Uncertain Management or Management of Uncertainty: Steller Sea Lion a Case Study

Transcription

1 Sea Lions of the World 521 Alaska Sea Grant College Program AK-SG-06-01, 2006 Uncertain Management or Management of Uncertainty: Steller Sea Lion a Case Study Robert J. Small Alaska Department of Fish and Game, Juneau, Alaska Douglas P. DeMaster NOAA Fisheries, Alaska Fisheries Science Center, Seattle, Washington Abstract The abundance of Steller sea lions (sea lions) declined ~15% per year during the 1980s in the Bering Sea, Aleutian Islands, and Gulf of Alaska regions, resulting in a threatened listing under the Endangered Species Act (ESA) in Numerous factors may have contributed to the decline, and there has been substantial uncertainty regarding the relative impact of these factors when management actions were implemented to promote recovery. One key hypothesis for the continued decline in the 1990s (~5%/year) has been a reduction in sea lion prey biomass and quality caused by either commercial fishing or an oceanographic regime shift resulting in substantial changes in the abundance or availability of dominant prey species, which may have subsequently resulted in nutritional stress on the sea lion population. Following the 1997 ESA endangered listing of the western population and the determination that competition with commercial groundfish fisheries in Alaska was likely, additional fishery management restrictions were implemented. Counts of sea lions in 2002 and 2004 indicate the decline of sea lions may have begun to cease. The evidence for nutritional stress, especially post-1990, is somewhat contradictory and equivocal which contributes to continued uncertainty. Given the ESA s mandate to U.S. federal regulatory agencies to manage in a strongly precautionary manner, greater uncertainty can be translated to mean more precautionary management. To address ongoing uncertainty about causal factors and the efficacy of conservation actions, we believe that a research strategy with four primary components should be pursued: (1) population monitoring and fundamental sea lion ecologi-

2 522 Small and DeMaster Steller Sea Lion Management cal research, (2) fishery interaction studies designed to test the localized depletion hypothesis, (3) determining the mechanism by which changes in prey biomass or nutritional quality of the prey species may result in chronic nutritional stress that results in decreased sea lion survival and reproduction, and (4) adaptive management experiments to assess the impact of fisheries on the sea lion prey field and subsequently sea lion demography. In addition, recently suggested modifications to conservation policy should be pursued: (a) establishing a specific quantitative standard for risk of extinction (under the ESA), (b) defining jeopardy and adverse modification of critical habitat (under the ESA) in terms of risk of extinction, and (c) establishing a quantitative standard for ecosystem protection in developing recovery strategies for ESA listed species. Implementation of these research and conservation policy recommendations could substantially decrease uncertainty and increase the probability of effective conservation of sea lions. Introduction The abundance of Steller sea lions (sea lions) declined at an annual rate of ~15% during the 1980s in the Bering Sea and Aleutian Islands (BSAI) and Gulf of Alaska (GOA) regions, with substantial spatial and temporal differences in the decline across their extensive geographic range. Although important life history and population assessment research was conducted on sea lions during the 1980s, knowledge of the functional relationships that had caused the overall abundance to decline by ~80% by 1990 was scant (Braham et al. 1980; Loughlin et al. 1984, 1992; Trites and Larkin 1996; Merrick et al. 1997; NMFS 2001). Numerous factors have been considered as contributing causes of the decline, including: incidental mortality in fisheries, pollution and contaminants, harassment and illegal shooting, commercial harvests of pups, Alaska Native subsistence harvests, disease, predation, and reduced prey biomass and quality due to oceanographic changes (i.e., regime shifts) and indirect competition for prey with commercial fisheries resulting in nutritional stress (Fritz et al. 1995, Loughlin and York 2000, NMFS 2000, NMFS 2001, Trites and Donnelly 2003, Springer et al. 2003). Evidence of decreased juvenile survival, based on mark-resight and modeling analyses, and a reduction in pregnancy and lactation rates of adult females between the 1970s and 1980s indicated that nutritional stress could be one contributing cause of the decline (Calkins and Goodwin 1988, York 1994, Loughlin 1998, Sease and Merrick 1997, Trites and Donnelly 2003). Although the functional mechanism by which nutritional stress could reduce survival and reproduction was unknown, the basic premise was a bottom up effect due to reduced prey biomass or availability and/or nutritional quality of the prey. Such nutritional stress would have occurred during the period when commercial fisheries ex-

3 Sea Lions of the World 523 panded in the BSAI and GOA regions, and followed a substantial regime shift in the late 1970s (Fritz et al. 1995, Calkins et al. 1998, Benson and Trites 2002). Both fisheries and the effect of regime shifts can potentially reduce sea lion prey biomass and quality, and both received substantial attention as the primary factors that were contributing to the continued sea lion decline (NMFS 2001); however, little consideration was given to the cumulative or synergistic effects of these two factors. Substantial uncertainty, associated with the potential causes of the severe decline that occurred during the 1980s, remained when sea lions of U.S. waters were listed as threatened under the Endangered Species Act (ESA) in Numerous conservation measures were implemented following the 1990 listing, including a prohibition on intentional killing (except for subsistence taking by Alaska Natives), a limit on incidental take in fisheries, increased monitoring of the subsistence harvest, reduced disturbance, and modified fishery management regulations. The Steller Sea Lion Recovery Team was formed in 1990 by the National Marine Fisheries Service, with the primary purpose of writing a recovery plan that outlined specific actions to promote recovery. Due to the substantial uncertainty regarding the causes of the sea lion decline, a large proportion of the recovery recommendations called for additional research. Critical habitat for Steller sea lions was designated under the ESA in 1993 (58 FR 45269), based primarily on a combination of satellite telemetry data from adult female sea lions, visual observations of sea lions at sea in locations assumed to represent common foraging areas, and the distribution of groundfish (i.e., sea lion prey) catches in the Bering Sea/ Gulf of Alaska and waters around the Aleutian Islands. Critical habitat, which included areas around both rookeries and major haul-outs and the additional three aquatic foraging areas, represented the spatial landscape from which federal actions would be evaluated under ESA Section 7 consultations. For most fisheries actions, the action agency (sustainable fisheries divisions with Regional Offices of NOAA Fisheries) and the consulting agency (protected resources divisions with Regional Offices of NOAA Fisheries) are both part of the same agency; i.e., NOAA Fisheries. If a proposed federal action is determined, through informal consultation, to be likely to adversely affect sea lions or their critical habitat, then the action is evaluated through a formal ESA Section 7 consultation under the ESA. The consulting agency conducts the formal consultation, which results in the preparation of a biological opinion. In that biological opinion, the consulting agency must make a decision as to whether the proposed action would jeopardize the continued existence of the ESA listed species, or result in the destruction or adverse modification of its critical habitat. The definition of jeopardize under the ESA is jeopardize the continued existence of means to engage in an action that reasonably would be expected, directly or indirectly, to reduce appreciably the likelihood of both the survival and recovery of a listed species in the wild

