Close encounters with eddies: oceanographic features increase growth of larval reef fishes during their journey to the reef

Like most benthic marine organisms, coral reef fishes produce larvae that traverse open ocean waters before settling and metamorphosing into juveniles. Where larvae are transported and how they survive is a central question in marine and fisheries ecology. While there is increasing success in modelling potential larval trajectories, our knowledge of the physical and biological processes contributing to larval survivorship during dispersal remains relatively poor. Mesoscale eddies (MEs) are ubiquitous throughout the world''s oceans and their propagation is often accompanied by upwelling and increased productivity. Enhanced production suggests that eddies may serve as important habitat for the larval stages of marine organisms, yet there is a lack of empirical data on the growth rates of larvae associated with these eddies. During three cruises in the Straits of Florida, we sampled larval fishes inside and outside five cyclonic MEs. Otolith microstructure analysis revealed that four of five species of reef fish examined had consistently faster growth inside these eddies. Because increased larval growth often leads to higher survivorship, larvae that encounter MEs during transit are more likely to contribute to reef populations. Successful dispersal in oligotrophic waters may rely on larval encounter with such oceanographic features.     

Variation in the effects of larval history on juvenile performance of a temperate reef fish

For organisms with complex life cycles, the transition between life stages can act as a significant demographic and selective bottleneck. Variation in developmental and growth rates among individuals present in one stage (e.g. larvae), due to initial differences in parental input and/or environmental conditions experienced, can propagate to future stages (e.g. juveniles), and such ‘carry‐over effects’ can shape fitness and phenotypic distributions within a population. However, variation in the strength of carry‐over effects between life stages and the intensity of selective mortality acting on intrinsic variation, and how these might be mediated by environmental variability in natural systems, is poorly known. Here, we evaluate variation in the strength to which larval growth histories can mediate juvenile performance (growth and survival), for a reef fish (Forsterygion lapillum) common to rocky reefs of New Zealand. We used otoliths to reconstruct demographic histories of recently settled fish that were sampled across cohorts, sites and microhabitats. We quantified sources of variation in the strength of carry‐over effects and selective mortality that operate on larval growth histories. We found overall that individuals that grew fast as larvae tended to experience proportional growth advantages as juveniles. However, the strength of growth advantages being maintained into the juvenile period varied among cohorts, sites and microhabitats. Specifically, a stronger growth advantage was found on some microhabitats (e.g. mixed stands of macroalgae) relative to others (e.g. monocultures of Carpophyllum maschalocarpum) for some cohorts and sites only. For other cohorts and sites, the degree of coupling between larval and juvenile growth rates was either indistinguishable between microhabitats or else not evident. Similarly, the intensity of growth‐based selective mortality varied among cohorts, sites and microhabitats: for the cohort and site where carry‐over effects differed between microhabitats, we also observed difference in the intensity to which fish with rapid larval growth rates were favoured. Overall, our results highlight how this spatial and temporal patchiness in extrinsic factors can interact with intrinsic variation of recruiting individuals to have a major influence on the resulting distribution of juveniles and their phenotypic traits.     

Impact of variable pelagic environments on natural larval growth and recruitment of the reef fish Thalassoma bifasciatum

New recruits of the bluehead wrasse Thalassoma bifasciatum were censused and collected from nearshore reefs of Barbados, West Indies, every 2 weeks for 20 months. Their temporal coincidence with low salinity (<34·5) water during their pelagic larval stage was determined by comparing the otolith records of new recruits with conductivity and temperature records from a current meter moored 2 km off the west coast of the island. Larval residence in a low salinity North Brazil Current (NBC) ring appeared to have a negative impact on growth. Larvae that encountered a NBC ring for at least 7 days during either the first half of the larval period exhibited slower larval growth than those that did not encounter a ring for 7 days during any part of their larval period. As a result of this slower growth, larvae that encountered low salinity waters had a longer pelagic larval duration and were larger at the time of settlement. The magnitude of settlement was not distinctly related to the presence or absence of a NBC ring, but the largest settlement event occurred at the end of the longest ring event. Early juvenile growth did not vary between fish that had encountered a ring and those that did not, so size differences at settlement were propagated through the first week of life on the reef. The potentially opposing attributes of fast and slow‐growing larvae ( e.g . fast growing larvae with shorter larval stage duration but smaller size at settlement and higher susceptibility to reef predation), and the resulting differential mortality on the reef may promote the persistence of individuals in the population with contrasting life history traits, and contribute to the lack of a relationship between larval growth and recruitment success. Positive transport related effects of rings ( i.e . enhanced retention during some ring events) may further complicate matters by outweighing the negative impact of rings on larval growth.     

