Bolbometopon Research Articles

The world’s largest parrotfish has slow growth and a complex reproductive ecology

The bumphead parrotfish (Bolbometopon muricatum) is an iconic coral reef species of commercial, subsistence, and cultural value that has faced severe declines across the Indo-Pacific. In this study, we summarized the age-based biological characteristics of B. muricatum based on comprehensive surveys of a small-scale but high-yield fishery in Solomon Islands. We examined the full breadth of the life history, including pelagic larval duration, growth patterns throughout the ontogeny (post-settlement, juvenile, and adult), life span, mortality, age at maturity, and reproductive timing, as well as the size-dependent relative contribution of females to overall reproductive effort. The age-based demographic information supports a sexual pattern of functional gonochorism, whereby sex ratios were consistent throughout the lifespan. After a 25-day pelagic larval duration, the species growth pattern is comparatively slow and differs by sex, where males generally reach larger sizes at a given age than females. This growth pattern is associated with a long life span (at least 30 yrs) and low mortality rates (< 0.2 yr−1). Annual and lunar tracking of ovary weights confirmed cyclical spawning activity synchronized just prior to new moon throughout the year. Surprisingly, ovary weights declined in the largest and oldest females, implying lower reproductive output. Instead, lower ovary weights may reflect alternative mating strategies among the largest females whereby spawning frequency and strategy differs among females of different body sizes. These results highlight several novel and previously unknown aspects of this species' biology, and our analyses generate information that can strengthen population models, facilitate stock assessments, support regional management, and provide a baseline for comparative work.

Mass spawning aggregation of the giant bumphead parrotfish Bolbometopon muricatum

The present study reports a previously undocumented mass spawning aggregation and group spawning phenomena of c. 1200 individual bumphead parrotfish Bolbometopon muricatum in Palau, Micronesia. Although B. muricatum are protected in Palau, it is further recommended that management strategies should consider establishment of no-take zones at B. muricatum spawning aggregations and concomitant sleeping grounds elsewhere.

Logging degrades nursery habitat for an iconic coral reef fish

The loss of nursery habitats is widely believed to contribute disproportionally to declines in abundance and productivity of fish populations. However, it has been difficult to establish links between the processes threatening nurseries and changes in population demography. Here we show that juvenile bumphead parrotfish (Bolbometopon muricatum), an iconic coral reef species that is globally threatened, depend on a highly specific micro-habitat that is vulnerable to sedimentation from logging operations. We conducted surveys on fringing reefs in Solomon Islands. Surveys covered reefs around an island that has been selectively logged, and an island where there has been no logging. B. muricatum juveniles were restricted to shallow lagoonal reefs that fringed mangrove forested shorelines and had a high proportion of live branching corals, with the smallest settlers found in Acropora aspera and Acropora micropthalma colonies that were occupied by damselfish. Statistical path models indicated a 24 times decline in juvenile abundance near logging operations due to the mediating effect of habitat loss, and a possible direct effect of sedimentation on abundance. Our study shows that sedimentation can pose a significant threat to near-shore coral reef fish and highlights the role of nursery habitats in sustaining recruitment to reef fish populations.

Complete mitochondrial genome sequence for the green humphead parrotfish Bolbometopon muricatum

Here we describe the complete mitochondrial genome sequence of humphead parrotfish, Bolbometopon muricatum. The circle genome (16,788 bp) consists of 13 protein coding, 22 tRNA, 2 rRNA genes and 1 control region. Generally it has the typical vertebrate mitochondrial gene arrangement but for the relative positions of the tRNAIle, tRNAGln, and tRNAMet, and a tRNAMet psuedogene was detected. This work provides fundamental molecular data which will be useful for species identification, forensic genetics and further researches on genetic diversity and conservation of this vulnerable marine fish.

Patterns of Coral-Reef Finfish Species Disappearances Inferred from Fishers' Knowledge in Global Epicentre of Marine Shorefish Diversity.