4 524 Small and DeMaster Steller Sea Lion Management by reducing the reproduction, numbers, or distribution of that species. (50 CFR ). The definition of destruction or adverse modification of critical habit under the ESA is... a direct or indirect alteration that appreciably diminishes the value of critical habitat for both the survival and recovery of a listed species. (50 CFR ). In the mid-1990s, researchers found genetic differences between sea lions on either side of 144ºW (near Cape Suckling, Alaska) (Bickham et al. 1996, Loughlin 1997). Also, sea lion abundance in the BSAI and GOA (west of Cape Suckling) regions continued to decline in the 1990s, whereas abundance in Southeast Alaska and farther south was stable or increasing. In 1997, the Steller sea lion was reclassified into two distinct population segments (50 CFR 24345). The western distinct population segment was changed to endangered due to the overall magnitude (>80%) and continuous nature of the decline, and the eastern distinct population segment was maintained as threatened due to uncertainty in recovery, especially in the southern portion of the range. The working hypothesis regarding sea lion interactions with the groundfish fishery in Alaska was that the fishery could adversely impact the ability of sea lions to forage in the GOA and BSAI by reducing the availability of prey (Fritz et al. 1995). Based on locations obtained through satellite transmitters attached to sea lions (Merrick and Loughlin 1997, Loughlin et al. 2003), it was determined that most foraging by sea lions was likely to occur near (<20 nautical miles) haul-outs and rookeries. Under the assumption that localized depletion of sea lion prey biomass and quality due to fisheries resulted in nutritional stress, and subsequently reduced survival and reproduction of sea lions, additional fisheries regulations were implemented in the 1990s. The primary intent of those regulations was to more evenly distribute the catch in time and space, thus reducing the potential for localized depletion (Fritz et al. 1995). In a retrospective analysis, Hennen (2006) found a significant, positive correlation between several metrics of fishing activity and the sea lion decline prior to No such relationship was found using data collected after Hennen interpreted his findings as consistent with an interpretation that management measures were effective in moderating the localized effects of fishing activity on sea lions. In 2000, a formal ESA Section 7 consultation on the fishery management plans for the BSAI and GOA resulted in a biological opinion that determined groundfish fisheries for Pacific cod and pollock jeopardized the continued existence of the western distinct population segment of sea lions, and adversely modified its critical habitat. As required by the ESA, whenever a jeopardy determination is made, the 2000 biological opinion included a reasonable and prudent alternative that consisted of management measures to mitigate the impacts of the groundfish fisheries for pollock, cod, and Atka mackerel in the Bering Sea, Aleutian Islands, and Gulf of Alaska. Those measures included an adaptive man-

5 Sea Lions of the World 525 agement experiment, with a series of large areas either open or closed to fisheries (Rusin 2002). The primary objectives of the proposed adaptive management experiment were to mitigate potential adverse impacts of the groundfish fishery on the western distinct population segment of sea lions in the areas closed to fishing, while also allowing NOAA Fisheries to assess the effectiveness of the management measures and determine whether further measures were necessary. However, the adaptive management experiment was not implemented, due in part to the anticipated adverse economic impacts to the groundfish fishery and concerns regarding the feasibility of the experimental design relative to sea lion ecology (NMFS 2001, Bowen et al. 2001). A Congressional appropriations bill provided a one-year time period for the North Pacific Fishery Management Council and NOAA Fisheries to craft an alternative suite of fishery management regulations that would remove jeopardy and adverse modification of critical habitat. The intent of Congress was that NOAA Fisheries would implement alternate regulations that minimized the economic impacts to the fishing industry while also accounting for the substantial uncertainty in both the knowledge of sea lion ecology and the impact of fisheries on the sea lion prey field. Ambiguity in the ESA definition of jeopardy (i.e., reasonably would be expected, reduce appreciably the likelihood ) contributed additional uncertainty at the policy level. The combined scientific and policy uncertainty generated extensive discussion and debate about developing a suite of fishery management regulations that would remove jeopardy and adverse modification of critical habitat. In 2001, NOAA Fisheries consulted on a revised set of management regulations, and released a biological opinion (NMFS 2001) that evaluated the potential for jeopardy or adverse modification of critical habitat under those regulations. The agency determined that the suite of management measures, if implemented, were not likely to result in jeopardy or adverse modification of critical habitat (Rusin 2002). The regulations were implemented without a large-scale adaptive management experiment, although several small-scale experiments were proposed to test the localized depletion hypothesis. In addition, Congress appropriated more than a tenfold increase in funding for sea lion research in fiscal year 2001, specifically to address thirteen areas of uncertainty. The results of this greatly enhanced research program are now starting to be reported in the published scientific literature. Current status Data similar to those collected during the s were not available from the 1990s, and thus a direct comparison to assess whether the level of nutritional stress has changed was not possible (M. Castellini, University of Alaska Fairbanks, unpubl.). Research on nutritional stress in the 1990s relied on indirect methods, including comparisons between the

