Endangered Species Act listing: three case studies of data deficiencies and consequences of ESA ‘threatened’ listing on research output

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ScienceDirect Endangered Species Act listing: three case studies of data deficiencies and consequences of ESA ‘threatened’ listing on research output Mariska Weijerman1,2, Charles Birkeland3, Gregory A Piniak4, Margaret W Miller5, C Mark Eakin6, Paul McElhany7, Matthew J Dunlap1, Matt Patterson8 and Russell E Brainard9 Determining whether a species warrants listing as threatened or endangered under the U.S. Endangered Species Act depends on the government’s assessment of the species’ extinction risk, usually in response to a petition. Deciding whether data are sufficient to make a listing determination is a challenging part of the process. We examined three case studies involving corals. A petition for deep-sea corals was rejected for full status review of the species, based on insufficient information on population trends and threats. Information on threats for 82 tropical corals was sufficient to propose listing of 66 species. Significant population declines and identified threats resulted in listing two Atlantic Acropora corals as ‘Threatened’. There was no decrease in journal publication rate on the Acropora species after that listing, and no decrease in research permit applications in marine protected areas. However, the effects of listings on research that might help to sustain or recover species remains largely unknown. Addresses 1 Joint Institute for Marine and Atmospheric Research, University of Hawaii at Manoa, Honolulu, HI 96822, United States 2 Environmental System Analysis Group, Wageningen University, PO Box 47, 6700 AA Wageningen, The Netherlands 3 Department of Biology, University of Hawaii at Manoa, Honolulu, HI 96822, United States 4 National Centers for Coastal Ocean Science, National Ocean Service, 1305 East-West Highway, Silver Spring, MD 20910, United States 5 Southeast Fisheries Science Center, National Marine Fisheries Service, 75 Virginia Beach Drive, Miami, FL 33149, United States 6 NOAA Coral Reef Watch, Center for Satellite Applications and Research, 5830 University Research Ct., College Park, MD 20740, United States 7 Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Boulevard East, Seattle, WA 98112, United States 8 National Park Service, 18001 Old Cutler Road, Suite 419, Palmetto Bay, FL 33157, United States 9 Pacific Islands Fisheries Science Center, National Marine Fisheries Service, 1125B Ala Moana Boulevard, Honolulu, HI 96814, United States Corresponding author: Weijerman, Mariska ([email protected]) Current Opinion in Environmental Sustainability 2014, 7:15–21 This review comes from a themed issue on Environmental change issues Edited by Georgios Tsounis and Bernhard Riegl For a complete overview see the Issue and the Editorial Available online 20th December 2013 1877-3435/$ – see front matter, # 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.cosust.2013.11.026

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Introduction Many coral reef ecosystems face numerous natural and human-induced threats, resulting in elevated coral extinction risks [1]. In the Indo-Pacific Ocean, coral cover has overall declined by approximately 40% from 1968 to 2003 [2], while Caribbean coral cover declined by 80% from 1977 to 2001 [3]. With a reduction in coral habitat and complexity [4], species with key functions in ecosystem maintenance also decline, further diminishing the chance of recovery [5]. Local and federal governments are challenged to conserve reefs, reverse the documented downward trends in coral cover and fish biomass, and sustain the economic and ecosystem benefits reefs provide. Recent, in-depth reviews concluded that the driving causes of coral cover decline are ocean warming and acidification — both originating from anthropogenic increases in atmospheric carbon dioxide (CO2) [6,7]. There are various regulatory mechanisms in place with the intention to curb CO2 and other greenhouse gas emissions and conserve coral reefs [8], though global emissions have not declined. Management of local threat reduction (e.g. through reduced fishing or land-based sources of pollution) can play a critical role in sustaining corals otherwise stressed by ocean warming and acidification [9,10–12]. Coral sustainability depends on protection against local population threats, successful recruitment at a variety of spatial scales, and the ability to cope with global ocean change [13]. Adding species to conservation status lists can generate additional benefits through regulations, recovery plans, and general increased awareness of conservation issues. For example, the World Conservation Union’s (IUCN) Red List includes 402 scleractinian coral species (6 Critically Endangered, 23 Endangered, 199 Vulnerable, and 174 Near Threatened) and this listing has increased a general awareness of the peril of these coral species. However, being on the IUCN Red List does not include any protective regulation. Being listed on the appendices of the Convention of International Trade in Endangered Species protects corals from international trade between signatory countries but offers no protection against other local or global threats. The U.S. Endangered Species Act (ESA) listings offer protection from ‘take’, may offer protection through ‘critical habitat’ designation, Current Opinion in Environmental Sustainability 2014, 7:15–21

