Daily Rules, Proposed Rules, and Notices of the Federal Government
On January 4, 2010, we received a petition from WildEarth Guardians to list the bumphead parrotfish (
On April 2, 2010, we published a 90-day finding with our determination that the petition presented substantial scientific and commercial information indicating that the petitioned action may be warranted (75 FR 16713). We initiated a comprehensive status review of bumphead parrotfish to determine if the species warrants listing under the ESA. The 90-day finding requested scientific and commercial information from the public to inform a status review of the species. We received ten public responses to the 90-day Finding; the information we received was considered in the comprehensive status review as described below in the Biological Review section. The status review of bumphead parrotfish was completed jointly by our Pacific Islands Fisheries Science Center (PIFSC) and Pacific Islands Regional Office (PIRO). A Bumphead Parrotfish Biological Review Team (BRT) comprising Federal scientists from the Hawaii Cooperative Fishery Research Unit of the United States Geological Survey, and our Southwest and Pacific Islands Fisheries Science Centers completed a biological report on the species (hereafter “BRT Report”, cited as Kobayashi
We are responsible for determining whether the bumphead parrotfish is threatened or endangered under the ESA (16 U.S.C. 1531
For the first step, the BRT completed a biological review of the taxonomy, distribution, abundance, life history and biology of the species (Kobayashi
For the second step, we assessed threats affecting the species' status. We did this by following guidance in the ESA that requires us to determine whether any species is endangered or threatened due to any of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence (sections 4(a)(1)(A) through (E)). The BRT Report examined factors A, B, C, and E (Kobayashi
For the third step, we completed an extinction risk analysis to determine the status of the species. We asked the BRT to develop an extinction risk analysis approach based on the best available information for bumphead parrotfish. Extinction risk results in Kobayashi
For the fourth step, results of the biological review, threats evaluation, and extinction risk analysis are considered to determine whether the bumphead parrotfish qualifies for threatened or endangered status. Section 3 of the ESA defines an endangered species as “any species which is in danger of extinction throughout all or a significant portion of its range” and a threatened species as one “which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” Thus, in the context of the ESA, the Services interpret an “endangered species” to be one that is presently at risk of extinction. A “threatened species,” on the other hand, is not currently at risk of extinction but is likely to become so. In other words, a key statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either now (endangered) or within the foreseeable future (threatened). Thus, a species may be listed as threatened if it is likely to become in danger of extinction throughout all or a significant portion of its range within the foreseeable future.
Whether a species is ultimately protected as endangered or threatened depends on the specific life history and ecology of the species, the nature of threats, the species' response to those threats, and population numbers and trends. In determining whether the species meets the standard of endangered or threatened, we must consider each of the threats identified, both individually and cumulatively. For purposes of our analysis, the mere identification of factors that could impact a species negatively is not sufficient to compel a finding that ESA listing is appropriate. In considering those factors that might constitute threats, we look beyond mere exposure of the species to the factor to determine whether the species responds, either to a single threat or multiple threats in combination, in a way that causes actual impacts at the species level. In making this finding, we have considered and evaluated the best available scientific and commercial information, including information received in response to our 90-day finding.
