Auditory and olfactory abilities of larvae of the Indo-Pacific coral trout Plectropomus leopardus (Lacepède) at settlement

Auditory and olfactory abilities of settlement-stage larvae of the coral trout Plectropomus leopardus (Pisces: Serranidae) were tested electrophysiologically to determine if these senses are sufficiently developed to aid larvae in detection of settlement habitats on coral reefs. Plectropomus leopardus larvae detected sounds from 100 to 2000 Hz with hearing most sensitive at the frequencies of 100, 200 and 600 Hz. The olfactory response of P. leopardus was similar for the two amino acids tested and for the water conditioned by conspecifics. Auditory and olfactory abilities of P. leopardus are well developed at settlement-stage, and apparently sufficient to detect auditory and olfactory cues from reefs.     

Identifying the ichthyoplankton of a coral reef using DNA barcodes

Marine fishes exhibit spectacular phenotypic changes during their ontogeny, and the identification of their early stages is challenging due to the paucity of diagnostic morphological characters at the species level. Meanwhile, the importance of early life stages in dispersal and connectivity has recently experienced an increasing interest in conservation programmes for coral reef fishes. This study aims at assessing the effectiveness of DNA barcoding for the automated identification of coral reef fish larvae through large‐scale ecosystemic sampling. Fish larvae were mainly collected using bongo nets and light traps around Moorea between September 2008 and August 2010 in 10 sites distributed in open waters. Fish larvae ranged from 2 to 100 mm of total length, with the most abundant individuals being <5 mm. Among the 505 individuals DNA barcoded, 373 larvae (i.e. 75%) were identified to the species level. A total of 106 species were detected, among which 11 corresponded to pelagic and bathypelagic species, while 95 corresponded to species observed at the adult stage on neighbouring reefs. This study highlights the benefits and pitfalls of using standardized molecular systems for species identification and illustrates the new possibilities enabled by DNA barcoding for future work on coral reef fish larval ecology.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

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.     

Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae)

Background  

Quantitative studies of the variation of disparity during ontogeny exhibited by the radiation of coral reef fishes are lacking. Such studies dealing with the variation of disparity, i.e. the diversity of organic form, over ontogeny could be a first step in detecting evolutionary mechanisms in these fishes. The damselfishes (Pomacentridae) have a bipartite life-cycle, as do the majority of demersal coral reef fishes. During their pelagic dispersion phase, all larvae feed on planktonic prey. On the other hand, juveniles and adults associated with the coral reef environment show a higher diversity of diets. Using geometric morphometrics, we study the ontogenetic dynamic of shape disparity of different head skeletal units (neurocranium, suspensorium and opercle, mandible and premaxilla) in this fish family. We expected that larvae of different species might be relatively similar in shapes. Alternatively, specialization may become notable even in the juvenile and adult phase.     

A comparative study of hearing ability in fishes: the auditory brainstem response approach

Auditory brainstem response (ABR) techniques, an electrophysiological far-field recording method widely used in clinical evaluation of human hearing, were adapted for fishes to overcome the major limitations of traditional behavioral and electrophysiological methods (e.g., invasive surgery, lengthy training of fishes, etc.) used for fish hearing research. Responses to clicks and tone bursts of different frequencies and amplitudes were recorded with cutaneous electrodes. To evaluate the effectiveness of this method, the auditory sensitivity of a hearing specialist (goldfish, Carassius auratus) and a hearing generalist (oscar, Astronotus ocellatus) was investigated and compared to audiograms obtained through psychophysical methods. The ABRs could be obtained between 100 Hz and 2000 Hz (oscar), and up to 5000 Hz (goldfish). The ABR audiograms are similar to those obtained by behavioral methods in both species. The ABR audiogram of curarized (i.e., Flaxedil-treated) goldfish did not differ significantly from two previously published behavioral curves but was lower than that obtained from uncurarized fish. In the oscar, ABR audiometry resulted in lower thresholds and a larger bandwidth than observed in behavioral tests. Comparison between methods revealed the advantages of this technique: rapid evaluation of hearing in untrained fishes, and no limitations on repeated testing of animals. Accepted: 8 August 1997     

How Nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes

Nearly all demersal teleost marine fishes have pelagic larval stages lasting from several days to several weeks, during which time they are subject to dispersal. Fish larvae have considerable swimming abilities, and swim in an oriented manner in the sea. Thus, they can influence their dispersal and thereby, the connectivity of their populations. However, the sensory cues marine fish larvae use for orientation in the pelagic environment remain unclear. We review current understanding of these cues and how sensory abilities of larvae develop and are used to achieve orientation with particular emphasis on coral-reef fishes. The use of sound is best understood; it travels well underwater with little attenuation, and is current-independent but location-dependent, so species that primarily utilize sound for orientation will have location-dependent orientation. Larvae of many species and families can hear over a range of ~100-1000 Hz, and can distinguish among sounds. They can localize sources of sounds, but the means by which they do so is unclear. Larvae can hear during much of their pelagic larval phase, and ontogenetically, hearing sensitivity, and frequency range improve dramatically. Species differ in sensitivity to sound and in the rate of improvement in hearing during ontogeny. Due to large differences among-species within families, no significant differences in hearing sensitivity among families have been identified. Thus, distances over which larvae can detect a given sound vary among species and greatly increase ontogenetically. Olfactory cues are current-dependent and location-dependent, so species that primarily utilize olfactory cues will have location-dependent orientation, but must be able to swim upstream to locate sources of odor. Larvae can detect odors (e.g., predators, conspecifics), during most of their pelagic phase, and at least on small scales, can localize sources of odors in shallow water, although whether they can do this in pelagic environments is unknown. Little is known of the ontogeny of olfactory ability or the range over which larvae can localize sources of odors. Imprinting on an odor has been shown in one species of reef-fish. Celestial cues are current- and location-independent, so species that primarily utilize them will have location-independent orientation that can apply over broad scales. Use of sun compass or polarized light for orientation by fish larvae is implied by some behaviors, but has not been proven. Use of neither magnetic fields nor direction of waves for orientation has been shown in marine fish larvae. We highlight research priorities in this area.     

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.     

Ontogeny of behaviour in larvae of marine demersal fishes

The development of behaviours that are relevant to larval dispersal of marine, demersal fishes is poorly understood. This review focuses on recent work that attempts to quantify the development of swimming, orientation, vertical distribution and sensory abilities. These behaviours are developed enough to influence dispersal outcomes during most of the pelagic larval stage. Larvae swim in the ocean at speeds similar to the currents found in many locations and at 3–15 body lengths per second (BL s⁻¹), although, based on laboratory measurements, species from cold environments swim slower than those from warm environments. At least in warm-water species, larvae swim in an inertial hydrodynamic environment for most of their pelagic period. Unfed swimming endurance is >10 km from about 8–10 mm, and reaches more than 50 km before settlement in several species. Larval fishes are efficient swimmers. In most species, a large majority of larvae have orientated swimming in the ocean, but the precision of orientation does not improve with growth. Swimming direction of the larvae frequently changes ontogenetically. Vertical distribution changes ontogenetically in most species, and both ontogenetic ascents and descents are found. Development of schooling is poorly understood, but it may influence speed, orientation and vertical distribution. Sensory abilities (hearing, olfaction, vision) form early, are well developed and are able to detect cues relevant to orientation for most of the pelagic larval stage. All this indicates that the passive portion of the pelagic larval duration will be short, at least in most warm-water species, and that behaviour must be taken into account when considering dispersal, and in particular in dispersal models. Although quantitative information on the ontogeny of some behaviours is available for a relatively small number of species, more research in this field is required, especially on species from colder waters.     

Development of the Acoustically Evoked Behavioral Response in Larval Plainfin Midshipman Fish,Porichthys notatus

The ontogeny of hearing in fishes has become a major interest among bioacoustics researchers studying fish behavior and sensory ecology. Most fish begin to detect acoustic stimuli during the larval stage which can be important for navigation, predator avoidance and settlement, however relatively little is known about the hearing capabilities of larval fishes. We characterized the acoustically evoked behavioral response (AEBR) in the plainfin midshipman fish, Porichthys notatus, and used this innate startle-like response to characterize this species'' auditory capability during larval development. Age and size of larval midshipman were highly correlated (r² = 0.92). The AEBR was first observed in larvae at 1.4 cm TL. At a size ≥1.8 cm TL, all larvae responded to a broadband stimulus of 154 dB re1 µPa or −15.2 dB re 1 g (z-axis). Lowest AEBR thresholds were 140–150 dB re 1 µPa or −33 to −23 dB re 1 g for frequencies below 225 Hz. Larval fish with size ranges of 1.9–2.4 cm TL had significantly lower best evoked frequencies than the other tested size groups. We also investigated the development of the lateral line organ and its function in mediating the AEBR. The lateral line organ is likely involved in mediating the AEBR but not necessary to evoke the startle-like response. The midshipman auditory and lateral line systems are functional during early development when the larvae are in the nest and the auditory system appears to have similar tuning characteristics throughout all life history stages.     

Do early life history characteristics determine species ranges and dispersal of coral reef fishes in the Indo‐Pacific?