Effect of larval fish and nutrient enrichment on plankton dynamics in experimental ponds

The hypotheses that larval fish density may potentially affect phytoplankton abundance through regulating zooplankton community structure, and that fish effect may also depend on nutrient levels were tested experimentally in ponds with three densities of larval walleye, Stizostedion vitreum (0, 25, and 50 fish m^–3), and two fertilizer types (inorganic vs organic fertilizer). A significant negative relationship between larval fish density and large zooplankton abundance was observed despite fertilizer types. Larval walleye significantly reduced the abundances of Daphnia, Bosmina, and Diaptomus but enhanced the abundance of various rotifer species (Brachionus, Polyarthra, and Keratella). When fish predation was excluded, Daphnia became dominant, but Daphnia grazing did not significantly suppress blue-green algae. Clearly, larval fish can be an important regulator for zooplankton community. Algal composition and abundance were affected more by fertilizer type than by fish density. Inorganic fertilizer with a high N:P ratio (20:1) enhanced blue-green algal blooms, while organic fertilizer with a lower N:P ratio (10:1) suppressed the abundance of blue-green algae. This result may be attributed to the high density of blue-green algae at the beginning of the experiment and the fertilizer type. Our data suggest that continuous release of nutrients from suspended organic fertilizer at a low rate may discourage the development of blue-green algae. Nutrient inputs at a low N:P ratio do not necessarily result in the dominance of blue-green algae.     

Veligers of an introduced bivalve,Limnoperna fortunei,are a new food resource that enhances growth of larval fish in the Paraná River (South America)

1. Larvae of ‘sábalo’, Prochilodus lineatus, whose adults represent over 60% of overall fish biomass in the Río de la Plata Catchment, have been observed to feed intensively on veligers of the exotic bivalve Limnoperna fortunei. 2. To assess the effects of this dietary shift on the growth of P. lineatus, 28‐day laboratory experiments were carried out feeding newly hatched P. lineatus larvae with three diets: zooplankton artificially enriched with L. fortunei veligers; natural zooplankton; and zooplankton artificially enriched with cladocerans and copepods. The average length, weight and gut contents of the fish larvae were assessed weekly and metabolic rates of fish larvae were measured. 3. Proportions of veligers in gut contents were always higher than those in the experimental diet: 100, 76 and 21% for veliger‐enriched, natural and low‐veliger diets, respectively. Larvae fed a veliger‐enriched diet grew to a significantly larger size than larvae fed the other two diets. In energetic balance comparisons using metabolic rates and prey energy content, all three diets were sufficient to support metabolism and growth. The greatest values of excess energy at the end of each week were in the veliger‐enriched experiments. 4. Feeding on veligers of L. fortunei significantly enhances the growth of P. lineatus larvae and supports the idea that this new and abundant resource is selectively preyed upon by P. lineatus during its larval stage. Higher growth rates may stem from the higher energy contents of veligers compared to crustaceans and/or from the lower energy costs of capturing slower prey.     

