Impact of cyclones on hard coral and metapopulation structure,connectivity and genetic diversity of coral reef fish

Cyclones have one of the greatest effects on the biodiversity of coral reefs and the associated species. But it is unknown how stochastic alterations in habitat structure influence metapopulation structure, connectivity and genetic diversity. From 1993 to 2018, the reefs of the Capricorn Bunker Reef group in the southern part of the Great Barrier Reef were impacted by three tropical cyclones including cyclone Hamish (2009, category 5). This resulted in substantial loss of live habitat-forming coral and coral reef fish communities. Within 6–8 years after cyclones had devastated, live hard corals recovered by 50–60%. We show the relationship between hard coral cover and the abundance of the neon damselfish (Pomacentrus coelestis), the first fish colonizing destroyed reefs. We present the first long-term (2008–2015 years corresponding to 16–24 generations of P. coelestis) population genetic study to understand the impact of cyclones on the meta-population structure, connectivity and genetic diversity of the neon damselfish. After the cyclone, we observed the largest change in the genetic structure at reef populations compared to other years. Simultaneously, allelic richness of genetic microsatellite markers dropped indicating a great loss of genetic diversity, which increased again in subsequent years. Over years, metapopulation dynamics were characterized by high connectivity among fish populations associated with the Capricorn Bunker reefs (2200 km²); however, despite high exchange, genetic patchiness was observed with annual strong genetic divergence between populations among reefs. Some broad similarities in the genetic structure in 2015 could be explained by dispersal from a source reef and the related expansion of local populations. This study has shown that alternating cyclone-driven changes and subsequent recovery phases of coral habitat can greatly influence patterns of reef fish connectivity. The frequency of disturbances determines abundance of fish and genetic diversity within species.

     

Pelagic larval duration is similar across 23° of latitude for two species of butterflyfish (Chaetodontidae) in eastern Australia

Duration of the pelagic phase of benthic marine fishes has been related to dispersal distance, with longer pelagic larval duration (PLD) expected to result in greater dispersal potential. Here, we examine PLDs of 2 species of coral-reef butterflyfish (Chaetodon auriga and C. flavirostris) across latitudes (14°S–37°S) along the Great Barrier Reef into south-eastern Australia; we predict that PLD will be higher for fish collected below the breeding latitudes of 24°S. For C. auriga, apart from significantly longer PLDs at Lord Howe Island and Jervis Bay (means of 54 and 52 days, respectively), all locations had similar PLDs (mean 41 days). For C. flavirostris, there was no significant location effect on PLD (mean 41.5 days); however, PLD at Lord Howe Island was 58 days with high variance precluding significance. Also, there was no significant variation in PLD among years for either species despite considerable variation in East Australian Current strength.     

Purification,Biochemical Characterization,and Cloning of Phospholipase D from <Emphasis Type="Italic">Streptomyces racemochromogenes</Emphasis> Strain 10-3

We previously isolated Streptomyces racemochromogenes strain 10-3, which produces a phospholipase D (PLD) with high transphosphatidylation activity. Here, we purified and cloned the PLD (PLD103) from the strain. PLD103 exerted the highest hydrolytic activity at a slightly alkaline pH, which is in contrast to the majority of known Streptomyces PLDs that have a slightly acidic optimum pH. PLD103 shares only 71–76% amino acid sequence identity with other Streptomyces PLDs that have a slightly acidic optimum pH; thus, the diversity in the primary structure might explain the discrepancy observed in the optimum pH. The purified PLD displayed high transphosphatidylation activity in the presence of glycerol, l-serine, and 2-aminoethanol hydrochloride with a conversion rate of 82–97% in a simple one-phase system, which was comparable to the rate of other Streptomyces PLDs in a complicated biphasic system.     