In the Philippines, very high fishing pressure coincides with the globally greatest number of shorefish species, yet no long-term fisheries data are available to explore species-level changes that may have occurred widely in the most species rich and vulnerable marine ecosystem, namely coral reefs. Through 2655 face-to-face interviews conducted between August 2012 and July 2014, we used fishers’ recall of past catch rates of reef-associated finfish to infer species disappearances from catches in five marine key biodiversity areas (Lanuza Bay, Danajon Bank, Verde Island Passage, Polillo Islands and Honda Bay). We modeled temporal trends in perceived catch per unit effort (CPUE) based on fishers’ reports of typical good days’ catches using Generalized Linear Mixed Modelling. Fifty-nine different finfish disappeared from catches between the 1950s and 2014; 42 fish were identified to species level, two to genus, seven to family and eight to local name only. Five species occurring at all sites with the greatest number of fishers reporting zero catches were the green bumphead parrotfish (Bolbometopon muricatum), humphead wrasse (Cheilinus undulatus), African pompano (Alectis ciliaris), giant grouper (Epinephelus lanceolatus) and mangrove red snapper (Lutjanus argentimaculatus). Between the 1950s and 2014, the mean perceived CPUE of bumphead parrotfish declined by 88%, that of humphead wrasse by 82%, African pompano by 66%, giant grouper by 74% and mangrove red snapper by 64%. These declines were mainly associated with excess and uncontrolled fishing, fish life-history traits like maximum body size and socio-economic factors like access to market infrastructure and services, and overpopulation. The fishers’ knowledge is indicative of extirpations where evidence for these losses was otherwise lacking. Our models provide information as basis for area-based conservation and regional resource management particularly for the more vulnerable, once common, large, yet wide-ranging reef finfish species.

Hyperstability masks declines in bumphead parrotfish (Bolbometopon muricatum) populations

Bolbometopon muricatum, the largest species of parrotfish, is a functionally important species that is characterised by the formation of aggregations for foraging, reproductive, and sleeping behaviours. Aggregations are restricted to shallow reef habitats, the locations of which are often known to local fishers. Bolbometopon muricatum fisheries are therefore vulnerable to overfishing and are likely to exhibit hyperstability, the maintenance of high catch per unit effort (CPUE) while population abundance declines. In this study, we provide a clear demonstration of hyperstable dynamics in a commercial B. muricatum fishery in Isabel Province, Solomon Islands. Initially, we used participatory mapping to demarcate the Kia fishing grounds into nine zones that had experienced different historic levels of fishing pressure. We then conducted comprehensive underwater visual census (UVC) and CPUE surveys across these zones over a 21-month period in 2012-2013. The individual sites for replicate UVC surveys were selected using a generalised random tessellation stratified variable probability design, while CPUE surveys involved trained provincial fisheries officers and local spearfishers. A comparison of fishery-independent abundance data and fishery-dependent CPUE data indicate extreme hyperstability, with CPUE maintained as B. muricatum abundance declines towards zero. Hyperstability may explain the sudden collapses of many B. muricatum spear fisheries across the Pacific and highlights the limitations of using data-poor fisheries assessment methods to evaluate the status of commercially valuable coral reef fishes that form predicable aggregations.

Spawning aggregation behavior and reproductive ecology of the giant bumphead parrotfish, Bolbometopon muricatum, in a remote marine reserve.

The giant bumphead parrotfish (Bolbometopon muricatum) has experienced precipitous population declines throughout its range due to its importance as a highly-prized fishery target and cultural resource. Because of its diet, Bolbometopon may serve as a keystone species on Indo-Pacific coral reefs, yet comprehensive descriptions of its reproductive ecology do not exist. We used a variety of underwater visual census (UVC) methods to study an intact population of Bolbometopon at Wake Atoll, a remote and protected coral atoll in the west Pacific. Key observations include spawning activities in the morning around the full and last quarter moon, with possible spawning extending to the new moon. We observed peaks in aggregation size just prior to and following the full and last quarter moon, respectively, and observed a distinct break in spawning at the site that persisted for four days; individuals returned to the aggregation site one day prior to the last quarter moon and resumed spawning the following day. The mating system was lek-based, characterized by early male arrival at the spawning site followed by vigorous defense (including head-butting between large males) of small territories. These territories were apparently used to attract females that arrived later in large schools, causing substantial changes in the sex ratio on the aggregation site at any given time during the morning spawning period. Aggression between males and courtship of females led to pair spawning within the upper water column. Mating interference was not witnessed but we noted instances suggesting that sperm competition might occur. Densities of Bolbometopon on the aggregation site averaged 10.07(±3.24 SE) fish per hectare (ha) with maximum densities of 51.5 fish per ha. By comparing our observations to the results of biennial surveys conducted by the National Oceanic and Atmospheric Administration (NOAA) Coral Reef Ecosystem Division (CRED), we confirmed spatial consistency of the aggregation across years as well as a temporal break in spawning activity and aggregation that occurred during the lunar phase. We estimated the area encompassed by the spawning aggregation to be 0.72 ha, suggesting that spawning site closures and temporal closures centered around the full to the new moon might form one component of a management and conservation plan for this species. Our study of the mating system and spawning aggregation behavior of Bolbometopon from the protected, relatively pristine population at Wake Atoll provides crucial baselines of population density, sex ratio composition, and productivity of a spawning aggregation site from an oceanic atoll. Such information is key for conservation efforts and provides a basic platform for the design of marine protected areas for this threatened iconic coral reef fish, as well as for species with similar ecological and life history characteristics.