Evolution of cannibalism in the larval stage of pelagic fish

Larvae of several ocean pelagic fish species, such as tunas and marlins, have been known to have large jaws, but the ecological significance of this unique morphological character has been hardly analyzed in evolutionary ecology. Pelagic spawners produce small and nutrition-poor ova, and spawning and nursery grounds of the open ocean migratory fishes are oligotrophic. We hypothesize that cannibalism would be a possible life style in the larval period and the large mouth gape would be an adaptive morphological characteristic for a cannibal in the oligotrophic pelagic environment. We showed that mouth gape size of the open ocean pelagic fish is significantly larger than that of offshore/coastal pelagic fish in larval period. A mathematical model demonstrated that cannibalism would tend to evolve in high sea environment. Our findings suggest an evolutionary pattern of cannibalism trait in the larval stage of pelagic fishes. This revised version was published online in July 2006 with corrections to the Cover Date.     

Development of feeding structures in larval fish with different life histories: winter flounder and Atlantic cod

The size at which feeding structures developed and shifts in head proportions occurred, differed between Atlantic cod Gadus morhua and winter flounder Pseudopleuronectes americanus. The sequence and timing of the development of feeding structures may not be dependent on size, but may occur because they are necessary to meet specific requirements offish larvae feeding in the plankton. In early larval stages development of feeding structures was similar in number and type and was necessary for first-feeding in both species. In later stages, significant differences between species occurred in the timing of the development of feeding structures. In cod differentiation of new structures and changes in head proportions occurred at about two-thirds of the way through larval life, which coincided with an increase in growth. In flounder changes in feeding morphology did not occur during the symmetrical larval stage, but occurred only after metamorphosis to the asymmetrical demersal juvenile stage. Differences between cod and flounder in the size at which feeding structures develop may reflect life history adaptations expressed in the duration of the pelagic larval stage, as well as differences in juvenile habitat and feeding ecology.     

Moon phase influences the diet of southern Ray's bream Brama australis

Diet composition of the southern Ray's bream Brama australis was examined from stomach contents of 399 specimens sampled by bottom trawl on Chatham Rise to the east of South Island, New Zealand, over 3 years. Prey items were predominantly mesopelagic fishes and crustaceans. Multivariate analysis indicated that moon phase explained more of the diet variability than any other predictor examined. It appears likely that diet composition is influenced by a combination of changes in both tidal flows and illumination. Different combinations of prey were consumed by B. australis at different times of the lunar cycle. An influence of moon phase on feeding by fishes has rarely been reported, but it is likely that moon phase influences the diets of other species that specialize in mesopelagic prey. The most important prey group by mass for B. australis was Myctophidae (primarily Lampanyctodes hectoris), followed by Stomiiformes (primarily Maurolicus australis) and shrimps (Sergestes spp). An ontogenetic shift in diet was observed, from numerical dominance by small crustaceans including amphipods and euphausiids (with some fishes) in smaller (mass <1045 g) B. australis to pelagic teleost prey (with a few larger crustaceans) in larger (>1440 g) B. australis.     

Differential effects of elevated nutrient and sediment inputs on survival,growth and biomass of a common larval fish species (Dorosoma cepedianum)