This section provides a summary of the BRT Report (Kobayashi
The two remaining comments contained information pertinent to existing regulatory mechanisms throughout bumphead parrotfish range. This information was provided to the staff compiling the management report. Following are summaries of key biological information presented in Kobayashi
The bumphead parrotfish is a member of a conspicuous group of shallow-water fishes (parrotfishes in the family Scaridae, order Perciformes) that are closely associated with coral reefs (Bellwood, 1994; Randall
The bumphead parrotfish is the largest member of the parrotfishes, growing to at least 110 cm total length (TL) (Kobayashi
English common names include buffalo parrotfish, bumphead parrotfish, double-headed parrotfish, giant humphead parrotfish, green humphead parrotfish, and humphead parrotfish. Non-English common names in the Pacific include: Lendeke, Kitkita, Topa, Topa kakara, Perroquet bossu vert, Togoba, Uloto'i, Gala Uloto'i, Laea Uloto'i, Loro cototo verde, Berdebed, Kalia, Kemedukl, Kemeik, and Tanguisson. Several of these names are a reflection of the different size ranges of the fish used within a society (Adams and Dalzell, 1994; ASFIS, 2010; Aswani and Hamilton, 2004; Hamilton, 2004; Hamilton
Currently, there is no population genetic information on bumphead parrotfish. Regional variation in morphology, meristics, coloration, or behavior has not been observed. Based on modeling of pelagic egg and larvae transport, the species likely has an interconnected population structure throughout its current range, with the possible exception of both the eastern and western edges of the current range (Kobayashi
One year of current data (2009) was chosen for use in the pelagic transport simulation; although some interannual variability exists in ocean currents, PIFSC data available at Oceanwatch (
Adult bumphead parrotfish are found primarily on shallow (1-15 m) barrier and fringing reefs during the day and rest in caves and shallow sandy lagoon habitats at night (Donaldson and Dulvy, 2004). Extensive reef structures on the Great Barrier Reef off the east coast of Australia with adjacent lagoons appear to provide an example of optimal habitat for bumphead parrotfish (Choat, personal communication). Lihou and Herald are two isolated islands in the Coral Sea approximately 1000 km from the Great Barrier Reef with little fishing pressure. Densities of bumphead parrotfish are over an order of magnitude higher on the Great Barrier Reef compared with these two island locations (see Figure 3 in Kobayashi
Based on limited information, juvenile bumphead parrotfish habitat is thought to consist mainly of mangrove swamps, seagrass beds, coral reef lagoons, and other benthic habitats that provide abundant cover (Kobayashi
Bumphead parrotfish are found in 45 countries in the Indo-Pacific as well as disputed areas in the South China Sea. The BRT divided this range into 63 strata, which are primarily country specific, but include subsections or regions within countries in some cases. Certain geographic strata are in or near the overall range polygon, but are not known to have bumphead parrotfish (e.g., Hawaii, Johnston Atoll, Cook Islands, Tokelau, Nauru, British Indian Ocean Territory, etc.). Although data are limited, we found no evidence to conclude that historical range was significantly different from current range. We therefore conclude that the historical and current ranges are equivalent (Kobayashi
The bumphead parrotfish is thought to have been abundant throughout its range historically (Dulvy and Polunin, 2004). Numerous reports suggest that fisheries exploitation has reduced local densities to a small fraction of their historical values in populated or fished areas (Bellwood
Densities of bumphead parrotfish in the Indian Ocean show a biogeographic density gradient with the highest densities adjacent to the western Australian coast, and densities decreasing to the west (Choat, unpublished data; see Figure 9 in Kobayashi
Surveys conducted by the Secretariat of the Pacific Community (SPC) in their Pacific Regional Oceanic and Coastal Fisheries project in 2001-2008 revealed relatively high numbers of bumphead parrotfish in Palau with slightly more than 1.5 individuals per station. Numbers in New Caledonia were approximately half of those observed in Palau. Sites in Papua New Guinea and the Federated States of Micronesia also recorded modest numbers of individuals. Low numbers in Tonga, Fiji, and the Solomon Islands may reflect fishing pressure (e.g., Dulvey and Polunin, 2004; Hamilton, 2004), while their absence from a number of locations is likely the result of the lack of suitable lagoon habitats for recruitment (i.e., Niue, Nauru) (Kobayashi
In the U.S. Pacific Islands, abundance of bumphead parrotfish has been assessed since 2000 as part of PIFSC's Reef Assessment and Monitoring Program. Bumphead parrotfish were most abundant at Wake Atoll in the Pacific Remote Island Areas (PRIAs) (∼300 fish per km