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and carry a legal mandate for species ‘recovery’ in U.S. waters. While few ESA-listed species have fully recovered, the ESA is credited with preventing the extinction of the vast majority of listed species [14] and reversing population declines [15]. At the time of earlier coral ESA listings, climate change was not identified as a sufficient threat to recommend intervention on anthropogenic climate change. However, climate change and ocean acidification are now considered to be the primary threats that could lead to ESA listing in the pending action (Policy Brief on Climate Change & Regulatory Policy; URL: http://www.aaas.org/spp/cstc/briefs/climatechange/ regpolicy.shtml). The ESA is the primary tool of the U.S. government for evaluating and protecting species sustainability. The administering agencies (National Marine Fisheries Service (NMFS) and U.S. Fish and Wildlife Services) must respond to ESA petitions from the public. The petitioner bears the burden to provide ‘substantial’ information that ‘would lead a reasonable person to believe that the measure proposed in the petition may be warranted’ (Federal Regulation 50 CFR 424.14(b)). The government then has 90 days to determine whether a species status review is warranted; if this 90-day finding is positive, the government has a year from the petition date to propose whether a species warrants listing under one of two categories: endangered for species currently in danger of extinction or threatened for species likely to become endangered within the foreseeable future. The agency makes that proposal based on the ‘best available scientific and commercial data’ on the likelihood of extinction in a sustainability assessment called a ‘status review’, with explicit considerations of the following factors specified in Section 4(a)(1): (A) the present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting the continued existence of the species.

The ESA does not have a ‘data deficient’ category as IUCN does (IUCN Red list; URL: http://www.iucnredlist.org/static/categories_criteria_2_3). Regardless of data availability, the law requires agencies to reach a decision as to whether to conduct a full status review and if a review is conducted, to decide whether listing is warranted. Here we present three case studies that had varying levels of ‘best available’ information, and discuss the assessment of coral sustainability in each case. The latest information may be re-examined as the sustainability of a species listed under the ESA is periodically Current Opinion in Environmental Sustainability 2014, 7:15–21

reevaluated in a ‘‘Status Update’’. In addition to case studies of the initial listing process, we explore how listing itself (under the threatened category) may affect the quality of future sustainability assessments. New research to inform future assessments may be affected by changes to funding or permitting. Assessments of coral sustainability

Case study 1: Alaska deep sea corals On August 20, 2012, the Center for Biological Diversity petitioned NMFS to list 44 deep-sea gorgonians, sea whips and pens, and hydrocorals in Alaskan waters, due to the threats posed by fishing activities, ocean acidification, ocean warming, and energy exploration [16]. Few population survey data were available because deep sea corals have only recently become a focus of research (e.g. 22 of the 44 petitioned species were described only in the last decade) and very little empirical data exist on the potential sensitivity of these organisms to threats related to climate or ocean changes. One measure of ‘substantial information’ is the extent of literature available to address a proposed listing. Twentysix references were cited in the deep sea coral petition, of which approximately 8 referred to research on threats to these species. The extreme longevity [17] and slow growth [18,19] of many deep sea species indicates their recovery from depletion would be slow [20,21]. They are subject to mortality from trawling [20,21], in some cases extensive [16]. However, the relevance of these global data to the petitioned species in Alaska is unclear [22]. One cited study showed that trawl gear can vertically redistribute layers of sediment, creating anaerobic conditions that may extend beyond the space that was trawled. Six monitoring areas in two regions protected from trawling showed no recovery at all during the first decade; because of the slow growth of deep corals as shown in three cited studies, recovery following protection from trawling ‘‘will take many decades, if not longer’’ [21]. Survey data on population declines in Alaska were limited to a few areas and data on threat impacts were mostly limited to the effects of trawling. The petition to list 44 species of deep-sea corals was rejected on the basis of a lack of substantial distributional information for each species [22]. In this case, NMFS determined that the burden to provide substantial, convincing information was not met in regards to criteria A (threats) and E (other human and natural factors) to warrant a sustainability assessment through the ESA process. Case study 2: Atlantic Acropora species On March 3, 2004, the Center for Biological Diversity petitioned NMFS to list three shallow Atlantic reef coral www.sciencedirect.com

Endangered Species Act listing and coral sustainability Weijerman et al. 17

species (Acropora palmata, A. cervicornis, and A. prolifera) based on widespread population decline over the preceding two decades [23]. The petition received a positive 90day finding, as the agency concurred that the petition presented substantial information [24]. The subsequent scientific status review report provided enough scientific data on population status and the threats to the sustainability of two petitioned coral species to warrant listing such that NMFS proposed a threatened listing for A. palmata and A. cervicornis [24] and made a final determination to list them as threatened [25].

to be largely affected by ocean warming, acidification, and disease [29]. In contrast to the Acropora case, the question of sustainability of petitioned corals was based less on population declines and more on effects of current and future threats. In this case, despite the deficiency of species level data on abundance and responses of corals to threats (with some exceptions), the status review contained sufficient evidence to justify a proposal to list these species [28].

