Endangered and Threatened Wildlife and Plants; Final Listing Determinations for Two Distinct Population Segments of Atlantic Sturgeon (Acipenser oxyrinchus oxyrinchus) in the Southeast

DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Part 224

[Docket No. 090219208-1762-02]

RIN 0648-XN50

Endangered and Threatened Wildlife and Plants; Final Listing Determinations for Two Distinct Population Segments of Atlantic Sturgeon (

Acipenser oxyrinchus oxyrinchus

) in the Southeast

AGENCY:

National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

ACTION:

Final rule.

SUMMARY:

We, NMFS, issue a final determination to list the Carolina and South Atlantic distinct population segments (DPSs) of Atlantic sturgeon (

Acipenser oxyrinchus oxyrinchus

) as endangered under the Endangered Species Act (ESA) of 1973, as amended. We have reviewed the status of the species and conservation efforts being made to protect the species, considered public and peer review comments, and we have made our determination that the Carolina and South Atlantic DPSs are in danger of extinction throughout their ranges, and should be listed as endangered, based on the best available scientific and commercial data.

DATES:

This final rule is effective April 6, 2012.

ADDRESSES:

Assistant Regional Administrator for Protected Resources, NMFS, Southeast Regional Office, 263 13th Avenue South, St. Petersburg, FL 33701-5505.

FOR FURTHER INFORMATION CONTACT:

Kelly Shotts, NMFS, Southeast Regional Office (727) 824-5312 or Lisa Manning, NMFS, Office of Protected Resources (301) 427-8466.

SUPPLEMENTARY INFORMATION:

Background

We first identified Atlantic sturgeon as a candidate species in 1991. On June 2, 1997, NMFS and U.S. Fish and Wildlife Service (USFWS; collectively, the Services) received a petition from the Biodiversity Legal Foundation requesting that we list Atlantic sturgeon in the United States, where it continues to exist, as threatened or endangered and designate critical habitat within a reasonable period of time following the listing. A notice was published in the

Federal Register

on October 17, 1997, stating that the Services had determined substantial information existed indicating the petitioned action may be warranted (62 FR 54018). In 1998, after completing a comprehensive status review, the Services published a 12-month determination in the

Federal Register

announcing that listing was not warranted at that time (63 FR 50187; September 21, 1998). We retained Atlantic sturgeon on the candidate species list (and subsequently transferred it to the Species of Concern List (69 FR 19975; April 15, 2004)). Concurrently, the Atlantic States Marine Fisheries Commission (ASMFC) completed Amendment 1 to the 1990 Atlantic Sturgeon Fishery Management Plan (FMP) that imposed a 20- to 40-year moratorium on all Atlantic sturgeon fisheries until the Atlantic Coast spawning stocks could be restored to a level where 20 subsequent year classes of adult females were protected (ASMFC, 1998). In 1999, pursuant to section 804(b) of the Atlantic Coastal Fisheries Cooperative Management Act (ACFCMA) (16 U.S.C. 5101

et seq.

), we followed this action by closing the Exclusive Economic Zone (EEZ) to Atlantic sturgeon retention. In 2003, we sponsored a workshop in Raleigh, North Carolina, with USFWS and ASMFC entitled, “The Status and Management of Atlantic Sturgeon,” to discuss the status of sturgeon along the Atlantic Coast and determine what obstacles, if any, were impeding their recovery. The workshop revealed mixed results in regards to the status of Atlantic sturgeon riverine populations, despite the coastwide fishing moratorium. Some populations seemed to be recovering while others were declining. Bycatch and habitat degradation were noted as possible causes for continued population declines.

Based on the information gathered from the 2003 workshop on Atlantic sturgeon, we decided that a new review of Atlantic sturgeon status was needed to determine if listing as threatened or endangered under the ESA was warranted. The Atlantic sturgeon status review team (ASSRT), consisting of four NMFS, four USFWS, and three U.S. Geological Survey (USGS) biologists prepared a draft status review report. The draft report was then reviewed and supplemented by eight state and regional experts who provided their individual expert opinions on the scientific facts contained in the report and provided additional information to ensure the report provided the best available data. Lastly, the report was peer reviewed by six experts from academia. A Notice of Availability of the final status review report was published in the

Federal Register

on April 3, 2007 (72 FR 15865). On October 6, 2009, we received a petition from the Natural Resources Defense Council to list Atlantic sturgeon as endangered under the ESA. As an alternative, the petitioner requested that the species be delineated and listed as the five DPSs described in the 2007 Atlantic sturgeon status review report (ASSRT, 2007): Gulf of Maine, New York Bight, Chesapeake Bay, Carolina, and South Atlantic DPSs, with the Gulf of Maine and South Atlantic DPSs listed as threatened, and the remaining three DPSs listed as endangered. The petitioner also requested that critical habitat be designated for Atlantic sturgeon under the ESA. We published a Notice of 90-Day Finding on January 6, 2010 (75 FR 838), stating that the petition presented substantial scientific or commercial information indicating that the petitioned actions may be warranted. On October 6, 2010, we published a proposed rule (75 FR 61904) to list the Carolina and South Atlantic DPSs, the two DPSs that spawn in the NMFS Southeast Region, as endangered. We originally solicited written public comments via email, fax, and letter on the proposed listing rule for 90 days and extended it for an additional 30 days by public request. We also accepted written and verbal comments at two public hearings in Wilmington, North Carolina, and Atlanta, Georgia, in December 2010. A separate proposed rule (75 FR 91872) was published on October 6, 2010, for the three DPSs of Atlantic sturgeon that spawn in the NMFS Northeast Region.

Listing Determinations Under the Endangered Species Act

We are responsible for determining whether Atlantic sturgeon are threatened or endangered under the ESA (16 U.S.C. 1531

et seq.

). To be considered for listing under the ESA, a group of organisms must constitute a “species,” which is defined in section 3 of the ESA to include “any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.” On February 7, 1996, the Services adopted a policy describing what constitutes a DPS of a taxonomic species (61 FR 4722). The joint DPS policy identified two elements that must be considered when identifying a DPS: (1) The discreteness of the population segment in relation to the remainder of the species (or subspecies) to which it belongs; and (2) the significance of the population segment to the remainder of the species (or subspecies) to which it

belongs. As stated in the joint DPS policy, Congress expressed its expectation that the Services would exercise authority with regard to DPSs sparingly and only when the biological evidence indicates such action is warranted.

Section 3 of the ESA defines an endangered species as “any species which is in danger of extinction throughout all or a significant portion of its range” and a threatened species as one “which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” The statute requires us to determine whether any species is endangered or threatened as a result of any one or a combination of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence (section 4(a)(1)(A)(E)). Section 4(b)(1)(A) of the ESA requires us to make listing determinations based solely on the best scientific and commercial data available after conducting a review of the status of the species and after taking into account efforts being made to protect the species. Accordingly, we have followed a stepwise approach in making our listing determination for Atlantic sturgeon. Considering biological evidence, such as the separation between river populations during spawning and the possibility of multiple distinct interbreeding Atlantic sturgeon populations, we evaluated whether Atlantic sturgeon population segments met the DPS Policy criteria. We then determined the status of each DPS (each “species”) and identified the factors and threats contributing to their status per section 4(a)(1) of the ESA. Finally, we assessed efforts being made to protect the species, determining if these efforts are adequate to mitigate impacts and threats to the species' statuses. We evaluated ongoing conservation efforts using the criteria outlined in the Policy for Evaluating Conservation Efforts (PECE; 68 FR 15100; March 28, 2003) to determine their certainties of implementation and effectiveness.