Refined bomb radiocarbon dating of two iconic fishes of the Great Barrier Reef

Refinements to the methodology of bomb radiocarbon dating made it possible to validate age estimates of the humphead wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum). Age for these species has been estimated from presumed annual growth zones in otoliths at ~30 and ~40 years respectively. The validity of these estimates was tested using bomb radiocarbon dating on the small and fragile otoliths of these species, and provided an opportunity to refine the method using advanced technologies. A regional Δ14C reference record from hermatypic coral cores from the Great Barrier Reef was assembled and Δ14C measurements from extracted otolith cores of adult otoliths were successful. Validated ages supported the accuracy of growth zone derived ages using sectioned sagittal otoliths.

Isolation and characterization of 29 microsatellite markers for the bumphead parrotfish, Bolbometopon muricatum, and cross amplification in 12 related species

We isolated and characterized 29 microsatellite loci for the bumphead parrotfish, Bolbometopon muricatum, a wide-ranging parrotfish listed as vulnerable by the International Union for Conservation of Nature (IUCN). The 29 loci were tested on 95 individuals sampled from the Solomon Islands. The number of alleles ranged from two to ten. Evidence of linkage disequilibrium was found for only one pair of loci (Bm54 and Bm112). Two loci (Bm20 and Bm119) showed significant departure from Hardy-Weinberg equilibrium. We also tested each locus for amplification and polymorphism on 11 other scarine labrid species and one labrid species. Amplification success ranged from zero to ten loci per species. These microsatellite loci are the first specific set for B. muricatum and will be a useful tool for assessing genetic population structure, genetic diversity, and parentage in future studies.

An update to the list of coral reef fishes from Koh Tao, Gulf of Thailand

Twenty-one species are reported for the first time from Koh Tao (Turtle Island) in the Gulf of Thailand. Information and photographs were obtained from local scuba divers in order to census rare ( i.e. , cryptic species or transient species only present during one season) or not previously recorded fish species living on or near coral reefs from the area. This is the first time that species belonging to the families Antennariidae (genera Antennatus and Histrio ), Ophichthyidae (genus Callechelys ), Platycephalidae (genus Thysanophrys ), Plotosidae (genus Plotosus ) and Synanceiidae (genera Inimicus and Synanceia ), and reef-fish genera of several families ( Pseudobalistes, Balistidae; Cyclichthys, Diodontidae; Bolbometopon, Scaridae; and Hippocampus, Syngnathidae), among others, have been recorded in Koh Tao. Of the 21 species reported for the first time from Koh Tao, 7 species ( Antennatus nummifer (Antennariidae), Pseudobalistes marginatus (Balistidae), Monacanthus chinensis (Monacanthidae), Callechelys marmorata (Ophichthyidae), Thysnophrys cf. chiltonae (Platycephalidae), Bolbometopon muricatum (Scaridae) and Synanceia cf. verrucosa (Synanceidae)) are new records for the Gulf of Thailand. To date, 223 species of coral reef fishes belonging to 53 families are known from Koh Tao, including the species found in the present study.

Positive and negative effects of a threatened parrotfish on reef ecosystems.