In summary, the abundance of bumphead parrotfish varies widely. Sites where bumphead parrotfish are found in abundance (densities as high as 300 fish per km
The BRT Report warns that “There are inadequate data on bumphead parrotfish population dynamics, demography, and temporal/spatial variability to use even the most rudimentary of stock assessment models. The data simply do not exist to allow one to credibly estimate changes in population size, or even the magnitude of population size, structured over space and time in a proper framework of metapopulation dynamics and demographics” for bumphead parrotfish. The BRT used the best available information on population density from recent (1997-2009) survey data to develop contemporary global estimates of adult bumphead parrotfish abundance. Contemporary global population estimates are based on the geographic range of bumphead parrotfish, amount of suitable adult bumphead parrotfish habitat within its range, and the density of adult bumphead parrotfish within the habitat. Population density data were available for 49 of 63 of the strata from SPC and ReefCheck underwater visual surveys. They then used a bootstrap resampling simulation approach to estimate global population density by randomly assigning from the actual density estimates one estimate to each stratum in each simulation model iteration (Kobayashi
The BRT used the bootstrap modeling approach to develop three estimates of global abundance: (1) A “regular-case” estimate based on the methods described above and resulting in a best estimate of 3.9 million adults (95 percent confidence interval = 69,000-61,000,000 adults); (2) a “worst-case” estimate which decreased the estimated amount of available habitat and resulted in an abundance estimate of 2.2 million adults (95 percent confidence interval = 28,000-36,000,000 adults); and (3) a “matched-case” estimate where density estimates for the 49 strata where surveys had occurred were based on those survey data, and estimates for the other 13 strata were based on the randomization process used in the “regular-case” estimate. This third method resulted in an estimated abundance of 4.6 million adults (95 percent confidence interval = 17,000-67,000,000 adults). The BRT concluded, and we agree, that the regular-case estimate provides the most reliable estimate of current global abundance of bumphead parrotfish. However, all models involved large confidence intervals, and high uncertainty is associated with all three estimates. Accordingly, all population estimates are to be interpreted with caution.
Anecdotal accounts abound of past abundance and recent declines of bumphead parrotfish in many parts of its range (see literature cited in Kobayashi
The BRT states that “the estimates of virgin abundance and related inferences about degree of population reduction are highly speculative and subject to a great deal of uncertainty” (Kobayashi
In order to quantitatively predict likely future global abundance trends for adult bumphead parrotfish, spatially-explicit data on current and projected levels of the various threats to bumphead parrotfish for each strata would need to be incorporated into a population model because these threats are variable throughout the species range (e.g., some strata are unfished, some strata are heavily fished, some strata may be trending independently of human impact). These data are not currently available so we cannot reliably quantify how trends in current and future human activities and other threats will impact the population into the future. The BRT was not able to estimate future population trends by strata, and accordingly, did not attempt a future projection. As such, we conclude that future global population trends for adult bumphead parrotfish are unquantifiable at this time. However, based on the information provided in the BRT Report (Kobayashi
The bumphead parrotfish appears to have a reasonably well-characterized growth curve and approaches its maximum size at approximately 10-20 years of age with a longevity estimated at approximately 40 years. Most individuals seen in adult habitat are likely older than approximately 5 years (Kobayashi
Data collected in the western Solomon Islands suggest differential growth between sexes for bumphead parrotfish. Studies indicate that males attain a larger asymptotic size than females and growth is slow but continuous throughout life. In contrast, females exhibit more determinate growth characteristics with asymptotic size established at around age 15 years (Hamilton, 2004).
Age and growth characteristics of juvenile bumphead parrotfish are less well known than those of adults. Pelagic larval duration was estimated at 31 days using pre-transitional otolith increments from just one specimen (Brothers and Thresher, 1985).