Finally, section 4(b)(1)(B) of the ESA requires us to give consideration to species which: (1) Have been designated as requiring protection from unrestricted commerce by any foreign nation or pursuant to an international agreement; or (2) have been identified as in danger of extinction, or likely to become so within the foreseeable future, by any state agency or by any agency of a foreign nation.

Peer Review and Public Comments

In December 2004, the Office of Management and Budget (OMB) issued a Final Information Quality Bulletin for Peer Review establishing minimum standards for peer review. Similarly, a joint NMFS/FWS policy (59 FR 34270; July 1, 1994) requires us to solicit independent expert review from at least three qualified specialists. We solicited peer review comments on the proposed listing rule from three peer reviewers, two from academia and one from a Federal resource agency, with expertise on Atlantic sturgeon. Written public comments were received from 59 commenters and 7 commenters provided verbal comments at the public hearings. Peer review comments are treated in the next section. In the following sections of the document, the public comments are categorized in the following areas: (1) The delineation of DPSs; (2) abundance and trends; (3) differences between the proposed rule and the conclusions in the 2007 and 1998 status reviews; (4) the need to list Atlantic sturgeon under the ESA and consequences of listing; (5) the analysis of threats (habitat modification and destruction, overutilization, disease and predation, the inadequacy of regulatory mechanisms, other natural and manmade factors); (6) recovery; (7) critical habitat; and (8) adequacy of the public hearing. Many comments were complex and had multiple inferences, and thus individual statements are addressed in multiple comments and responses below. Information and data provided by commenters supported or did not conflict with our findings for the Carolina and South Atlantic DPSs. Some information submitted by commenters as “new” information was information already included and evaluated in our proposed listing rule determination. Some commenters asked us to consider information, such as increased compliance responsibilities and economic costs on agencies and the public, that the ESA and its implementing regulations prohibit us from considering in making listing determinations. Many commenters stated that NMFS should postpone a listing determination until the results of recent research are available, further research can be undertaken, state and Federal moratoria on the harvest and possession of Atlantic sturgeon have been in effect for the full planned duration, and/or until non-listing alternatives (

e.g.,

entering into multi-agency partnerships and expanding existing programs) have been explored. Because we were petitioned to list the Atlantic sturgeon, we cannot delay an assessment of the status of Atlantic sturgeon. We were required to evaluate the status of the species and the threats it is currently facing and make a finding on whether the petitioned action was warranted within 12 months, which resulted in our proposed listing determination of endangered for the Carolina and South Atlantic DPSs of Atlantic sturgeon. We believe the current body of information on the declines of Atlantic sturgeon, the failure of their population numbers to rebound despite harvest prohibitions, and the ongoing impacts from bycatch, habitat modification, and the inadequacy of existing regulatory mechanisms or protective efforts to control or mitigate for these impacts, warrant listing the Carolina and South Atlantic DPSs as endangered. The information provided in the peer review and public comments did not provide a basis for revising our evaluation of the status of Atlantic sturgeon, the nature and significance of the threats and impacts they face, or our listing determinations. In the following sections of the document, we summarize the comments pertaining to the proposed listing rule for the Carolina and South Atlantic DPSs and provide our responses to those comments. Complete copies of the peer review comments, the written public comments, and transcripts of the public hearings are available on the Internet at

www.regulations.gov.

Peer Review Comments

In this section, we refer to peer reviewers 1, 2, and 3, which correspond to the way the peer reviewers are identified on

http://www.regulations.gov.

Comment 1 (definitions of endangered and threatened):

Two of the three peer reviewers disagreed, all or in part, with our proposed listing of the Carolina and South Atlantic DPSs as endangered. Each peer reviewer provided their own definitions of endangered and threatened.

Peer reviewer 1 believed that a DPS warranted an endangered listing only if no single historical spawning river within the DPS sustained an abundant and regularly reproducing Atlantic sturgeon population. Peer reviewer 1 stated that no substantive biological justification or new evidence is presented in the proposed listing of the Carolina and South Atlantic DPSs as endangered to change the conclusions presented in the 2007 status review, which concluded that the Carolina DPS should be listed as threatened and made

no conclusion with regard to the South Atlantic DPS due to lack of information to allow a full assessment of subpopulations within the DPS. Peer reviewer 1 stated that an endangered listing would be appropriate if no single historical spawning river within that DPS appeared to sustain both a relatively abundant and simultaneously regularly-reproducing Atlantic sturgeon population.

Based on the available information on abundance, reproduction, and the presence of early life history stages, the reviewer stated that the Carolina DPS comes closest to conforming to the standard of an endangered species. The reviewer cited data from the proposed listing rule that two of the original three major spawning populations (the Roanoke and Santee-Cooper populations) in the Carolina DPS appear to remain functional, and not particularly vulnerable to extinction. The reviewer also stated the proposed listing of the South Atlantic DPS did not appear to be supported by the best available scientific information, since there is evidence of at least one viable, reproducing, and increasing Atlantic sturgeon population in the South Atlantic DPS, the Altamaha River population (Schueller and Peterson, 2006, 2010). The reviewer further cited both the Savannah River and the ACE (Ashepoo, Combahee, and Edisto Rivers) Basin systems as appearing to support reproducing Atlantic sturgeon populations, and stated Atlantic sturgeon appear to be abundant in the ACE system. The reviewer questioned whether the remaining South Atlantic DPS river populations in the smaller and less well-studied Ogeechee and Satilla rivers together constitute a significant portion of the species' range over which extinction is probable in order to justify an “endangered” designation for the entire DPS. The reviewer noted that the 2007 status review report deferred from such a designation and that it appears the South Atlantic DPS does not closely conform to the standard of being endangered. Based on the available scientific evidence concerning population size and reproduction in the historically most important populations, the resilience of sturgeons to extirpation, and their capacity for re-population from small effective population size, the reviewer believed the appropriate ESA designation for both DPSs would seem to be threatened. The reviewer suggested that the threatened status would provide protection for the species from direct take of any kind and a basis for habitat restoration, while providing greater flexibility for scientific sampling, tissue analyses, and experimental manipulation than would endangered status. The reviewer stated the downside is that threatened status would provide a lower level of legal leverage relative to the larger industrial impacts,

e.g.,

dams and bycatch, either of which may represent an insurmountable impasse to sturgeon recovery. The reviewer offered that under existing direct harvest prohibitions, threatened status has worked effectively for Gulf sturgeon recovery in rivers where dams and bycatch are not significant issues. It has not worked effectively where dams and bycatch are significant issues (

e.g.,

the Pearl, Pascagoula, and Apalachicola rivers), although none of those populations seem in danger of extinction.

Peer reviewer 2 stated that implicit in the definition of “endangered” is that the species must be on a significant downward trend, or at least there is cause to believe that such a trend is happening now, or will happen soon, and concluded that is not the case on the Altamaha River in Georgia. However, this reviewer also commented that every single Atlantic sturgeon population has been decimated by overfishing and habitat degradation and that we have very little quantified evidence that the species as a whole has recovered, despite 14 years of the protection afforded under the current moratorium on harvest and possession. Peer reviewer 2 recommended that a “threatened” listing would seem appropriate for almost every Atlantic coast river, including the St. Marys, Satilla, Ogeechee, and Savannah Rivers in Georgia, with the Altamaha being the one exception, and an endangered listing would be difficult to support.