Species that are strong interactors play disproportionately important roles in the dynamics of natural ecosystems. It has been proposed that their presence is necessary for positively shaping the structure and functioning of ecosystems. We evaluated this hypothesis using the case of the world's largest parrotfish (Bolbometopon muricatum), a globally imperiled species. We used direct observation, animal tracking, and computer simulations to examine the diverse routes through which B. muricatum affects the diversity, dispersal, relative abundance, and survival of the corals that comprise the foundation of reef ecosystems. Our results suggest that this species can influence reef building corals in both positive and negative ways. Field observation and simulation outputs indicated that B. muricatum reduced the abundance of macroalgae that can outcompete corals, but they also feed directly on corals, decreasing coral abundance, diversity, and colony size. B. muricatum appeared to facilitate coral advancement by mechanically dispersing coral fragments and opening up bare space for coral settlement, but they also damaged adult corals and remobilized a large volume of potentially stressful carbonate sediment. The impacts this species has on reefs appears to be regulated in part by its abundance-the effects of B. muricatum were more intense in simulation scenarios populated with high densities of these fish. Observations conducted in regions with high and low predator (e.g., sharks) abundance generated results that are consistent with the hypothesis that these predators of B. muricatum may play a role in governing their abundance; thus, predation may modulate the intensity of the effects they have on reef dynamics. Overall our results illustrate that functionally unique and threatened species may not have universally positive impacts on ecosystems and that it may be necessary for environmental managers to consider the diverse effects of such species and the forces that mediate the strength of their influence.

Incorporating Surrogate Species and Seascape Connectivity to Improve Marine Conservation Outcomes

Conservation focuses on maintaining biodiversity and ecosystem functioning, but gaps in our knowledge of species biology and ecological processes often impede progress. For this reason, focal species and habitats are used as surrogates for multispecies conservation, but species-based approaches are not widely adopted in marine ecosystems. Reserves in the Solomon Islands were designed on the basis of local ecological knowledge to conserve bumphead parrotfish (Bolbometopon muricatum) and to protect food security and ecosystem functioning. Bumphead parrotfish are an iconic threatened species and may be a useful surrogate for multispecies conservation. They move across tropical seascapes throughout their life history, in a pattern of habitat use that is shared with many other species. We examined their value as a conservation surrogate and assessed the importance of seascape connectivity (i.e., the physical connectedness of patches in the seascape) among reefs, mangroves, and seagrass to marine reserve performance. Reserves were designed for bumphead parrotfish, but also enhanced the abundance of other species. Integration of local ecological knowledge and seascape connectivity enhanced the abundance of 17 other harvested fish species in local reserves. This result has important implications for ecosystem functioning and local villagers because many of these species perform important ecological processes and provide the foundation for extensive subsistence fisheries. Our findings suggest greater success in maintaining and restoring marine ecosystems may be achieved when they are managed to conserve surrogate species and preserve functional seascape connections.

Coexistence of Low Coral Cover and High Fish Biomass at Farquhar Atoll, Seychelles

We report a reef ecosystem where corals may have lost their role as major reef engineering species but fish biomass and assemblage structure is comparable to unfished reefs elsewhere around the world. This scenario is based on an extensive assessment of the coral reefs of Farquhar Atoll, the most southern of the Seychelles Islands. Coral cover and overall benthic community condition at Farquhar was poor, likely due to a combination of limited habitat, localized upwelling, past coral bleaching, and cyclones. Farquhar Atoll harbors a relatively intact reef fish assemblage with very large biomass (3.2 t ha−1) reflecting natural ecological processes that are not influenced by fishing or other local anthropogenic factors. The most striking feature of the reef fish assemblage is the dominance by large groupers, snappers, and jacks with large (>1 m) potato cod (Epinephelus tukula) and marbled grouper (E. polyphekadion), commonly observed at many locations. Napoleon wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum) are listed as endangered and vulnerable, respectively, but were frequently encountered at Farquhar. The high abundance and large sizes of parrotfishes at Farquhar also appears to regulate macroalgal abundance and enhance the dominance of crustose corallines, which are a necessary condition for maintenance of healthy reef communities. Overall fish biomass and biomass of large predators at Farquhar are substantially higher than other areas within the Seychelles, and are some of the highest recorded in the Indian Ocean. Remote islands like Farquhar Atoll with low human populations and limited fishing pressure offer ideal opportunities for understanding whether reefs can be resilient from global threats if local threats are minimized.