6 526 Small and DeMaster Steller Sea Lion Management western and eastern distinct populations, which could be problematic (e.g., Davis et al. 2006; B.S. Fadely, NMFS NMML, unpubl.; L.A. Hoopes, Texas A&M University, unpubl.) The majority of research has been conducted on adult females and their pups during the summer period, and results indicate little or no evidence of nutritional stress during the 1990s and beyond (Trites and Donnelly 2003). Overall, the evidence for nutritional stress in all age classes and all seasons post 1990 is less than there was in the 1980s, and the evidence reported in the post 1990 period is limited; e.g., decreased reproduction (Holmes and York 2003). Several other issues contribute to continued uncertainty about whether nutritional stress persisted as a threat to the recovery of sea lions in the 1990s. Specifically, the adult females with pups studied on rookeries could represent animals that survived the impact of nutritional stress, whereas those females that were unable to complete gestation due to nutritional stress may have remained at sea and did not return to the rookeries. As noted by the NRC (2003), This attendance behavior is a critical limitation in monitoring pup production rates and female condition. Essentially, only those females healthy enough to produce pups arrive at rookeries. In addition, other cohorts that were not well studied, especially recently weaned juveniles, may have been more susceptible to the impacts of nutritional stress. At the ecosystem level, if the sea lion population has now begun to stabilize at a reduced carrying capacity, nutritional stress will likely be less pronounced compared to the periods of dramatic population declines, assuming the relative influence of food availability on population regulation has remained similar. In addition to a general lack of compelling evidence for the nutritional stress hypothesis in the post-1990 period, several publications have suggested that top-down forcing (i.e., predation) may be an important factor in understanding the past, as well as the current, dynamics of sea lions (Springer et al. 2003, Williams et al. 2004). In particular, the publication by Springer et al. (2003) speculated that predation by killer whales is the most likely cause of the rapid decline of the western sea lion population in the 1980s and the continued decline in the 1990s. However, the Springer et al. (2003) paper has generated considerable controversy, and several recent publications contend that the available data do not support the assumptions and hypotheses within Springer et al. (DeMaster et al. 2006, Trites et al. 2006, Mizroch and Rice 2006). Subsequently, research efforts to further understand the importance of predation on the western distinct population segment of sea lions have been undertaken; unfortunately, results from these studies are not yet available. Counts of sea lions in 2002 and 2004 increased relative to counts obtained during However, three additional biennial counts are required to statistically confirm the decline has stopped and that the western population was increasing at ~5% per biennium as indicated by the 2002 and 2004 counts (NMFS 2000, DeMaster unpubl.). Results from the

7 Sea Lions of the World 527 sea lion research program, which expanded in the later 1990s and again in 2001, have substantially increased the knowledge of sea lion ecology and improved the understanding of how various factors may affect the population. Yet, although some factors are now considered relatively minor threats (NRC 2003), substantial uncertainty persists concerning the suite of factors that may be impeding recovery, and the cumulative and synergistic effects among these factors remain largely unknown (Loughlin and York 2000). Linking research priorities and conservation measures Thus, although the most recent counts of sea lions do not indicate a continued decline of the western distinct population segment, substantial uncertainty persists on what factors are impeding recovery and what management measures will be most effective in promoting recovery. Certainly, population monitoring and fundamental sea lion ecological research must continue, including studies of population abundance and trend, age-specific vital rates, foraging ecology, diet, essential habitat, environmental monitoring (e.g., regime shifts), and improved estimates of the abundance, diet, and movement patterns of transient killer whales. Beyond such sea lion monitoring research, however, a more explicit link between research priorities and management measures is required to reduce the uncertainty associated with the factors impeding recovery and to determine which management measures to implement. Specifically, research that has a direct bearing on jeopardy or adverse modification of critical habitat findings and the effectiveness of conservation measures should receive the highest priority, as recommended by Bowen et al. (2001). We believe a primary link would be to further examine how both commercial fisheries and the variability in oceanographic conditions affect the seasonal distribution and abundance of the sea lion prey field, and how such changes affect sea lion population dynamics. Below, we present some specifics of this approach. Fishery management measures have been implemented based on the assumption that fisheries may jeopardize the continued existence of the western distinct population segment of sea lions and may adversely modify critical habitat through a local reduction in prey biomass and quality. Thus, research studies designed to determine if fisheries indeed deplete or disturb the sea lion prey field, to the extent that foraging success is reduced, need to be completed. Specifically, fishery interaction studies designed to assess prey biomass before, during, and after fishing in a treatment area with comparisons to prey biomass in an unfished control area should continue (Loughlin and Mattson 1998, Wilson et al. 2003, Conners et al. 2004), and need to be expanded. Such studies must be conducted at spatial and temporal scales relevant to both foraging sea