The Indo‐Pacific consists of extensive continuous coastlines and many island groups of varying sizes and isolation. The species ranges of coral reef fishes vary enormously from Indo‐Pacific wide to highly endemic. There is also great variation in the early life history characteristics of coral reef fishes ( e.g . pelagic larval durations, spawning strategies and swimming abilities). We use individual‐based models (IBMs) to simulate the dispersal of coral reef fishes in the Indo‐Pacific. The development of dispersal strategies is explored based on ecological and geographical constraints. Simulations are presented for climatic and anthropogenically‐induced events.     

Sun-Compass Orientation in Mediterranean Fish Larvae

Mortality is very high during the pelagic larval phase of fishes but the factors that determine recruitment success remain unclear and hard to predict. Because of their bipartite life history, larvae of coastal species have to head back to the shore at the end of their pelagic episode, to settle. These settlement-stage larvae are known to display strong sensory and motile abilities, but most work has been focused on tropical, insular environments and on the influence of coast-related cues on orientation. In this study we quantified the in situ orientation behavior of settlement-stage larvae in a temperate region, with a continuous coast and a dominant along-shore current, and inspected both coast-dependent and independent cues. We tested six species: one Pomacentridae, Chromis chromis, and five Sparidae, Boops boops, Diplodus annularis, Oblada melanura, Spicara smaris and Spondyliosoma cantharus. Over 85% of larvae were highly capable of keeping a bearing, which is comparable to the orientation abilities of tropical species. Sun-related cues influenced the precision of bearing-keeping at individual level. Three species, out of the four tested in sufficient numbers, oriented significantly relative to the sun position. These are the first in situ observations demonstrating the use of a sun compass for orientation by wild-caught settlement-stage larvae. This mechanism has potential for large-scale orientation of fish larvae globally.     

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.     

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.     

Survival dynamics of scleractinian coral larvae and implications for dispersal

Survival of pelagic marine larvae is an important determinant of dispersal potential. Despite this, few estimates of larval survival are available. For scleractinian corals, few studies of larval survival are long enough to provide accurate estimates of longevity. Moreover, changes in mortality rates during larval life, expected on theoretical grounds, have implications for the degree of connectivity among reefs and have not been quantified for any coral species. This study quantified the survival of larvae from five broadcast-spawning scleractinian corals (Acropora latistella, Favia pallida, Pectinia paeonia, Goniastrea aspera, and Montastraea magnistellata) to estimate larval longevity, and to test for changes in mortality rates as larvae age. Maximum lifespans ranged from 195 to 244 d. These longevities substantially exceed those documented previously for coral larvae that lack zooxanthellae, and they exceed predictions based on metabolic rates prevailing early in larval life. In addition, larval mortality rates exhibited strong patterns of variation throughout the larval stage. Three periods were identified in four species: high initial rates of mortality; followed by a low, approximately constant rate of mortality; and finally, progressively increasing mortality after approximately 100 d. The lifetimes observed in this study suggest that the potential for long-distance dispersal may be substantially greater than previously thought. Indeed, detection of increasing mortality rates late in life suggests that energy reserves do not reach critically low levels until approximately 100 d after spawning. Conversely, increased mortality rates early in life decrease the likelihood that larvae transported away from their natal reef will survive to reach nearby reefs, and thus decrease connectivity at regional scales. These results show how variation in larval survivorship with age may help to explain the seeming paradox of high genetic structure at metapopulation scales, coupled with the maintenance of extensive geographic ranges observed in many coral species. Communicated by Environment Editor Prof. van Woesik.     

Importance of visual cues of conspecifics and predators during the habitat selection of coral reef fish larvae

The study investigated visual recognition of conspecifics and predators by settlement-stage coral reef fish larvae in a set of three experiments using a dual-choice aquarium (Moorea Island). Experiments 1 and 2 were conducted under artificial light conditions. Experiment 3 was conducted under natural light during new and full moon nights. In experiment 1, five out of six species preferred conspecifics rather than heterospecifics (Acanthurus triostegus, Chromis viridis, Ostorhinchus angustatus, Stegastes fasciolatus, Valenciaenna strigata). In experiment 2, three out of six species were repulsed by predators (Mulloidichtys flavolineatus, O. angustatus, V. strigata). In experiment 3 (conducted on one species), A. triostegus was attracted to conspecifics during bright nights, but did not show such behavior during dark nights. Our study raises the question of trade-off for fish larvae to settle during the night with high light intensities to favor the visual recognition of conspecifics and predators, or during darker nights to reduce reef predation.     