1. Elevated allochthonous inputs of nutrients and sediments to aquatic ecosystems are associated with eutrophication and sedimentation. Reservoirs receive substantial subsidies of nutrients and sediments from catchments due to their large catchment : lake area ratios. We examined the effect of elevated subsidies of sediments and/or dissolved nutrients on the success (survival, growth, biomass and condition factor) of larval gizzard shad (Dorosoma cepedianum), a widespread and dominant omnivorous fish in reservoir ecosystems. 2. We simulated allochthonous agricultural subsides by manipulating dissolved nutrients and sediment inputs in a 2 × 2 factorial design in experimental mesocosms. We predicted that larval fish success would be greater under elevated nutrients. However, we propose two alternative hypotheses with respect to the overall effect of allochthonous sediment inputs. If sediment inputs negatively affect larval gizzard feeding success, larval success would be highest when only nutrients are added and lowest when only sediments are added (+N > +N+S ≥ C > +S). If high turbidity enhances larval foraging activity (due to greater contrast between prey and background), we predict that larval success would be highest when both subsidy types (nutrients and sediment) are elevated, intermediate when either nutrients or sediments are added and the lowest when no subsidies are added (+N+S > +N ≥ +S > C). 3. Our results indicate that elevated nutrient and sediment conditions enhanced larval gizzard shad biomass, but the overall nutrient addition effect was greater than the sediment addition effect (+N ～ +N+S > +S > C). We observed differential effects of nutrient and sediment inputs on larval survival, growth and condition factors. 4. The enhancement of fish biomass in elevated nutrients (+N, +N+S) relative to control conditions was associated with improved gizzard shad survival and not greater growth. The enhancement of fish biomass in the elevated sediment treatment (+S) relative to the control conditions was caused by an increase in survival that more than compensated for a negative effect of sediment addition on growth. 5. Our findings support the recommendation that reservoir management practices must consider the links between land use practices and food web dynamics. Our results suggest that reduction of subsidies of nutrients and sediments to productive reservoirs would decrease survival of larval gizzard shad due to lower food availability.     

Identification of larval fish in mangrove areas of Peninsular Malaysia using morphology and DNA barcoding methods

The identification of larval fish has been an important morphological issue in marine biology due to the dramatic transformations that most species undergo from early larval stages to adulthood. Insufficient morphological diagnostic characters in larval fishes made it easy to misidentify them and a difficult process to key to genus and species level. The experiment aims to find out, by applying DNA barcoding, how consistent the morphological identifications can be among larval fish. Larval fish were mainly collected using plankton nets around mangrove areas in Pendas (Johor), Setiu (Terengganu), Pekan (Pahang) and Matang (Perak) Malaysia between April 2015 and October 2015. A total of 354 samples were morphologically identified, mostly to the family level and a few to the genus level. Larval fish ranged from 1.5 mm to 31 mm of total length, with the most abundant individuals being <3 mm. Among them, a total of 177 individuals were selected for DNA barcoding analyses. Molecular works involved polymerase chain reaction (PCR) and sequencing of mitochondrial Cytochrome c Oxidase I (COI) gene fragment (655 base pairs) methods. DNA barcoding enabled all samples to be identified down to species level. The overall genetic identities ranged from 91% to 100%. Morphological identification classified the specimens into 19 families and 11 genera while DNA barcoding identified them into 19 families 33 genera and 40 species. A comparison between the two methods showed a mismatched identification of 42.6% where the accuracy percentage for morphological identification was moderate for the family level (67.8%) but was low for genus level identification (30%). The DNA barcoding method also managed to successfully identify 86.4% of the samples up to their species level where morphological method has failed to do so. The most misidentified families in the study were Blenniidae, Sparidae, Apogonidae Ambassidae and Monachantidae while almost all samples from the family Gobiidae and Engraulidae were correctly identified to family level because of their distinct morphology. In conclusion, taxonomic studies of larval fish should continue using combination of both morphology and DNA barcoding methods. Morphological identification should be more conservative i.e., when in doubt, it is better to key only to family and not to the genus and species level. DNA barcoding is a better method for deeper taxonomic levels identification with the existence of robust sequence reference libraries and should be able to validate the accuracy of traditional larval fish identification.     

Ocean acidification increases fatty acids levels of larval fish

Rising levels of anthropogenic carbon dioxide in the atmosphere are acidifying the oceans and producing diverse and important effects on marine ecosystems, including the production of fatty acids (FAs) by primary producers and their transfer through food webs. FAs, particularly essential FAs, are necessary for normal structure and function in animals and influence composition and trophic structure of marine food webs. To test the effect of ocean acidification (OA) on the FA composition of fish, we conducted a replicated experiment in which larvae of the marine fish red drum (Sciaenops ocellatus) were reared under a climate change scenario of elevated CO₂ levels (2100 µatm) and under current control levels (400 µatm). We found significantly higher whole-body levels of FAs, including nine of the 11 essential FAs, and altered relative proportions of FAs in the larvae reared under higher levels of CO₂. Consequences of this effect of OA could include alterations in performance and survival of fish larvae and transfer of FAs through food webs.     

