Endangered and Threatened Wildlife and Plants; Notice of 12-Month Finding on Petitions To List the Pinto Abalone as Threatened or Endangered Under the Endangered Species Act (ESA)
Federal Register, Volume 79 Issue 248 (Monday, December 29, 2014)
Federal Register Volume 79, Number 248 (Monday, December 29, 2014)
Proposed Rules
Pages 77998-78022
From the Federal Register Online via the Government Printing Office www.gpo.gov
FR Doc No: 2014-30345
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
50 CFR Part 224
Docket No. 130808698-4999-02
RIN 0648-XC809
Endangered and Threatened Wildlife and Plants; Notice of 12-Month Finding on Petitions To List the Pinto Abalone as Threatened or Endangered Under the Endangered Species Act (ESA)
AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.
ACTION: Notice of 12-month finding and availability of a status review report.
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SUMMARY: We, NMFS, announce a 12-month finding on two petitions to list the pinto abalone (Haliotis kamtschatkana) as threatened or endangered under the Endangered Species Act (ESA). We have completed a comprehensive status review of the pinto abalone in response to these petitions. Based on the best scientific and commercial information available, we have determined that the species does not warrant listing at this time. We conclude that the pinto abalone is not currently in danger of extinction throughout all or a significant portion of its range and is not likely to become so within the foreseeable future. The species will remain on the NMFS Species of Concern list, with one revision to apply the Species of Concern status throughout the species' range (Alaska to Mexico). We also announce the availability of the pinto abalone status review report.
DATES: This finding was made on December 29, 2014.
ADDRESSES: The pinto abalone status review report is available electronically at: http://www.westcoast.fisheries.noaa.gov/. You may also receive a copy by submitting a request to the Protected Resources Division, West Coast Region, NMFS, 501 West Ocean Blvd., Suite 4200, Long Beach, CA 90802-4213, Attention: Pinto Abalone 12-month Finding.
FOR FURTHER INFORMATION CONTACT: Melissa Neuman, NMFS, West Coast Region (562) 980-4115; or Lisa Manning, NMFS, Office of Protected Resources (301) 427-8466.
SUPPLEMENTARY INFORMATION:
Background
The pinto abalone (Haliotis kamtschatkana) was added to the National Marine Fisheries Service's (NMFS') ``Species of Concern'' list on April 15, 2004 (69 FR 19975). On July 1, 2013, the National Marine Fisheries Service (NMFS) received a petition from the Natural Resources Defense Council (NRDC) requesting that the pinto
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abalone be listed as threatened or endangered under the Endangered Species Act (ESA) and that critical habitat be designated for the species. On August 5, 2013, we received a second petition, filed by the Center for Biological Diversity (CBD) to list the pinto abalone under the ESA and designate critical habitat. On November 18, 2013, NMFS determined that the petitions presented substantial information indicating that the petitioned action may be warranted for pinto abalone (a ``positive 90-day finding'') and published the finding in the Federal Register (78 FR 69033), pursuant to 50 CFR 424.14.
In the fall of 2013, we assembled a Status Review Team (SRT) to compile and review the best available information, assess the extinction risk and threats facing the species, and produce an ESA status review report for pinto abalone. The status review report (NMFS 2014) provides a thorough account of pinto abalone biology and natural history, and an assessment of demographic risks, threats and limiting factors, and overall extinction risk for the species. The status review report was subjected to independent peer review as required by the Office of Management and Budget Final Information Quality Bulletin for Peer Review (M-05-03; December 16, 2004). The key background information and findings of the status review report are summarized below.
Species Description
The pinto abalone is a marine gastropod of the genus Haliotis. It is one of seven species of abalone native to the west coast of North America and occurs in both rocky intertidal and subtidal habitats from Baja California to Alaska (Geiger 1999). Like all abalone, pinto abalone are benthic, occurring on hard substrate, relatively sedentary, and generally herbivorous, feeding on attached or drifting algal material. The shell is scallop-edged, multi-colored (mottled red and/or green), and characterized by irregular lumps, with three to seven open respiratory pores that are slightly raised above the shell's surface and paralleling a deep groove (Stevick 2010). The pinto abalone's muscular foot is tan and is used to adhere to hard substrate and for locomotion. The epipodium (the circular fringe of skin around the foot) and tentacles are mottled yellow to dark tan with vertical banding patterns. The maximum recorded shell length for pinto abalone is 190 mm (see status review report). The maximum age is not known, but estimated longevity of at least 15-20 years is reasonable for pinto abalone (Shepherd et al. 2000, cited in Committee on the Status of Endangered Wildlife in Canada (COSEWIC) 2009)
Distribution
Of the seven species of abalone found along the west coast of North America (Geiger 1999), pinto abalone have the broadest latitudinal range, extending from Salisbury Sound, Sitka Island, Alaska to Bahia Tortugas, Baja California, Mexico (Campbell 2000), and are the predominant abalone found in Washington and Alaska, and in British Columbia, Canada. Other than a few observations on the Oregon coast, we are not aware of any records of pinto abalone along the outer coast of Washington from Neah Bay to Cape Mendocino in California, indicating a gap in the species distribution (Geiger 2000 and 2004 (ABMAP: http://www.vetigastropoda.com/ABMAP/NEPacific.html)).
Two subspecies of pinto abalone have been recognized by taxonomists, based on differences in shell shape and pattern (McLean 1966). The northern form (Haliotis kamtschatkana kamtschatkana) is generally distributed from Alaska south to Point Conception, California. The southern form, or ``threaded abalone'' (Haliotis kamtschatkana assimilis) is generally distributed from central California to Turtle Bay in Baja California, Mexico (Geiger 1999). As discussed below under ``the Species Question'' section of this notice, recent evidence suggests that the two subspecies overlap throughout their range, with examples of the northern form observed in Baja California and examples of the southern form in British Columbia and Washington.
Population Structure and Genetics
We are aware of only one published assessment of population structure in H. kamtschatkana to date, conducted by Withler et al. (2001). The assessment estimated variation at 12 microsatellite loci for abalone sampled at 18 sites located throughout coastal British Columbia and at one site in Sitka Sound, Alaska. The results indicated a lack of differentiation among sites and suggest historically high gene flow among populations within the region from British Columbia to Alaska. This study is limited in that it only examines populations in one part of the species range and uses one set of microsatellite loci; however, it represents the best available information to date regarding population structure.
Other studies have examined whether there is a genetic basis for the delineation of two subspecies, which has been based entirely on differences in shell morphology. Studies thus far have examined the portions of the mitochondrial genes cytochrome oxidase subunit one (COI) and cytochrome b (Cyt b), as well as the reproductive proteins lysin and VERL (vitelline envelope receptor for lysin), and have found no genetic differentiation between the two purported subspecies (Gruenthal and Burton 2005, Straus 2010, Supernault et al. 2010, Schwenke and Park, unpublished data cited in the status review report). We discuss this further in the section of this notice titled ``the Species Question.''
Habitat
Pinto abalone are generally found in rocky intertidal and subtidal habitats with ample algal cover. The specific depth ranges and habitats occupied vary across the species range, as described below. The species occurs in areas with little freshwater influence (salinity >= 30 parts per thousand), and can tolerate wide ranges in temperature, from 2 to 24 degrees Celsius, based on laboratory experiments (Paul and Paul 1998).
In the northern part of its range (e.g., Alaska to Washington), the species occurs in shallower habitats ranging from the lower intertidal to 20m deep relative to mean lower low water (MLLW); they are most commonly found from the intertidal to 10m deep relative to MLLW (Rothaus et al. 2008). In Alaska, pinto abalone are primarily found in the lower intertidal and subtidal surge zones on the outer coast of Southeast Alaska, as well as in the Inside Passage of southern Southeast Alaska (Alaska Department of Fish and Game (ADF&G) comments to NMFS, 17 January 2014). In British Columbia, pinto abalone occur on rocky intertidal and subtidal habitats within areas ranging from sheltered bays to exposed coastlines (COSEWIC 2009). In Washington, the recorded depth range of pinto abalone is 3 to 20 m deep relative to MLLW. Occupied habitats vary with respect to exposure and contain hard substrate (bedrock and boulders/cobble) with ample quantities of benthic diatoms and micro- and macro-algae.