The average size of individual bumphead parrotfish observed from SPC surveys was 59.7 cm TL (SD = 20.8), with the largest individual being 110 cm and the smallest being 14 cm. Notable size differences were observed at different locations. These size differences could reflect variable habitat-related growth conditions, recruitment problems, or some level of population structure, but more likely reflect differences in the intensity of harvest and the degree to which size structure of populations has been truncated (Kobayashi
Parrotfishes as a family are primarily considered herbivores. A majority of
Bumphead parrotfish are classified as excavators feeding on a variety of benthic organisms including corals, epilithic algae, sponges, and other microinvertebrates (Bellwood
Bumphead parrotfish show little evidence of feeding selectivity; however, a significant portion (up to 50 percent) of their diet consists of live coral (Bellwood and Choat, 1990; Bellwood
Adult bumphead parrotfish movement patterns are distinct between day and night. Diurnal movement patterns are characterized by groups of individuals foraging among forereef, reef flat, reef pass, and clear outer lagoon habitats at depths of 1-30 m (Donaldson and Dulvy, 2004). The bumphead parrotfish is a gregarious species that can be observed foraging during the day in schools of 20 to more than 100 individuals (Gladstone, 1986; Bellwood
Dispersal of bumphead parrotfish occurs primarily by passive dispersal of pelagic fertilized eggs and larvae. Many details of the early life history of the species are unknown. In other parrotfishes, eggs are pelagic, small, and spindle shaped (1.5-3 mm long and 0.5-1 mm wide; Leis and Rennis, 1983). Time to hatching is unknown, but is likely between 20 hours and 3 days, as for other reef fishes observed spawning on the shelf-edge (Colin and Clavijo, 1988). Bumphead parrotfish pelagic ecology is unknown, but successful settlement appears to be limited to shallow lagoon habitats characterized by low-energy wave action and plant life (e.g., mangroves, seagrass, or plumose algae) (Kobayashi
Connectivity in bumphead parrotfish was examined by the BRT using a computer simulation of larval transport (Kobayashi
Single-generation and multi-generation connectivity probabilities were tested. A number of sites appear to have significant potential as stepping stones with a broad range of input and output strata interconnected in a multi-generational context. Most sites with significant seeding potential are located in close proximity to other sites (e.g., east Africa, central Indo-Pacific). The BRT concluded that bumphead parrotfish likely have an interconnected population structure due to oceanographic transport of pelagic eggs
Unlike most parrotfishes which are protogynous (sequential) hermaphrodites, bumphead parrotfish appear to be gonochoristic (unisexual). Females reach sexual maturity over a broad size range. While they begin to reach sexual maturity at about 500 mm TL, 100 percent of females attain maturity by about 700 mm TL and age 11 yrs. The size at which 50 percent of females have reached maturity is estimated at 550-650 mm TL at age 7-9 yrs (Hamilton, 2004; Hamilton
Spawning may occur in most months of the year. Hamilton
Observations of spawning have involved a single male and female. In other parrotfishes, Thresher (1984) describes the establishment of temporary spawning territories by males, with females being courted by males as they passed through spawning territories, and an assemblage of individuals acting as a spawning school. Although Gladstone (1986) described a simple mobile group of bumphead parrotfish individuals from which pair spawning took place, others have described what appeared to be a dominant male spawning with females and smaller sneaker males attempting to participate in spawning. The putative dominant male displayed bright green coloration during spawning. The evidence that males grow to larger sizes than females (Hamilton, 2004) supports the existence of a nonrandom mating system where a reproductive advantage is conferred to larger dominant males (Ghiselin, 1969; Kobayashi
As with many other aspects of bumphead parrotfish biology, little is known about the processes following settlement of larvae in the benthic environment. Juveniles appear to gradually work their way towards adult habitats on the forereef areas, but timing and duration of this movement are unknown. The smallest size at which bumpheads enter the adult population on forereef areas is approximately 40 cm TL. These large juveniles are not often seen in surveys and may remain cryptic until adopting the wide-ranging swimming and foraging behavior of adults. Certain areas, for example the Great Barrier Reef, do not appear to receive significant recruitment (Bellwood and Choat, 2011). Adults on the Great Barrier Reef are thought to originate from elsewhere (north), which may explain the latitudinal trend of decreasing abundance toward southern portions of the area (Kobayashi
Despite typically low abundance, bumphead parrotfish can have a disproportionately large impact on their ecosystem as a result of their size and trophic role. Their role as non-selective, excavator feeders is likely important for maintaining species diversity of corals and other benthic organisms. For example, certain species of coral (i.e., plate-forming) and algae can quickly monopolize substrate if unchecked. Non-selective feeding prevents any one organism from dominating the benthic ecosystem. Hence the species may be a classic example of a keystone species. The role of bumphead parrotfish in bioerosion and sand generation is also of notable importance; this effect is clearly seen by the persistence of dead coral skeletons in areas where excavating herbivores have been reduced (Bellwood
There is no evidence regarding limiting factors for bumphead parrotfish population growth, particularly under pristine conditions. Some likely limiting factors for past, present, and/or future bumphead parrotfish population growth include settlement and recruitment limitation factors (Doherty, 1983; Sale, 2004), juvenile habitat, adult sleeping habitat, requisite abundance of conspecifics for successful group foraging or reproduction, and human harvest. Most of these factors are likely to become more limiting over time (Kobayashi
Threats Evaluation is the second step in the process of making an ESA listing determination for bumphead parrotfish as described above in “Listing Determinations Under the ESA”. This step follows guidance in the ESA that requires us to determine whether any species is endangered or threatened due to any of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence (sections 4(a)(1)(A) through (E)).
