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Hindawi Publishing CorporationJournal of Marine BiologyVolume 2011, Article ID 749131, 14 pagesdoi:10.1155/2011/749131

Review Article

Tempering Expectations of Recovery for Previously ExploitedPopulations in a Fully Protected Marine Reserve

Jennifer K. Schultz,1 Joseph M. O’Malley,1 Elizabeth E. Kehn,2 Jeffrey J. Polovina,3

Frank A. Parrish,3 and Randall K. Kosaki2

1 Hawai‘i Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawai‘i at Manoa,P.O. Box 1346, Kaneohe, HI 96744, USA

2 Papahanaumokuakea Marine National Monument, NOAA, 6600 Kalaniana‘ole Highway no. 300, Honolulu, HI 96825, USA3 Pacific Islands Fisheries Science Center, National Marine Fisheries Services, NOAA, 2570 Dole Street, Honolulu, HI 96822, USA

Correspondence should be addressed to Jennifer K. Schultz, [email protected]

Received 15 June 2010; Revised 13 September 2010; Accepted 2 October 2010

Academic Editor: Benjamin S. Halpern

Copyright © 2011 Jennifer K. Schultz et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

Centuries of resource extraction have impacted coral reef ecosystems worldwide. In response, area and fishery closures are oftenenacted to restore previously exploited populations and reestablish diminished ecosystem function. During the 19th and 20thcenturies, monk seals, pearl oysters, and two lobster species were overharvested in the Northwestern Hawaiian Islands, nowmanaged as the Papahanaumokuakea Marine National Monument, one of the largest conservation areas in the world. Despiteyears of protection, these taxa have failed to recover. Here, we review each case, discussing possible factors that limit populationgrowth, including: Allee effects, interspecific interactions, and time lags. Additionally, large-scale climate changes may have alteredthe overall productivity of the system. We conclude that overfishing of coral reef fauna may have broad and lasting results; oncelost, valuable resources and services do not quickly rebound to pre-exploitation levels. In such instances, management options maybe limited to difficult choices: waiting hundreds of years for recovery, actively restoring populations, or accepting the new, oftenless desirable, alternate state.

1. Introduction

For centuries, coral reef ecosystems have been viewed asrenewable resources, from which countless organisms havebeen harvested to serve dependent human communities [1,2]. There is an underlying assumption that marine speciesare highly resilient to large population reductions and thatabundance may be quickly restored by area or fishery closures[3–5]. The capacity for self-repair, however, is dependentupon the extent of human impact and system resilience[6, 7]. Excessive and prolonged anthropogenic exploitationmay reduce resilience, that is, the capacity of a system topersist while maintaining key relationships and absorbingdisturbances [8]. For example, 15 years after fishery closures,there has been little recovery of several marine fish stocksthat were previously reduced 45%–99% [9, 10]. Thrush andDayton [11] review several examples of marine ecosystem

ratchets, in which recovery to pre-exploitation levels is nolonger possible [12]. In such instances, managers are forcedto accept the new, often less desirable, alternate ecosystemstate.

The Northwestern Hawaiian Islands (NWHI) span thecenter of the Hawaiian-Emperor seamount chain, the world’smost geographically isolated archipelago (Figure 1) [13]. Asof 2006, these small islands, atolls, reefs, and surroundingareas comprise the Papahanaumokuakea Marine NationalMonument, one of the largest marine protected areas in theworld. Fishing is not permitted, and the human populationis small (i.e., managers, researchers, and a small crew tostaff an emergency runway at Midway Atoll). Thus, theNWHI coral reef ecosystem is widely regarded to be “nearlypristine,” hosting predator-dominated communities, largefish populations, numerous coral species, and a healthy algalassemblage [14]. It has not, however, escaped human impact

2 Journal of Marine Biology

KureAtoll

Midway Atoll

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Laysan Island

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French Frigate Shoals

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Kaua'i

O'ahuMoloka'i

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Ladd Seamount

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Neva Shoal

North Hampton Seamounts

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Figure 1: The Northwestern Hawaiian Islands, protected as the Papahanaumokuakea Marine National Monument since 2006 (NOAA map).

[15], and modern species assemblages may only appearto be intact because baseline levels of abundance prior toexploitation are unknown (i.e., shifting baseline theory) [16].

2. Objectives

Here, we review anthropogenic impacts on the NWHI coralreef ecosystem, focusing on four of the best-studied species:Hawaiian monk seal (Monachus schauinslandi), black-lippedpearl oyster (Pinctada margaritifera), Hawaiian spiny lobster(Panulirus marginatus), and scaly slipper lobster (Scyllaridessquammosus). The lack of recovery demonstrated by thesetaxa may be a result of Allee effects, inter-specific competi-tion, and time lags. In addition, large-scale climate processesmay have altered the carrying capacity of the entire system.We consider the implications of these losses and providerecommendations for ecosystem-based management in theNWHI, now protected as the Papahanaumokuakea MarineNational Monument.