Response:

We must rely on the definition of “endangered” and “threatened” species provided in section 3 of the ESA, the implementing regulations, and case law in applying the definitions to marine and anadromous species. Section 3 of the ESA defines an endangered species as one that is in danger of extinction throughout all or a significant portion of its range, and a threatened species as one that is likely to become endangered within the foreseeable future. Recent case law (

In Re Polar Bear Endangered Species Act Listing and § 4(d) Rule Litigation,

D.D.C. WL 2601604 (June 30, 2011 Order); 748 F.Supp.2d 19 (D.D.C. 2010)) regarding USFWS's listing of the polar bear as threatened provides a thorough discussion of the ESA's definitions and the Services' broad discretion to determine on a case by case basis whether a species is in danger of extinction. Upon listing the polar bear as threatened, USFWS's rule was challenged by a number of parties who claimed that the polar bear was in danger of extinction and should have been listed as endangered, and by others who conversely argued that the bear did not warrant listing even as threatened. The Court determined that neither the ESA nor its legislative history compels the interpretation of “endangered” as a species being in “imminent” risk of extinction, finding instead that the phrase “in danger of extinction” is ambiguous. The Court held that there is a temporal distinction between endangered and threatened species in terms of the proximity of the “danger” of extinction, noting that the definition of “endangered species” is phrased in the present tense, whereas a threatened species is “likely to become” so in the future. Thus, in the context of the ESA, the Services interpret an “endangered species” to be one that is presently at risk of extinction. A “threatened species,” on the other hand, is not currently at risk of extinction, but is likely to become so. In other words, a key statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either now (endangered) or in the foreseeable future (threatened). The Court concluded, however, that the distinction is not based “solely and unambiguously” on the imminence of the species' anticipated extinction,” and that Congress delegated responsibility to the Services to determine whether a species is presently `in danger of extinction' in light of the five ESA section 4(a)(1) factors and the best available science for that species. The Court ruled that although imminence of harm is clearly one factor that the Services weigh in their decision-making process, it is not necessarily a limiting factor. In many cases, the Services might appropriately find that the imminence of a particular threat is the dispositive factor that warrants listing a species as `threatened' rather than `endangered,' or vice versa. The Services have broad discretion to decide that other factors outweigh the imminence of the threat. In conclusion, the Court confirmed that the Services have flexibility to determine “endangerment” on a case-by-case basis. Congress did not intend to make any single factor controlling when drawing the distinction between endangered and threatened species, nor did it seek to limit the applicability of the endangered

category to only those species facing imminent extinction.

Thus, contrary to the peer reviewers' comments, there is no per se requirement that a species be experiencing current or imminent significant downward trends, or that there are no single historical spawning river populations within the DPSs that are relatively abundant and simultaneously regularly-reproducing, in order to be listed as endangered (we discuss the status and data on the Altamaha River population in more detail in Comment 2 below). Our determination of endangerment for the Carolina and South Atlantic DPSs is based on the exercise of our expert professional judgment on the basis of the best available information for each DPS. In addition, we agree with the USFWS' judgment, discussed in its supplemental explanation filed in the polar bear litigation, that to be listed as endangered does not require that extinction be certain or probable, and that it is possible for a species validly listed as “endangered” to actually persist indefinitely.

We determined that the Carolina and South Atlantic DPSs of Atlantic sturgeon are currently in danger of extinction throughout their ranges, on the basis of precipitous declines to population sizes, the protracted period in which sturgeon populations have been depressed, the limited amount of current spawning, and the impacts and threats that have and will continue to prevent population recovery. Populations of Atlantic sturgeon declined precipitously decades ago due to directed commercial fishing. The failure of Atlantic sturgeon numbers within the Carolina and South Atlantic DPSs to rebound even after the moratorium on directed fishing was established in 1998 indicates that impacts and threats from limits on habitat for spawning and development, habitat alteration, and bycatch are responsible for the risk of extinction faced by both DPSs. In addition, the persistence of these impacts and threats points to the inadequacy of existing regulatory mechanisms to address and reduce habitat alterations and bycatch. As described in the proposed listing rule, the Carolina DPS is estimated to number less than 3 percent of its historical population size; the South Atlantic DPS is estimated to number less than 6 percent of its historical population size, with all river populations except the Altamaha estimated to be less than 1 percent of historical abundance. There are an estimated 343 adults that spawn annually in the Altamaha River and less than 300 adults spawning annually (total of both sexes) in the river systems where spawning still occurs for each DPS (not all of the river systems occupied by the two Southeast DPSs currently support spawning, or effective spawning leading to recruitment).

In light of threats and impacts, the low population numbers of every river population in the Carolina and South Atlantic DPSs suggests that the DPSs are currently in danger of extinction throughout their ranges; none of the populations are large or stable enough to alone or in combination provide any level of certainty for continued existence of either DPS, and thus, the peer reviewer's suggestion that these DPSs may not be endangered rangewide or in a significant portion of their ranges is erroneous. While the directed fishery that originally drastically reduced the numbers of Atlantic sturgeon has been closed, recovery of depleted populations is an inherently slow process for a late-maturing species such as Atlantic sturgeon, and they continue to face a variety of other threats that contribute to their risk of extinction. Their late age at maturity (5 to 19 years in the Southeast) provides more opportunities for individual Atlantic sturgeon to be removed from the population before reproducing. While a long life-span also allows multiple opportunities to contribute to future generations, it increases the timeframe over which exposure to the multitude of threats facing the Carolina and South Atlantic DPS can occur.

Based on available information, we determined that to be viable, the Carolina and South Atlantic DPSs require multiple stable riverine populations, and we have added discussion to the final determination to better explain our reasoning. The importance of having multiple stable riverine spawning populations within each DPS and the need to maintain suitable habitat to support the various life functions (spawning, feeding, growth) of Atlantic sturgeon is best understood by looking at the concept of metapopulations. Each DPS, made up of multiple river populations, is analogous to a metapopulation, which is a “population of populations” (Levins, 1969), a group of spatially separated populations of the same species which interact at some level. Separation into metapopulations is expected by sturgeon and other anadromous fishes. While recolonization of northern rivers following post-Pleistocene deglaciation likely occurred following a stepping-stone sequential model (Waldman

et al.,

2002), genetic analyses reveal that currently, there are very low rates of exchange between river populations. The amount and effectiveness of movement separates a metapopulation from a single large, patchy population. Low rates of connectivity through dispersal, with little to no effective movement, allow individual populations to remain distinct as the rate of migration between local populations is low enough not to have an impact on local dynamics or evolutionary lineages and distinguishes a metapopulation from a patchy population (Harrison 1994).

Metapopulation persistence depends on the balance of extinction and colonization in a static environment (Hanski 1996). If habitat remains suitable following local extirpation, recolonization via immigrants into now-empty habitat may replace at least some of those losses (Thomas, 1994). However, if the cause of extinction is a deterministic population response to unsuitable conditions (

e.g.,

lack of suitable spawning habitat, poor water quality, or disturbance of substrates through repeated dredging), the local habitat is likely to remain unsuitable after extinction and be unavailable for effective recolonization (Thomas, 1994). Therefore, recolonization is dependent upon both immigration from adjacent, healthy populations and habitat suitability. Because the DPSs are groups of populations, the stability, viability, and persistence of individual populations affects the persistence and viability of the larger DPS. The loss of any population within a DPS will result in: (1) A long-term gap in the range of the DPS that is unlikely to be recolonized, or recolonized only very slowly; (2) loss of reproducing individuals; (3) loss of genetic biodiversity; (4) potential loss of unique haplotypes; (5) potential loss of adaptive traits; and (6) reduction in total number. The loss of a population will negatively impact the persistence and viability of the DPS as a whole as fewer than two individuals per generation currently spawn outside their natal rivers (Wirgin

et al.,

2000; King

et al.,

2001; Waldman

et al.,

2002).