8 528 Small and DeMaster Steller Sea Lion Management lions and current operational fisheries to assess the magnitude and duration of changes in the prey field, both with and without the influence of fisheries, with an experimental design that reduces potential biases and alternative interpretations. Several years, and possibly decades, of research may be required to account for natural variability in prey biomass and distribution. In addition to field research studies, models should be developed that integrate sea lion foraging parameters and reproductive energetics within a spatially explicit demographic model to identify the types of perturbations to the prey field that negatively impact sea lion fitness. Additional modeling is also needed to assess the impact of singlespecies fisheries management on ecosystem carrying capacity (Goodman et al. 2002, Pikitch et al. 2004). Another research priority is to determine the mechanism by which changes in prey biomass and quality may result in chronic nutritional stress (Trites and Donnelly 2003) that subsequently decreases sea lion survival and reproduction. As recommended by Bowen et al. (2001), research examining the physiological response of sea lions to changes in prey biomass and quality must ultimately provide insights as to how such changes affect sea lion demography in order for the results to be applied toward sea lion recovery and conservation. Further, understanding the demographic effect of changes in prey and the mechanism of nutritional stress is important because sea lion populations may respond to changes in more than one factor (e.g., regime shifts, fisheries, interspecific competition) in the same manner. Two extensive reviews of sea lion interactions with fisheries have recommended an adaptive management approach to examine the hypothesized mechanisms of a negative influence of fisheries on sea lions (Bowen et al. 2001, NRC 2003). We believe such an adaptive management approach is required to examine how a potential reduction in prey biomass and quality could lead to physiological responses by sea lions that directly (e.g., reduced fecundity) or indirectly (e.g., increased mortality from predators due to increased foraging) reduces their population growth, both in the short-term and possibly over the long-term that could result in a lower carrying capacity. An experiment under such an adaptive management approach should be at a finer spatial scale than proposed in the 2000 biological opinion, and should integrate the objectives of the fishery interaction studies mentioned above with the monitoring of a suite of sea lion demographic and behavioral response parameters. Such a complex experiment has not been attempted previously in marine ecosystems, and prior to initiating such an experiment several important questions must be thoroughly addressed. First, are such experiments necessary? Boyd (1995) recommended that individually based models should be developed to explore whether or not the impact of localized depletion can be sufficiently assessed prior to experiments. Fishery interaction studies could determine that fisheries

9 Sea Lions of the World 529 do not cause significant short-term reductions in prey biomass. Whether such studies can determine the potential long-term impact of fisheries on the prey field needs to be addressed. Second, are such experiments feasible? The challenge to develop a robust experimental design for the experiments is tremendous (Punt and Fay 2006, Bowen et al. 2001), especially due to the spatial and temporal scale that would be required to account for the movement of sea lions and their prey, and the inherent variability in the marine ecosystem. Critical to a successful and informative experiment will be selecting the suite of variables to measure for both the prey field (e.g., species composition, biomass, age structure) and sea lions (e.g., foraging effort, body condition) and determining how they will be interpreted. Finally, the ESA has restrictions on the type of experimental treatments that may negatively impact a listed species, and such restrictions will need to be met in developing the experimental design. As stated by Goodman (2005), Mechanisms are needed to deal rationally with the uncertainties about causes of population declines and uncertainties about eventual effectiveness of planned conservation measures. Uncertainty would most likely be reduced resulting in a more robust conservation strategy with the continued, and refined, implementation of the four research components outlined above: (1) population monitoring and fundamental sea lion ecological research, (2) fishery interaction studies designed to test the localized depletion hypothesis, (3) determining the mechanism by which changes in prey biomass and quality may result in chronic nutritional stress that results in decreased sea lion survival and reproduction, and (4) adaptive management experiments to assess the impact of fisheries on the sea lion prey field and subsequently sea lion demography. Such a strategy should increase the likelihood that conservation measures are implemented, maintained, or modified such that they can be effective without unnecessary burden on commercial fisheries. Without such a strategy, there will be a much lower likelihood of gaining additional insights on how different threats may influence sea lion population dynamics. In addition, the opportunity to distinguish between the effects of human activities versus those that may occur naturally could be greatly diminished. Conservation policy Opportunities also exist to reduce the uncertainty inherent in conservation policy, which would further enhance the effectiveness of the sea lion conservation strategy. Goodman (2005) described the need to develop more explicit policy standards, which could result in reduced litigation and more consistent implementation of conservation policies. Below we briefly discuss three specific policy modifications outlined by Goodman (2005) that are relevant to sea lion conservation.

10 530 Small and DeMaster Steller Sea Lion Management First, the current ESA definitions of endangered ( in danger of extinction throughout all or a significant portion of its range ) and threatened ( likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range ) species imply a time horizon and level of probability. The lack of a more specific standard associated with these definitions results in substantial uncertainty as to when species should be listed or delisted. For example, the western distinct population segment of sea lions was listed as endangered when its abundance of adults was ~40,000, yet the abundance of the discrete population of Cook Inlet beluga whales had declined over several years to ~350 animals when the decision by NOAA Fisheries, which was upheld by an Appeals Court judge, was made that they were not threatened with extinction. Modifying the ESA definitions of endangered and threatened to include a specific standard for extinction, for example a 1% probability of becoming extinct in 100 years (see DeMaster et al. 2004), would reduce uncertainty and increase consistency in listing decisions. The second policy modification needed is to employ the extinction standard used in ESA listings into ESA Section 7 consultations. Specifically, determining whether an action would result in jeopardy or adverse modification of critical habitat would be linked to a change in the risk of extinction. Further, a decision rule that quantitatively accounts for uncertainty, associated with both the action (e.g., fisheries) and the listed species, should be developed to assess whether the standard has been met. For example, if a proposal to substantially modify fishery operations (i.e., the action) resulted in a formal ESA Section 7 consultation, the knowledge and associated uncertainty of how the fishery could influence the sea lion prey field and subsequently affect sea lion demography would be examined and assessed relative to the extinction standard. Third, uncertainty could be reduced by establishing a quantitative standard for the ecosystem protection provision of the Magnuson-Stevens Fishery Conservation and Management Act and the joint U.S. Fish and Wildlife Service NOAA Fisheries policy on ecosystem considerations in developing recovery strategies for ESA listed species. Acknowledging that uncertainty and indeterminacy are fundamental characteristics of our knowledge of ecosystems, long-term monitoring of biological and climate indices is needed to improve the understanding of how natural oceanic and climate variability affect the dynamic behavior and biological composition of ecosystems. As our understanding of ecosystem dynamics improve through such monitoring, one example of how a quantitative standard for ecosystem protection could be applied to sea lions would be in assessing the potential impact of managing fisheries at the single-species level. Certainly, substantial challenges exist when undertaking fisheries management at the ecosystem level (Pikitch et al. 2004). However, data and modeling approaches exist to assess the impact