3. A Brief History of Anthropogenic Impacts inthe NWHI Coral Reef Ecosystem

The NWHI ecosystem has been significantly altered byhumans, beginning with early Native Hawaiian settlers(1000–1700 AD) and Western explorers of the late 18th

century [17]. Habitat disturbances include: guano mining atLaysan; modification of essential beach habitat by militaryactions at Midway Island, French Frigate Shoals, and KureAtoll; creation of channels at Midway and FFS; marine debrisaccumulation; and pollution [18–20]. In addition, a myriadof species occupying several trophic levels were harvested forsubsistence, food markets, bait, feathers, and shells (Table 1).

Between 1842 and 1915, a minimum of 1.3 millionseabirds was harvested at Laysan, Lisianski, and MidwayIslands [18, 21, 22]. Hunted for human consumption andto be used as shark bait, Hawaiian monk seals (Monachusschauinsalndi) and green sea turtles (Chelonia mydas) werenearly extirpated by the 20th century [19, 23]. Sharks wereheavily fished during the late 19th century [24–26] andas recently as 2000, when 990 individuals were taken in asingle 21-day exploratory shark-fishing trip [27]. Bottomfishstocks have been fished since the 1930s [28]. Harvest ofpelagic and nearshore fish species, including scrombridsand trevally, began after World War II and continued untilthe early 1990s. Approximately 150,000 black-lipped pearloysters (Pinctada margaritifera) were harvested at Pearl andHermes Reef between 1928 and 1930, severely depletingthe population [29]. Precious coral beds (Corallium spp.)have been exploited since 1965 [30]. In the mid-1970s, acommercial lobster fishery targeting Hawaiian spiny lobsters(Panulirus marginatus) and scaly slipper lobsters (Scyllaridessquammosus) became the state’s most valuable demersal

Journal of Marine Biology 3

Table 1: A brief history of extraction in the NWHI: Kure Atoll (Kur), Midway Island (Mid), Pearl and Hermes Reef (PHR), Lisianski Island(Lis), Laysan Island (Lay), and French Frigate Shoals (FFS). This list is not exhaustive and does not represent all extraction occurring in theNWHI.

Year(s) Site Taxa Notes

1842–1915LayLisMid

Seabirds:Sooty tern (Onychoprion fuscatus)Laysan albatross (Phoebastriaimmutabilis)Black-footed albatross (P. nigripes)Grey-backed tern (Sterna lunata)White tern (Gygis alba)Masked booby (Sula dactylatra)Lesser frigate bird (Fregata ariel)Great frigate bird (F. minor)Red-tailed tropicbird (Phaethonrubricauda)

1.3 million taken (recorded legal and illegalharvests); this does not include: records ofimplied harvest at additional locations and inadditional years, consumption by shipwreckedsailors, egg harvest, nesting habitat loss fromguano harvest (450,000 tons at Laysan Island),introduced species, and chick mortality due toremoval of parents [18–116].

19th century NWHIHawaiian monk seal (Monachusschauinslandi)

Hunted to near-extinction for meat, skins, andbait for shark fishery [23, 35]. For details, seeTable 2.

18th–19th centuries NWHI Green sea turtle (Chelonia mydas)

Extensively hunted for meat and eggs. Also usedas bait in shark fishery. Exploited for subsistenceand market in the 1940s and 1950s by commercialfishermen on FFS [117, 118].

1859–1900; 2000 NWHI

Sharks:Tiger (Galeocerdo cuvier)Galapagos (Carcharhinus galapagensis)Sandbar (C. plumbeus)Grey reef (C. amblyrhynchos)Blacktip (C. limbatus)

From 1859 to 1900, several vessels took part in afishery for shark fins and oil, removed a large butunknown number of sharks [25]. In 2000, 990sharks removed in a single 21-day shark fishingtrip to Nihoa Island, Necker Island, GardnerPinnacles, St. Rogatien Bank, and FFS [27].

1913–2002 NWHI

Fish:Trevally (Pseudocaranx spp.)Amberjacks (Seriola spp.)Big-eyed scad (Selar crumenopthalmus)Yellowfin tuna (Thunnus albacares)Bigeye (T. obesus)Skipjack tuna (Katsuwonus pelamis)Pink snapper (Pristipomoidesfilamentosus)Oblique-banded snapper (P. zonatus)Lavender snapper (P. seiboldii)Longtail snapper (Etelis coruscans)Squirrelfish snapper (Etelis carbunculus)Hawaiian grouper (Epinephelus quernus)Grey jobfish (Aprion virescens)

In 1913, Honolulu-based sampans began fishingfor trevally and amberjacks. A bottomfish fisheryoperated from 1930 to 2010. Following WorldWar II, vessels from Honolulu participated in aNWHI mixed-species fishery for bottomfish,lobsters, reef fish, inshore species, and turtles. In1946, fishing companies began using FFS as a baseof operations with planes exporting, among otherspecies, big-eyed scad [119]. Foreign anddomestic longline fleets exploited yellowfin andbigeye tuna while pole-and-line fleets targetedskipjack tuna and baitfish as early as the 1950s.The foreign longline fishery ended in 1980, thedomestic longline fishery lasted until 1991. Arecreational fishery for a variety of speciesoperated at Midway Island from 1996 to 2002,breaking several International Game FishAssociation line class world records.

1882

LayLisPHRFFS

Sea cucumber (Holothuria)

755 sea cucumbers (beche-de-mer) wereharvested at Lay, Lis, and PHR; an unknownamount were taken from FFS by the vessel Ada[18, 21, 27].