LC-MS/MS analysis of palytoxin analogues in blue humphead parrotfish Scarus ovifrons causing human poisoning in Japan

Since 1953, a total of 27 human poisoning cases caused by the consumption of blue humphead parrotfish, Scarus ovifrons, have been reported in Japan. Characteristic symptoms are severe muscle pain associated with rhabdomyolysis. Although it is believed that palytoxin, which is one of the most potent non-protein marine biotoxins, is the most likely causative toxin in blue humphead parrotfish poisoning, palytoxin has not been proven conclusively as the causative toxin because of lack of a reliable and sensitive analytical method for palytoxin. In 2011, human poisoning cases caused by the consumption of blue humphead parrotfish occurred in Miyazaki and Tokyo. In our present study, an LC-MS/MS method for palytoxin and its analogues in the blue humphead parrotfish samples causing the human poisoning cases in 2011 was developed and the samples were analysed by using the newly developed LC-MS/MS method. Palytoxin and its analogues were not detected in the samples from the food poisoning cases. The LC-MS/MS findings therefore do not support the recently accepted hypothesis that palytoxin is the causative agent in blue humphead parrotfish poisoning in Japan.

The IUCN Red List of Threatened Species: an assessment of coral reef fishes in the US Pacific Islands

Widespread declines among many coral reef fisheries have led scientists and managers to become increasingly concerned over the extinction risk facing some species. To aid in assessing the extinction risks facing coral reef fishes, large-scale censuses of the abundance and distribution of individual species are critically important. We use fisheries-independent data collected as part of the NOAA Pacific Reef Assessment and Monitoring Program from 2000 to 2009 to describe the range and density across the US Pacific of coral reef fishes included on The International Union for the Conservation of Nature’s (IUCN) 2011 Red List of Threatened Species. Forty-five species, including sharks, rays, groupers, humphead wrasse (Cheilinus undulatus), and bumphead parrotfish (Bolbometopon muricatum), included on the IUCN List, were recorded in the US Pacific Islands. Most species were generally rare in the US Pacific with the exception of a few species, principally small groupers and reef sharks. The greatest diversity and densities of IUCN-listed fishes were recorded at remote and uninhabited islands of the Pacific Remote Island Areas; in general, lower densities were observed at reefs of inhabited islands. Our findings complement IUCN assessment efforts, emphasize the efficacy of large-scale assessment and monitoring efforts in providing quantitative data on reef fish assemblages, and highlight the importance of protecting populations at remote and uninhabited islands where some species included on the IUCN Red List of Threatened Species can be observed in abundance.

Extraordinary Aggressive Behavior from the Giant Coral Reef Fish, Bolbometopon muricatum, in a Remote Marine Reserve

Human impacts to terrestrial and marine communities are widespread and typically begin with the local extirpation of large-bodied animals. In the marine environment, few pristine areas relatively free of human impact remain to provide baselines of ecosystem function and goals for restoration efforts. Recent comparisons of remote and/or protected coral reefs versus impacted sites suggest remote systems are dominated by apex predators, yet in these systems the ecological role of non-predatory, large-bodied, highly vulnerable species such as the giant bumphead parrotfish (Bolbometopon muricatum) has received less attention. Overfishing of Bolbometopon has lead to precipitous declines in population density and avoidance of humans throughout its range, contributing to its status as a candidate species under the U. S. Endangered Species Act and limiting opportunities to study unexploited populations. Here we show that extraordinary ecological processes, such as violent headbutting contests by the world’s largest parrotfish, can be revealed by studying unexploited ecosystems, such as the coral reefs of Wake Atoll where we studied an abundant population of Bolbometopon. Bolbometopon is among the largest of coral reef fishes and is a well known, charismatic species, yet to our knowledge, no scientific documentation of ritualized headbutting exists for marine fishes. Our observations of aggressive headbutting by Bolbometopon underscore that remote locations and marine reserves, by inhibiting negative responses to human observers and by allowing the persistence of historical conditions, can provide valuable opportunities to study ecosystems in their natural state, thereby facilitating the discovery, conservation, and interpretation of a range of sometimes remarkable behavioral and ecological processes.