The persistence of individual populations, and in turn the DPS, depends on successful spawning and rearing within the freshwater habitat, the immigration into marine habitats to grow, and then the return of adults to natal rivers to spawn. Information on Atlantic sturgeon spawning within the Carolina and South Carolina DPSs is limited. In the proposed listing rule, we presumed spawning was occurring if young-of-the-year (YOY) were observed or mature adults were present in freshwater portions of the system.

Within the Carolina DPS, we concluded that spawning is occurring, or occurred in the recent past, in the following rivers based on these data:

1. Roanoke River—collection of 15 YOY (1997-1998); single YOY (2005).

2. Tar and Neuse Rivers—one YOY (2005).

3. Cape Fear—upstream migration of adults in the fall, carcass of ripe female upstream in mid-September.

4. Winyah Bay—running ripe male in Great Pee Dee River (2003).

Within the South Atlantic DPS, we concluded that spawning is occurring, or has occurred in the recent past, in the following rivers based on these data:

1. ACE Basin—1,331 YOY (1994-2001); gravid female and running ripe male in the Edisto (1997); 39 spawning adults (1998).

2. Savannah River—22 YOY (1999-2006); running ripe male (1997).

3. Ogeechee River—age-1 captures, but high inter-annual variability (1991-1998); 17 YOY (2003); 9 YOY (2004).

4. Altamaha River—74 captured/308 estimated spawning adults (2004); 139 captured/378 estimated spawning adults (2005).

5. Satilla River—4 YOY and spawning adults (1995-1996).

These data indicate that spawning occurs within the Carolina and South Atlantic DPSs; they do not indicate the frequency of annual spawning events or the degree to which spawning in these systems leads to population growth, persistence, or viability. The extent and effectiveness of spawning events is unknown and likely precarious in many rivers, given ongoing threats that limit population size and spawning success, such as water quality and restricted access to upstream spawning areas (75 FR 61904). Peer reviewer 1 stated that data from the proposed listing rule indicate the spawning populations in the Santee-Cooper system appear to remain functional and not particularly vulnerable to extinction; however, in the proposed listing rule, we noted our determination that spawning may occur in the Santee and/or the Cooper Rivers, but it may not result in successful recruitment. Lack of access to historical spawning habitat due to dams restricts spawning to areas just below the dam. The proximity of these spawning areas to salt water may result in very high mortality to any larvae spawned in those systems.

In addition to spawning success, it is difficult to quantify spawning potential within the two DPSs, given the lack of population estimates. Currently, the number of Atlantic sturgeon in the Carolina DPS is estimated to be 3 percent of historical population size and the South Atlantic DPS is estimated to be 1 percent of historical population size, with the exception of the Altamaha River population, estimated to be at 6 percent of historical population size. Although the largest impact that caused the precipitous decline of the species has been curtailed (directed fishing), the population size has remained relatively constant at these greatly reduced levels for approximately 100 years.

In response to comments about divergence from the status review report's listing conclusions for the Carolina and South Atlantic DPSs, NMFS' Protected Resources Divisions have the responsibility to make listing recommendations to the Assistant Administrator. Status review reports are an important part of the information base for such recommendations, but NMFS must independently review the information in status review reports and apply the ESA's listing determination requirements in accordance with regulations, case law, and agency guidance. The Atlantic Sturgeon Status Review Report states that “risks of extinction assessments are performed to help summarize the status of the species, and do not represent a decision by the Status Review Team on whether the species should be proposed for listing as endangered or threatened under the ESA” (page 106; ASSRT, 2007). Subsequent to the status review report, we conducted a comprehensive assessment of the combined impact of the five ESA section 4(a)(1) factors across the Carolina and South Atlantic DPSs in classifying extinction risk for each DPS. We focused on evaluating whether the DPSs are presently in danger of extinction or the danger of extinction is likely to develop in the future. In our proposed rules to list 5 DPSs of Atlantic sturgeon, we determined that each DPS was at greater risk of extinction than determined by the 2007 ASSRT. While the ASSRT did discuss and consider how multiple threats might act in concert on a given subpopulation, they ultimately classified extinction risk using the highest single threat score on an individual population within a DPS, or within what they considered to be a significant portion of a DPS's range (pages 108-109; ASSRT, 2007). We evaluated the overall stability and viability of the DPSs as a whole based on the combined statuses of the component river populations and the impacts of threats and impacts across the DPS, when determining extinction risk of each DPS, because, as discussed above, the Carolina and South Atlantic DPSs require multiple stable river populations. In addition, because of the lapse in time between the development of the status review report (ASSRT, 2007) and the publication of the proposed listing rule (75 FR 61904, October 6, 2010), new information on bycatch (ASMFC, 2007) and water quality (USEPA, 2008), as well as climate change (IPCC, 2008) and drought (

e.g.,

USGS, 2007), became available to us, and we incorporated this information into our listing determinations.

Since publication of the proposed rules, a Federal District Court has thoroughly reviewed and considered the distinction between the definitions of threatened and endangered species in the ESA, explained by the USFWS in litigation challenging their determination to list the polar bear as threatened and not endangered, as discussed above (

In re. Polar Bear Endangered Species Act Litigation

). Prompted by this decision and the comments received by the Services requesting further explanation of the divergence of our proposed listing statuses and the conclusions of the ASSRT, we have reviewed our determinations and concluded that all the proposed listings of specific DPSs as “threatened species” or “endangered species,” respectively, satisfy the requirements of the relevant ESA definition. Thus, we have not changed these classifications in the final rules. We found that the Carolina and South Atlantic DPSs are presently in danger of extinction, and thus, listing them as endangered is warranted.

As discussed above, because a DPS is a group of populations (a metapopulation), the stability, viability, and persistence of individual populations affects the persistence and viability of the larger DPS. The persistence of individual populations, and in turn the DPS, depends on successful spawning and rearing within the freshwater habitat, the immigration into marine habitats to grow, and then the return of adults to natal rivers to spawn. While the directed fishery that originally drastically reduced the numbers of Atlantic sturgeon has been closed, modification and curtailment of Atlantic sturgeon habitat resulting from dams, dredging, and degraded water quality are inhibiting spawning and population rebounding throughout both DPSs, and contributing to their endangered statuses. Existing water allocation issues will likely be compounded by human population growth and potentially by climate change as well. Climate change is predicted to elevate water temperatures and exacerbate nutrient-loading,

pollution inputs, and lower dissolved oxygen (DO), all of which are currently negatively impacting the Carolina and South Atlantic DPSs. Continued overutilization of Atlantic sturgeon from bycatch in multiple commercial fisheries in both their marine and freshwater habitats is another ongoing impact to the Carolina and South Atlantic DPSs that is contributing to their endangered status. Atlantic sturgeon taken as bycatch may suffer immediate mortality. In addition, stress or injury to Atlantic sturgeon taken as bycatch but released alive may result in increased susceptibility to other threats, such as poor water quality (

e.g.,

exposure to toxins and low DO). This may result in reduced ability to perform major life functions, such as foraging and spawning, or may even result in post-capture mortality. Several of the river populations in the South Atlantic DPS (

e.g.,

the Ogeechee and the Satilla) are stressed to the degree that any level of bycatch could have an adverse impact on the status of the DPS (ASSRT, 2007).