1928–1930 PHRBlack-lipped pearl oyster (Pinctadamargaritifera)

∼150,000 harvested [29].

1965–1980sNWHIGardnerLay

Pink coral (Corallium spp.)

Since 1965, foreign vessels used tangle nets toharvest precious coral; Taiwanese vessels illegallypoached 100 tons near Gardner Pinnacles and Lay[30].

1970–1999 NWHI

Hawaiian spiny lobster (Panulirusmarginatus)Scaly slipper lobster (Scyllaridessquammosus)

11 million individuals landed [32].


fishery, worth $6 million per year and landing ∼11 millionindividuals between 1983 and 1999 [31, 32].

Among the most heavily exploited species were seabirds,sea turtles, monk seals, pearl oysters, and lobsters. Dramaticpopulation declines precipitated taxon-specific legislation toprotect and promote growth within each of these species.The earliest protection of NWHI fauna was awarded toseabirds in 1909 via establishment of the Hawaiian IslandsReservation. Overharvesting of black-lipped pearl oystersat Pearl and Hermes Reef resulted in a 1930 moratoriumon harvest that was never lifted. The Hawaiian monk sealbecame protected under the US Marine Mammal ProtectionAct (1972) and the US Endangered Species Act (ESA 1976).The green sea turtle was listed under the ESA in 1978.The NWHI lobster fishery was closed indefinitely in 2000.Such legislative acts were accompanied by requirements forstock assessments. As a result, these taxa have become thebest-monitored species in the NWHI, and the only onesfor which long-term time-series data are available (i.e., thepopulation status of sharks, bony fishes, and precious coralsare uncertain due to infrequent, outdated and spatiallylimited fishery and survey data). In addition, broad habitatprotections were awarded to the NWHI when it was nameda Coral Reef Ecosystem Reserve under NOAA’s Office ofNational Marine Sanctuaries in 2000 and a Marine NationalMonument in 2006. These two executive acts have essentiallyprotected coral reef habitats and eliminated all recreationaland commercial exploitation within the NWHI.

Dedicated research surveys have since documented largepopulations of seabirds and sea turtles in the NWHI; how-ever, four species have not rebounded to pre-exploitationlevels: the Hawaiian monk seal, black-lipped pearl oyster,Hawaiian spiny lobster, and scaly slipper lobster. The lack ofpopulation growth in these taxa may be a result of species-specific factors, including Allee effects (mechanisms that leadto inverse density dependence at small population sizes [33]),redefined inter-specific interactions, or simply an inadequateamount of recovery time. Alternatively, large-scale climateprocesses may have altered productivity and trophic functionof the entire ecosystem. Here, we explore how variousfactors may have prevented the recovery of seals, oysters,and lobsters in the NWHI and discuss implications formanagement of the Papahanaumokuakea Marine NationalMonument.

4. Hawaiian Monk Seal

In 1805, Russian explorer Yuri Lisianski provided the firstwritten account of the Hawaiian monk seal [34]. Early on,population abundance was described in historical docu-ments as “numerous,” “many,” and “considerable” [35]. Inthe next 80 years, hundreds to thousands of seals were killedfor their meat, skins, and oil by sealers and shipwreckedsailors [23]. By the turn of the century, few seals wereobserved over 1–14 months, as reported by several vesselstraveling throughout the NWHI (Table 2) [35]. Commercialhunting ceased due to a lack of profitability, and the specieswas thought to be extinct.

Observations of monk seals in the early 20th centuryindicated that at least 23 individuals must have survivedat the nadir of the bottleneck [36]. By 1958, 916 nonpupseals (i.e., seals over the age of one) were counted in thefirst systematic beach survey [37, 38]. From this count, totalpopulation size was estimated to be 1350–2962 individuals[38, 39]. The species was thought to be on the path torecovery, similar to other previously exploited pinnipedpopulations.

By 1978, however, low juvenile survival had resulted in a50% population decline (Table 2). Despite active protectionand management, overall species abundance continues todecline at ∼4.1% per year as a result of low reproductiverates and high juvenile mortality, attributed to emaciation,shark predation, and entanglement in marine debris [40, 41].The most recent estimate of total population size is 1,146individuals [41]. The International Union for Conservationof Nature (IUCN) has listed the species as Critically Endan-gered, reflecting its high risk of extinction in the wild [42].

The stunted recovery and subsequent decline of theHawaiian monk seal may be attributed to Allee effects. Videofootage reveals that female seals defend their preweanedpups against predation by Galapagos sharks. A larger num-ber of nursing females would provide increased vigilance(e.g., observance and barking) and aggression (e.g., biting).Inbreeding depression (i.e., diminished fitness of inbredindividuals) is a common Allee effect that often results inhigh juvenile mortality rates and low reproductive rates, bothof which are exhibited by the species. Further research isrequired to determine the impact of inbreeding depressionon the population [36]. Genetic diversity has been virtuallylost throughout the genome, likely as a result of long-termpopulation reduction [36, 43–46]. Though genetic diversityis essential for population persistence and to mount aneffective immune response [47], its contribution to thecurrent decline of the species remains unknown.