Aggregation pheromone in Dermestes maculatus: effects on larval growth and developmental rhythms

Observations on the effect of an aggregation pheromone of Dermestes maculatus indicate the production and liberation with faeces of two different compounds of a primer type. One is produced by larvae themselves and accelerates growth, the other is produced by adults and inhibits larval development. Both larval and adult pheromones synchronize larval ecdyses.     

Climate change and larval transport in the ocean: fractional effects from physical and physiological factors

Changes in larval import, export, and self‐seeding will affect the resilience of coral reef ecosystems. Climate change will alter the ocean currents that transport larvae and also increase sea surface temperatures (SST), hastening development, and shortening larval durations. Here, we use transport simulations to estimate future larval connectivity due to: (1) physical transport of larvae from altered circulation alone, and (2) the combined effects of altered currents plus physiological response to warming. Virtual larvae from islands throughout Micronesia were moved according to present‐day and future ocean circulation models. The Hybrid Coordinate Ocean Model (HYCOM) spanning 2004–2012 represented present‐day currents. For future currents, we altered HYCOM using analysis from the National Center for Atmospheric Research Community Earth System Model, version 1‐Biogeochemistry, Representative Concentration Pathway 8.5 experiment. Based on the NCAR model, regional SST is estimated to rise 2.74 °C which corresponds to a ~17% decline in larval duration for some taxa. This reduction was the basis for a separate set of simulations. Results predict an increase in self‐seeding in 100 years such that 62–76% of islands experienced increased self‐seeding, there was an average domainwide increase of ~1–3% points in self‐seeding, and increases of up to 25% points for several individual islands. When changed currents alone were considered, approximately half (i.e., random) of all island pairs experienced decreased connectivity but when reduced PLD was added as an effect, ~65% of connections were weakened. Orientation of archipelagos relative to currents determined the directional bias in connectivity changes. There was no universal relationship between climate change and connectivity applicable to all taxa and settings. Islands that presently export large numbers of larvae but that also maintain or enhance this role into the future should be the focus of conservation measures that promote long‐term resilience of larval supply.     

Ontogenetic changes in the longitudinal distribution of two species of larval fish in a turbid well-mixed estuary

The relationship between vertical migration, estuarine retention and species-specific patterns of longitudinal distribution of the pelagic larvae of rainbow smelt, Osmerus mordax , and tomcod, Microgadus tomcod , was investigated in the upper section of the St Lawrence Middle Estuary. We hypothesized that the species-specific use of the vertical pattern of current exhibited by the two species results in the partitioning of the estuarine habitat in the longitudinal plane while assuring retention. Important differences in the longitudinal distribution of tomcod and smelt larvae were related to the ontogeny of their vertical distribution in the water column. In June, small tomcod and smelt larvae are generally associated with waters of salinities less than 5%o. As the larvae grow, their vertical distribution patterns change, leading to a horizontal separation of the two species. Tomcod juveniles migrate downstream into colder, more saline waters, whereas larger smelt larvae migrate upstream into warmer, tidal fresh waters. Ontogenetic changes in vertical distribution serve to concentrate larvae in specific conditions that may optimize physiological conditions and also permit population persistence.     