The petition included 198 references. The status review of the two Acropora species cited approximately 400 references, most related to distribution and abundance, and about 40 references were on threats to these corals [26]. Responses of the corals to natural and anthropogenic stressors were documented at some island/regional scales but at the time of this petition, climate change was included only as temperature-induced bleaching as little was known at that time (early 2000s) about the effects of ocean acidification. In the status review, Acropora abundance data showed declines of up to 97% due largely to disease, resulting in substantial changes in reef structure. These low population levels led to reduced reproduction, further reducing coral sustainability [26]. In this case, documented declines of A. palmata and A. cervicornis in combination with recognized threats were deemed sufficient to warrant a final listing determination as threatened.

Through the implementation of recovery plans and other actions, the ESA has been effective in fostering the recovery of many listed species [14,15]. It is less apparent how the ESA affects research on listed species. On one hand, there is a perception within the scientific community that regulations and permitting processes that accompany research on listed species will make research on these species burdensome (public comments for NOAA-NMFS-2010-0036 found at www.regulations.gov). Yet recovery planning may require new research to fill critical information gaps. A Google Scholar search for publications with ‘‘Acropora palmata’’ and ‘‘Acropora cervicornis’’ in the title from 1990 to 2012 showed a steady increase in publications in the early 2000s with a jump in 2006 (the year the species were listed as threatened) and then the number of publications flattened out but remained at a relatively high level (approximately 15 per year). To put these findings into context, we ran similar searches for all other Acropora species, and for the coral genera Porites, Montipora, and Pocillopora (Figure 1).

Case study 3: 82 Indo-Pacific and Atlantic corals On October 20, 2009, the Center for Biological Diversity petitioned NMFS to list 83 tropical scleractinian species from Atlantic and Indo-Pacific waters, based largely on bleaching, ocean acidification, and other climate impacts [27]. The petition presented enough data on threats to the 83 petitioned species for NMFS to issue a positive 90-day finding on 82 of them, and a status review for these 82 species was completed in 2011. The information presented in the status review was deemed substantial enough that NMFS issued a proposal that 66 of these species warranted endangered (12 species) or threatened (54 species) status [28] in December 2012. A final decision by NMFS on the listing is pending.

Consequences of ‘threatened’ listing under ESA for coral research

To normalize for the number of papers produced overall and more directly compare across genera, we divided the number of publications on a genus with the number of publications on the two listed Acropora species (Figure 2). A two-tailed Students t-test showed no significant difference in the mean ratio before and after 2006 for all four genera (Table 1), suggesting that the ESA threatened listing did not negatively affect the research output on the listed Acropora species. Nor do the data suggest an increased focus of research on the species because of listing.

Table 1

The petition included 209 references. The Status Review Report included approximately 1350 citations, including around 600 on local and global threats [29]. Distribution data of the 82 coral species were fairly substantial but abundance data were available from only a few regions and largely not species specific. However, abundance data were available for close relatives of some species on the petition list (e.g. Pacific Acropora in the same genus as Caribbean Acropora with abundance data described in Case Study 2). Sustainability of the corals was determined www.sciencedirect.com

Results of two-tailed Students t-test on the ratio of publications on four coral genera each to the publication of the two listed Acropora species (A2) before and after 2006 Mean (SD)

Ratio Pre-2006 Porites:A2 All other Acropora:A2 Montipora:A2 Pocillopora:A2

3.06 2.12 0.75 1.32

(1.85) (0.89) (0.65) (0.87)

Post-2006 2.47 3.07 0.74 1.23

(0.61) (1.14) (0.37) (0.28)

p 0.47 0.08 0.97 0.81

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Figure 1

20 15 10 5

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Number of publications with the genus name in the title from Google Scholar searches. For A. cervicornis + A. palmata we summed the number of publications with A. cervicornis in the title and A. palmata in the title.