The Carolina and South Atlantic DPSs are in danger of extinction now, due to precipitous declines from historical abundances to population sizes that are low and potentially unstable throughout the DPSs. As discussed above, both DPSs exhibit sporadic spawning with uncertain effectiveness. Population rebuilding and recovery in both DPSs is being inhibited by impacts due to habitat curtailment and degradation, and due to capture as bycatch in commercial fisheries. The current low levels of abundance noted previously in combination with the high degree of threat to the two Southeast DPSs put them in danger of extinction throughout their ranges; none of the populations making up the DPSs are large or stable enough to provide any level of certainty for continued existence of either DPS.

Regarding the conclusion that the Carolina and South Atlantic DPSs should be listed as threatened, peer reviewer 1 incorrectly stated that listing as threatened provides protection from direct take of any kind. The ESA's prohibition against take contained in section 9 only applies to endangered species, unless a section 4(d) rule is in place to extend the take prohibition to a threatened species. If we determine that the Carolina and South Carolina DPSs meet the ESA's definition of endangered, then we cannot list the species as threatened for the purposes of providing flexibility for scientific sampling, tissue analyses, and experimental manipulation. We also cannot list the DPSs as endangered to obtain legal leverage relative to the larger industrial impacts,

e.g.,

dams and bycatch, as suggested by the reviewer. Rather, we must make our listing determination based on application of the statutory factors.

Comment 2 (new information on Altamaha River population):

Peer reviewer 2 presented data on the estimated abundance of age-1, river resident Atlantic sturgeon in the Altamaha River from 2004 to 2010, which showed large estimated increases in this age group in 2009 and 2010. The peer reviewer also stated that he and other researchers are beginning to detect slower growth in age-1 Atlantic sturgeon in the Altamaha and he attributed this to density-dependent factors that are beginning to limit available resources. The reviewer stated that a few more years of data are needed to determine if the increasing trend is real, but none of the other variables tested (

e.g.,

river flows or temperature) explain the trend. The peer reviewer attributed the apparent increases in juveniles in the Altamaha to the moratorium on the harvest of adults. The peer reviewer stated that data are not available to determine whether this trend is occurring in other spawning populations. The reviewer stated that catch per unit effort (CPUE) data are worthless without calibration or validation and we do not have historical abundance data to know what abundance should be on any of the river systems, though there is general agreement that populations are a fraction (less than 1 to 10 percent) of historical abundance. The reviewer recommended that long-term monitoring of recruitment using mark-recapture of age-1 juveniles be implemented on key river systems.

Response:

We are encouraged by the apparent increases in juvenile Atlantic sturgeon estimated by the peer reviewer's research in the Altamaha River and appreciate the contribution of this information for our consideration in our listing determination. We revised the relevant discussion in the text from the proposed listing rule to include this information. We agree that additional years of data are necessary to confirm this trend in the Altamaha and that we cannot determine whether similar trends may be occurring in other river populations. This information is consistent with information we provided in the proposed listing rule, which refers to the Altamaha River as having a larger and healthier Atlantic sturgeon population than any other river in the Southeast. The proposed listing rule also stated that juvenile Atlantic sturgeon from the Altamaha are relatively more abundant in comparison to other rivers in the region.

Peer reviewer 2 noted that density-dependent factors may be starting to limit available resources. We are interested in working with the reviewer and other researchers to determine whether habitat modification, which we describe in detail in the proposed listing rule, is a contributing factor to the limitation of resources in addition to the increase in numbers of juvenile Atlantic sturgeon utilizing the resources. While water quality in the Altamaha River is good at this time, the drainage basin is dominated by silviculture and agriculture, with two paper mills and over two dozen other industries or municipalities discharging effluent into the river. Nitrogen and phosphorus concentrations are increasing, and eutrophication and loss of thermal refugia are growing concerns for this and other rivers in the South Atlantic DPS. The Altamaha is one of the rivers with current and pending water allocation issues. We are currently funding a project through the ESA section 6 program to map habitats in four Georgia rivers, including the Altamaha, and this may be a valuable step in answering this question.

We agree that CPUE data should be used in the proper context and that historical abundance data, other than data from commercial fisheries in the late 19th century, are not available. However, as required by section 4(b)(1)(A) of the ESA, we must make our listing determination based on the best scientific and commercial data available. When only CPUE and other fishery-dependent data were available to us, we clarified and acknowledged the constraints of the data, and we conclude that we used them in a valid manner. This is further addressed in our responses to several public comments on specific sections of the proposed listing rule (

e.g.,

comments 19, 23, 24, 25, and 29).

Comment 3 (import of the 2003 workshop):

Peer reviewer 1 stated the proposed listing rule appeared to dismiss any evidence of an increase in Carolina DPS populations of Atlantic sturgeon, citing a statement in the proposed listing rule (page 61904-61905) that “the [NMFS-sponsored 2003] workshop revealed mixed results in regards to the status of Atlantic sturgeon populations, despite the coast-wide fishing moratorium. Some populations seemed to be recovering while others were declining.” The reviewer stated that at the time of the 2003 workshop, the moratorium on direct harvest and possession of Atlantic sturgeon had only been in effect for 4 years and this was not sufficient time for populations to increase in response

to the protective measures. The reviewer concluded the observations available at the time of the 2003 workshop do not provide a scientific basis for listing the Carolina DPS as endangered.

Response:

The information we evaluated in making our proposed listing determination of endangered for the Carolina and South Atlantic DPSs of Atlantic sturgeon was not confined to the results of the 2003 workshop. As stated in the proposed listing rule, the information gathered at the 2003 workshop, including the equivocal evidence that some populations appeared to be recovering while others were declining, prompted us to complete a new review of Atlantic sturgeon status, which was published in 2007. Since the ASSRT's completion of its status review, we obtained and evaluated additional information on threats to Atlantic sturgeon (see our response to comment 1). Our evaluation of this information indicates that the moratorium on directed fisheries has not and will not be sufficient to address the impacts that are preventing sturgeon populations from recovering (including lack of access to required habitat, and habitat quality issues). Section 4(b)(1)(A) of the ESA stipulates that listing decisions be made using the best available scientific and commercial information, therefore we used information from the 2007 status review report (which incorporated information from the 2003 workshop) and new information in forming our determination. Our responses to comments from the public further detail our use of information available at the time of the proposed listing rule, as well as our consideration of new information submitted during the public comment period.

Comment 4 (viability of small Atlantic sturgeon populations):

The estimated 343 spawning adult Atlantic sturgeon in the Altamaha River exceeds the number of spawning adults in the “very viable” Yellow River Gulf sturgeon population, according to peer reviewer 1. Peer reviewer 1 stated that information presented in Schueller and Peterson (2010) suggests a very robust reproductive response to protection of adult spawners under the Atlantic sturgeon moratorium. From these data, the reviewer stated that it seems highly improbable that the Altamaha River population is at risk of extinction and a listing of endangered does not seem applicable to the Altamaha population within the South Atlantic DPS. The reviewer stated that if the Altamaha population follows the model of the Suwannee River Gulf sturgeon population after harvest was banned, then overall population growth in the next decade will be exponential until density-dependent population controls come into play. Peer reviewer 1 also stated that the “less than 300 spawning adults” criterion in the proposed listing rule for classifying a river population as vulnerable to extinction sets a “very high, probably unrealistic, bar,” and one not conforming to scientific literature documenting sturgeon population recovery from much smaller effective breeding population sizes (20-80 spawning females, based on examples provided by the reviewer). Peer reviewer 1 stated that sturgeon species have the documented ability to establish/re-establish viable populations over a short timeframe (10 to 20 years), starting from “a few tens” of spawning adults without negative fitness impacts from low genetic diversity.