11 Sea Lions of the World 531 of single-species fisheries management on ecosystem carrying capacity (Goodman et al. 2002). In summary, the dramatic decline of Steller sea lions in the BSAI and GOA regions over the last 25 years has resulted in an immense research and management effort designed to promote the species recovery. Due to limited baseline information on the ecology of sea lions and their marine ecosystem, combined with the inherent complexity and variability of both, substantial uncertainty has persisted in the development, implementation, and justification of conservation strategies. Since ESA listing of sea lions in 1990, required decisions are based on the best available data with the burden of proof favoring protection and recovery of the sea lion population. Without clear evidence that commercial fisheries do not adversely affect sea lions or their critical habitat, restrictive fishery management actions will be necessary. We have outlined four components of a robust research strategy that would substantially reduce uncertainty. In addition, we encourage management agencies to pursue recently suggested modifications to conservation policy; in particular, the development of more explicit quantitative policy standards for ESA listing should increase consistency in the implementation of conservation efforts and reduce the potential for litigation. Implementation of these research and policy recommendations could substantially increase the probability of effective conservation: precautionary actions needed for the recovery for the endangered sea lion and minimal unnecessary burden on commercial fisheries. Acknowledgments We thank the Steller Sea Lion Recovery Team for their numerous discussions on the diverse issues involved in determining how best to promote the recovery of sea lions. Two anonymous reviewers, Shane Capron, Lloyd Lowry, and Tim Ragen provided comments that improved earlier versions of this manuscript. References Benson, A.J., and A.W. Trites Ecological effects of regime shifts in the Bering Sea and eastern North Pacific Ocean. Fish Fish. 3: Bickham, J.W., J.C. Patton, and T.R. Loughlin High variability for control-region sequences in a marine mammal: Implications for conservation and biogeography of Steller sea lions (Eumetopias jubatus). J. Mammal. 77: Bowen, W.D., H. Harwood, D. Goodman, and G.L. Swartzman Review of the November 2000 Biological Opinion and Incidental Take Statement with respect to the western stock of the Steller sea lion. Final Report to the North Pacific Fishery Management Council, May, pp.

12 532 Small and DeMaster Steller Sea Lion Management Boyd, I.L Steller sea lion research. National Marine Mammal Laboratory, Seattle, pp Braham, H.W., R.D. Everitt, and D.J. Rugh Northern sea lion decline in the eastern Aleutian Islands. J. Wildl. Manag. 44: Calkins, D.G., and E. Goodwin Investigation of the declining sea lion population in the Gulf of Alaska. Unpubl. Rep., Alaska Department of Fish and Game, 333 Raspberry Road, Anchorage, AK pp. Calkins, D.G., E.F. Becker, and K.W. Pitcher Reduced body size of female Steller sea lions from a declining population in the Gulf of Alaska. Mar. Mamm. Sci. 14: Conners, M.E., P. Munro, and S. Neidetcher Pacific cod pot studies AFSC Processed Rep , NOAA, NMFS Alaska Fisheries Science Center, 7600 Sand Point Way NE, Seattle, WA pp. Davis, R.W., E.A.A. Brandon, D.G. Calkins, and T.R. Loughlin Female attendance and neonatal pup growth in Steller sea lions (Eumetopias jubatus). In: A.W. Trites, S.W. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea, and K.M. Wynne (eds.), Sea lions of the world. Alaska Sea Grant College Program, University of Alaska Fairbanks. DeMaster, D.P., A.W. Trites, P. Clapham, S. Mizroch, P. Wade, R.J. Small, and J. Verhoef The sequential megafaunal collapse hypothesis: Testing with existing data. Prog. Oceanogr. DeMaster, D., R. Angliss, J. Cochrane, P. Mace, R. Merrick, M. Miller, S. Rumsey, B. Taylor, G. Thompson, and R. Waples Recommendations to NOAA Fisheries: ESA listing criteria by the Quantitative Working Group, 10 June NOAA Tech. Memo. NMFS-F/SPO pp. Fritz, L.W., R.C. Ferrero, and R.J. Berg The threatened status of Steller sea lions, Eumetopias jubatus, under the Endangered Species Act: Effects on Alaska groundfish fisheries. Mar. Fish. Rev. 57: Goodman, D Adapting regulatory protection to cope with future change. In: J.E. Reynolds III, W.F. Perrin, R.R. Reeves, S. Montgomery, and T.J. Ragen (eds.), Marine mammal research: Conservation beyond crisis. Johns Hopkins University Press, Baltimore, pp Goodman, D., M. Mangel, G. Parkes, T. Quinn, V. Restrepo, T. Smith, and K. Stokes Scientific review of the harvest strategy currently used in the BSAI and GOA groundfish fishery management plans. North Pacific Fishery Management Council, 605 West 4th Ave., Suite 306, Anchorage, AK Hennen, D.R Associations between the Steller sea ion decline and the Gulf of Alaska and Bering Sea commercial fisheries. Ecol. Appl. 16. Holmes, E., and A.E. York Using age structure to detect impacts on threatened populations: A case study using Steller sea lions. Conserv. Biol. 17: Loughlin, T.R Using the phylogeographic method to identify Steller sea lion stocks. In: A.E. Dizon, S.J. Chivers, and W.F. Perrin (eds.), Molecular genetics of marine mammals. Society for Marine Mammalogy Spec. Publ. 3:

13 Sea Lions of the World 533 Loughlin, T.R The Steller sea lion: A declining species. Biosphere Conservation 1(2): Loughlin, T., and T. Mattson Panel recommendations from an experimental design workshop on testing the efficacy of Steller sea lion no-trawl fishery exclusion zones in Alaska, 6-7 May NOAA, NMFS, Alaska Fisheries Science Center, Seattle. 32 pp. Loughlin, T.R., and A.E. York An accounting of the sources of Steller sea lion, Eumetopias jubatus, mortality. Mar. Fish. Rev. 62(4): Loughlin, T.R., D.J. Rugh, and C.H. Fiscus Northern sea lion distribution and abundance: J. Wildl. Manag. 48: Loughlin, T.R., A.S. Perlov, and V.A. Vladimirov Range-wide survey and estimation of total number of Steller sea lions in Mar. Mamm. Sci. 8: Loughlin, T.R., J.T. Sterling, R.L. Merrick, J.L. Sease, and A.E. York Diving behavior of immature Steller sea lions (Eumetopias jubatus). Fish. Bull. U.S. 101(3): Merrick, R.L., and T.R. Loughlin Foraging behavior of adult female and youngof-the-year Steller sea lions in Alaskan waters. Can. J. Zool. 75: Merrick, R.L., M.K. Chumbley, and G.V. Byrd Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: A potential relationship. Can. J. Fish. Aquat. Sci. 54(6): Mizroch, S.A., and D.W. Rice Have north pacific killer whales switched prey species in response to depletion of the great whale populations? Mar. Ecol. Prog. Ser. NMFS Section 7 consultation on the authorization of the Bering Sea and Aleutian Islands groundfish fishery under the BSAI FMP and the authorization of the Gulf of Alaska groundfish fishery under the GOA FMP. NOAA Fisheries, Office of Protected Resources, Nov. 30, NMFS Steller Sea Lion Protection Measures Final Supplemental Environmental Impact Statement. Implemented under the Fishery Management Plans for the Groundfish of the GOA and the Groundfish of the BSAI NMFS, Alaska Region, P.O. Box 21668, Juneau, AK NRC Decline of the Steller sea lion in Alaskan waters; untangling food webs and fishing nets. National Research Council, National Academy Press, Washington, D.C. 184 pp. Pikitch, E.K., C. Santora, E.A. Babcock, A. Bakun, R. Bonfil, D.O. Conover, P. Dayton, P. Doukakis, D. Fluharty, B. Heneman, E.D. Houde, J. Link, P.A. Livingston, M. Mangel, M.K. McAllister, J. Pope, and K.J. Sainsbury Ecosystem-based fisheries management. Science 305: Punt, A.E., and G. Fay Can experimental manipulation be used to determine the cause of the decline of the western stock of Steller sea lions (Eumetopias jubatus)? In: A.W. Trites, S.K. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea, and K.M. Wynne (eds.), Sea lions of the world. Alaska Sea Grant College Program, University of Alaska Fairbanks.

14 534 Small and DeMaster Steller Sea Lion Management Rusin, J.D Management of the western Alaska Steller sea lion, Eumetopias jubatus, under the Endangered Species Act: Evolution of interagency consultation and impacts on Alaska groundfish fisheries. Master s thesis, University of Washington. 117 pp. Sease, J.L., and R.L. Merrick Status and population trends of Steller sea lions. In: G. Stone, J. Goebel, and S. Webster (eds.), Pinniped populations, eastern North Pacific: Status, trends and issues. A symposium of the 127th Annual Meeting of the American Fisheries Society. New England Aquarium, Conservation Department, Central Wharf, Boston, MA 02110, pp Springer, A.M., J.A. Estes, G.B. van Vliet, T.M. Williams, D.F. Doak, E.M. Danner, K.A. Forney, and B. Pfister Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? PNAS 100: Trites, A.W., and C.P. Donnelly The decline of Steller sea lions in Alaska: A review of the nutritional stress hypothesis. Mamm. Rev. 33:3-28. Trites, A.W., and P.A. Larkin Changes in the abundance of Steller sea lions (Eumetopias jubatus) in Alaska from 1956 to 1992: How many were there? Aquat. Mamm. 22: Trites, A.W., V.B. Deecke, E.J. Gregr, J.K.B. Ford, and P.F. Olesiuk Killer whales, whaling and sequential megafaunal collapse in the North Pacific: A comparative analysis of the dynamics of marine mammals in Alaska and British Columbia following commercial whaling. Mar. Mamm. Sci. 22. Williams, T.M., J.A. Estes, D.F. Doak, and A.M. Springer Killer appetites: Assessing the role of predators in ecological communities. Ecology 85: Wilson, C.D., A.B. Hollowed, M. Shima, P. Walline, and S. Stienessen Interactions between commercial fishing and walleye pollock. Alaska Fishery Research Bulletin 10(1): York, A The population dynamics of the northern sea lions, Mar. Mamm. Sci. 10:38-51.

15 Sea Lions of the World 535 Alaska Sea Grant College Program AK-SG-06-01, 2006 Avoidance of Artificial Stimuli by the Steller Sea Lion Kohji Iida, Tae-Geon Park, Tohru Mukai, and Shoji Kotani Hokkaido University, Graduate School of Fisheries Sciences, Hakodate, Hokkaido, Japan Abstract Every winter, hundreds of Steller sea lions (Eumetopias jubatus) visit the coast of Hokkaido, northern Japan. Their foraging behavior destroys fishing gear, which is a serious problem. In order to find a solution that allows the coexistence of both Steller sea lions and fishing activities, attempts have been made to control their behavior using acoustical and optical stimuli. This study examined methods of repelling Steller sea lions from fishery gear using aerial and underwater sounds and flashing lights. In this study, we (1) observed and analyzed the relationship between the calls and the behavior of Steller sea lions; (2) searched for effective stimuli for repelling Steller sea lions; (3) developed a displacing system that generates artificial stimuli to repel Steller sea lions using sounds and lights; and (4) tested the displacing system. Experiments were conducted at a Steller sea lion haul-out located on the west coast of Hokkaido, on the Sea of Japan. Steller sea lions were exposed to acoustical and optical stimuli consisting of repeated intermittent sounds with or without flashing lights. This system was controlled from the edge of a cliff, and the reactions of Steller sea lions were monitored using a video camera and microphone. Most of the Steller sea lions responded to the stimuli by vocalizing toward the source, while moving away and jumping in the water. The most effective stimuli for repelling Steller sea lions were aerial sounds, underwater sounds, and flashing lights in that order. Introduction Every winter, a few hundred Steller sea lions (Eumetopias jubatus) from Sakhalin and the northern Kuril Islands visit the coast of Hokkaido, northern Japan (Davies 1958, Scheffer 1958, Peterson and Bartholomew 1967,