Spatial variation in sea urchins, fish predators, and bioerosion rates on coral reefs of Belize

Although sea urchins are critical for controlling macroalgae on heavily fished coral reefs, high densities threaten reefs, as urchins are also prodigous bioeroders. This study examined urchin population characteristics, bioerosion rates, their fish predators (Labridae), and potential competitors (Scaridae) on unprotected reefs and a reef within a marine protected area (MPA) in the lagoonal regions off Belize. Urchin density (<1 m⁻²) and bioerosion rates (∼0.2 kg CaCO₃ m⁻² year⁻¹) were lowest and members of the Labridae were the highest (∼20 fish 200 m⁻³) within the MPA, while several unprotected reefs had higher (∼18–40 m⁻²) urchin densities, lower Labridae abundances (1–3 fish 200 m⁻³), and bioerosion rates ranging from ∼0.3–2.6 kg CaCO₃ m⁻² year⁻¹. Urchin abundances were inversely related to Labridae (wrasses and hogfish) densities; however, on reef ridges, low algal cover (∼15%), small urchin size (∼14 mm), and low proportion of organic material in urchin guts suggested food limitation. Both top–down (predation) and bottom–up factors (food limitation) likely contribute to the control of urchins, predominantly Echinometra viridis, off Belize, thereby potentially diminishing the negative impacts of bioerosion activities by urchins.     

Settlement behaviour of larvae of the Stripey Snapper, <Emphasis Type="Italic">Lutjanus carponotatus</Emphasis> (Teleostei: Lutjanidae)

Larval behaviour is important to dispersal and settlement, but is seldom quantified. Behavioural capabilities of larval Lutjanus carponotatus in both offshore pelagic and reef environments at Lizard Island, Great Barrier Reef were observed in situ to determine if they were sufficient to influence dispersal. Offshore, larvae swam with higher directional precision and faster on the windward side of the island (28 cm.s⁻¹) than on the leeward side (16 cm s⁻¹). Most larvae swam directionally. Mean swimming directions were southerly in the windward area and northerly in the leeward area. Larvae avoided the surface and remained mostly between 3–15 m. Larvae released near reefs were 2–3 times faster swimming away from reefs (19 cm s⁻¹) than swimming toward or over them (6–8 cm s⁻¹). Speed swimming away was similar to that offshore. Of 41 larvae released near reefs, 73% reached the reef, 59% settled, and 13% of those reaching the reef were eaten. Larvae settled onto hard and soft coral (58%), topographic reef features (29%) and sand and rubble (13%). Settlement depth averaged 5.5 m (2–8 m). Before settling larvae spent up to 800 s over the reef (mean 231 s) and swam up to 53 m (mean 14 m). About half of the larvae interacted with reef residents including predatory attacks and aggressive approaches by residents and aggressive approaches by settling larvae. Settlement behaviour of L. carponotatus was more similar to a serranid than to pomacentrids. Settlement-stage larvae of L. carponotatus are behaviourally capable, and have a complex settlement behaviour.     

Trawl fishery resources in the “southern waters” of Japan

Settlement-stage larvae of the coral reef fishes Ostorhinchus doederleini (Apogonidae) and Pomacentrus coelestis (Pomacentridae) prefer the odor of their settlement reef to that of other nearby reefs. It was unknown whether these olfactory preferences are temporally stable or the result of recent olfactory experience. Ostorhinchus doederleini and P. coelestis larvae were held in aquaria and exposed to water from either their settlement reef or a neighboring reef for 5–9 days and their olfactory preference was tested. We show that exposure to water from another reef did not influence olfactory preference. Ostorhinchus doederleini olfactory preference declined slightly over time whereas P. coelestis preference was gradually lost after 2–3 days in captivity. Neither species switched their preference to the new reef odor. While we cannot determine conclusively the time window of odor learning, imprinting at or shortly after birth is logical and has been demonstrated in other fish species.     