In the southern part of the range, pinto abalone occur in deeper subtidal waters from approximately 12 to 40 m deep relative to MLLW (Geiger and Owen 2012) and are commonly found on open rock surfaces. Distribution in areas along the Southern California mainland is patchy and may be correlated with substrate type, relief, algal composition, and the presence of intermittent sand channels that may
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accumulate drift kelp (an important food source). Pinto abalone appear to prefer flat rock over uneven rock, low relief with scattered rock and boulders over high relief habitats, and areas with Pelagophycus porra, Laminaria farlowii, Agarum fimbriatum, Pterygophora californica, and coralline algae (articulated and crustose) (unpublished data from Bill Hagey et al. and Melissa Neuman et al., cited in the status review report). A recent study reported that in Mexico, H. k. assimilis and H. sorenseni occurred at depths ranging from 11 to 25 m (relative to MLLW), with the majority found between 13 to 15 m and 19 to 21 m deep, although this may reflect a bias toward the depths that were visited most frequently (Boch et al. 2014).
Movement
Little is known about movement patterns of larval or juvenile pinto abalone anywhere in their range. The planktonic larval stage is short (approximately 5-6 days; Olsen 1984, cited in Sloan and Breen 1988), and thus dispersal is likely to be limited and almost certainly determined primarily by patterns of water movement in nearshore habitats near spawning sites. Larval settlement and metamorphosis in pinto abalone is likely to be associated with chemical cues present in crustose red algae, as has been found for red abalone (H. rufescens) (Morse and Morse 1984). Small juvenile (40-50 mm shell length) face mortality from human removal, disease, predation, variation in food supply, physical disturbance, and pollution. Human removal of pinto abalone occurs through commercial, recreational, and subsistence harvest; purposeful illegal harvest; and accidental lethal injury. We discuss fisheries harvest of pinto abalone for commercial, recreational, and subsistence purposes in more detail under the ``Abundance'' section of this notice. Predation by sea otters has been highlighted as an important factor contributing to the continued decline of pinto abalone populations in places like Alaska where sea otter populations are increasing (ADF&G comments to NMFS, 17 January 2014). Other sources of natural mortality include diseases such as withering syndrome, ganglioneuritis (and the related amyotrophia), vibriosis, and shell deformities (sabellidosis). These sources of mortality and their impact on the species are discussed in more detail in the ``Summary of Factors
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Affecting the Species'' section later in this document.
Abundance
There are two types of data that can be examined to provide a better understanding of variation in pinto abalone abundance over time: fishery-dependent and fishery-independent data. Due to the general lack of formal data, we also include observations reported by individuals or groups of people. We summarize the available information by region (Alaska, British Columbia, Washington, Oregon, California, and Mexico), because both species abundance and the level of information available vary by geographic region. The status review report provides a more detailed account of the available information for each region.
Alaska
Several fisheries for pinto abalone have existed in Alaska, including a commercial fishery and sport fishery (both of which are now closed) and personal use and subsistence fisheries (both of which are still in operation). Data are not available on the number of pinto abalone taken in the fisheries, but trends in commercial fisheries harvest levels indicate a decline in pinto abalone, with harvest in Southeast Alaska falling from a peak of 378,685 lbs in 1979/1980 to a low of 14,352 lbs in 1995/1996 (the fishery closed in 1995; Rumble and Hebert 2011). Between the 1993/1994 season and 1994/1995 season, harvest per unit effort for the fishery was estimated to have declined by 64 percent (Rumble and Hebert 2011).
Commercial harvest of pinto abalone in Southeast Alaska began in the 1960s with a significant increase in effort and harvest in the late 1970s and early 1980s, followed by a steep decline in catch in the late 1980s and 1990s (Rumble and Hebert 2011). The increase in effort can be attributed in large part to an increase in value from less than one dollar per pound in the early 1970s to greater than six dollars per pound in 1993-1994 (Woodby et al. 2000). Harvest peaked at 378,685 pounds in 1979-1980, followed by a decline in harvest that was likely due in part to declines in pinto abalone abundance as well as changes in regulations to limit the fishery, including harvest limits and area and seasonal closures (Rumble and Hebert 2011). The commercial fishery for pinto abalone was closed in 1995 and remains closed (Woodby et al. 2000). Commercial harvest was primarily conducted using scuba or hookah dive gear in the subtidal zone, though pinto abalone can be picked by hand in the intertidal zone during extreme low tides (Rumble and Hebert 2011).
Data from the subsistence abalone fishery are available from 1972 to 1997 and indicate a significant decline (98 percent decrease) in the subsistence harvest from an average of 350-397 pinto abalone per household in 1972 to an average of 3-9 pinto abalone per household in 1997 (Bowers et al. 2011). Subsistence harvest of pinto abalone in Alaska is believed to remain low (ADF&G comments to NMFS on 17 January 2014). In 2012, the Alaska Board of Fisheries reduced the daily bag limit for subsistence harvest to 5 abalone, with no closed season and no annual limit (Bowers et al. 2011). Prior to 2012, the daily bag limit for subsistence harvest was 50 abalone. The minimum size limit is 3.5 inches and legal harvest methods include snorkel equipment, abalone irons, or collection by hand. Scuba and hookah diving for subsistence abalone harvest has been prohibited since 1996.
Abalone harvest has also occurred in the sport abalone fishery (for non-residents) and personal use abalone fishery (for state residents), but data on trends in harvest are not available. In the sport fishery, the daily bag limit was 5 abalone per day (minimum size: 3.5 inches), with no closed season. Scuba and hookah gear were allowed until 1996. The Alaska Board of Fisheries closed the sport abalone fishery in 2012 and it remains closed to present. In the personal use abalone fishery, the daily bag limit was 50 abalone per person (except in one area around Sitka where the daily bag limit was 20 abalone per person), with a minimum size limit of 3.5 inches and no closed season. In 2012, the Alaska Board of Fisheries reduced the daily bag limit to 5 abalone per person. Scuba and hookah diving were allowed until 1996. The personal use abalone fishery remains open, but harvest is believed to be low (ADF&G comments to NMFS on 17 January 2014).
There are limited fishery-independent data on pinto abalone populations in Alaska. No long-term monitoring of pinto abalone populations in Alaska has been conducted. However, observations of pinto abalone have been made by ADF&G biologists while conducting dive surveys to monitor other benthic invertebrate species for management purposes. From 1996 to 2000, about 125 to almost 250 pinto abalone were observed per year during red sea urchin dive surveys; in 2001, the number observed dropped to about 50 pinto abalone, and in 2002-2011, fewer than 20 pinto abalone were observed per year (ADF&G comments to NMFS, 17 January 2014). These observations suggest a continued decline in pinto abalone populations since closure of the commercial fishery. ADF&G noted an increase in empty abalone shells observed on red sea urchin survey transects in Southeast Alaska between 2001 and 2012 (pers. comm. with K. Hebert, ADF&G). These observations are coincident with increased sea otter abundance in Southeast Alaska and suggest that sea otters are having an impact on pinto abalone abundance where the two species overlap (pers. comm. with K. Hebert, ADF&G). The one exception to this observed pattern is in Sitka Sound, where sea otters and a small population of pinto abalone appear to co-exist (pers. comm. with K. Hebert, ADF&G). ADF&G has observed mixed age classes in some areas in Southeast Alaska, including juveniles (S. Walker, pers. comm.).
British Columbia
Although also limited, data are available from both fishery-
dependent and fishery-independent sources regarding the abundance of pinto abalone in British Columbia, making this region relatively data rich compared to other regions of the coast. The available data indicate a decline in pinto abalone populations during and even after closure of abalone fisheries, with signs of increases in abundance in the past five years attributed to a reduction in poaching.
Harvest of pinto abalone has a long history in British Columbia. Pinto abalone were harvested in commercial, recreational, and traditional First Nations food, social, and ceremonial fisheries. Prior to the advent of scuba gear around 1960, abalone harvest by First Nations and recreational fishers occurred primarily at low tide by shore picking (Farlinger and Campbell 1992), although some First Nations used a two-pronged spear to take abalone as deep as 2 m below the lowest tide (Jones 2000). After the advent of scuba gear, the recreational fishery became widespread along the coast (Farlinger and Campbell 1992). No landing statistics are available for either the First Nations or recreational fisheries (Sloan and Breen 1988, Farlinger and Campbell 1992). However, during the recreational fishery in 1983, McElderry and Richards (1984) estimated that scuba divers in the Strait of Georgia collected 1,172 pinto abalone per thousand sport dives and that between 76,000 and 172,000 recreational dives occurred in that year in the Canadian portion of the Strait of Georgia.