Response:

As explained above, NMFS does not agree with peer reviewer 1's premise that an endangered listing would only be appropriate if no single historical spawning river within that DPS appeared to sustain both a relatively abundant and simultaneously regularly-reproducing Atlantic sturgeon population. We note that the Yellow River population of Gulf sturgeon referred to as “very viable” by the reviewer is listed as threatened under the ESA. While the number of spawning adult Atlantic sturgeon in the Altamaha River may be larger than that of Gulf sturgeon in the Yellow River, the peer reviewer noted that the Yellow River population is one that has rebounded since it was listed. The Altamaha River population of Atlantic sturgeon is estimated to be at only 6 percent of its historical abundance. While there is a moratorium on harvest and possession of Atlantic sturgeon, the species is not currently afforded the protections of section 9 of the ESA, nor do they benefit from the consultation and permitting responsibilities of ESA sections 7 and 10, that apply to the listed Gulf sturgeon. Information provided by peer reviewers 1 and 2 indicated recent (2009-2010) increases in the estimated number of juveniles in the Altamaha River. We are encouraged by this and hope that the Altamaha River population does exhibit exponential growth, as the Suwannee River Gulf sturgeon population did following listing. However, our listing determination is based on the best information currently available to us, and we do not feel that the information provided on increases in juvenile Atlantic sturgeon in the Altamaha River or the comparison to Gulf sturgeon populations in the Suwannee and Yellow Rivers provides a basis for revising our proposed determination that the South Atlantic DPS be listed as endangered.

In response to the reviewer's comment that the “less than 300 spawning adults criterion” sets a “very high, probably unrealistic, bar”, we clarify that the 300 spawning adults per year was an estimate of the relative sizes of Atlantic sturgeon river spawning populations, based on the available information on the annual spawning adult abundance measured in the Altamaha River (343 spawning adults) and the fact that it is the largest population in the Southeast, combined with qualitative and quantitative anecdotal information from the other river systems. The 300 spawning adults per year estimate does not constitute a criterion or a bar for listing and/or recovery as a general matter. Rather, the estimate is evaluated in the specific context of the Atlantic sturgeon river populations and the impacts and threats they face. These populations likely have the capacity to recover, as the reviewer suggested, if existing and future impacts and threats are alleviated. The low estimated population numbers in each of the river systems within the DPSs (1-6 percent of historical abundance), combined with the ongoing impacts and threats from habitat modification and bycatch, indicate that the populations are small and vulnerable, and the DPSs they comprise are in danger of extinction.

Comment 5 (sturgeon ability to recolonize systems; genetic exchange):

Peer reviewer 1 stated that sturgeon species are resilient and capable of repopulating an extirpated river, or colonizing a new river, if habitat remains available, dams do not block spawning ground access, water quality is satisfactory, and a competing sturgeon population is not already established. A natal river population, well-established over a long span of geological time and highly adapted to its respective natal river, would not realize success in colonizing another river already populated by a second population better adapted to its respective natal river than a potential colonist. The reviewer stated that the low rate of genetic exchange displayed among adjacent sturgeon populations does not reflect the incapacity of the species to colonize, but the competitive advantage held by a pre-established natal river population facing migrant individuals. The reviewer provided examples of recolonization by Atlantic sturgeon in bays and rivers from New England to Labrador and Newfoundland within a span of 10,000 years following deglaciation. The

reviewer stated the northernmost and most genetically conservative Atlantic sturgeon population re-colonized over 1,500 miles of coastline within 40 generations (and probably much fewer) in addition to undertaking a successful, essentially instantaneous, 3,300 mile migration to colonize the Baltic Sea 1,200 years ago. The reviewer also provided an example of Gulf sturgeon rebounding in Gulf Coast river systems. Peer reviewer 1 stated that following state harvest prohibitions on the Gulf sturgeon and its listing as threatened under the ESA, some river populations have rebounded (the Yellow, Choctawhatchee, and Suwannee river populations). The reviewer concluded the logic in the proposed listing rule is not compelling that if one of the DPSs were to be completely extirpated, it would remain so over a long span of time. Peer reviewer 3 stated, in reference to the genetic analyses showing fewer than two individuals per generation spawn outside their natal rivers, that this reflects the average number of individuals and noted it would be useful to compare this to straying determined from tagging data.

Response:

We agree with the peer reviewer's comment that the low rate of genetic exchange displayed between Atlantic sturgeon river populations may reflect the competitive advantage held by pre-established natal river populations facing migrant individuals. We revised the relevant discussion in the text from the proposed listing rule to include this information. However, as stated in the proposed listing rule, we do not expect Atlantic sturgeon that originate from other river systems to recolonize extirpated systems and establish new spawning populations, except perhaps over a long time frame (

i.e.,

many Atlantic sturgeon generations). Though the reviewer provided an example of Atlantic sturgeon colonizing the Baltic Sea 1,200 years ago after a single migration, other examples of recolonization provided took 40 generations (approximately 1,000 years, based on a 25-year generation period) to 10,000 years, which is consistent with our statement in the proposed listing rule. Further, recolonization occurred in the absence of present-day human impacts, such as habitat modifications and mechanized fishing.

We noted the reviewer's comment that sturgeon species are resilient and capable of repopulating an extirpated river or colonizing a new river if habitat remains available, dams do not block spawning ground access, and water quality is satisfactory. As discussed extensively in the proposed listing rule and in our responses to comments in this document, Atlantic sturgeon in the Carolina and South Atlantic DPSs and the rivers within their ranges are affected by habitat modification and destruction, blocked access to spawning grounds, downstream habitat impacts caused by dams, and water quality (and quantity) issues. Thus, the commenter's stated conditions for expecting recolonization by Atlantic sturgeon are not met. Atlantic sturgeon from the Carolina and South Atlantic DPSs are also taken as bycatch in fisheries. Regarding the statement that following state harvest prohibitions on the Gulf sturgeon and its listing as threatened under the ESA, some river populations have rebounded (the Yellow, Choctawhatchee, and Suwannee river populations), the rivers that have rebounded have two factors in common versus those which have not rebounded (

e.g.,

the Apalachicola, Pascagoula, and Pearl river populations): (1) No mainstem dam on the natal river limiting Gulf sturgeon access to upriver spawning grounds or YOY access to riverine feeding habitat; and, (2) no major commercial fishery causing Gulf sturgeon bycatch mortality in the natal river, natal river estuary, or adjacent marine waters. Assessing the impacts of these two factors may be equally as important to sturgeon population recovery as is protection from all other impacts, now that direct harvest has been stopped. We agree with these comments by the peer reviewer and also believe that these threats associated with dams, habitat, water quality, and bycatch would hamper and slow recolonization of extirpated river systems. One reviewer acknowledged that rivers, watersheds, and coastal habitats inhabited by Atlantic sturgeon have been drastically modified and impacted by human activities (dammed, channelized, de-watered, diverted, dredged, mined, sedimented, polluted, deforested, developed, populated by introduced species,

etc.

) and that it would be remarkable to achieve recovery to even 10-30 percent of the 1890 carrying capacity of individual sturgeon rivers.

In reference to peer reviewer 3's suggestion about comparing the degree of straying from tagging studies to the estimate of straying from the genetic studies, we agree this could be a valuable exercise in the future when we have the necessary information on river of origin (based on genetic analyses) and the degree of straying (from tagging and relocation studies). While the estimate of less than 2 individuals spawning in rivers outside their natal system is a measure of successful transfer of genetic information from a fish originating from another system, the analysis suggested by the peer reviewer would provide us with knowledge of how many fish actually stray into another system and potentially attempt to spawn. This could also provide insight into the comments by the first peer reviewer that lack of gene flow between river populations is due to reduced success from competition and not from lack of attempts at migrant spawning.