Phase shift to algal dominated communities at mesophotic depths associated with lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>) invasion on a Bahamian coral reef

Mesophotic coral reefs (30–150 m) have been assumed to be physically and biologically connected to their shallow-water counterparts, and thus may serve as refugia for important taxonomic groups such as corals, sponges, and fish. The recent invasion of the Indo–Pacific lionfish (Pterois volitans) onto shallow reefs of the Caribbean and Bahamas has had significant, negative, effects on shallow coral reef fish populations. In the Bahamas, lionfish have extended their habitat range into mesophotic depths down to 91 m where they have reduced the diversity of several important fish guilds, including herbivores. A phase shift to an algal dominated (>50% benthic cover) community occurred simultaneously with the loss of herbivores to a depth of 61 m and caused a significant decline in corals and sponges at mesophotic depths. The effects of this invasive lionfish on mesophotic coral reefs and the subsequent changes in benthic community structure could not be explained by coral bleaching, overfishing, hurricanes, or disease independently or in combination. The significant ecological effects of the lionfish invasion into mesophotic depths of coral reefs casts doubt on whether these communities have the resilience to recover themselves or contribute to the recovery of their shallow water counterparts as refugia for key coral reef taxa.     

Juvenile coral reef fish use sound to locate habitats

There is limited knowledge of the orientation cues used by reef fish in their movement among different habitats, especially those cues used during darkness. Although acoustic cues have been found to be important for settlement-stage fish as they seek settlement habitats, only a small number of studies support the possible role of acoustic cues in the orientation of post-settled and adult reef fish. Therefore, the aim of this study was to determine whether habitat-specific acoustic cues were involved in the nocturnal movements of juvenile reef fish to small experimental patch reefs that were broadcasting sound previously recorded from different habitats (Fringing Reef, Lagoon, Silent). Juvenile fish arriving at each patch reef were caught the next morning by divers and were identified. There were a greater number of occasions when juvenile fish (from all species together) moved onto the patch reefs broadcasting Fringing Reef and Lagoon sound (43 and 38%, respectively) compared to Silent reefs (19%) (χ² = 33.5; P < 0.05). There were significantly more occasions when juvenile fish from the family Nemipteridae were attracted to the patch reefs broadcasting Lagoon sound (63%) versus those reefs broadcasting either Fringing Reef sound (31%) or Silent (6%). In contrast, there were more occasions when juveniles from the family Pomacentridae were attracted to the patch reefs broadcasting Fringing Reef sound (56%) than either Lagoon (24%) or Silent patch reefs (20%) (χ² = 19.5; P < 0.05). These results indicate that some juvenile fish use specific habitat sounds to guide their nocturnal movements. Therefore, the fish are able to not only use the directional information contained in acoustic cues, but can also interpret the content of the acoustic signals for relevant habitat information which is then used in their decision-making for orientation.     

Temperate macroalgae impacts tropical fish recruitment at forefronts of range expansion

Warming waters and changing ocean currents are increasing the supply of tropical fish larvae to temperature regions where they are exposed to novel habitats, namely temperate macroalgae and barren reefs. Here, we use underwater surveys on the temperate reefs of south-eastern (SE) Australia and western Japan (~33.5°N and S, respectively) to investigate how temperate macroalgal and non-macroalgal habitats influence recruitment success of a range of tropical fishes. We show that temperate macroalgae strongly affected recruitment of many tropical fish species in both regions and across three recruitment seasons in SE Australia. Densities and richness of recruiting tropical fishes, primarily planktivores and herbivores, were over seven times greater in non-macroalgal than macroalgal reef habitat. Species and trophic diversity (K-dominance) were also greater in non-macroalgal habitat. Temperate macroalgal cover was a stronger predictor of tropical fish assemblages than temperate fish assemblages, reef rugosities or wave exposure. Tropical fish richness, diversity and density were greater on barren reef than on reef dominated by turfing algae. One common species, the neon damselfish (Pomacentrus coelestis), chose non-macroalgal habitat over temperate macroalgae for settlement in an aquarium experiment. This study highlights that temperate macroalgae may partly account for spatial variation in recruitment success of many tropical fishes into higher latitudes. Hence, habitat composition of temperate reefs may need to be considered to accurately predict the geographic responses of many tropical fishes to climate change.