Another explanation for the current decline in monkseals is inter-specific competition and reduced prey abun-dance. Emaciation and poor survival of juvenile seals in theNWHI suggests food limitation and stress in the forage base[48]. Dietary overlap has been documented between sealsand large predatory fish in the region [49–53], and overallprey scarcity intensifies competition among these top-levelpredators. Cameras mounted on the backs of seals showjacks, snappers, and sharks attempting to steal prey that sealshave flushed from cover; these predatory fish also bully theseal for prey in its mouth [53]. Juvenile seals appear to bemost vulnerable to the impacts of competition. Furthermore,pre-weaned pups are increasingly preyed upon by sharks inthe NWHI [40]. In contrast, there is high pup and juvenilesurvivorship in the main Hawaiian Islands [54], where thebiomass of large predatory fish is an order of magnitudelower [55]. Without time-series data on shark, jack, and preypopulations in the NWHI, we cannot determine whetherpredatory fish have assumed the niche once held by seals, norwhether there is increased competition due to diminishedprey abundance.

Compared to other apex predators, seals are unique intheir ability to forage across a wide depth range and to


Table 2: Historical counts of Hawaiian monk seals in the NWHI, at: Kure Atoll (Kur), Midway Island (Mid), Pearl and Hermes Reef (PHR),Lisianski Island (Lis), Laysan Island (Lay), and French Frigate Shoals (FFS). These do not represent overall population estimates. Numbersin bold represent seals killed; numbers in italics represent seals observed. Annotated from Ragen [5] and Hiruki and Ragen [6].

Year Site Seals taken or observed Notes

1805 Lis 4 Exploratory tour of NWHI [34]

1842 Kur ∼ 60 Food for shipwrecked crew [120]

1850 Lis ? Food for shipwrecked crew [121]

1850 PHR 10–12 Food for visiting crew [122]

1859 NWHI 1500? Returned with “1500 seal and shark skins” [123]

1870 Mid, Kur >60 Food for shipwrecked sailors [124]

1886 Lay ? Bait for shark fishing [125]

1888 Mid 0 Shipwrecked crew observed no seals in 14 months [125, 126]

1891 NWHI 1 Sealing mission; only one seal observed [127]

1891 Lay 0 No seals observed in six weeks [128]

1896 Lay 0 No seals observed in three months [129]

1905 Lay 0 No seals observed [130]

1911 Lay 0 No seals observed in six weeks [131]

1912 FFS 0 No seals observed [126]

1912 Lay 1 One seal observed in three months [126]

1912 Lis 2 Two seals observed [126]

1913 Mid 5-6 [132]

1923 Lay 4 [132]

1923 Lis 10 10 seals taken [126]

1923 PHR 125 [119]

1923 Kur 40–50 Seals observed [133]

1934 Kur 50–60 Seen in water or land [21]

1941 Mid 6 Observed over 6 month period [134]

1949 Lay 20–30 Partial count [126]

1949 PHR 100 More than 100 seals [126]

1950 Lis 100 At least 100 seals observed [135]

1958 NWHI 916 Beach count of nonpups [37, 38]

1968 NWHI 456 Incomplete beach count (J. Baker, pers. comm.) [136]

1978 NWHI 468 Incomplete beach count (J. Baker, pers. comm.) [136]

1988 NWHI 486 Beach count of nonpups (J. Baker, pers. comm.) [40]

1998 NWHI 391 Beach count of nonpups (J. Baker, pers. comm.) [40]

2008 NWHI 293 Beach count of nonpups [41]

access cryptic prey found under rocks and buried in thesand. As central-place foragers, they undertake extensivemovements to feed at neighboring banks, across habitat typesand down to subphotic depths [56]. They are generalists andexert top-down pressure that can structure their diverse preycommunity, including demersal and benthic species [49, 52].Patterns of prey depletion persist in the slow-growing fishcommunities at subphotic depths close to the seal colonies[57]. Therefore, changes in monk seal abundance could havemajor impacts at lower trophic levels.

5. Black-Lipped Pearl Oyster

The black-lipped pearl oyster is harvested and cultivatedthroughout its range in the Indian and Pacific Oceans forpearls and the nacre of the shell, or “mother of pearl.”Though the species is uncommon throughout the NWHI,

there was once a large population at Pearl and HermesReef [58]. Between 1928 and 1930, approximately 150,000pearl oysters were taken, eliciting a ban on harvest by theHawai‘i Territorial government with the expectation that thefishery would reopen in five years [59]. In 1930, Galtsoff[29] conducted a six-week abundance survey of the Pearland Hermes Reef stock; he found 480 individuals andconcluded that the population was too depleted to sustainfurther harvesting. A 1993 study indicated that pearl oysterdensities had not increased after 60 years of protection [60].Additional surveys in 2000 and 2002 found few oysters [61].In 2003, Keenan et al. [59] conducted an in-depth survey ofpearl oyster abundance and found a lower average densitythan that of similar areas in 1930 (Table 3). Additionalsurveys (2004–2006) confirmed that the Pearl and HermesReef population remains in its depleted state after 80 years ofprotection [58].


Table 3: Harvested numbers and survey counts of black-lipped pearl oysters at Pearl and Hermes Reef.

