously published results allow us to propose a generalization of parasite biodiversity for four major families of reef-associated fishes (Lutjanidae, Nemipteridae, Serranidae and Lethrinidae): well-sampled fish have a mean of 20 host-parasite combinations per fish species, and the number of parasites identified at the species level is 10 per fish species. CONCLUSIONS: Since all precautions have been taken to minimize taxon numbers, it is safe to affirm than the number of fish parasites is at least ten times the number of fish species in coral reefs, for species of similar size or larger than the species in the four families studied; this is a major improvement to our estimate of biodiversity in coral reefs. Our results suggest that extinction of a coral reef fish species would eventually result in the coextinction of at least ten species of parasites.     

Early life history and settlement of the slender filefish, <Emphasis Type="Italic">Monacanthus tuckeri</Emphasis> (Monacanthidae), at Calabash Caye,Turneffe Atoll,Belize

Synopsis We examined early life history traits and patterns of settlement of the slender filefish, Monacanthus tuckeri, at Calabash Caye, Turneffe Atoll, Belize. A settlement peak was evident at the new moon, and no settlement occurred at the full moon. However, settlement rates at the quarter moons could not be estimated due to sampling gaps. Many reef fishes show new moon settlement peaks, so M. tuckeri shares some characteristics with the primarily perciform species on coral reefs. Pelagic larval duration was long (mean = 42 days) and variable, suggesting that dispersal patterns might be diverse. Size at settlement was large (mean = 32 mm total length) and also variable. Larval duration and size at settlement were outside of the average values exhibited by reef fishes, but are not beyond the extreme end of the range, and might be explained by association with pelagic debris prior to settlement. There were no differences in overall settlement rates on reef and seagrass habitats, and fish settling to either habitat did not differ in larval duration, size at settlement, or larval growth rate. This suggests that settlement to alternative habitats may be random, or driven by availability of suitable microhabitat, rather than habitat quality or individual traits.     

Validation of a technique for reconstructing daily patterns in the recruitment of coral reef damselfish

Counting growth increments in otoliths recently has become an accepted method of ageing tropical fishes, however, verification is essential for each new species. In this study, growth increments in otoliths of the juveniles of several coral reef damselfishes (Pomacentridae) were deposited daily and a distinct transition from wide to narrow increments coincided with settlement from the pelagic larval phase into the demersal habitat. Thus, the data of settlement for each individual fish could be calculated with acceptable accuracy. The daily pattern of recruitment to a coral reef was successfully reconstructed using the otoliths from a large sample of juvenile fish collected at the end of the breeding season. This was because the original pattern of settlement was preserved in the age distribution for at least 4 to 5 months. This application of otolith ageing techniques may be extended to reveal the temporal patterns of recruitment to many localities encompassing spatial scales larger than would be logistically possible using visual censuses.     

Structure of the parasite communities of a coral reef fish assemblage (Labridae): testing ecological and phylogenetic host factors

The role of ecological and phylogenetic processes is fundamental to understanding how parasite communities are structured. However, for coral reef fishes, such information is almost nonexistent. In this study, we analyzed the structure of the parasite communities based on composition, richness, abundance, and biovolume of ecto- and endoparasites of 14 wrasse species (Labridae) from Lizard Island, Great Barrier Reef, Australia. We determine whether the structure of the parasite communities from these fishes was related to ecological characteristics (body size, abundance, swimming ability, and diet) and/or the phylogenetic relatedness of the hosts. We examined 264 fishes from which almost 37,000 individual parasites and 98 parasite categories (types and species) were recorded. Gnathiid and cestode larvae were the most prevalent and abundant parasites in most fishes. Mean richness, abundance, and biovolume of ectoparasites per fish species were positively correlated with host body size only after controlling for the host phylogeny, whereas no such correlation was found for endoparasites with any host variable. Because most ectoparasites have direct transmission, one possible explanation for this pattern is that increased space (host body size) may increase the colonization and recruitment of ectoparasites. However, endoparasites generally have indirect transmission that can be affected by many other variables, such as number of prey infected and rate of parasite transmission.     

The effect of microhabitat patch size on settlement differs among co-occurring coral reef fishes

Over small spatial scales, coral reefs represent a mosaic of suitable settlement microhabitat patches of varying size for late-stage larval reef fishes. Few studies have specifically examined how variation in patch size influences density of recently settled coral reef fishes (recruits). Using standardized units of coral rubble settlement substrate deployed on sandy bottom, we monitored the concurrent settlement of three reef fish taxa onto differently sized patches (0.28–1.68 m²) at 5-d intervals during a lunar settlement peak. We found marked differences among taxa in how recruit density scaled with patch size. Recruit density of a damselfish and a parrotfish decreased and increased, respectively, with the increase in patch size, while that of a wrasse was similar among patch sizes. Our results highlight the importance of the interaction between taxon-specific settlement behaviour and patch size in establishing initial spatial differences in density within and among coral reef fish taxa in a heterogeneous landscape.