16 536 Iida et al. Avoidance of Artificial Stimuli Figure 1. Steller sea lions hauled out on reefs near Cape Ofuyu in Hokkaido, Japan. Schusterman 1981, King 1983, Loughlin et al. 1984). They land on reefs in coastal areas with steep cliffs, and forage for food from these bases (Fig. 1). There are also many active coastal fisheries along this coast, including set net and gillnet fisheries that catch cod, pollock, and greenlings. However, fisheries resources around this area have been decreasing for decades. The areas of Steller sea lion and fishery activity overlap. Steller sea lions not only forage for food in the fishing grounds, but also break nets while foraging. The estimated damage to the fisheries due to Steller sea lions exceeds US $10 million annually. In order to reduce fishery damage by Steller sea lions, while allowing their coexistence in coastal waters, we tested methods to repel Steller sea lions from fishing gear using acoustical and optical stimuli. Steller sea lions have very good hearing, and can identify the noise emitted by hunting boats (Moore and Schusterman 1976, Schusterman 1981, Richardson et al. 1995, Akamatsu et al. 1996, Kastak and Schusterman 1998, Schusterman et al. 2000). In order to drive Steller sea lions away from fishing gear, a displacing system that emits sounds and lights was developed. Prior to the field experiments, reactions of captive Steller sea lions in an aquarium to sound and light stimuli were observed.

17 Sea Lions of the World 537 Radio Control Receiver MP3 Player Power Amplifier Aerial Loudspeaker Radio Control Transmitter Underwater Loudspeaker Battery 12V 52AH Stroboscopic Generator Xenon Lamp Xenon Lamp Switching Controller Figure 2. Remote controlled displacing aerial and underwater sounds and flashing stroboscopic light generators. Reactions of wild Steller sea lions to the displacing system were investigated. Materials and methods Displacing sound generator and characteristics of the sound The system was intended to control the behavior of animals using multiple stimuli, combining aerial and underwater sounds and a flashing stroboscopic light. It was designed to emit high-intensity sounds audible to the animals over a wide frequency range, while not damaging either the operators or the animals, or affecting the environment. Loudness of the sound is the same level as the sea lion s roar, and the sound stimuli are emitted intermittently. The sound generator consisted of a sound source, an amplifier, an antenna, an underwater loudspeaker, and a remote control system (Fig. 2). The sounds used consisted of engine noises generated by a fishing boat, the sounds of explosions generated by firecrackers, and digitally synthesized sounds. The emitted sound was audible and had a major component at frequencies less than 1,000 Hz. A 30 W amplifier was

18 538 Iida et al. Avoidance of Artificial Stimuli Figure 3. Sonograms of artificial sound stimuli used for displacing Steller sea lions: (a) logarithmic frequency sweep sound, (b) linear frequency sweep sound, (c) successive logarithmic frequency sweep sound, and (d) hammering sound. used to obtain a sufficiently high sound pressure within a range of 100 m. The digitally synthesized displacing sounds included three types of chirp sound that swept the frequency range from 100 to 1,000 Hz, which included the frequencies audible to Steller sea lions. The waveforms, frequency spectra, and sonograms are shown in Fig. 3a,b,c. Displacing light generator and characteristics of the flashing light A flashing stroboscopic light was tried as a stimulus for displacing Steller sea lions. A dispelling light generator was designed as shown in Fig. 4. A xenon lamp was used as the light source in order to obtain an intense light covering a wide area. The xenon lamp was flashed intermittently so as not to decrease its dispelling effects. Since the energy consumption of the battery depended on the frequency of flashes, one emission consisted of 30 flashes at 1 second intervals. A single emission requires a power of 235 Joules (470 µf, 1,000 V), thus the lamp could emit 9,700 flashes when using a 65AH battery.

19 Sea Lions of the World 539 DC+12V-8V SW 5V/12V Power Transformer VT1 DC 300V DC 30V Trigger Strobo Generator SG2 Xenon Tube Control SG1 Detect Signal GND Signal Converter VT2 Transformer Power 60V-300V Light Bulb Figure 4. Block diagram of displacing light generator. Observations of the reactions of captive Steller sea lions to artificial stimuli Prior to the experiment to displace wild Steller sea lions by artificial stimuli, the reactions of captive Steller sea lions to the artificial sounds and lights were observed on three animals kept at Muroran Aquarium. The reactions of animals were observed using a video camera and the artificial sound was analyzed using a sonograph. A video camera and microphone were placed outside the cage facing the pool, and the behavior of the Steller sea lions was recorded using a videocassette recorder (VCR) placed in a shed 30 m from the pool. The artificial stimuli consisted of hammering sounds and a flashing stroboscopic light. Hammering sounds were played in the pool for a few hours, while the light was flashed intermittently 50 times at a frequency of 1 to 3 times per minute. A sonogram of the hammering sound is shown in Fig. 3d. Observing the avoidance behavior of wild Steller sea lions in response to displacing sounds and flashing lights In order to observe the avoidance behavior of wild Steller sea lions in response to the displacing sound and flashing light, experiments using a sound generator and a xenon lamp were conducted in the early spring of 2003 and 2004 on a reef near Cape Ofuyu, where wild Steller sea lions land. A sound generator and xenon lamp were placed on the reef facing the Steller sea lion haul-out, and these were operated by radio remote control from a cliff 300 m from the reef (Fig. 5). In order to monitor the reaction to the stimuli at close range, a video camera and microphone were placed on the reef and continuous recordings with a VCR were made. An underwater loudspeaker was submerged near the reef at a depth of 3 m. An antenna for receiving radio control signals was built on the reef. An antenna for transmitting the radio control signals and a video camera

20 540 Iida et al. Avoidance of Artificial Stimuli Antenna for remote control Figure 5. Displacing system placed on the top of the reef. The system was operated by radio remote control from a cliff 300 m from the reef.