     

Fish assemblages on artificial and natural reefs in the Flower Garden Banks National Marine Sanctuary, USA

 Visual censusing was used to characterize fish assemblages on artificial and natural reefs located within the boundaries of the Flower Garden Banks National Marine Sanctuary (FGBNMS) in the northwestern Gulf of Mexico. Emphasis was placed on determining spatial and temporal patterns in habitat utilization by fishes on an offshore artificial reef (Mobil Platform HI-A389A). Overall, 43 species were observed during diurnal surveys in the upper 24 m of the artificial reef. Midwater pelagic fishes (i.e., carangids and scombrids) accounted for over 50% of all taxa enumerated on the artificial reef; however, these taxa were transient members of the assemblage and were observed infrequently. Labrids, pomacentrids, and serranids were the dominant reef-dependent taxa. Distinct trends in vertical, diel, and seasonal abundances were observed for juvenile and adult fishes. Of the three designated depth zones (upper 1.5–9.0, middle 9.0–16.5; lower 16.5–24.0 m), abundance and species diversity were lowest in the upper zone. Nocturnal counts were characterized by a marked reduction or complete absence of most species, due in part to twilight cover-seeking and movement activities. Seasonal variation in community composition and species abundance (May versus September) was primarily due to recruitment of juveniles (0-age fishes) to the artificial reef in late summer. Increases in total fish abundance (all taxa combined) coincided with both increasing habitat rugosity and degree of fouling. Species richness on natural coral reefs in the FGBNMS was higher than on the artificial reef. Unlike the artificial reef, fish assemblages on the natural reefs were dominated by a single family (Pomacentridae) which accounted for over 50% of all individuals observed. Accepted: 1 August 1996     

A deep nursery for juveniles of the zebra angelfish <Emphasis Type="Italic">Genicanthus caudovittatus</Emphasis>

Juveniles of many coral reef fish species are thought to either follow the same bathymetric distribution patterns as the adults, or to occupy shallower waters. However, our knowledge base suffers a dearth of data from the deep reefs (>40 m). In a recent survey of the deep reefs of the northern Gulf of Aqaba (<65 m), we examined the bathymetric distribution of 26 diurnal zooplanktivorous species. In sharp contrast to the general trend known from the literature and from this research, the abundance of juvenile zebra angelfish, Genicanthus caudovittatus, peaked at deeper waters (60–65 m) compared with the adults (30 m). This suggests that the deeper reefs may serve as nursery grounds for the zebra angelfish. Peak juvenile abundance coincided with relatively low predator abundances. This raises the question, which factors constrain the bathymetric distribution of the remaining species. Our findings stress the potential importance of deep coral reef research for understanding the ecological patterns and processes that govern reef community structure.     

Maintenance of fish diversity on disturbed coral reefs

Habitat perturbations play a major role in shaping community structure; however, the elements of disturbance-related habitat change that affect diversity are not always apparent. This study examined the effects of habitat disturbances on species richness of coral reef fish assemblages using annual surveys of habitat and 210 fish species from 10 reefs on the Great Barrier Reef (GBR). Over a period of 11 years, major disturbances, including localised outbreaks of crown-of-thorns sea star (Acanthaster planci), severe storms or coral bleaching, resulted in coral decline of 46–96% in all the 10 reefs. Despite declines in coral cover, structural complexity of the reef framework was retained on five and species richness of coral reef fishes maintained on nine of the disturbed reefs. Extensive loss of coral resulted in localised declines of highly specialised coral-dependent species, but this loss of diversity was more than compensated for by increases in the number of species that feed on the epilithic algal matrix (EAM). A unimodal relationship between areal coral cover and species richness indicated species richness was greatest at approximately 20% coral cover declining by 3–4 species (6–8% of average richness) at higher and lower coral cover. Results revealed that declines in coral cover on reefs may have limited short-term impact on the diversity of coral reef fishes, though there may be fundamental changes in the community structure of fishes.     