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The commercial abalone fishery began in British Columbia as early as 1889 as a small, local, and sporadic fishery (Mowat 1890), but expanded significantly in the 1970s when landings increased to nearly 60 metric tons (mt) in 1972 and then to 273 mt in 1976 (Federenko and Sprout 1982). Commercial landings peaked at over 480 and 400 mt in 1977 and 1978, but dropped to about 200 mt in 1979 when a quota was put in place for the first time. Landings leveled out to between 44 and 47 mt under quota management and numerous other management actions taken following 1977 (Sloan and Breen 1988). Reasons for the increase in abalone harvest in the 1970's include the advent of scuba and dry-
diving suits, allowing more diver submergence time; the advent of on-
board boat freezers; emergence of a market in Japan for pinto abalone; tripling of the price per pound between 1972 and 1976 to over three Canadian dollars per pound; restricted access to salmon and herring fisheries; and unrestricted access to the abalone fishery prior to 1977 (Sloan and Breen 1988, Farlinger and Campbell 1992). All pinto abalone fisheries in British Columbia were closed in December 1990 due to observed declines and overall low population levels (Egli and Lessard 2011) and remain closed to date.
Breen (1986) estimated that at the beginning of 1976 the abalone stock stood at 1,800 mt in areas that were open to harvest (closed areas (Fedorenko and Sprout 1982): Juan Perez Sound, Lower Johnstone Strait, Strait of Georgia, and Strait of Juan de Fuca). By the end of 1980, the stock size had been reduced to an estimated 450 mt (Breen 1986). The SRT attempted to estimate the number of individual pinto abalone landed each year from 1952-1990 in the commercial fishery, based on landed biomass and the predicted mean weight of legal-sized northern abalone (>= 90 mm from 1952-1976 and >= 100 mm after 1976). An estimated 2.5 million abalone were harvested in 1977, with at least a million abalone harvested each year from 1976 to 1979 and over 240,000 harvested each year during the last decade of the fishery (see status review report). Most of the commercial harvest occurred at Haida Gwaii (formerly known as the Queen Charlotte Islands) and along the North Coast (Sloan and Breen 1988, Egli and Lessard 2011).
Fishery-independent data for pinto abalone in British Columbia primarily consist of data from index site surveys conducted by the DFO since 1978, although some data exist for the period prior to the 1970s (i.e., prior to when the fishery expanded significantly). Surveys from the early 1900's indicate pinto abalone were present in sufficient numbers for harvesting around Haida Gwaii and in Queen Charlotte Sound (Thompson 1914). Exploratory surveys conducted in the same areas in 1955 found few pinto abalone in southeastern Haida Gwaii, and many areas with no abalone, indicating a decline in the region's population (Quayle 1962, Sloan and Breen 1988). In contrast, surveys conducted in 1978 in the same area found few sites with no abalone and an estimated density of 0.58 legal-sized abalone per sq m with an overall mean density of 2.5 abalone per sq m (Breen and Adkins 1979, Sloan and Breen 1988). Breen (1986) attributed these differences between surveys in 1914, 1955, and 1978 to natural variation in pinto abalone abundance, rather than to differences in survey methods or observer experience. Pinto abalone were previously not thought to occur in the Strait of Georgia (formerly known as the Gulf of Georgia) (Thompson 1914), but have since been found there, though relatively scarce compared to other areas in British Columbia and only at depths of 7m or greater (Quayle 1962, Sloan and Breen 1988).
DFO index site surveys for pinto abalone have been conducted every 4-5 years since 1978, providing valuable time series and size frequency data. Surveys at Haida Gwaii and along the North and Central Coast began in 1978, and on the West Coast of Vancouver Island, Queen Charlotte Strait, and the Strait of Georgia in 2003 and 2004. The status review report summarizes the best available data on pinto abalone abundance and trends from these surveys. The data indicate that although recruitment is occurring, the density of mature adults (defined as pinto abalone gteqt 100 mm SL for the purposes of the index site surveys) has been declining, either due to a high rate of juvenile mortality before they reach maturity or due to a high rate of adult mortality that is offsetting juvenile survival (COSEWIC 2009). Densities of immature abalone have increased by 29 percent at the Central Coast sites since 1989 and by 35 percent at the Haida Gwaii sites since 1990, whereas densities of mature abalone have declined by about 44 percent since 1990 (the year the abalone fisheries closed) (COSEWIC 2009).
Overall, the survey data from 1978 to 2009 indicate that mature abalone densities declined by 88-89 percent and total abalone densities have declined by 81-83 percent at the Central Coast and Haida Gwaii sites (COSEWIC 2009). However, preliminary results from more recent surveys in 2011 and 2012 indicate signs of increasing populations, potentially due to reductions in illegal take. In 2009, abalone were found at 41 percent of the 34 sites surveyed in Queen Charlotte Strait, with an overall density of 0.109 per sq m and a mature abalone density of 0.072 per sq m (Lessard and Egli 2011). These densities were four times greater than the densities found in 2004 and indicate that abalone populations in Queen Charlotte Strait are stable (Lessard and Egli 2011). Results from the 2011 surveys along the Central Coast show an increase in the mean density of abalone (all sizes) and a decrease in the estimated mortality rate between 2006 and 2011 (pers. comm. with J. Lessard, DFO, on 24 April 2014). The density of mature abalone (>= 70 mm shell length) was at or above the short-term recovery objective of 0.32 abalone per sq m (as defined in DFO's 2007 Recovery Strategy for pinto abalone) at 6 of the 8 index survey sites and above the long-
term goal of one abalone per sq m at one site (pers. comm. with J. Lessard, DFO, on 24 April 2014). Similarly, results from the 2012 surveys at Haida Gwaii indicate an increase in the mean density of both immature and mature abalone and a decrease in the estimated mortality rate between 2007 and 2012, as well as densities of mature abalone (>= 70 mm shell length) at or above the recovery objective of 0.32 abalone per sq m at 5 of the 9 index survey sites (pers. comm. with Joanne Lessard, DFO, on 24 April 2014). Evidence of successful juvenile recruitment throughout the years and these recent increases in adult abundance and density indicate that removing or reducing illegal harvest to minimal levels would likely allow populations to rebuild. However, with the continued spread of sea otters in the region, populations are not expected to return to levels observed during the 1970s when sea otters were absent from the region (COSEWIC 2009).
Washington
Data on abundance and trends in pinto abalone populations in Washington are limited to fishery-independent data from timed swim and index site surveys. Although estimates of recreational harvest are available, they do not provide information on trends in abundance over time. Overall, the survey data indicate that populations in Washington have declined over time, despite closure of the fisheries in 1994, and local recruitment failure may be occurring.
Fishery-dependent data for Washington are limited. Washington has never had a commercial fishery for pinto abalone. Subsistence harvest by
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indigenous peoples and early residents reportedly occurred, but the magnitude and extent of the fishery are not well documented (WDFW 2014). Pinto abalone were first recognized as a recreationally harvestable shellfish with a daily possession limit of 3 abalone by Washington Administrative Code (WAC) orders first published in 1959. Between 1959 and when the recreational fishery was closed in 1994, the possession limit fluctuated between 3 and 5 abalone per day and several other measures, including minimum size limits and gear restrictions, were imposed to manage the fishery.
Although recreational harvest records were not collected, some estimates of annual harvest are available from compilations of recreational sport diver interviews, returned questionnaires, diver logbook records, and information from dive clubs (Bargmann 1984, Gesselbracht 1991). In the early 1980s, approximately 91 percent of pinto abalone harvest occurred in the North Puget Sound region, including the San Juan Islands Archipelago, and the remainder occurred in the Strait of Juan de Fuca and just north of Admiralty Inlet (Bargmann 1984). Bargmann (1984) estimated that sport divers harvested 34,800 and 3,400 pinto abalone annually from the North Sound and the Strait/Admiralty regions, respectively, based on data over the period from April 1982 to March 1983. Gesselbracht (1991, cited in WDFW 2014) estimated that 40,934 pinto abalone were harvested annually, based on interviews with sport divers from September 1989 to August 1990.