The BRT Report assessed 14 specific threats according to factors A, B, C, and E as follows: for factor (A), the BRT identified three threats: adult habitat loss or degradation, juvenile habitat loss or degradation, and pollution; for factor (B), the BRT assessed harvest or harvest-related adult mortality, and capture or capture-related juvenile mortality; for factor (C), the BRT identified five threats: competition, disease, parasites, predation, and starvation; and for factor (E), the BRT discussed four threats: global warming, ocean acidification, low population effect, and recruitment limitation or variability. The BRT determined the severity, scope, and certainty for these threats at three points in time—historically (40-100 years ago or as otherwise noted in the table), currently, and in the future (40-100 years from now; Kobayashi
Of the 14 threats, the BRT Report determined that five had insufficient data to determine severity, scope, or
Factor D threats (related to inadequacy of existing regulatory mechanisms), were assessed in the Management Report (NMFS, 2012). Two public comments received in response to the 90-Day Finding contained information relevant to existing regulatory mechanisms that was considered in the Management Report. One comment provided information on cultural significance, harvest methods, and the importance of Marine Protected Areas (MPAs) and remote areas with limited access that may provide refuge for the species within a narrow portion of its range. The second comment provided information pertaining to existing regulatory mechanisms in some parts of the species range and the effectiveness of MPAs in providing some benefit to the species. In the Management Report, we summarized existing regulatory mechanisms in each of the 46 areas where bumphead parrotfish occur, including fisheries regulations and MPAs. Additionally, we developed a comprehensive catalog of protected areas containing coral reef and mangrove habitat within the range of the species (NMFS 2012, Appendix A-1 and A-2) and evaluated how the MPA network addresses threats to the species (NMFS 2012, Sections 188.8.131.52-46 and 4). The Management Report authors did not determine the severity, scope, and certainty for Factor D threats at three points in time—historically, currently, and in the future—as did the BRT. They compiled information on the presence of international, national, and local scale regulations and then discussed general themes and patterns that emerged in order to assess whether the inadequacy of existing regulatory mechanisms is a factor that changes the extinction risk analysis results provided by the BRT.
Juvenile habitat loss or degradation was rated by the BRT as one of the two (along with adult harvest) most severe threats to bumphead parrotfish, rating its severity as “medium” historically and as “high” both currently and over a 40-100 year future time horizon. As described by the BRT, shallow mangrove, seagrass, and coral reef lagoon habitats are susceptible to pollution, modification, and increased harvest pressure, among other anthropogenic pressures. The juvenile habitat specificity of bumphead parrotfish highlights this phase of the life history as highly vulnerable (Kobayashi
In contrast to juvenile habitat, the BRT concluded that adult habitat loss and/or degradation is not a high priority concern, rating its severity as “medium” both currently and over a 40-100 year future time horizon (with a historical rating of low). Drastic morphological changes to coral reefs might impact bumphead parrotfish if high-energy zones were reduced or wave energy was diffused or if nocturnal resting/sleeping locations were no longer available (Kobayashi
The BRT concluded that pollution is not a high priority concern, rating its severity as “low” both historically and currently, and “medium -” over a 40-100 year future time horizon. Pollution events (e.g., oil spills) can be catastrophic to coral reef ecosystems. However, such events remain episodic, rare, and are usually localized in the context of a widely-distributed, mobile species. Habitat modification as a result of pollution is most likely to be an issue with juvenile habitat since it is more exposed to anthropogenic impacts because of proximity, shallowness, and tendency to be more contained (e.g., lagoons, as opposed to open coastal waters). The BRT Report expressed high concern about the effects of pollution on the quantity and quality of juvenile habitat, but expressed less concern about adult habitat since adult habitat is larger, spans a wider geographic range, and is typically a more open environment (Kobayashi
The BRT rated harvest of adults as one of the two most severe threats (along with juvenile habitat loss) to bumphead parrotfish, with severity rated as “high” historically, currently, and over a 40-100 year future time horizon. In contrast to adult harvest, the BRT concluded that juvenile harvest is less of a concern, rating its severity as “medium”, both currently and over a 40-100 year future time horizon (rated as “nil” historically). While the BRT rated the threat of harvest differently by life stage, we first discuss general harvesting issues applicable to both life stages, then consider specific justifications for the different rankings.