1928–1930 (harvest) 1930 (post harvest) 2003(recent survey)

No. of pearl oysters observed ∼150,000 480 1047

Density (ind./km2) Unknown 209–349 177

Average shell length (cm) Unknown 20.2 20.2

Depth range (m) Unknown 2.5–15 0.3–6.0

Depth most abundant (m) 1.0–3.0 4.4–8.3 0.5–2.2

Source [29] [29] [59]

As described by Keenan et al. [59], Allee effects may haveprevented recovery of the black-lipped pearl oyster at Pearland Hermes Reef. Depletion of the adult population likelyresulted in reduced reproductive potential of these broadcastspawners, as a result of an overall decrease in the abundanceof gametes and a reduced chance of fertilization [62].Additionally, pearl oysters are protandrous hermaphrodites,starting life as males with a proportion of the populationbecoming female when larger. The removal of the largestadults would have removed a high percentage of the females,thereby skewing the sex ratio and decreasing the overallfecundity of the population [62]. Because the planktoniclarvae settle gregariously on the shells of adult oysters, theloss of settlement cues would also diminish recruitment [59].The importance of these processes is highlighted by the factthat the Pearl and Hermes Reef pearl oyster population hasnot increased for nearly 80 years after the cessation of harvest.

Though the last harvest of NWHI pearl oysters occurredin 1930, population recovery may require additional time.Unlike the monk seal, pearl oysters are not endemic toHawai‘i, and their recovery may be aided by externalrecruitment. Pearl oysters are sessile as adults, and the pelagiclarvae settle 20–23 days after fertilization [63]. Given theextreme isolation of the Hawaiian Archipelago and the rarityof the species throughout Hawai‘i, external recruitment islikely uncommon, but the chance of such an occurrenceincreases with time. Also, it is possible that environmentalconditions are rarely favorable to produce or support largepopulations in the NWHI, accounting for their scarcitythroughout the archipelago. Therefore, recovery may requireevolutionary time scales (i.e., hundreds of years or more)rather than management time scales (i.e., years or decades).

As filter feeders, pearl oyster populations have thepotential to greatly affect levels of phytoplankton in thesurrounding water column [62]. The black-lipped pearloyster has a large gill size and a high pumping rate, whichmakes it viable even in nutrient poor waters [64]. It can grazeplankton down to extremely low levels [65]. For this reason,oysters are a mechanism for strong benthic-pelagic coupling,transferring planktonic energy to the benthic environment[66]. The organics and minerals from the water columnmake up the shell and soft body tissue of the oyster, andthe unassimilated portion of the filtered plankton (discardedas feces) enriches the seafloor [65]. These filter-feeders alsoinfluence the ecosystem by decreasing the particle load inthe water column, which allows light penetration to depthsand improves conditions for photosynthesis. Therefore, the

depletion of the large population at Pearl and Hermes Reeflikely had a strong impact on ecosystem function, as a resultof the loss of the benthic/pelagic coupling and filteringcapacity.

6. Hawaiian Spiny Lobster andScaly Slipper Lobster

In 1975, the National Marine Fisheries Service, the U.S.Fish and Wildlife Service, and the Hawai‘i Division of Fishand Game conducted a five-year survey and assessmentof the marine resources of the NWHI. Populations of theendemic Hawaiian spiny lobster were found throughoutthe NWHI, with particularly high concentrations at NeckerIsland and Maro Reef [67]. Survey catch rates “showedexcellent potential for development” [68] and were followedby industrialized commercial exploitation. Fishing effortsremained relatively low (<10 vessels, 400 traps hauled/vesselday) until 1984 when the introduction of new traps resultedin a fourfold increase in effort in just two years (16 vessels,1000 traps hauled/vessel day). In addition, the new traps hada smaller mesh size that increased catch of the scaly slipperlobster, also found throughout the NWHI (Figure 2) [69, 70].

The NWHI lobster fishery was unregulated and unmon-itored until 1983. Despite several management measures,the fishery suffered severe declines in catch per unit effort(CPUE) as determined in near-annual stock assessmentsfrom 1985 to 2000 (Figure 3). Archipelago-wide spiny lobstertrap CPUE, considered an adequate proxy for density [71,72], fell from 3.41 in 1983 to 1.0 in 1986. In particular, thehistorically high density Necker Island population CPUE fellfrom 4.0 in 1983 to 1.2 in 1987. Archipelago-wide slipperlobster CPUE also declined quickly from a high of 1.21 in1985 to 0.17 in 1991. The declining CPUE of both speciesresulted in a complete fishery closure in 1993, a shortened (8week) fishery in 1994, and a one vessel exploratory fisheryin 1995. The fishery was indefinitely closed in 2000 becauseof increasing uncertainty in the population models usedto assess stock status [73]. An extensive tagging program,designed to examine lobster dynamics, demonstrated thatNWHI lobster abundances have not increased appreciablyfrom 1999 levels. Spiny lobster CPUE in 2008 was 0.80, 0.29,and 0.77 at Necker Island, Gardner Pinnacles, and Maro Reef,respectively [74]. Slipper lobster CPUE was 0.26, 0.23, and0.75 at Necker Island, Gardner Pinnacles, and Maro Reef,respectively.


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Figure 2: Commercial catch (×1000) of Hawaiian spiny lobster(Panulirus marginatus) and scaly slipper lobster (Scyllarides squam-mosus) in the NWHI from 1983 to 1999. The fishery was closed in1993, and management measures impacted catch in 1994 and 1995.