Fishery-independent data are available from timed swim and index site surveys in the San Juan Islands Archipelago. Both sets of data indicate continuing declines in pinto abalone populations since the fisheries closed in 1994. From 1979-1981, WDFW conducted timed swim surveys (designed to quantify pinto abalone abundance) at 30 sites, with a mean encounter rate of about 1.1 pinto abalone per minute or 25.5 pinto abalone per dive (WDFW 2014). These were likely underestimates of pinto abalone abundance, because swim times were not adjusted for the time taken to measure abalone size (WDFW 2014). In contrast, WDFW divers encountered an average of about 1.1 abalone per dive across all 30 sites in 2010-2011, indicating a reduction in encounter rate of about 96 percent (WDFW 2014). This reduction in the encounter rate of pinto abalone per dive indicates a decline in pinto abalone density among the 30 survey sites. In 2005, Rogers-Bennett et al. (2007 and 2011) surveyed 10 sites in the San Juan Islands Archipelago where pinto abalone populations were abundant in the past, and found only 17 pinto abalone (range in shell length = 75-142 mm); 14 of those abalone were found at just two sites. This number was substantially lower than the number of pinto abalone found at the sites in 1979 by WDFW (Rogers-Bennett et al. 2011). Index site surveys show similar declines in pinto abalone densities around the San Juan Islands Archipelago. From 1992 to 2013, WDFW has conducted periodic surveys at 10 index sites, originally selected in areas known to have high pinto abalone abundance. The mean density at the 10 index sites declined from 0.18 abalone per sq m in 1992 to 0.04 abalone per sq m in 2006 (Rothaus et al. 2008) and 0.01 abalone per sq m in 2013 (WDFW 2014).
Recent data suggests limited recruitment is occurring in the San Juan Islands Archipelago. The proportion of emergent juvenile pinto abalone (shell length 50 percent) of animals in pairs within four meters of one another indicate that the species is extremely patchy, and that densities recorded on a per sq m basis may not be the best metric for evaluating population viability.
Mexico
Little information is available on pinto abalone distribution and abundance in Mexico. Because pinto abalone and white abalone overlap in range and are difficult to distinguish morphologically, the two species are often grouped and reported on together. In Mexico, the abalone fishery has been operating since the 1860s (Croker 1931) and is still operating, but modern commercial harvests did not develop until the 1940s. Historically, the fishery primarily harvested H. fulgens and H. corrugata, but H. kamtschatkana/sorenseni were also considered relatively abundant and harvested.
A recent collaborative study was conducted in August 2012 as a preliminary assessment of abalone species in the nearshore at El Rosario, Baja California, and provided density data on pinto and white abalone in five survey areas (Boch et al. 2014). Pinto and white abalone were grouped and referred to as a two species complex in the study, due to similarities in shell morphology and possibly misidentification by observers. However, the authors estimated that 75 percent of the abalone in this group were pinto abalone (H. k. assimilis) (pers. comm. with C. Boch, Stanford University). The survey included twenty-four transects, each covering a 400 sq sq m area within depths of 11-25 m. A total of 178 H. k. assimilis/sorenseni were found, ranging in size from 40 to 240 mm SL, with the majority ranging in size from 40 to 180 mm. Assuming that 75 percent of these were likely H. k. assimilis, the estimated density of H. k. assimilis for the study area would be 0.0139 per sq m. Recent recruitment was evident in at least one area where the population consisted primarily of animals ranging from 40 to 80 mm in size.
The ``Species'' Question
The ESA defines a species as ``any species or subspecies of wildlife or plants, or any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.'' The pinto abalone is a marine invertebrate species that has been taxonomically subdivided into two subspecies: Haliotis kamtschatkana kamtschatkana (i.e., the northern form that is described as ranging from Sitka Island, Alaska to Point Conception, California), and Haliotis kamtschatkana assimilis (i.e., the southern form that is described as ranging from Monterey, California to Turtle Bay, Baja California, Mexico) (McLean 1966). The two subspecies were initially described as separate species by Jonas (Haliotis kamtschatkana) in 1845 and Dall (Haliotis assimilis) in 1878. McLean (1966) argued that the two previously described species were unique forms, or subspecies, representing geographic extremes of a single species, with differences in shell morphology likely related to varying environmental conditions along a latitudinal gradient within the species' range. Geiger (1999) upheld the subspecies classification scheme based on the morphological descriptions of shells provided by McLean (1966) and also maintained the subspecies range descriptions as described above.
More recently, two lines of evidence have raised uncertainty regarding the taxonomic structure of pinto abalone as
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consisting of two subspecies. First, none of the genetic tools and analyses conducted to date have been able to confirm a discernible difference between H. k. kamtschatkana and H. k. assimilis. Studies conducted thus far tend to indicate high intraspecific (within species) variability in pinto abalone, depending on the gene sequenced, but no genetic differentiation between subspecies. One highly conserved portion of the genome that has been investigated and that geneticists would have expected to be different between subspecies, is the area that controls the production of the reproductive proteins lysin and VERL (vitelline envelope receptor for lysin). Supernault et al. (2010) examined this portion of the genome for forensic analyses of northeastern Pacific abalone species. Results indicated that all species recognized on the basis of morphological differences have been confirmed to be distinct on the basis of genetic sequences, with only the two subspecies, H. k. kamtschatkana and H. k. assimilis, indistinguishable through molecular analysis. Gruenthal and Burton (2005) had similar results, concluding H. k. kamtschatkana and H. k. assimilis were statistically indistinguishable at sequenced portions of the mitochondrial genes cytochrome oxidase subunit one (COI) and cytochrome b (CytB), as well as VERL, although the sample sizes were small. Straus (2010) also found no statistically significant differences in either COI or lysin, stating that the two subspecies share identical sequences at both mitochondrial and nuclear loci and cannot be differentiated. Most recently, Schwenke and Park (unpublished data, cited in the status review report) constructed bootstrapped neighbor-joining trees of new and archived mitochondrial COI and VERL sequences, finding that VERL is currently the best marker available to resolve the most closely related abalone species group found along the Northeastern Pacific coast (white, pinto, flat, and red), whereas COI separates this group from the remaining species (i.e. black, pink, and green; pers. comm. with P. Schwenke, NMFS Northwest Fisheries Science Center, cited in status review report). Again, however, neither marker provided subspecies level resolution. Thus, to date, the subspecies remain indistinguishable at the molecular level, although future analyses using newer methods that search the entire genome (such as single nucleotide polymorphisms or SNPs) may be able to find genetic support for the delineation of the two putative subspecies.
Second, collections from several shell collectors contain multiple examples of the southern form (H. k. assimilis) in British Columbia and Washington and of the northern form (H. k. kamtschatkana) in Baja California, Mexico, as well as multiple specimens collected from both the northern and southern portion of the species' range that exhibit morphologies representative of both subspecies (pers. comm. with B. Owen and A. Rafferty, cited in status review report). We recognize that shell collections may not represent a random sample of shells from the population and that these shells may constitute a relatively small population of outliers in the wild. Despite this, these examples suggest that the range overlap between the two putative subspecies is much more extensive than was previously thought (Canada to Mexico, rather than just along the central California coast) and that this degree of overlap (approximately 80 percent of the species' range) does not meet the definition of subspecies as allopatric populations (Futuyma 1986).
The SRT concluded, and NMFS agrees, that the pinto abalone should be considered as one species throughout its range for the purposes of the status review. This conclusion was based on the lack of evidence for species divergence at the molecular level, the degree of overlap between the subspecies, and the fact that there are other examples of marine invertebrate species with broad geographic ranges (e.g., ochre and bat stars) and/or pronounced morphological plasticity (e.g., periwinkle snails) extending on the order of 1,000s of kilometers. We do not reject the possible existence of pinto abalone subspecies. However, the lack of genetic, geographic, or ecological justification for treating the two subspecies as separate species led the SRT to consider the status of the species and its extinction risk throughout its range from Alaska to Mexico.
Assessment of Risk of Extinction
Approach to Extinction Risk Assessment
The ESA defines an endangered species as ``any species which is in danger of extinction throughout all or a significant portion of its range.'' A threatened species is ``any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.'' Thus, we interpret an ``endangered species'' to be one that is presently in danger of extinction. A ``threatened species,'' on the other hand, is not presently in danger of extinction, but is likely to become so in the foreseeable future (that is, at a later time). In other words, the primary statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either presently (endangered) or in the foreseeable future (threatened).