Comment 6 (issues with estimating sturgeon abundance):

According to one peer reviewer, targeted Atlantic sturgeon population studies in the Roanoke River and Santee-Cooper system, as well as most other river systems, have been limited in duration, intensity, and continuity such that population estimates may be substantially underestimated. Peer reviewer 1 noted that sturgeon species are cryptic fish found in deep, mainstem rivers. They are rarely observed visually, not typically sampled in many commercial river fisheries targeting other fish species (with the exception of the shad gill net fishery), and are rarely caught by recreational anglers. The reviewer stated that this illustrates that presence and abundance of sturgeon cannot be based on incidental catches from commercial fisheries or scientific sampling not specifically targeting sturgeon. The reviewer stated that in the past, sturgeon abundance has often been vastly underestimated until an appropriate and dedicated reporting or sampling program was undertaken. The reviewer recommended that only continuous, standardized mark-recapture efforts spanning sufficient time (a minimum of 3 years, but realistically greater than 5 years) can provide reliable preliminary abundance estimates.

Response:

The majority of the data presented in the proposed listing rule came from studies targeting Atlantic sturgeon or from fisheries that are known to have a high incidence of interaction with Atlantic sturgeon (

i.e.,

gillnet fisheries). As much as possible, we clarified the data collection methods and constraints, and any assumptions we made. This is also discussed in our response to comment 2. We have used the best available commercial and scientific information to evaluate the status of the Carolina and South Atlantic DPSs, but we agree with the reviewer that long-term, continuous, standardized studies of Atlantic sturgeon abundance are needed.

Comment 7 (viable population sizes and sturgeon genetics):

Peer reviewer 1 stated the minimum viable population

sizes of several hundreds to several thousands of individuals advanced in the literature are not particularly instructive with respect to sturgeon species based on new genetic information (Kreiger

et al.,

2006). The reviewer commented that sturgeon are polyploid and the significance of polyploidy upon genetic diversity has just emerged. Most fishes are diploid with 40-50 chromosomes, a number similar to most vertebrates. However, all sturgeons are polyploid, having approximately 120 chromosomes (tetraploid, 4N), 240 chromosomes (octoploid, 8N) or more, including species with 12N or 16N ploidy. Polyploidy allows for multiple alleles (not just two as in diploid species) at a given gene locus, allowing for intra-individual genetic variation (Kreiger

et al.

2006). The reviewer suggested that this might explain the high degree of plasticity displayed by sturgeon populations and the documented ability of sturgeons to repopulate from very few spawning adults without apparent inbreeding depression. He concluded that until we gain a deeper understanding of the genetics of polyploidy and the implications regarding sturgeon population dynamics, any discussion of minimum viable population size for sturgeon populations cannot be phrased in terms of what we know about inbreeding depression in diploid mammal populations. Thus, the 50/500 rule of thumb cited in the proposed listing rule may be an inappropriate criterion by which to assess viability of sturgeon populations, and we do not know how few polyploid sturgeons are too few to sustain a viable population.

Response:

We appreciate the peer reviewer's input on the polyploid nature of Atlantic sturgeon and how this genetic characteristic may affect our evaluation of minimum viable population sizes in our listing determination. We revised the relevant discussion in the text from the proposed listing rule to include this information. As noted by the reviewer, we need a deeper understanding of the genetics of polyploidy and the implications regarding sturgeon population dynamics. We are not sure how polyploidy in Atlantic sturgeon will affect their recovery, but even if it allows the species to repopulate from relatively fewer individuals without inbreeding depression, there is no assurance that this will occur. Other polyploid Acipenser species have required listing under the ESA, such as shortnose sturgeon (listed as endangered in 1967), Gulf sturgeon (listed as threatened in 1991), and green sturgeon (listed as threatened in 2006). In the case of the shortnose sturgeon, recovery has not been achieved even though it has been protected for almost 45 years. Further, the polyploid nature of Atlantic sturgeon may further support the need for protection under the ESA. Southern populations of Atlantic sturgeon exhibit high diversity and many low frequency (and sometimes private) haplotypes (Grunwald

et al.,

2008). Allendorf and Leary (1988) noted that in polyploid cutthroat trout, alleles constituting the majority of the variation in the species are found in only one or two local populations, but they often occur at high frequencies in those populations. They concluded preserving the genetic variation in cutthroat trout entails preserving as many local populations as possible. Finally, a polyploid nature may not be sufficient to promote recovery in Atlantic sturgeon populations, even if it is indicative of smaller viable population sizes, given the nature and number of ongoing impacts and threats to sturgeon and their habitats.

Comment 8 (ACE Basin populations):

Peer reviewer 1 commented that the statement in the proposed listing rule that “the low population numbers of every river population in the Carolina and South Atlantic DPSs put them in danger of extinction throughout their ranges; none of the populations are large or stable enough to provide with any level of certainty for continued existence of Atlantic sturgeon in this part of its range,” seems contrary to the data from recent Atlantic sturgeon sampling results for the Altamaha, Savannah, and ACE Basin. This reviewer asserts that collection of 3,000 juvenile Atlantic sturgeon from the ACE Basin in seven years of sampling is not a low number.

Response:

The proposed listing rule stated that 3,000 juvenile Atlantic sturgeon were collected in the ACE Basin (consisting of the Ashepoo, Combahee, and Edisto Rivers) between 1994 and 2001. While the reviewer did not believe this is a low number, we disagree. The ACE Basin and every system in the South Atlantic DPS, with the exception of the Altamaha River, is estimated to be at 1 percent of its historical abundance and to have less than 300 adult Atlantic sturgeon spawning per year (the Altamaha is estimated to be at 6 percent of its historical abundance and have 343 spawning adults per year). However, the statement from the proposed listing rule referred to by the peer reviewer was not referring strictly to population size, but rather to the restrictive effects of low population numbers in all component river populations on the DPSs' ability to respond to threats. This statement was taken from a section of the proposed listing rule addressing viable population size, and the statement was meant to be taken in the context of the statements that preceded it: “The concept of a viable population able to adapt to changing environmental conditions is critical to Atlantic sturgeon, and the low population numbers of every river population in the Carolina and South Atlantic DPSs put them in danger of extinction throughout their ranges.” Low population numbers hamper recovery by making the populations less resilient to the dangers they continue to face from being taken as bycatch and from the loss, reduction, and degradation of habitat resulting from dams, dredging, and changes in water quality parameters (such as depth, temperature, velocity, and dissolved oxygen). Because these DPSs are groups of populations, the stability, viability, and persistence of individual populations affects the persistence and viability of the larger DPS. In the example of the ACE Basin, the capture of 3,000 juvenile Atlantic sturgeon between 1994 and 2001 (an average of 375 Atlantic sturgeon juveniles per year) alone is not sufficient to indicate that the DPS can persist, given the low population numbers in each of the river systems in the DPS and the existing threats to the species (

e.g.,

bycatch, habitat degradation), some of which may worsen as a result of water allocation issues and climate change.

Comment 9 (relevance of historical abundance estimates):

Peer reviewer 1 commented on the statements in the proposed listing rule that the Carolina DPS is estimated to number less than 3 percent of its historical population size; the Altamaha River is suspected to be less than 6 percent of its historical abundance; and the abundances of the remaining river populations within the South Atlantic DPS are estimated to be less than 1 percent of what they were historically. This describes the depleted status of these populations, and provides a reference point from which to gauge re-population. Peer reviewer 1 commented that caution should be exercised in using 1890s fisheries abundance as the recovery target, and similarly as a metric against which population recovery can be measured. Rivers, watersheds, and coastal habitats inhabited by Atlantic sturgeon have been drastically modified and impacted by human activities (dammed, channelized, de-watered, diverted, dredged, mined, sedimented, polluted,

deforested, developed, populated by introduced species,

etc.