The adaptive significance of larval dispersal in coral reef fishes

Synopsis Coral reef fishes almost universally disperse over relatively great distances during a pelagic larval phase. Barlow (1981) suggested that this dispersal is adaptive because adult fishes inhabit a patchy, uncertain environment. This reiterated an older idea that the random extinction of local populations necessarily favours dispersal, since ultimately all populations of non-dispersers will disappear. Whereas this view is based on adult survival, we emphasize a less frequent view that substantial larval dispersal may be adaptive when offspring experience patchy and unpredictable survival in the pelagic habitat. We do not address the question of why these animals ‘broadcast’ rather than ‘brood’, but suggest that species committed to pelagic offspring will be under selection to disperse siblings to spread the risk of failure among members of a cohort. Our arguments are supported by a heuristic computer simulation.     

Spatial connectivity in an adult‐sedentary reef fish with extended pelagic larval phase

Understanding the spatial scale of demographic connectivity in marine reef fishes dispersing pelagic larvae is a challenging task because of the technical difficulties associated with tagging and monitoring the movements of progeny at early life stages. Several studies highlighted a strong importance of local retention with levels of dispersal of ecological significance restricted to short distances. To date little information is available in species where pelagic dispersal lasts for long periods of time. In this work, population structure and connectivity were studied in the grey triggerfish, Balistes capriscus. Grey triggerfish larvae and juveniles remain associated with floating Sargassum sp. beds for an estimated period of 4–7 months before settling on benthic habitats where they remain sedentary as adults. Analysis of genetic variation among populations along the continental shelf of the northern Gulf of Mexico and U.S. east coast, encompassing over 3,100 km of coastline, revealed homogeneous allele frequencies and a weak isolation‐by‐distance pattern. Moment and maximum‐likelihood estimates of dispersal parameters both indicated occurrence of large neighbourhoods with estimates of the dispersal distribution parameter σ of 914 and 780 km, respectively. Simulated distributions of dispersal distances using several distribution functions all featured substantial fractions of long‐distance dispersal events with the 90% percentiles of travel distance prior to settlement averaging 1,809 km. These results suggest a high dependency of local recruitment on the output of nonlocal spawning stocks located hundreds of kilometres away and a reduced role of local retention in this species.     

Ontogenetic changes in the critical swimming speed of Gadus morhua (Atlantic cod) and Myoxocephalus scorpius (shorthorn sculpin) larvae and the role of temperature

Most studies on behavioural contributions to dispersal and recruitment during early life history stages of fishes have focused on coral reef species. For cold ocean environments, high variation in seasonal temperature and development times suggest that parallel studies on active behaviour are needed for cold-water species. Thus, we examined the critical swimming speed (U_crit) of marine fish larvae from 2 contrasting species: Gadus morhua (Atlantic cod) and Myoxocephalus scorpius (shorthorn sculpin), a pelagic and bottom spawner respectively. Within-species comparisons showed that sculpin reared at 6 °C had lower initial U_crit values, but a faster U_crit increase through development compared with 3 °C conspecifics, ultimately resulting in faster critical swimming speeds at metamorphosis (10.5 vs. 9.1 cm·s^− 1). In contrast, although cod larvae reared at 10 °C were faster swimmers at first feeding than 6 °C fish, temperature differences were absent after the first week. These results show that temperature influences the trajectory of larval critical swimming speed development, but that the relationship is species-specific. Although 6 °C sculpin and cod of similar length had equivalent U_crit values, the smaller size of cod at hatch (5.3 vs. 10.8 mm for sculpin) resulted in much lower age-specific U_crit values for cod. These data have significant implications for how swimming activity of the two species might affect dispersal, particularly in the first few weeks post-hatch. Overall, our data suggest that temperature during larval development influences the swimming capacity of cold-water marine fishes, and has important ramifications for biophysical models of dispersal.     

Speciation in coral-reef fishes

Covering <0·1% of the ocean’s surface, coral reefs harbour about one‐third of all marine fishes or c. 5000 species. Allopatry (geographic isolation) is believed to be the primary mode of speciation, yet few biogeographic barriers exist between reefs, and most reef fishes have a pelagic larval stage capable of extensive dispersal. Under these circumstances, why are there so many species of reef fishes? Since most biogeographic barriers in the oceans are either spatially or temporally permeable on a relatively short time frame, the requirement of isolation during allopatric speciation is hard to satisfy. Evidence from empirical and theoretical studies, the biological characteristics of coral reefs, and a reanalysis of biogeographic barriers indicate that sympatric speciation is possible but not common at small spatial scales and that parapatric speciation is a common (and probably the prevalent) mode of diversification in coral‐reef fishes. Regardless of the speciation mode, previous hypotheses of accelerated diversification in the Pleistocene due to sea level fluctuations are not supported by phylogenetic analyses. Recent developments in the area of comparative genomics can fuel a new revolution in the way marine speciation is studied.