To evaluate whether the pinto abalone meets the definition of threatened or endangered, we considered the best available information and applied professional judgment in evaluating the level of risk faced by the species. We evaluated both demographic risks, such as low abundance and productivity, and threats to the species including those related to the factors specified by the ESA section 4(a)(1)(A)-(E). In a separate evaluation (see the ``Efforts Being Made to Protect the Species'' section below), we also considered conservation efforts being made to protect the species.
As described above, we convened an SRT, comprised of nine fishery biologists and abalone experts from the NMFS West Coast and Alaska Regions, the NMFS Northwest and Southwest Fisheries Science Centers, NMFS Office of Science and Technology, the National Park Service, and the U.S. Geological Survey/University of Washington. The SRT was asked to review the best available information on the species and to evaluate the overall risk of extinction facing pinto abalone now and in the foreseeable future. The ability to measure or document risk factors for pinto abalone is limited and the available information is often not quantitative, or less than ideal. Therefore, in assessing risk, we included both qualitative and quantitative information and modeled the assessment on the approaches used in previous NMFS status reviews to organize and summarize the professional judgment of the SRT members.
The SRT first performed a threats assessment for pinto abalone by scoring the severity and scope of threats to the species, as well as the time frame over which the threats are affecting the species and the level of data that is available regarding the threats and their effects. The SRT considered past factors for decline, as well as present and future threats faced by the species. Detailed definitions of these risk scores can be found in the status review report. The results of this threats assessment are summarized below under ``Summary of Factors Affecting the Species.''
The SRT then assessed the demographic risks for pinto abalone. The SRT considered demographic
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information reflecting the past and present condition of pinto abalone populations. This information is detailed in the status review report and summarized above under the ``Background'' section of this notice, and included the best available information on population abundance or density, population trends and growth rates, the number and distribution of populations, exchange rates of individuals among populations, and the ecological, life history, or genetic diversity among populations. In some cases, information was not available or severely limited.
As in previous NMFS status reviews, the SRT analyzed the collective condition of individual populations at the species level according to four demographic risk criteria: Abundance, growth rate/productivity, spatial structure/connectivity, and diversity. These four general viability criteria, reviewed in McElhany et al. (2000), reflect concepts that are well-founded in conservation biology, are generally applicable to a wide variety of species, and describe demographic risks that individually and collectively provide strong indicators of extinction risk. The SRT's methods and conclusions for the demographic risk assessment are described in more detail below in the ``Analysis of Demographic Risk'' section of this notice.
The SRT members were then asked to make an overall extinction risk determination for pinto abalone now and in the foreseeable future. For this analysis, the SRT considered the best available information regarding the status of the species along with the results of the threats assessment and demographic risk analysis. The SRT defined five levels of overall extinction risk: No/Very Low risk, Low risk, Moderate risk, High risk, and Very High risk. To allow individuals to express uncertainty in determining the overall level of extinction risk facing the species, the SRT adopted the ``likelihood point'' (Forest Ecosystem Management Assessment Team, or FEMAT, 1993) method, in which each SRT member distributed 10 `likelihood points' among the five levels of risks. The scores were then tallied and summarized. This approach has been used in previous NMFS status reviews (e.g., for Pacific salmon, rockfish in Puget Sound, Pacific herring, black abalone, scalloped hammerhead) to structure the team's analysis and express levels of uncertainty when assigning risk categories.
The SRT did not make recommendations as to whether the species should be listed as threatened or endangered, or if it did not warrant listing. Rather, the SRT drew scientific conclusions about the overall risk of extinction faced by pinto abalone under present conditions and in the foreseeable future (defined as 30 years and 100 years) based on an evaluation of the species' demographic risks and assessment of threats. NMFS considered the SRT's assessment of overall extinction risk, along with the best available information regarding the species status and ongoing and future conservation efforts, in making a final determination regarding whether the species meets the definition of threatened or endangered.
Summary of Factors Affecting the Species
According to section 4 of the ESA, the Secretary of Commerce determines whether a species is threatened or endangered because of any (or a combination) of the following factors: The present or threatened destruction, modification, or curtailment of its habitat or range; overutilization for commercial, recreational, scientific or educational purposes; disease or predation; inadequacy of existing regulatory mechanisms; or other natural or man-made factors affecting its continued existence. We examined these factors for their historic, current, and/or potential impact on pinto abalone and considered them, along with current species distribution and abundance, to help determine the species' present vulnerability to extinction. When considering the effects of the threat into the foreseeable future, the time frame considered by the SRT varied based on the threat, but generally ranged from 30 to 100 years. A time frame of 30 years represents approximately 3 generation times for pinto abalone (McDougall et al. 2006, COSEWIC 2009) and was considered a reasonable period over which predictions regarding the threats and their effects on the species could be made. A time frame of 100 years was considered a reasonable period over which predictions regarding longer-term threats (e.g., ocean acidification, effects of climate change) have been or could be made. The time frames for foreseeable future are discussed in more detail under the ``SRT Assessment of Overall Extinction Risk'' section of this notice.
For each of these factors, the SRT identified and evaluated several stressors that either have or may contribute to declines in pinto abalone. Overall, the SRT rated most of these stressors as low threats and several as moderate threats to pinto abalone, but did not identify any high or very high threats. Among the moderate threats, the SRT was most concerned about low densities that have resulted from past fisheries harvest of pinto abalone, the potential threat posed by ocean acidification, and illegal take due to poaching and inadequate law enforcement. The potential for reduced genetic diversity as a consequence of low population densities and the potential for predation (particularly by sea otters) to further reduce local densities were also identified as threats of greater concern. Finally, oil spills and disease outbreaks (through the spread of pathogens) were highlighted as highly uncertain risks that need to be addressed through careful planning, monitoring, and management. Below, we discuss the threats associated with each factor and our assessment of each factor's contribution to extinction risk to the species. Where relevant, we discuss the risks posed by a factor in combination with other factors (e.g., risks posed by disease and inadequate regulatory mechanisms).
Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range
Most of the threats that result in substrate destruction or modification, such as coastal development, recreational access, cable repairs, nearshore military operations, and benthic community shifts, occur infrequently, have a narrow geographic scope, or have uncertain or indirect effects on pinto abalone. Some exceptions may exist in the cases of water temperature increases and reduced food quantity and quality associated with the ENSOs, PDOs, IPOs, and long-term climate change, as well as sea level rise due to long-term climate change, in that these threats have the potential to produce more widespread impacts, but the certainty in how these factors will affect pinto abalone is low. For example, increased water temperatures associated with climate change may be widespread throughout the U.S. West Coast, though the latest climate report suggests that impacts will be least felt in the Pacific Northwest (Mote et al. 2014). Increased water temperatures could affect the health and range of pinto abalone, particularly at the northern and southern extreme of the species range. However, pinto abalone have a wide temperature tolerance and may be able to adapt to changing temperatures over time, such as by seeking depth refuges. It is also not clear how El Nintildeo/Southern Oscillation (ENSO) events, Pacific Decadal Oscillation (PDO) events,
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Interdecadal Pacific Oscillation (IPO) events, and climate change may affect food quantity and quality for pinto abalone. Sea level rise may result in loss of suitable habitat in a preferred depth range because of increased erosion, turbidity and siltation; however, the effects on pinto abalone are uncertain because pinto abalone typically occupy subtidal habitats throughout much of their range. We are not aware of any studies that have examined the potential effects of sea level rise on abalone, and therefore, we currently lack information to determine whether these habitat changes will be important factors for species decline.
Climate change impacts, such as ocean acidification, could affect settlement habitat by affecting the growth of crustose coralline algae, but the effects to pinto abalone are unclear. For example, McCoy (2013) and McCoy and Ragazzola (2014) found morphological changes (e.g., reduced thickness or density) in crustose coralline algal species in response to ocean acidification, with responses varying by species. However, Johnson et al. (2014) found that crustose coralline algal species exposed to varying carbon dioxide levels may be acclimatized to ocean acidification, with species-specific variation in the responses. North Pacific waters, including the California Current Ecosystem, have relatively low seawater pH values due to a variety of natural oceanographic processes (Feely et al. 2004, Feely et al. 2008, Feely et al. 2009, Hauri et al. 2009), and this may make crustose coralline algal species within the pinto abalone's range better able to adapt to the effects of ocean acidification. In addition, it is unclear how ocean acidification may affect the chemical cues that are believed to attract pinto abalone to settle on crustose coralline algae. Overall, climate change impacts such as ocean acidification could affect settlement habitat, but the effects are highly uncertain at this time.