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Figure 3: Commercial catch per-unit effort (CPUE; number of lob-sters captured per trap haul) for Hawaiian spiny lobsters (Panulirusmarginatus) and scaly slipper lobster (Scyllarides squammosus) inthe NWHI from 1983 to 1999. The fishery was closed in 1993.

Allee effects could be delaying the recovery of lobstersin the NWHI. Spiny and slipper lobster egg productionwas significantly reduced by the removal of females inpast decades. The loss of larger females was particularlydamaging, because they produce a disproportionately greaternumber of eggs [75, 76]. As lobster densities decreased dueto fishing, Necker Island spiny lobster size-specific fecundityincreased, a negative density-dependent, or compensatory,response [76, 77]. Although the long pelagic duration stagetypically decouples recruitment success from fecundity [78],the lack of recovery indicates that the compensatory responsemay not have been enough to counter survival componentAllee effects, such as the “dilution effect” (as prey groupsget smaller or prey populations sparser, individual preyvulnerability increases [79]), during the pelagic or earlybenthic stage. The gregarious nature of palinurids andscyllarids also leaves them vulnerable to Allee effects. While

it is unclear exactly which cues pelagic-phase NWHI lobsters(phyllosoma, puerulus, and nisto) utilize to orient towardstheir benthic settlement habitat, laboratory and field researchof P. argus suggest that conspecific cues play an importantrole [80]. The gregarious behavior is also generally thoughtto be a defense mechanism via group vigilance, aggression,and the dilution effect [81, 82]. At minimum, the “guide”effect reduces individual exposure to predation by allowingconspecifics to locate nearby, high-quality shelter [83, 84].

The recovery of lobster populations may be only amatter of time. At the time of the fishery closure, it wasassumed that lobster populations would rebound quicklyand commercial fishing would commence in a few years.Palinurids are resilient to high fishing mortality and havethe potential to recover quickly from low abundances.Pollock [85] attributes this to density-dependent factors,such as labile size-at-maturity, juvenile growth, and survivalrates, which increase egg production at lower populationdensities. Several highly exploited species rebounded inless than a decade, including New Zealand and Australianrock lobsters (Jasus edwardsii and P. cygnus), the ornatespiny lobster (P. ornatus) of the Torres Strait and PapuaNew Guinea, and six species of Palinurus in Japan [86–89]. Therefore, it is somewhat surprising that NWHI lob-ster populations have not recovered in the past decade,especially since fishing has ceased, egg production shouldbe increasing, and oceanographic conditions favorable tolobster recruitment occurred in 1988–2002 and 2007–2009(http://jisao.washington.edu/pdo/PDO.latest).

Severe declines in lobster populations likely impactedecosystem function. Lobsters and other macroheterotrophsfeed on the detrital and planktonic energy that is storedin the benthos as infauna (micro molluscs, annalids, etc.).Field evaluations of lobsters have found that their nutritionalcondition can vary over space and time, presumably inrelation to prey availability [90]. Gleaning energy fromthe benthos, populations of macro-heterotrophs comprise apathway to higher trophic levels, serving as prey items forsharks, jacks, and seals [49, 51, 91, 92]. A sizable reductionin macro-hetereotrophs has the potential for reducing theflux of energy through the benthos and up the food web.Therefore, the loss of lobster populations could result in abenthic energy sink, constraining the flow of energy to uppertrophic levels.

7. Oceanographic Processes

Large-scale oceanographic processes have the potential toalter trophic interactions throughout a food web. Suchregime shifts result in profoundly different ecosystem struc-ture. There is some evidence for large-scale ecosystemchanges in the NWHI, linked to productivity. Of the six taxafor which long-term, in-depth population data is available,only two have recovered to significant abundance: seabirdsand sea turtles. These species differ from seals, oysters, andlobsters in that they utilize the NWHI for reproductivepurposes only and not to forage. Turtles and seabirds receive


little energy input from the NWHI and are not trophicallydependent upon this coral reef ecosystem.

Alternatively, species dependent on the NWHI fornutrient uptake have not rebounded to pre-exploitationlevels. The Hawaiian monk seal, black-lipped pearl oyster,Hawaiian spiny lobster, and scaly slipper lobster representvarious trophic levels in a coral reef ecosystem. The monkseal is a high trophic level species that exerts top-downpredation pressure in shallow and deep-water reefs. Lobstersare low trophic level heterotrophic benthos carnivores thattransfer benthic productivity up the food chain. Pearl oystersharvest planktonic productivity from surrounding waters,such that these nutrients become incorporated into coral reeffood webs. Though these taxa have different life histories,population dynamics, and ecological niches, all have failed torecover from exploitation. What mechanisms could accountfor diminished productivity across such varied trophic levels?Marine ecosystems in the Hawaiian Archipelago may beimpacted by three large-scale climate processes operatingon different time scales: the inter-annual El Nino SouthernOscillation (ENSO), the Pacific Decadal Oscillation (PDO),and long-term, global climate change. At any time, all threeof these climate signals may be impacting Hawai‘i withvarying intensities.