     

Terrestrial chemical cues help coral reef fish larvae locate settlement habitat surrounding islands

Understanding the degree of connectivity between coastal and island landscapes and nearby coral reefs is vital to the integrated management of terrestrial and marine environments in the tropics. Coral reef fish are capable of navigating appropriate settlement habitats following their pelagic larval phase, but the mechanisms by which they do this are unclear. The importance of olfactory cues in settlement site selection has been demonstrated, and there is increasing evidence that chemical cues from terrestrial sources may be important for some species. Here, we test the olfactory preferences of eight island-associated coral reef fish recruits and one generalist species to discern the capacity for terrestrial cue recognition that may aid in settlement site selection. A series of pairwise choice experiments were used to evaluate the potential role that terrestrial, water-borne olfactory cues play in island-reef recognition. Olfactory stimuli tested included near-shore water, terrestrial rainforest leaf litter, and olfactory cues collected from different reef types (reefs surrounding vegetated islands, and reefs with no islands present). All eight island-associated species demonstrated high levels of olfactory discrimination and responded positively toward olfactory cues indicating the presence of a vegetated island. We hypothesize that although these fish use a suite of cues for settlement site recognition, one mechanism in locating their island/reef habitat is through the olfactory cues produced by vegetated islands. This research highlights the role terrestrial olfactory cues play in large-scale settlement site selection and suggests a high degree of ecosystem connectivity.     

Phylogenetic perspectives on reef fish functional traits

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef‐associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid‐sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.     

The morphology and ultrastructure of the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus Bleeker (Gobiidae, Teleostei)

We examined the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus (SL=5.8mm+/-0.8mm, N=15), by the aid of electron microscopy (scanning and transmission) and light microscopy. Two bilateral olfactory placodes were present in each fish. They were oval-shaped and located medio-ventrally, one in each of the olfactory chambers. Each placode had a continuous cover of cilia. The placode epithelium contained three different types of olfactory receptor neurons: ciliated, microvillous and crypt cells. The latter type was rare. Following a pelagic larval phase, P. xanthosomus settle to the reef and form an obligate association with one species of coral, Seriatopora hystrix. Their well-developed olfactory organs likely enable larvae of P. xanthosomus to detect chemical cues that assist in navigating towards and selecting appropriate coral habitat at settlement. Our findings support past studies showing that the peripheral olfactory organ develops early in coral reef fishes.     

Habitat choice,recruitment and the response of coral reef fishes to coral degradation

The global degradation of coral reefs is having profound effects on the structure and species richness of associated reef fish assemblages. Historically, variation in the composition of fish communities has largely been attributed to factors affecting settlement of reef fish larvae. However, the mechanisms that determine how fish settlers respond to different stages of coral stress and the extent of coral loss on fish settlement are poorly understood. Here, we examined the effects of habitat degradation on fish settlement using a two-stage experimental approach. First, we employed laboratory choice experiments to test how settlers responded to early and terminal stages of coral degradation. We then quantified the settlement response of the whole reef fish assemblage in a field perturbation experiment. The laboratory choice experiments tested how juveniles from nine common Indo-Pacific fishes chose among live colonies, partially degraded colonies, and dead colonies with recent algal growth. Many species did not distinguish between live and partially degraded colonies, suggesting settlement patterns are resilient to the early stages of declining coral health. Several species preferred live or degraded corals, and none preferred to associate with dead, algal-covered colonies. In the field experiment, fish recruitment to coral colonies was monitored before and after the introduction of a coral predator (the crown-of-thorns starfish) and compared with undisturbed control colonies. Starfish reduced live coral cover by 95–100%, causing persistent negative effects on the recruitment of coral-associated fishes. Rapid reductions in new recruit abundance, greater numbers of unoccupied colonies and a shift in the recruit community structure from one dominated by coral-associated fishes before degradation to one predominantly composed of algal-associated fish species were observed. Our results suggest that while resistant to coral stress, coral death alters the process of replenishment of coral reef fish communities.     

Evidence of an original scale development during the settlement phase of a coral reef fish (Acanthurus triostegus)

As the majority of coral reef fishes, the Convict Surgeonfish Acanthurus triostegus (Acanthuridae) has a complex life cycle that involves an ontogenetic change in morphology, physiology and behaviour as its pelagic larval stage colonizes the benthic habitat. Few studies are devoted to the changes in skeleton during the settlement phase of coral reef fishes. In the present study, we highlighted an unexpected scales development in A. trisostegus just after the reef settlement. At settlement (t₀), A. triostegus showed calcified and very thin vertical plates, lying in the dermis on the whole body. During the first 9 days after settlement, thin vertical plates regressed and adult scales began to appear simultaneously. At 12 days post‐settlement, the whole body was covered with small scales. Overall, such a rapid skeletal transformation is an example of morphological changes dealing with ‘metamorphosis’ of coral reef fishes.     