Oil spill and response activities were also identified as a concern for pinto abalone, for both the potential effects on habitat (substrate destruction or modification) and on the abalone themselves (environmental pollutant/toxins, under ``Other Natural or Man-made Factors''). These effects would be of particular concern where the species occurs in intertidal and shallower waters (e.g., Alaska and British Columbia). The threat of an oil spill is greater in areas with higher ship traffic and human development. If a spill were to occur, acute effects could be very damaging in the localized area of the spill. However, there is little information available on the effects of oil spills on subtidal habitats where pinto abalone tend to occur throughout most of their range, as well as little information available on the effects of oil on abalone.
Overall, the best available information does not indicate that the threats discussed above have resulted in the destruction of or substantial adverse effects on pinto abalone habitat, or in curtailment of the species' range. Evaluations in British Columbia (COSEWIC 2009) and Washington (Vadopalas and Watson 2013) indicate that habitat does not appear to be a limiting factor for the species at this time. Future effects on the species' habitat and/or range may result from ENSOs/
PDOs/IPOs or the impacts of long-term climate change; however, the magnitude, scope, and nature of these effects are highly uncertain at this time. We conclude that the habitat threats discussed above are not contributing substantially to the species' risk of extinction now. The future impacts of climate- and/or oil spill-related habitat changes are highly uncertain, but based on past impacts our best judgment leads us to conclude that impacts will not contribute substantially to the species' risk of extinction in the foreseeable future.
Overutilization for Commercial, Recreational, Scientific or Educational Purposes
Fisheries harvest of pinto abalone for commercial and recreational purposes (i.e., prior to the fishery closures) has contributed to population declines and low densities throughout the species' range (see the ``Abundance'' section above). Harvest of pinto abalone is currently prohibited throughout the coast except in Alaska (i.e., for personal use and subsistence harvest) and Mexico. Data on harvest levels and the impacts on pinto abalone are not available for Alaska and Mexico. In Mexico, green and pink abalone are the focus of the abalone fishery, with other abalone species (including pinto abalone) making up only one percent of the abalone fishery (Boch et al. 2014). In Alaska, the daily limits for personal use and subsistence harvest were reduced in 2012 from 50 to 5 abalone per day. We do not have data to assess how this harvest level would affect pinto abalone populations in Alaska. ADF&G believes that personal use and subsistence harvest of pinto abalone is currently low (ADF&G comments to NMFS on 17 January 2014). Bowers et al. (2011) found that the average subsistence harvest of pinto abalone ranged from 350-382 abalone per household in 1972 but decreased to 3-9 abalone per household in 1997. In recent interviews, local residents have indicated to ADF&G that they are not participating in the personal use fishery due to the lack of abalone (Bowers et al. 2011). Based on this information, it is likely that personal use and subsistence harvest of pinto abalone in Alaska is low. The SRT expressed concern regarding the continued harvest of pinto abalone in Alaska and Mexico, but rated fisheries harvest as a Moderate threat overall, due to prohibitions on harvest throughout most of the species' range and what appears to be low levels of harvest in Alaska and Mexico presently. However, monitoring of harvest levels and pinto abalone populations is needed to obtain a better understanding of the impacts of these fisheries in Alaska and Mexico.
The effects of past fisheries harvest on local densities still persist today throughout the species' range. Past harvest levels, particularly in commercial fisheries in Alaska and British Columbia, were not sustainable and reduced densities to very low or non-existent levels. Some populations (e.g., at the San Juan Islands Archipelago in Washington) appear to be experiencing recruitment failure. There are also a few areas where pinto abalone have not been observed in recent surveys in Washington and British Columbia. However, pinto abalone populations continue to persist throughout most survey sites. In addition, evidence of recent recruitment events have been observed at several areas throughout the species' range. Since the closure of abalone fisheries in British Columbia in 1990, small size classes of pinto abalone have been observed regularly during index site surveys at Haida Gwaii and along the Central Coast (two areas that once supported a large proportion of fisheries harvest) (COSEWIC 2009). Small pinto abalone have also been observed in surveys conducted within the last 10 years off Alaska (pers. comm. with S. Walker, ADF&G, cited in status review report), California (pers. comm. and unpublished data from A. Bird, CSUF, and Ed Parnell, UCSD, cited in status review report), and Mexico (Boch et al. 2014), indicating recent recruitment events (see the ``Reproduction and Spawning Density'' section of this notice for more details). These observations show that densities at those locations remain high enough to support reproduction and recruitment, and also that we have much more to learn about the species' population dynamics and the factors influencing successful reproduction and
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recruitment. For example, mean adult densities may not be an appropriate metric for predicting reproductive and recruitment success because it does not adequately represent the patchy distribution of abalone within an area. Fine-scale spatial distribution patterns (e.g., aggregations) may be more important for reproductive and recruitment success than the overall density of adults in an area.
Reduced genetic diversity is a potential risk associated with low densities. Withler et al. (2001) provide the only published assessment of population structure in pinto abalone and found high levels of genetic variation in pinto abalone populations sampled at 18 sites throughout coastal British Columbia and at one site in Sitka Sound, Alaska. Unfortunately, research on populations throughout the remainder of the species' range has not been conducted, and thus the Wither et al. (2001) study represents the best available information. Based on this, the SRT expressed a moderate degree of concern, but most members felt that the species' genetic diversity likely remains high.
Overall we conclude that past fisheries harvest has reduced the abundance of pinto abalone populations throughout its range, but not to a point that contributes substantially to the species risk of extinction now or in the foreseeable future. The presence of small, newly-recruited animals in multiple areas spanning the species' range (except for the San Juan Islands) suggests that abundance levels are not low enough to lead to repeated recruitment failure. The threat of overutilization from fisheries harvest has largely been removed, because fisheries harvest of pinto abalone has been prohibited throughout most of the species range. Presently, harvest of pinto abalone is only allowed in Alaska's personal use and subsistence fisheries and in Mexico. The best available information indicates that these fisheries are not contributing substantially to the species' risk of extinction; however, data on harvest levels are needed to better assess how these fisheries may be affecting the status of the species in Alaska and Mexico.
Disease or Predation
Disease has been identified as a major threat to abalone species worldwide, with four significant abalone diseases emerging over the past several decades (withering syndrome, ganglioneuritis, vibriosis, and shell deformities). Pinto abalone are likely susceptible to all of these diseases, and have been confirmed to be highly susceptible to withering syndrome, a disease that has resulted in significant declines in black abalone populations throughout southern California. No infectious diseases affecting wild pinto abalone have been reported in Alaska, Washington, or California, but two abalone pathogens have been reported in British Columbia. To date, no outbreaks have been observed in wild populations and there is no evidence indicating that disease has been a major source of mortality in the recent past or currently. However, multiple sources and pathways exist for pathogens or invasive species to be introduced into wild pinto abalone populations, including aquaculture facilities and the movement of abalone (e.g., import, transfer) for aquaculture, research, and food/hobby markets (identified under the ``Inadequacy of existing regulatory mechanisms'' factor below). Great care is needed to closely monitor and manage these sources and pathways, to protect wild populations from potentially devastating pathogens and invasives.
Abalone face non-anthropogenic predatory pressure from a number of consumer species such as gastropods, octopuses, lobsters, sea stars, fishes and sea otters (Ault 1985; Estes and VanBlaricom, 1985; Shepherd and Breen 1992). Pinto abalone have been exposed to varying predation pressure through time and this pressure is likely to continue. However, in the past, pinto abalone populations may have been better able to absorb losses due to predation without compromising viability. Specifically, predation by sea otters has been raised as a potentially significant factor in the continued decline and/or lack of recovery of pinto abalone populations in areas where the two species overlap.
Sea otters were hunted to near extinction in the mid-1700s to 1800s, but have begun to recover in recent decades with protection from the North Pacific Fur Seal Convention of 1911, the Marine Mammal Protection Act, and the help of reintroductions in Southeast Alaska, British Columbia, and Washington in the late 1960s. Within the geographic range of pinto abalone, contemporary sea otter populations are present in Southeast Alaska, in two discrete population segments off British Columbia, from Cape Flattery to Destruction Island off Washington, from Half Moon Bay to near Gaviota on the mainland California coast, and at San Nicolas Island off southern California. Sea otter populations in these areas have been expanding in both abundance and distribution in recent years and are likely to continue to expand as the populations grow. Sea otters remain regionally extinct in the marine waters of Oregon and Baja California, Mexico.