Grazing pressure of herbivorous coral reef fishes on low coral-cover reefs

The impact of grazing by herbivorous fishes (Acanthuridae, Scaridae, and Pomacentridae) on low coral-cover reefs was assessed by measuring rates of benthic algal production and consumption on inshore and offshore reefs in the upper Florida Keys. Algal production rates, determined in situ with caged and uncaged experimental plates, were low (mean 1.05 g C m⁻² day⁻¹) and similar among reef types. Algal consumption rates were estimated using two different models, a detailed model incorporating fish bite rates and algal yield-per-bite for one species extrapolated to a guild-wide value, and a general regression relating fish biomass to algal consumption. Algal consumption differed among reef types: a majority of algal production was consumed on offshore reefs (55–100%), whereas consumption on inshore patch reefs was 31–51%. Spatial variation in algal consumption was driven by differences in herbivorous fish species composition, density, and size-structure among reef types. Algal consumption rates also varied temporally due to seasonal declines in bite rates and intermittent presence of large-bodied, vagile, schooling species. Spatial coherence of benthic community structure and temporal stability of algal turf over 3 years suggests that grazing intensity is currently sufficient to limit further spread of macroalgal cover on these low coral-cover reefs, but not to exclude it from the system.     

Differences in the behavior and diet between shoaling and solitary surgeonfish (Acanthurus triostegus)

Variation in behavior within marine and terrestrial species can influence the functioning of the ecosystems they inhabit. However, the contribution of social behavior to ecosystem function remains underexplored. Many coral reef fish species provide potentially insightful models for exploring how social behavior shapes ecological function because they exhibit radical intraspecific variation in sociality within a shared habitat. Here, we provide an empirical exploration on how the ecological function of a shoaling surgeonfish (Acanthurus triostegus) may differ from that of solitary conspecifics on two Pacific coral reefs combining insight from behavioral observations, stable isotope analysis, and macronutrient analysis of gut and fecal matter. We detected important differences in how the social mode of A. triostegus affected its spatial and feeding ecology, as well as that of other reef fish species. Specifically, we found increased distance traveled and area covered by shoaling fish relative to solitary A. triostegus. Additionally, shoaling A. triostegus primarily grazed within territories of other herbivorous fish and had piscivorous and nonpiscivorous heterospecific fish associated with the shoal, while solitary A. triostegus grazed largely grazed outside of any territories and did not have any such interactions with heterospecific fish. Results from stable isotope analysis show a difference in δ15N isotopes between shoaling and solitary fish, which suggests that these different social modes are persistent. Further, we found a strong interaction between social behavior and site and carbohydrate and protein percentages in the macronutrient analysis, indicating that these differences in sociality are associated with measurable differences in both the feeding ecology and nutrient excretion patterns. Our study suggests that the social behavior of individuals may play an important and underappreciated role in mediating their ecological function.     

Behavioral and energetic costs of group membership in a coral reef fish

Animals in social aggregations often spend more time foraging than solitary conspecifics. This may be a product of the relative safety afforded by aggregations: group members can devote more time to foraging and less time to antipredator behaviors than solitary animals (the “risk reduction” effect). All else being equal, risk reduction should result in higher food intake for grouped animals. However, intragroup competition may force group members to spend more time foraging in order to obtain the same food ration as solitary individuals (the “resource competition” effect). We compared these opposing explanations of foraging time allocation in a coral reef fish, bluehead wrasse (Thalassoma bifasciatum). Aggregations of juvenile bluehead wrasse experience safety-in-numbers, and preliminary observations suggested that juveniles in aggregations spent more time foraging for copepods in the water column than solitary juveniles. However, the risk reduction and resource competition hypotheses are indistinguishable on the basis of behavioral observations alone. Therefore, we collected behavioral, dietary, and growth data (using otolith growth rings) for bluehead wrasse at multiple reefs around a Caribbean island. Despite spending more time foraging in the water column, grouped fish did not capture more prey items and had slower growth rates than solitary fish. Thus, the increased foraging time of grouped fish appears to reflect resource competition, not risk reduction. This competition may limit the size and frequency of aggregations among juvenile bluehead wrasse, which have been shown to experience reduced mortality rates in larger groups. Bluehead wrasse recruits also spent less time foraging but grew faster at sites where planktonic copepod prey were more abundant. This suggests the possibility that large-scale spatiotemporal variability in the abundance of planktonic copepods over coral reefs may produce corresponding variability in the dynamics of reef fish populations. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Cyclone effects on coral reef habitats in New Caledonia (South Pacific)