Bumphead parrotfish are highly prized throughout their range. In addition to their commercial value, bumphead parrotfish are culturally significant for many coastal communities and used in feasts for specialized ceremonial rites (Severance, pers. comm.; Riesenberg, 1968). As such, fisheries for this species have been in place since human inhabitation of these coastal regions (Johannes, 1978; 1981). Following are descriptions of life history characteristics of the species that affect vulnerability to harvest, harvest gears and methods, and summaries of harvest data from the few locales where available.
Immature bumphead parrotfish (40-50 cm TL, sub-adults) recruit to adult habitat (coral reef forereefs); thus, the following descriptions of life history characteristics and methods/gears relate to sub-adults and adults. Several life history characteristics increase the vulnerability of sub-adult and adult bumphead parrotfish to harvest such as nocturnal resting behavior, diurnal feeding behavior, large size and conspicuous coloration. At night, bumphead parrotfish frequently remain motionless while resting in refuge sites and they consistently return to specific resting sites. Unlike other parrotfish species, bumphead parrotfish do not excrete a mucus cocoon to rest within. Thus, resting in shallow water in large groups and returning to the same unprotected resting sites all increase vulnerability of adult bumphead parrotfish to harvest at night (NMFS, 2012). Adult bumphead parrotfish schools effectively announce their
It is likely that juvenile bumphead parrotfish are more vulnerable to harvest in populated regions based on their aggregating behavior and tendency to inhabit shallow lagoon environments. They suffer the same vulnerability from night time harvest as adults and sub-adults as they also use traditional nocturnal resting refuge sites.
Historically, fishing for bumpheads typically took place at night while fish were motionless in their nocturnal resting sites. Fishermen armed with hand spears would paddle wooden canoes or simply walk across shallow reef habitats using a torch assembled from dried coconut fronds in search of resting fish (Dulvy and Polunin, 2004). With the advent of dive lights, SCUBA, freezers, and more sophisticated spears and spear guns, the ability to exploit bumphead parrotfish has increased dramatically over the last several decades (Hamilton, 2003; Aswani and Hamilton, 2004).
Current Indo-Pacific coral reef fisheries are nearly as diverse as the species they target, and include many subsistence, commercial, and sport/recreational fisheries employing a vast array of traditional, modern, and hybrid methods and gears (Newton
Data pertaining to harvest are sparse, incomplete, or lacking for a majority of regions across the range of bumphead parrotfish, though efforts have been made over the past 30 years to obtain fisheries harvest information at a few sites in the central and western Pacific. However, most of the available harvest data combine all parrotfish species into one category, making it difficult to identify bumphead parrotfish harvest amounts. Harvest data specific to bumphead parrotfish exist for Palau (Kitalong and Dalzell, 1994), Guam (NOAA, The Western Pacific Fisheries Information Network), Solomon Islands (Aswani and Hamilton, 2004; Hamilton, 2003), Fiji (Dulvy and Polunin, 2004), and Papua New Guinea (Wright and Richards, 1985).
In Palau, efforts to assess commercial landings of reef fishes were made from 1976 to 1990 (Kitalong and Dalzell, 1994). All harvest data were collected at the main commercial landing site and it is estimated that these data accounted for 50-70 percent of the total commercial catch. Overall, bumphead parrotfish represented 10 percent of reef fisheries landings in Palau, making it the second most important commercial reef fish. It was estimated that an average of 13 metric tons of bumphead parrotfish were sold annually during the study. The highest landings were recorded in the mid-1980s, with a maximum of 34 metric tons sold in 1984. Declines in total catch were observed following the mid-1980s, creating