21 Sea Lions of the World 541 equipped with a telephoto lens were placed on the cliff to observe the entire reef area, and the behavior of Steller sea lions was recorded using another VCR. Results Acoustical behavior and the reaction of captive Steller sea lions to sound and light Ordinarily, the captive Steller sea lions wake around sunrise, are active in the pool during the day, and sleep in the pool after sunset. They enter the water or holding room in cold weather and bask at poolside in warm weather. They rest after meals and increase their roaring before a meal, as they have been conditioned to the behavior of their keepers. The relationship between calls and behavior were investigated by analyzing the calls emitted in response to sound stimuli. The calls of the three captive Steller sea lions were classified into three categories: acknowledge calls, communication calls, and wheedling calls (Evance 1966, Park et al. 2006). The acoustic characteristics of these sounds are shown in Table 1. The adult pair of sea lions conducted a roaring duet to request food that increased until they were fed. Moreover, their three-year-old male pup, which was kept in a small pool 50 m from the main pool, frequently roared with them from sunrise until the morning meal. In response to a single artificial hammering sound, they initially showed an aversive reaction, with roaring. With successive hammering sounds, they showed avoidance behavior, moving away from the sound source. According to the sonogram (Fig. 3d), the hammering sound lasted for 0.5 s and had a peak frequency at 1 khz with a band width about 7 khz at 10 db. In response to a flashing xenon lamp, the Steller sea lions showed an acknowledge reaction, in which they stared at the light source, and an aversive reaction, in which they roared briefly. Generally, they noticed the onset of the stimulus and stared at the lamp, but they soon lost interest in successive light flashes (Fig. 6). Moreover, they ignored all light stimuli at night. Avoidance of the displacing sound and light stimuli by wild Steller sea lions Reaction to the stroboscopic light Three experiments in which wild Steller sea lions were exposed to lights from a xenon lamp were conducted in April Flashing lights were emitted for 30 minutes at a frequency of 80 times per second. While the Steller sea lions showed an acknowledge reaction in 2 trials, the light was ignored in the another two trials (upper rows in Table 2).

22 542 Iida et al. Avoidance of Artificial Stimuli Table 1. Acoustic characteristics of calls made by captive Steller sea lions for each sound category (Park et al. 2006). Sex Age Weight (kg) Call category Dominant F1 (Hz) Fundamental F0 (Hz) Duration T (s) Density PRR (Hz) N Ave. S.D. N Ave. S.D. N Ave. S.D. N Ave. S.D. Male 23 >850 Communication Wheedling Female Communication Acknowledge Threat Male pup Communication

23 Sea Lions of the World Staring Roaring Number of Reactions Elapsed Time (Min.) Figure 6. Changes in reactions to flashing lights for captive Steller sea lions. An acknowledge reaction (staring) and an aversive reaction (roaring) were observed. Reaction to an aerial displacing sound Displacing experiments using aerial sounds were conducted at Cape Ofuyu three times in April 2003, and once in March The sound stimuli consisted of a single chirp sound and successive chirp sounds that repeated the single chirp sound for 1-2 minutes. Figure 7 shows the avoidance behavior of wild Steller sea lions to the aerial displacing sound. Wild Steller sea lions near the sound source showed (a) an acknowledge reaction to the single chirp sound, (b) escaping behavior consisting of moving away from the source, and last (c,d) diving into the water in response to successive chirp sounds. In addition, a duet reaction to the sound stimuli, a searching reaction for the sound source, and an aversion reaction to the sound source were observed (middle rows in Table 2). Generally, wild Steller sea lions appeared cautious when exposed to novel artificial stimuli, such as chirp sounds. Animals near the sound source abruptly initiated avoidance behavior. When combined with a flashing light, the effect was compounded. In 2003, 2 of 5 landed animals dove into the water, and 26 of 37 landed animals did the same in Reaction to an underwater displacing sound A displacing experiment using underwater sound was conducted at Cape Ofuyu in April A displacing sound was emitted by an underwater loudspeaker at a depth of 3 m. In 28 trials, wild Steller sea lions showed avoidance behavior in response to the sound, including 9 landing reactions in which swimming animals abruptly landed on the reef, 5

24 544 Iida et al. Avoidance of Artificial Stimuli Figure 7. Escaping behavior to the aerial displacing sound for wild Steller sea lions on the reef. Sea lions near the sound source showed (a) an acknowledge reaction to the single chirp sound, (b) escaping behavior consisting of moving away from the source, and lastly (c,d) diving into the water in response to successive chirp sounds. swimming reactions in which animals in the water swam to escape the sound source, and 10 diving reactions in which floating animals dove into the water abruptly (lower rows in Table 2). These results showed that animals both diving and swimming on the surface with their head submerged could hear the underwater sound. The degree of avoidance behavior appeared to be higher in the landing reaction than in the swimming reaction, whereas the diving reaction was thought to be a scouting behavior. Discussion Detecting wild Steller sea lions by call analysis As the dominant frequency of the call of Steller sea lions ranges from 200 to 500 Hz (frequencies that propagate well on the sea surface) and the intensity of the call is high (Thomas and Kuechle 1982), it is possible to