Commercial coral-reef fisheries across Micronesia: A need for improving management

A dearth of scientific data surrounding Micronesia’s coral-reef fisheries has limited their formal assessment and continues to hinder local and regional management efforts. We approach this problem by comparing catch-based datasets from market landings across Micronesia to evaluate fishery status in the Commonwealth of the Northern Mariana Islands (CNMI), Guam, Yap, and Pohnpei. Initial examinations found that calm weather and low lunar illumination predicted between 6% (Yap) and 30% (CNMI) of the variances in daily commercial landings. Both environmentally driven catch success and daily catch variability increased in accordance with reef-fish demand indices. Subsequent insight from species composition and size-at-capture data supported these findings, highlighting reduced trophic levels and capture sizes where higher human-population-per-reef-area existed. Among the 12–15 target species and/or species complexes that accounted for 70% of the harvest biomass, capture sizes were consistently smallest for CNMI and Guam, often below the reported mean reproductive sizes. Comparatively, Pohnpei has the greatest potential for reef fisheries, with a large reef area (303 km2) and a moderate human population (34,000 people). However, the estimated harvest volume of 476 mt year−1 was 8–9 times higher than other jurisdictions. Even on Yap where the reef-fish demand index was lowest (67.7 people km−2 reef habitat), many target fish were harvested below their mean reproductive sizes, including the iconic green bumphead parrotfish and humphead wrasse, as well as several other herbivores. We discuss our results with respect to the contemporary doctrine surrounding size-spectra, catch composition, and catch frequencies that afford insight into fishery pressure and status. We posit that regional catch-based policies (initially) instituted at the market level, combined with area and gear-based restrictions, represent plausible vectors for improving Micronesian fisheries.

Dangerous demographics: the lack of juvenile humphead parrotfishes Bolbometopon muricatum on the Great Barrier Reef

The humphead parrotfish, Bolbometopon muricatum, the largest of all parrotfish species, is heavily fished throughout most of its range. In remote and heavily protected locations, such as the Great Barrier Reef (GBR), it is a major component of parrotfish biomass and plays a critical role in ecosystem processes. However, extensive surveys of GBR populations have revealed a striking lack of juveniles. Of 633 individuals censused, just four were juveniles. This represents 0.6% juveniles and contrasts markedly with the 20.2–40.2% juveniles recorded in eight other medium to large parrotfish species. These low values in Bolbometopon are corroborated by over 5,000 h of independent observations and extensive museum collections. Whilst there is no evidence to suggest that this is an extraordinary new condition for GBR Bolbometopon, it may nevertheless expose them to special risks in a changing and unpredictable world. Despite excellent management on the GBR, Bolbometopon populations may be more vulnerable than previously thought.

Cowfish (Umisuzume, Lactoria diaphana) Poisoning with Rhabdomyolysis

A 40-year-old man developed weakness and myalgia of the shoulders and brachia nine hours after eating a cowfish (Umisuzume, Lactoria diaphana). A clinical symptom showed rhabdomyolysis and serum creatine phosphokinase was elevated to 180,000 IU/L on day 3. Cardiopulmonary arrest and acute renal failure developed after 59 hours and hemodiafiltration was performed. Cerebral death was diagnosed on day 9 and the patient died on day 16. The case has the characteristic clinical course of palytoxin poisoning, which has also been reported as blue humphead parrotfish poisoning from other kinds of fish.

Sexual development and reproductive demography of the green humphead parrotfish (Bolbometopon muricatum) in the Solomon Islands

An investigation of the reproductive biology of the green humphead parrotfish (Bolbometopon muricatum) from three areas in the Western Province of the Solomon Islands revealed that B. muricatum exhibits several features that differ from the pattern of reproductive development observed in most parrotfishes. Unlike most parrotfishes, histological evidence suggests that the sexual pattern of B. muricatum is essentially gonochoristic with high incidences of anatomical but non-functional hermaphroditism. B. muricatum also differs from other parrotfishes in that all males pass through an immature female (or bisexual) phase as demonstrated by all adult testis retaining the ex-ovarian lumen and peripheral sperm sinuses in the gonad wall. However, a protogynous diandric reproductive strategy cannot be excluded given that sampling may have missed transitional individuals. Marked variation in the demography of male B. muricatum between the three locations examined is considered to reflect variation in historical fishing effort.