Available data on red abalone in California suggests that sea otter predation typically reduces red abalone density by about 90 percent (Ebert 1968, Lowry and Pearse 1973, Cooper et al. 1977, Hines and Pearse 1982, Ostfeld 1982, Wendell 1994, Fanshawe et al. 2003) and eliminates viable commercial and recreational harvests of red abalone (Wild and Ames 1974, Estes and VanBlaricom 1985). Relationships of sea otters with pinto, white, and black abalone are uncertain because of lesser overlap in habitat characteristics, especially water depth. Sea otters are known to feed on pinto abalone, but the level of predation pressure and effects on pinto abalone populations have not been directly investigated and remain poorly known. To our knowledge there are no published data documenting effects of predation by sea otters on pinto abalone at the population level.
Continued growth of the sea otter population will encompass an increasing proportion of pinto abalone habitat and will increase the risk of predation by sea otters on pinto abalone populations. However, the effects are not clear. Observations by divers for the ADF&G on the outer coast of Southeast Alaska suggest that sea otters preferentially select red sea urchins and pinto abalone as prey when foraging in rocky subtidal habitats (Rumble and Hebert 2011). The dramatic increase in sea otter numbers and range has thus caused significant concern about benthic invertebrate fisheries in Southeast Alaska. However, in British Columbia, in at least two index sites where sea otters have been present for several years, densities of pinto abalone are higher than in areas with no sea otters (pers. comm. with J. Lessard, DFO, 24 April 2014). At one of these sites, the density of mature abalone in 2011 exceeded DFO's long-term recovery target of one abalone per sq m (pers. comm. with Joanne Lessard, DFO, on 24 April 2014). As in other areas along the coast, however, data are not available to determine the natural population levels of pinto abalone prior to the local extirpation of sea otters in British Columbia in the early 1920s. Thus, we lack historical data with which to compare current density estimates.
Sea otter predation will likely affect pinto abalone populations, but in no case has local extinction of any abalone population or species in the northeastern Pacific been documented as a result of predation by sea otters. Sea otters have been present in significant
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numbers in the coastal North Pacific Rim since the Pleistocene, and in northern hemisphere oceans of the earth for approximately seven million years. It seems certain that undisturbed populations of sea otters and abalones can sustainably co-exist as a consequence of co-evolved interactions.
Overall, the best available information indicates that threats associated with disease are not contributing substantially to the pinto abalone's risk of extinction now or in the foreseeable future. Disease could pose a risk to pinto abalone in the future if an outbreak of sufficient magnitude and scope occurs among wild populations, but the likelihood of such an outbreak is difficult to predict. The SRT emphasized the importance of closely monitoring and managing potential sources and pathways by which pathogens or invasive species could be introduced to wild populations (e.g., import or transfer of abalone for aquaculture, research, and food/hobby markets). Such precautions are important for the protection of all abalone species throughout the coast.
In addition, the best available information indicates that predation is not contributing substantially to the pinto abalone's risk of extinction presently or in the foreseeable future. Sea otter predation has likely contributed to continued declines and/or lack of recovery of pinto abalone populations where the two species overlap. However, we agree with the SRT's conclusion that sea otters and abalone can sustainably co-exist and that our criteria for healthy, sustainable abalone populations must account for the presence of sea otters in the ecosystem.
Inadequate Regulatory Mechanisms
Poaching has been a source of mortality for pinto abalone throughout their range since the establishment of harvesting regulations by the States and Canada. The problem of poaching clearly persists in some regions along the coast, particularly in British Columbia. The continued declines in mature pinto abalone densities at Haida Gwaii and along the Central Coast, despite the fisheries closures and observed recruitment events, were mainly attributed to illegal harvest (COSEWIC 2009). However, recent index site surveys in 2011 and 2012 indicate a decline in annual mortality at both the Haida Gwaii and Central Coast sites and an increase in both immature and mature abalone densities (pers. comm. with J. Lessard, DFO, on 24 April 2014). This decrease in annual mortality and increase in densities is most likely due to a decrease in poaching pressure as a result of existing regulatory mechanisms and outreach and education programs; however, it may also be due to other factors such as improved oceanographic conditions to support juvenile survival or the benefits of the fisheries closures finally being manifested in population recovery (pers. comm. with Joanne Lessard, DFO, on 24 April 2014). We are not aware of any evidence indicating illegal harvest is currently occurring in Washington, although several cases of illegal harvest and laundering of pinto abalone product were investigated in the late 1980s and periodic cases of illegal sport harvest were reported after the 1994 fishery closure (WDFW 2014). It is generally believed that current populations in Washington no longer exist at commercially-viable quantities, and the effort vs. reward deters poaching. WDFW enforcement covers the entire coast and includes at-sea monitoring of commercial and recreational fisheries and periodic patrols of commercial buyers and markets. However, Vadopalas and Watson (2013) identify poaching as a major threat to abalone in Washington. In other regions along the coast, poaching is recognized as a historical and future risk, but specific information on current levels of poaching is lacking. We are not aware of any enforcement cases or evidence for poaching, but continued efforts to enforce the regulations and monitor their effectiveness are needed to protect the species from this threat.
As discussed above (under ``Disease and Predation''), the introduction of pathogens or invasive species was also a concern identified by the SRT, given the potentially high risks posed by disease to pinto abalone. Regulatory mechanisms are advisable to ensure adequate monitoring whenever animals are moved (e.g., imports, transporting between facilities) for aquaculture, research, and/or food/hobby markets, to protect wild populations from pathogens and invasive species. In California, state regulations require abalone health monitoring at aquaculture facilities and control the importation/exportation of abalone between facilities. The State also monitors aquaculture facilities for introduced organisms and disease on a regular basis and restricts out-planting abalone from facilities that have not met certification standards. These measures will likely reduce the transmission of pathogens or invasive species from aquaculture facilities. In Washington and British Columbia, where abalone hatcheries are operated in support of restoration efforts, disease monitoring is also conducted and precautions are taken to avoid and minimize the transmission of pathogens and invasive species. Some improvements to existing regulations are needed to further protect the species. Although a permit is required to import non-native abalone species into California, a permit is not needed to import native abalone species, even if the source of those abalone is outside of the U.S. This presents a potential risk because live abalone imported into the State could carry pathogens. Information is not available regarding the amount of native abalone species that are imported into the U.S. from other countries each year.
Overall, based on the best available information, we conclude that existing regulatory mechanisms are adequate and that existing deficiencies in regulatory mechanisms are not contributing substantially to the pinto abalone's risk of extinction now or in the foreseeable future. Prohibitions on the harvest of pinto abalone throughout most of the coast provide a high level of protection for the species. Poaching continues to occur in British Columbia; however, recent increases in abalone densities at index sites were most likely due to reduced poaching pressure as a result of enforcement and outreach efforts, although favorable oceanographic conditions and reduced harvest pressure could have also contributed to these increases. In other areas, information on poaching is limited. Enforcement measures are in place throughout the coast, but monitoring is needed to ensure illegal take is not occurring. In addition, regulations and measures have been implemented to minimize the risk of transmitting pathogens or invasive species to wild populations. However, some improvements are advisable (e.g., to regulations on live abalone imports) to further protect pinto abalone and other abalone species.
Other Natural or Man-Made Factors
Among the other natural or human factors affecting pinto abalone, the SRT identified ocean acidification as a threat of greater concern. Ocean acidification is a concern particularly for early life stages because of the potential for reduced larval survival and shell growth, as well as increased shell abnormalities. The impacts of ocean acidification can be patchy in space and time and may develop slowly. Effects of ocean acidification on early life stages of pinto abalone are beginning to be understood. Laboratory studies indicate that reduced larval survival and shell abnormalities or decreased shell size
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occur at elevated levels of CO2 (800 and 1800 ppm CO2), compared to lower levels (400 ppm CO2) (Crim et al. 2011). Friedman et al. (unpublished data) have also found reduced larval survival occurs at elevated pCO2 and are studying the synergistic effects of increased pCO2, varying temperature, and exposure to Vibrio tubiashii on early life stages of pinto abalone (results pending).