Elevated carbon dioxide affects behavioural lateralization in a coral reef fish

Elevated carbon dioxide (CO(2)) has recently been shown to affect chemosensory and auditory behaviour, and activity levels of larval reef fishes, increasing their risk of predation. However, the mechanisms underlying these changes are unknown. Behavioural lateralization is an expression of brain functional asymmetries, and thus provides a unique test of the hypothesis that elevated CO(2) affects brain function in larval fishes. We tested the effect of near-future CO(2) concentrations (880 μatm) on behavioural lateralization in the reef fish, Neopomacentrus azysron. Individuals exposed to current-day or elevated CO(2) were observed in a detour test where they made repeated decisions about turning left or right. No preference for right or left turns was observed at the population level. However, individual control fish turned either left or right with greater frequency than expected by chance. Exposure to elevated-CO(2) disrupted individual lateralization, with values that were not different from a random expectation. These results provide compelling evidence that elevated CO(2) directly affects brain function in larval fishes. Given that lateralization enhances performance in a number of cognitive tasks and anti-predator behaviours, it is possible that a loss of lateralization could increase the vulnerability of larval fishes to predation in a future high-CO(2) ocean.     

Long-term cleaner fish presence affects growth of a coral reef fish

Cleaning behaviour is considered to be a classical example of mutualism. However, no studies, to our knowledge, have measured the benefits to clients in terms of growth. In the longest experimental study of its kind, over an 8 year period, cleaner fish Labroides dimidiatus were consistently removed from seven patch reefs (61-285 m(2)) and left undisturbed on nine control reefs, and the growth and parasite load of the damselfish Pomacentrus moluccensis determined. After 8 years, growth was reduced and parasitic copepod abundance was higher on fish from removal reefs compared with controls, but only in larger individuals. Behavioural observations revealed that P. moluccensis cleaned by L. dimidiatus were 27 per cent larger than nearby conspecifics. The selective cleaning by L. dimidiatus probably explains why only larger P. moluccensis individuals benefited from cleaning. This is the first demonstration, to our knowledge, that cleaners affect the growth rate of client individuals; a greater size for a given age should result in increased fecundity at a given time. The effect of the removal of so few small fish on the size of another fish species is unprecedented on coral reefs.     

Lunar and daily spawning rhythms of Senegal sole Solea senegalensis

A periodicity of 29 days was observed in spawning rhythms in Senegal sole Solea senegalensis , with an acrophase around the last quarter and the new moon. In both spring and autumn, a very marked nocturnal spawning rhythm was registered, with spawning beginning after dusk and the acrophase occurring around 2300 hours. When the photoperiod was artificially extended (from 10L:14D to 14L:10D), S. senegalensis synchronized to the new photoperiod: spawning took place after the new 'dusk', the beginning gradually shifting from 2100 to 2300 hours and the acrophase from 2325 to 0032 hours. Under continuous light conditions, fish sustained rhythmicity for 2 days, with an acrophase at 2249 hours, which suggested the existence of an endogenous pacemaker controlling the daily spawning rhythm. These findings provided new insights for better understanding the reproductive physiology of this species and for optimizing the timing protocols of egg collection and larvae production in S. senegalensis aquaculture.     

Bigger? Fatter? Or is faster growth better? Considerations on condition in larval and juvenile coral-reef fish

Abstract Analyses of condition data are conspicuous by their paucity in the extensive tropical reef-fish literature. Researchers typically quantify abundance at settlement, with little regard for the demonstrably variable quality of newly settled fishes. Condition may be functionally classified by indices of growth (e.g. the RNA-DNA index or peripheral growth increments of the otolith), starvation (e.g. height of midgut mucosal cells), storage (e.g. lipid content), or morphometry (e.g. dry weight/length’), all of which are variably correlated with each other. At present all indices are species-, stage-, technique- and therefore often investigation-specific, as laboratory-reared larvae for calibrating field-collected condition indices are often specific to the rearing procedure. RNA indices are particularly appropriate for estimating larval condition. In pelagic juveniles, or in recently settled juveniles, the width of peripheral growth increments of the otolith estimates average growth rate in length or dry weight during the previous few days, which discerns increasing from decreasing condition. Increment width changes in otoliths are particularly responsive to starvation events, and are correlated with RNA indices. Growth indices have great potential for determining which individuals were growing faster, thereby reducing their pelagic duration, and thus increasing their survival potential. The recent debate regarding whether bigger larvae have better survival could be re-addressed, by determining if larvae with faster growth indices have relatively enhanced survival.