The impacts of the unusually strong Cyclone Erica (March 2003) on coral reef habitats at a site located on the northwest coast of New Caledonia (South Pacific) were assessed using a 6-year data set (2002–2007). We examined the interannual variations of key variables describing reef habitats (live hard and soft corals, dead corals in place, coral debris, algae and relative proportion of mechanically vulnerable and resistant live hard corals). The cyclone-induced disturbances of habitats differed according to three reef types: patch reefs, barrier reefs far from passes (more than 3 km from the nearest pass) and barrier reefs near passes (less than 3 km from the nearest pass). Short-term mechanical damage was detected on the three-dimensional structure of reef habitats with a notable shift from a community dominated by mechanically vulnerable corals to one dominated by resistant corals on barrier reefs far from passes. The history of habitats and their pre-disturbance characteristics, in link with local hydrodynamics, was found to influence their short-term susceptibility to extreme events such as cyclones. However, the most significant effects appeared in the midterm (within 2 years after the cyclone) as the cover of live hard corals significantly decreased by approximately 45% between 2002 and 2004 on all reef types. The short- and midterm disturbances of coral reef habitats are discussed with regard to published temporal variations in reef fish assemblages, underlining the delayed effects of this cyclonic event on fish as well as benthic habitats. Coral reef habitats and live corals had shown significant patterns of recovery 4 years after the cyclone, followed by similar recovery in fish community, suggesting good resilience in a face of this major natural disturbance in an area under moderate anthropogenic pressure.     

Neogene reef coral assemblages of the Bocas del Toro region, Panama: the rise of Acropora palmata

Temporal patterns are evaluated in Neogene reef coral assemblages from the Bocas del Toro Basin of Panama in order to understand how reef ecosystems respond to long-term environmental change. Analyses are based on a total of 1,702 zooxanthellate coral specimens collected from six coral-bearing units ranging in age from the earliest Late Miocene to the Early Pleistocene: (1) Valiente Formation (12–11 Ma), (2) Fish Hole Member of the Old Bank Formation (5.8–5.6 Ma), (3) La Gruta Member of the Isla Colon Formation (2.2–1.4 Ma), (4) Ground Creek Member of the Isla Colon Formation (2.2–1.4 Ma), (5) Mimitimbi Member of the Urracá Formation (1.2–0.8 Ma), and (6) Hill Point Member of the Urracá Formation (1.2–0.8 Ma). Over 100 coral species occur in the six units, with faunal assemblages ranging from less than 10% extant taxa (Valiente Formation) to over 85% extant taxa (Ground Creek Member). The collections provide new temporal constraints on the emergence of modern Caribbean reefs, with the La Gruta Member containing the earliest occurrence of large monospecific stands of the dominant Caribbean reef coral Acropora palmata, and the Urracá Formation containing the last fossil occurrences of 15 regionally extinct taxa. Canonical correspondence analysis of 41 Late Miocene to Recent reef coral assemblages from the Caribbean region suggests changes in community structure coincident with effective oceanic closure of the Central American Seaway (~3.5 Ma). These changes, including increased Acropora dominance, may have contributed to a protracted period of elevated extinction debt prior to the major peak in regional coral extinctions (~2–1 Ma).     

Growth forms and palaeoenvironmental interpretation of stromatoporoids in a Middle Devonian reef, southern Morocco (west Sahara)

Growth forms of well-preserved stromatoporoids, including genera Actinostroma, Stachyodes, and Stromatopora, are described for the first time from the Devonian Sabkhat Lafayrina reef complex of southern Morocco (west Sahara), one of the best exposed Middle-Devonian stromatoporoid-dominated fossil reefs. Three facies types representing the well illuminated fore-reef, reef-core and transition to back-reef facies display the distribution and growth of stromatoporoids in a high latitude setting at 40–50° south of the palaeoequator. Stromatoporoids are largely in growth position and reflect the well-preserved reef architecture. Although outcrops are low topography, the reef's prominent profile is indicated by presence of spur and groove form and a clearly defined reef margin. Stromatoporoids are mostly laminar and domical forms, with little evidence of ragged margins, and indicate normal turbulence shallow waters, with low sediment deposition.