Other climate-change related effects that may impact pinto abalone include increased water temperatures and decreased salinity (due to freshwater intrusions). Bouma's (2007) studies with cultured pinto abalone indicated that laboratory rearing temperatures of 11, 16, and 21 degC did not affect post-larval survival. Larvae tolerated temperatures of 12-21 degC, with mortality at 24 degC. Captive adult pinto abalone in Alaska showed no behavioral abnormalities at 2-
24 degC, but high mortality at 0.5 degC and 26.5 degC. Low salinity intrusions from freshwater inputs to Puget Sound and the San Juan Islands Archipelago may also have negative effects on pinto abalone recruitment. In laboratory experiments, early life stages of pinto abalone appear to be intolerant to low salinities below 26 psu (Bouma 2007). Bouma (2007) found that when introduced into a halocline microcosm (where salinity levels change with depth along the water column), larvae actively avoided areas of lower salinity. Later larval stages appear to be more tolerant of sub-optimal salinity levels (Bouma 2007).
In evaluating the threat of ocean acidification and other climate change impacts, the SRT recognized that some information is available regarding the potential effects of ocean acification, elevated water temperatures, and low salinity intrusions on pinto abalone. However, the SRT also recognized that our understanding of these effects includes a high degree of uncertainty, due to limited studies involving pinto abalone and the uncertainty and spatial variability in predictions regarding ocean acidification and climate change impacts into the future. The overall level of data available is low, especially regarding how ocean acidification may affect the species throughout its range, given variability in local conditions throughout the coast, natural variation in ocean pH, species adaptability, and projections of future carbon dioxide emissions.
Environmental pollutants and toxins are likely present in areas where pinto abalone have occurred and still do occur, but evidence suggesting causal and/or indirect negative effects on pinto abalone due to exposure to pollutants or toxins is lacking. In addition, very little is known regarding entrainment and/or impingement risks posed by coastal facilities. Direct effects would be focused on larval stages and be very localized in area. Despite uncertainties due to lack of data, the SRT felt that the risk posed by environmental pollutant/
toxins and entrainment or impingement is likely low given their limited geographic scope.
Overall, the best available information regarding other natural or manmade factors affecting pinto abalone do not indicate that these factors are contributing substantially to the species' risk of extinction now or in the foreseeable future. Ocean acidification and climate change impacts could affect pinto abalone in the future; however, the magnitude, scope, and nature of these effects are highly uncertain at this time.
Analysis of Demographic Risk
The SRT first identified a series of questions related to the four demographic risk criteria (abundance, growth rate/productivity, spatial structure/connectivity, and diversity), in order to structure their evaluation of these four criteria. For example, one of the questions related to the abundance criterion was: Is the species' abundance so low, or variability in abundance so high, that it is at risk of extinction due to depensatory processes? The SRT then assessed these questions using a voting process that was first used in an ESA status review by Brainard et al. (2011) to assess extinction risk for 82 coral species.
For each question, each SRT member scored the likelihood that the answer to each question was true, by anonymously assigning 10 points across the following eight likelihood bins, developed by the IPCC (Intergovernmental Panel on Climate Change 2007): exceptionally unlikely (99 percent). The IPCC (2007) developed this approach as one method for assessing the uncertainty of specific outcomes using expert judgment and, where available, quantitative information. The IPCC (2007) used this approach to evaluate the probability of occurrence of different climate change model outcomes, whereas Brainard et al. (2011) used this approach to qualitatively evaluate the likelihood that different coral species would fall below a defined critical risk threshold. In this status review, the SRT applied this approach to qualitatively evaluate the likelihood that pinto abalone are at risk of extinction due to different demographic risks. For each question, the scores were tallied (mean and range for each SRT member and across all SRT members) and reviewed, and the range of perspectives was discussed by the SRT. Each SRT member then had the opportunity to change their scores before submitting their final scores. Below, we summarize the SRT's conclusions regarding demographic risks. Additional details are provided in the status review report.
The SRT concluded that the risks to the species associated with abundance and population growth are moderate. Team members agreed that depensatory processes due to low and/or highly variable abundance or low population growth were a concern for pinto abalone in a number of locations (e.g., San Juan Island Archipelago, Alaska). Pinto abalone abundance and population growth have declined throughout the species' range, and, while there is some indication that recent recruitment has occurred in localized areas (e.g., Mexico, Point Loma, Palos Verdes, Mendocino County, British Columbia, Alaska), the rate of population growth is unknown. The SRT expressed some concern that population growth may not be occurring at a pace or extent sufficient to buffer against possible further declines due to processes happening over longer (e.g., PDO, IPO, climate change, and ocean acidification over decades; ENSO events over years) and/or uncertain time scales (e.g., cumulative oil spill impacts, poaching events, or harvest impacts). However, the SRT also expressed a high degree of uncertainty regarding the species' abundance and productivity.
The majority of SRT members agreed that spatial structure and diversity pose a low risk to pinto abalone. The SRT expressed a low level of concern regarding loss of variation in life history traits, population demography, morphology, behavior, or genetic characteristics. Most SRT members agreed that it is very unlikely that the species is at risk due to the loss of or changes in diversity, or due to alterations in the natural processes of dispersal, migration, and/or gene flow, or those that cause ecological variation. The SRT acknowledged that the species has experienced population declines and currently has a patchy distribution, but noted that the species has historically existed with a highly patchy distribution. The SRT was concerned about the potential loss of source populations or subpopulations in some areas due to past fishing pressure;
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however, they also expressed a high level of uncertainty regarding this risk, given the limited information on source-sink dynamics for pinto abalone. Recent evidence of localized recruitment in a few areas, spread over a wide geographic range (Alaska to Mexico) suggests that local populations are dense enough to support reproduction. The SRT's prevailing justification for concluding that spatial structure and diversity pose low risk to pinto abalone was that other related species of abalone that were overfished (e.g., red, pink, and green abalone) and that may exhibit lower spatial connectivity and/or genetic diversity than is suspected for pinto abalone, made remarkable recoveries in many locations range-wide over a period of roughly two decades (see status review report).
Overall, despite their high degree of uncertainty, the SRT members expressed low to moderate levels of concern for the majority of the questions and demographic categories. The SRT expressed a higher degree of uncertainty regarding the species' abundance and productivity and the risks posed by these demographic factors. However, none of the SRT members placed any of their likelihood points in the highest risk category (>99 percent) and they placed very few points ( In Alaska: (a) Establishment of regular, long-term monitoring of pinto abalone population abundance, trends, and distribution; and (b) monitoring and management of personal use and subsistence harvest to minimize impacts to pinto abalone. As discussed under the ``Summary of factors affecting the species'' (see the section on ``Overutilization''), ADF&G believes that personal use and subsistence harvest is currently low, but regulations still allow harvest of up to five pinto abalone per person per day. Monitoring would provide the data needed to estimate current harvest levels and to evaluate the impacts of these harvest levels (allowed and actual) on the pinto abalone population in Alaska.
In Washington: Surveys to evaluate the presence, abundance, and distribution of pinto abalone along the outer coast of Washington.
In Oregon: Surveys to evaluate the presence, abundance, and distribution of pinto abalone along the outer coast of Oregon. Revision of the fisheries regulations may also be needed to clarify that harvest of pinto abalone is prohibited.
In California: Establishment of regular, long-term monitoring of pinto abalone population abundance, trends, and distribution.
In Mexico: (a) Establishment of regular, long-term monitoring of pinto abalone population abundance, trends, and distribution; and (b) monitoring of pinto abalone harvest and, as needed, management measures to minimize impacts of fisheries harvest on pinto abalone. As discussed under the ``Summary of factors affecting the species'' (see the section on ``Overutilization''), current harvest levels of pinto abalone in Mexico are thought to be low. Monitoring would provide the data needed to estimate current harvest levels and their impacts on the pinto abalone population in Mexico.
Given the data gaps and uncertainties associated with our current understanding of the status of the species, we plan to retain pinto abalone on the NMFS Species of Concern list with one revision to apply the Species of Concern status throughout the species' range (Alaska to Mexico).
References
A complete list of all references cited herein is available on the NMFS West Coast Region Web site (http://www.westcoast.fisheries.noaa.gov/) and upon request (see FOR FURTHER INFORMATION CONTACT).
Authority: The authority for this action is the Endangered Species Act of 1973, as amended (16 U.S.C. 1531 et seq.).
Dated: December 22, 2014.
Eileen Sobeck,
Assistant Administrator, National Marine Fisheries Service.
FR Doc. 2014-30345 Filed 12-22-14; 4:15 pm
BILLING CODE 3510-22-P