The best evidence of a link between climate and anecosystem response in the NWHI occurs at the northernatolls. In some winters, often during El Nino years, thevertically mixed high-surface chlorophyll transition zone,termed the Transition Zone Chlorophyll Front (TZCF), shiftssufficiently far south that the three northern atolls (i.e.,Kure Atoll, Midway Island, and Pearl and Hermes Reef) liewithin its productive waters (Figure 4) [93]. The temporaldynamics of monk seal populations at these northern atolls ischaracterized by large interannual variation in pup survival,rather than the long-term declining trend observed for thelargest population at French Frigate Shoals [94]. Further,monk seal pup survival increases two years after the TZCFshifts southward. The two-year lag between the position ofthe TZCF and monk seal pup survival is thought to representa temporal lag between changes at the base of the food weband monk seal prey items several trophic steps removed[94]. This hypothesis is supported by an ocean-planktonmodel indicating a strong physical, chemical, and biologicalgradient that impacts lower trophic level productivity [95].The relationship appears only to impact the northern atolls,so it does not account for overall monk seal dynamics or thetrends observed in lobster species at the southern atolls. Itmay, however, have a profound impact on pearl oysters inthe NWHI, which have only ever occurred in large numbersat Pearl and Hermes Reef.

Changes in the PDO (i.e., the interdecadal shift betweenwarm and cool surface waters in the North Pacific) will alsoresult in atmospheric and oceanic changes that could impactproductivity and circulation in Hawaiian waters, potentiallyresulting in ecosystem regime shifts. The intensificationof the Aleutian Low Pressure System during 1977–1988,characteristic of the positive phase of the PDO, may haveresulted in increased deep mixing, leading to more nutrientsin the mixed layer and ultimately enhanced ecosystem

productivity [96]. After this event ended, productivity inthe NWHI diminished. In the late 1980s, 30%–50% declineswere documented for seabird reproductive success, monkseal pup survival and spiny lobster recruitment [96]. Betweenthe mid-1990s and 2010, the PDO has gone throughanother cycle of positive and negative modes, but similarshifts in productivity have not been repeated. This lack ofrepeatability may disprove the existence of a relationshipbetween PDO and productivity, or the relationship may bemore complicated, as a result of time lags and complexecosystem interactions.

ENSO and PDO oscillate between two well-definedalternate states or modes; however, the global climatechange signal is expressed as an increasing temporal trend.One impact attributed to this trend is increased verticalstratification in the subtropical gyre. This leads to a reductionin nutrients mixed into the euphotic zone and reducedprimary production. Based on satellite remotely sensedestimates of surface chlorophyll, the least productive areasof major oceans (i.e., the core of the subtropical gyres) haveexpanded over the past decade [97]. Though the time seriesof SeaWiFS chlorophyll data are limited to the past 12 years,this trend could be responsible for long-term reduction ofcarrying capacity in the NWHI ecosystem. Further researchis required to determine whether the change in productivityis responsible for the lack of recovery in seals, oysters, andlobsters.

8. Implications and Recommendations forEcosystem-Based Management

Marine ecosystem-based management (EBM) is designed toprotect ecosystem integrity and to achieve long-term sustain-ability [98–101]. Specific objectives of EBM often includethe maintenance of viable populations and the restorationof depleted resources [102, 103]. Marine mammals, bivalves,and lobsters are often considered keystone species [104, 105]and may be essential in maintaining ecosystem integrity[106, 107], as the removal of apex predators, suspensionfeeders, and grazers has diminished the capacity for resiliencein other systems [1]. Even the loss of a single species withinthese functional groups reduces overall biodiversity andmay be detrimental to natural ecological dynamics [6, 108].Therefore, while single species are not the target of protec-tion, they remain important to management considerations[109].

Management interventions, such as fishery or areaclosures, are often enacted to recover depleted taxa. Wehave shown that these actions do not automatically resultin immediate or rapid population growth. Overexploitationcan result in widespread impacts that resonate throughthe system for decades, especially if intra- and interspeciesdynamics have changed, or if energy input has been reduced.In such instances, managers generally have three options:provide additional time for recovery, actively try to restorepopulations, or accept that irreversible change has occurredand adapt to the new, altered system [6]. We will considereach of these options as it pertains to the NWHI (which


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Figure 4: Surface chlorophyll estimated from SeaWiFS ocean color for (a) March 2000 basin-scale, (b) March 2000 wherenorthern atolls remain in low chlorophyll water, and (c) March 2004 where high-chlorophyll waters reach the northern atolls(http://oceancolor.gsfc.nasa.gov/SeaWiFS/).

since 2006 have been protected as the PapahanaumokuakeaMarine National Monument) and provide suggestions forresearch and management.