ESA listing may increase applications for research permits because of funding increases, regulatory requirements for research, desire of scientists to work on species with high public interest, or other reasons. Preparing to conduct research on listed species may be also more burdensome as a result of the extra administrative steps required to apply for research permits. For the threatened Acropora listing, permitting authority was delegated under section 4(d) of the ESA. The Florida Keys National Marine Sanctuary is probably the largest single U.S. jurisdiction dealing with the Atlantic Acropora, and already had robust permit requirements in place for all coral research prior to Current Opinion in Environmental Sustainability 2014, 7:15–21

the listing. Data show that permit applications for Acropora work increased from 6 per year during 2000–2005 (37 permits for Acropora research in total or approximately 30% of all issued research permits per year) to 16 per year between 2007 and 2012 (99 permits in total or 43% per year; Florida Keys National Marine Sanctuary database). For Biscayne National Park, permit applications showed an increase as well. For the time period 2000–2005, 6 out of 57 (11%) research permits in the coral reef environment were focused on Acropora research and for 2007–2012, 7 out of 45 (16%) (National Park Service Research Permit and Reporting System. URL: www.sciencedirect.com

Endangered Species Act listing and coral sustainability Weijerman et al. 19

Figure 2

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Ratio of the annual number of publications on a coral genus to the two listed Acropora species. Number of publications resulted from a search on Google Scholar, for example, ‘‘Porites’’ in the title per year. Vertical line indicates 2006 when the two Acropora species were listed.

https://irma.nps.gov/rprs/Permit/Search). Similar results were obtained from Dry Tortugas National Park with 0 out of 26 research permit applications focused on Acropora research from 2000 to 2005 and 3 out of 49 (6%) for 2007–2012. However, for threatened species there is more permitting flexibility compared to the species listed as endangered for which mandatory stringent permitting requirements apply under section 10 of the ESA. No corals have yet been listed as endangered, and the potential effects on permitting and research productivity for endangered coral species remain unknown.

Conclusions The meaning of the term ‘substantial information’ and the quality of ‘best available information’ are subjective and evaluated by the responsible government agencies on a case-by-case basis. Likewise, interpretation and evaluation of the data used in status reviews are somewhat subjective and variations in interpretation will exist even when status review teams follow the same guidelines. Because of this subjectivity, there is some concern that different ESA assessments may reach different conclusions simply because they are conducted by different groups of people www.sciencedirect.com

[30]. To reduce the potential ‘team effect’, ESA status evaluations, including those described in these three case studies, undergo an extensive review process. The coral case studies illustrate ESA decisions based on different types of available information: (1) Limited evidence that the species is declining or faces clear threats (Alaska coral — data insufficient to warrant a status review); (2) Speciesspecific evidence of population and recruitment declines in addition to severe documented threats (Acropora sp. — ESA listed); and, (3) Limited species-specific data on population declines, but clear evidence of declines in related groups of species and clear evidence of specific threats (82 coral species — a subset proposed for listing). This last case study shows that coral sustainability assessments do not necessarily require substantial quantitative data on changes in abundance and/or distribution of petitioned species. Information on the threats to petitioned species or their close relatives can provide adequate evidence of endangerment. If thorough population assessments had been required in Case study 3 above, the high cost of acquiring abundance data on all species throughout their range would have made listing of these species unlikely. However, at least some information on population status or clear threats to the species is required to Current Opinion in Environmental Sustainability 2014, 7:15–21

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meet the initial burden of proof that the species is at risk. The ESA requires that a decision must be made in a timely manner with the best available scientific data. Though inevitably involving uncertainty, decisions often are made with limited data. The ESA requires that the status of listed species be reviewed every five years. Although initial decisions must be made even with limited information, a reevaluation based on new research allows response to changes in status or refinement of initial analyses. The listing process itself can affect the research activity on the species. For example, millions of dollars were spent on research on Pacific salmon in response to ESA listing activities [31,32]. However, in the coral research community, there is concern that permitting of research on listed species will become excessively burdensome (public comments for NOAA-NMFS-20100036 found at www.regulations.gov). This concern is not substantiated for ‘threatened’ listings by the number of publications on the listed Atlantic Acropora species. Anecdotal evidence suggests that ESA listing has actually focused additional efforts on these species and some funding opportunities have specifically targeted listed species. This suggests that a threatened listing will not dampen research for improved future status evaluations. However, it must be acknowledged that the administrative burden for endangered species is greater (e.g. an additional, publicly vetted permitting process specified under Section 10 of the ESA) than for threatened species. Currently proposed endangered species in the Atlantic/Caribbean region include common species heavily targeted in research activities (e.g. the two Acropora species [proposed for change in listing] and the three species in the Orbicella annularis [previously Montastraea annularis] complex), whereas the proposed endangered species in the Pacific region are rarer and less common research subjects. NMFS Office of Permits has been proactive in preparing this permitting process for proposed endangered corals to (http://www.nmfs.noaa.gov/pr/permits/corals.htm) ensure researchers have opportunity to obtain required permits prior to any final listing implementation (expected summer 2014). The actual effect of ESA listing to research on these coral species remains to be seen.

Acknowledgement The contents of this article are solely the findings and opinions of the authors and do not constitute a statement of policy, decision, or position on behalf of NOAA or the US Government.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

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