The effects of age and size on habitat selection during settlement of a damselfish

The adults of many coral reef fish species are site-attached, and their habitat is selected at the time of settlement by their larvae. The length of the planktonic larval period varies both intra- and interspecifically, and it is unknown how the age and size of larvae may affect their selection of habitat. To investigate the influence of age and size on habitat selection, I collected newly settled Hawaiian domino damselfish, Dascyllus albisella, daily from grids containing three coral species at four locations in Kaneohe Bay, Oahu, Hawaii. I recorded the coral species each fish was collected on, and measured and aged (by otoliths) the collected fish. The results indicate that the coral Pocillopora meandrina was selected by settling fish significantly more than the other two coral species. Younger and smaller larvae selected this coral species more frequently than older/larger larvae. In addition, younger/smaller individuals were found more commonly inside the bay than older/larger settling larvae. Differences in the choice of coral species and location of settlement may be partly due to ontogenetic differences in the sensory capacities of larvae to detect corals, conspecifics, and predators, or to a larval competency period. This revised version was published online in July 2006 with corrections to the Cover Date.     

Otolith growth of Springer's demoiselle, Chrysiptera springeri (Pomacentridae, Allen & Lubbock), on a protected and non-protected coral reef

The structural complexity of coral reefs is important for their function as shelter and feeding habitats for coral reef fishes, but physical disturbance by human activities often reduce complexity of the reefs by selectively destroying fragile and more complex coral species. The damselfish Springer's demoiselle Chrysiptera springeri primarily utilize complex coral heads for shelter and are hence vulnerable to human disturbance. In order to evaluate the potential effect of habitat degradation on juvenile fish growth, coral reef cover, fish age at settling and otolith growth, juvenile Springer's demoiselle was investigated on a protected and non‐protected coral reef in Darvel Bay, Borneo. The protected reef had higher coverage of complex branching corals and exhibited a more complex 3‐dimensional structure than the non‐protected reef. Springer's demoiselle settled at the same age on non‐protected and protected reefs. The growth rates of the otoliths from Springer's demoiselle were similar during the pre‐settlement period on the two reefs (manova , P > 0.05), but from age 20 to 48 days (post‐settlement period) the otolith growth rate of juveniles on the non‐protected reef was reduced compared to those from the protected reef (manova , P = 0.017). However, the differences in the otolith size, and by inference, fish size, after 48 days were small. The small effect of habitat degradation on growth is likely related to the fact that the Springer's demoiselles collected on the non‐protected reef were associated with the few remaining complex coral heads. Increased foraging‐predation tradeoffs on the non‐protected reef may decrease food intake and growth of juvenile Springer's demoiselle, but the main effect of habitat degradation on their abundance is likely to be related to lack of suitable shelter, and consequently reduced carrying capacity, on disturbed reefs.     

Parasites of native and exotic freshwater fishes in south‐western Australia

In this study, 1429 fishes of 18 different species (12 native and six exotic) were sampled from 29 localities to compare the levels of parasitism between native and exotic fish species and to examine the relationship between environmental degradation and parasite diversity. Forty‐four putative species of parasites were found and most of these appear to be native parasites, which have not previously been described. Two parasite species, Lernaea cyprinacea and Ligula intestinalis, are probably introduced. Both were found on or in a range of native fish species, where they may cause severe disease. Levels of parasitism and parasite diversity were significantly greater in native fishes than in exotic species, and this may contribute to an enhanced demographic performance and competitive ability in invading exotics. Levels of parasitism and parasite diversity in native fishes were negatively related to habitat disturbance, in particular to a suite of factors that indicate increased human use of the river and surrounding environment. This was due principally to the absence in more disturbed habitats of a number of species of endoparasites with complex life cycles, involving transmission between different host species.     

Climate change and coral reef connectivity

This review assesses and predicts the impacts that rapid climate change will have on population connectivity in coral reef ecosystems, using fishes as a model group. Increased ocean temperatures are expected to accelerate larval development, potentially leading to reduced pelagic durations and earlier reef-seeking behaviour. Depending on the spatial arrangement of reefs, the expectation would be a reduction in dispersal distances and the spatial scale of connectivity. Small increase in temperature might enhance the number of larvae surviving the pelagic phase, but larger increases are likely to reduce reproductive output and increase larval mortality. Changes to ocean currents could alter the dynamics of larval supply and changes to planktonic productivity could affect how many larvae survive the pelagic stage and their condition at settlement; however, these patterns are likely to vary greatly from place-to-place and projections of how oceanographic features will change in the future lack sufficient certainty and resolution to make robust predictions. Connectivity could also be compromised by the increased fragmentation of reef habitat due to the effects of coral bleaching and ocean acidification. Changes to the spatial and temporal scales of connectivity have implications for the management of coral reef ecosystems, especially the design and placement of marine-protected areas. The size and spacing of protected areas may need to be strategically adjusted if reserve networks are to retain their efficacy in the future.     

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.