Though it appears that adequate time has passed forseal, oyster, and lobster populations to recover from previousexploitation, we may need to alter our expectations ofpopulation growth following excessive take. For exam-ple, Hawaiian lobster and monk seal dynamics may beexplained by metapopulation theory [110], in which survivaland growth rates vary spatially among metapopulations,connected by gene flow [74, 111, 112]. Extinction and

recolonization events may occur at broad spatial andtemporal scales, most of which are beyond the scope ofcontemporary research. These natural troughs and peaksoccur even in the absence of anthropogenic stressors butmay be exacerbated by over-exploitation. Another possibilityis that reef species have low-frequency recruitment pulses,perhaps linked to stochastic local environmental processes.Oyster and lobster populations, for example, may havevery low annual recruitment, with the exception that onceevery 50–100 years, they experience a period of highrecruitment. Such theories would suggest that it is difficult


to sustain single-species fisheries in coral reef ecosystems.The Papahanaumokuakea Marine National Monument isone of the largest marine protected areas in the world. Asno recreational or commercial extraction occurs within itswaters, it provides a natural laboratory in which to evaluatethe amount of time required for population recovery whenanthropogenic impacts are controlled (with the exceptionof global pollution and climate change). Within a protectedarea such as this, research becomes the main managementactivity. Thus, we recommend focus on the following astopics for future study:

(i) long-term monitoring of multiple species to detectshifting population trends,

(ii) research on inter-specific interactions to determinehow systems shift over time after a perturbation,

(iii) research on metapopulation dynamics to establishbaseline levels of recruitment, connectivity and spa-tial/temporal shifts in abundance.

Another option is active management and restoration.At French Frigate Shoals, translocation of at-risk Hawaiianmonk seals and removal of ten Galapagos sharks over fouryears reduced predation on pre-weaned and recently weanedpups from 31 in 1997 to 11 in 2003 [40]. The continuationand expansion of such initiatives should be considered.Monk seals and pearl oysters may benefit from captive breed-ing and eventual release, though the risks associated withsuch activities are high and must be thoroughly researched.Aquaculture of black-lipped pearl oysters from Pearl andHermes Reef could aid in the recovery of the population[113]. Because bivalves settle in the presence of conspecifics[114], discarded shells left on the beach at Pearl and Hermescould be placed on the reef to encourage settlement. Inaddition, live adult oysters could be moved closer together toincrease fertilization success as well as induce the settlementof larvae. These interventions could alleviate certain Alleeeffects, but other factors may contribute to the lack of popu-lation growth. If oceanographic processes influence carryingcapacity, such management actions may be unsuccessful.Furthermore, well-intentioned attempts at restoration couldhave unintended and unpredictable ecological impacts of amagnitude comparable to those of overextraction. Therefore,this option requires:

(i) historical data on preimpact abundance (includingtraditional Hawaiian knowledge in the form of orallytransmitted histories, chants, and genealogies),

(ii) knowledge of climate patterns,

(iii) flexibility (i.e., adaptive management) to mitigateunforeseen complications.

Managers may be limited to the third option: loweringtheir expectations of productivity in the altered system.Coral reefs have been described as oases of biodiversity inoligotrophic, oceanic deserts [49]. They may foster intensecompetition among species within the same functionalgroup, such that when one species is depleted via exploita-tion, another fills its niche and prevents subsequent recovery.

This paradigm of coral reef dynamics suggests low resilienceof any one species but high functional group resilience; thus,focus on the preservation of trophic guilds is appropriate.However, catastrophic phase shifts (e.g., over-fishing ofherbivorous fish followed by a sea urchin disease epidemicled to algal-dominated reefs in the Caribbean) stress theneed to maintain highly diverse functional groups in orderto sustain healthy ecosystems [115]. The NWHI can serveas a natural laboratory to examine hypotheses regardingfactors thought to confer resistance or resilience (e.g.,species diversity, genetic diversity, diversity within trophicguilds, and functional redundancy) without a plethora ofconfounding local impacts and stressors. As such, it providesa “control” for comparison with reefs elsewhere in Hawai‘iand throughout the world. Therefore, appropriate objectivesfor EMB are:

(i) maintenance of food-web dynamics and intricacies,

(ii) investigation of ecosystem function and energy flow,including research at and across all trophic levels toquantify productivity and address redundancy,

(iii) assessment of capacity for resilience against potentialanthropogenic disturbances, such as climate change,pollution, or invasive species.

9. Conclusions

Though far from pristine, the NWHI coral reef ecosystem isnot beyond repair. We recommend that managers continueto provide time for recovery while permitting minor inter-ventions for research and restoration purposes. The examplesdiscussed in this paper require that we change the way wethink about the recovery of previously exploited populations.Time should be considered in the context of the slowgradual changes and sudden shifts characteristic of naturalprocesses. Ecosystems do not operate at a single stable stateand may not recover to the original wilderness conditionafter a disturbance. Populations that fail to recover shouldnot be considered isolated events, but rather interpreted asthe loss of essential ecosystem components that possiblyreflect broad-scale changes. The NWHI coral reef ecosys-tem provides an important cautionary lesson: a perturbedecosystem does not automatically revert to its previous statewhen stressors are removed. This message, utilized as aneducational tool, will be important in informing marinemanagement in the Papahanaumokuakea Marine NationalMonument and throughout the world.

Acknowledgments

The authors thank editor B. Halpern and two anonymousreviewers for their insightful recommendations that greatlyimproved this paper. They also would like to thank C. Wienerand T. McGovern for helpful comments on an earlier versionof the paper. J. K. Schultz was supported by a SOEST YoungInvestigator fellowship and a grant from the Marine BiologyConservation Institute. This is contribution no. 1413 fromthe Hawai‘i Institute of Marine Biology and contribution


no. 8027 from the School of Ocean and Earth Science andTechnology at the University of Hawai‘i.

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