) and it would be remarkable to achieve recovery to even 10-30 percent of the 1890 carrying capacity of individual sturgeon rivers. The reviewer believed the remaining 1-6 percent of the historical population numbers represents a good foundation for population recovery at the beginning of an unprecedented era of harvest prohibition, habitat restoration, and conservation awareness.

Response:

The discussion in the proposed listing rule of current population size relative to historical levels was not meant to imply those levels would be recovery targets. Relative population size was intended as a metric of the depth of the DPS' decline over time. The reviewer's observation that permanent habitat modifications have reduced potential population levels by 70-90 percent underscores the significance of the multiple habitat threats facing Atlantic sturgeon.

Comment 10:

Peer reviewer 1 took issue with the statement in the proposed listing rule that “recovery of depleted populations is an inherently slow process for a late-maturing species such as Atlantic sturgeon.” This reviewer stated this thesis is fundamentally faulty for sturgeon and other species. Late maturity in a species has little to do with speed of population increase beyond the initial lag period of one generation span or less, after which reproduction is continuous. As per the theory of Malthus, the reviewer stated that any population of any species in nature, whether of mice or elephants, will increase geometrically, as long as resources are not limiting. For a sturgeon population depleted by overfishing, once subadults are permitted to mature and spawn without being harvested first, recovery can be quite rapid if other human impacts have not removed or severely restricted essential resources.

Response:

We have considered the peer reviewer's comment. However, we continue to find that the Atlantic sturgeon's life history traits are hindering its recovery in several ways, as supported by scientific literature. For example, Meyers and Worm (2005) state, “from the land it is well known that large species with high ages at maturity are particularly vulnerable to extinction (Purvis

et al.,

2000). There is no reason to believe that this may be different in the ocean (Myers & Mertz, 1998; Hutchings, 2001; Dulvy and Reynolds, 2002; Dulvy

et al.,

2003).” Specifically regarding the Atlantic sturgeon, Balazik

et al.

(2010) state that “the Atlantic sturgeon's life history (high age of maturation and 2-5 years between female broods) probably inhibits population recovery (Boreman, 1997; Smith and Clugston, 1997).” Gardmark

et al.

(2003) states that “small populations are sensitive to stochastic effects, especially so if not all mature individuals reproduce,” and as noted in the proposed listing rule (as well as Balazik

et al.,

2010, above), adult Atlantic sturgeon do not reproduce every year.

There are several ways the Atlantic sturgeon's life history traits may be hampering recovery. The species' late age at maturity provides more opportunities for individuals to be removed from the population before reproducing. The limited ability of small populations with non-annual spawning adults to respond to stochastic effects could greatly affect Atlantic sturgeon recovery, and human population increases and climate change are likely to exacerbate existing water quality and quantity problems. Based on their life history, Atlantic sturgeon populations are more sensitive to fishing (bycatch) mortality than other coastal fish species. Like other K-selected species (which have large body size, long

life expectancy

, and produce fewer offspring, versus r-selected species, which are characterized as having high fecundity, small body size, early maturity onset, short generation time, and the ability to disperse offspring widely), Atlantic sturgeon are long-lived, have an older age at maturity, and have lower maximum fecundity values, with 50 percent of the lifetime egg production for Atlantic sturgeon occurring later in life (Boreman, 1997). That species with K-selected life history traits, such as Atlantic sturgeon, exhibit greater sensitivity to bycatch mortality is also supported by Baskett

et al.

(2006): “fisheries have a greater long-term negative impact on species with lower population growth rates, later maturation, larger organism size, and greater longevity than on species with faster production (Jennings

et al.,

1998; Heino and Godø, 2002).”

We agree with the peer reviewer's comments that any species with discrete generations or distinct breeding seasons will increase geometrically, “as long as resources are not limiting.” We also agree that Atlantic sturgeon can recover if fisheries mortality is reduced, allowing sub-adults to recruit to the spawning population, and “if other human impacts have not removed or severely restricted essential resources.” We stated in the proposed listing rule that the species' “long life-span also allows multiple opportunities to contribute to future generations provided the appropriate spawning habitat and conditions are available.” However, we believe that even though prohibitions on direct harvest and possession of Atlantic sturgeon have been in place for years, their life history characteristics, small population sizes, and the continued threats associated with bycatch and habitat modification are hampering the recovery of Atlantic sturgeon.

Comment 11:

Peer reviewer 3 questioned why the use of samples from YOY and mature adult Atlantic sturgeon in the genetic analysis by Wirgin and King (2006) ensured that the samples came from fish originating in the sampled river system. The reviewer stated this implies that intermediate size fish stray more than adults. The reviewer also asked if the adults sampled were running ripe adults.

Response:

Whether all of the adults utilized in the study were running ripe (

i.e.,

were making a spawning run) is unclear. However, adults generally only enter freshwater to spawn and the vast majority of Atlantic sturgeon spawn in their natal river (with estimates of less than 2 individuals per generation spawning outside their natal system). Therefore, the use of genetic samples in this study from adults captured in the freshwater portion of a river would indicate that the fish originated from that river and had returned to spawn. Similarly, Atlantic sturgeon spend the first year of their life in their natal river. Therefore, using genetic samples from YOY in a river system ensures that the fish originated in that river. Subadult (fish older than 1 to 2 years old) Atlantic sturgeon, as well as non-spawning adults, are known to make extensive coastal migrations. Subadults may use multiple estuarine or riverine areas for refuge, foraging, and nursery habitat, while non-spawning adults make extensive marine migrations. These life stages were excluded from the study because the river of origin cannot be determined from the location the fish are captured.

Comment 12:

Peer reviewer 3 noted that 88 percent average accuracy in determining a sturgeon's natal river of origin was high and questioned whether the 94 percent average accuracy in assigning a sturgeon to one of the 5 DPSs was significantly better. The reviewer asked if the variance around the 88 and 94 percent figures is known. The proposed listing rule stated that the loss of either the Carolina or the South Atlantic DPS would constitute an important loss of genetic diversity for the Atlantic sturgeon. The reviewer commented that additional context on

the amount of genetic diversity within river populations, among river populations within a DPS, and between the 5 DPSs would better support that the loss of a DPS would represent a significant loss of diversity.

Response:

The overall accuracy in assigning an Atlantic sturgeon to its natal river ranged from 60 to 94.8 percent (60 to 91.7 percent for southeastern rivers), while the overall accuracy in identifying a sturgeon to one of the 5 DPSs ranged between 88.1 and 95.9 percent (91.7 to 95.9 percent for the two southeastern DPSs). The peer reviewer's point is well-taken that, while there is higher accuracy in identifying a sturgeon to its DPS because of clearer genetic differences between the DPSs, the accuracy in identifying a sturgeon to its natal river is also quite high. We also agree with the peer reviewer that the broader context of the amount of genetic diversity exhibited by Atlantic sturgeon, within a DPS as well as among DPSs, provides additional support for our conclusion that the loss of a DPS would constitute a significant loss of genetic diversity. The high accuracy (60 to 92 percent) in utilizing genetic differences to assign Atlantic sturgeon in the Southeast to their natal rivers indicates that there is a significant amount of genetic diversity among rivers within a DPS, as well as between the two Southeast DPSs. Grunwald

et al.

(2008) reports that southern Atlantic sturgeon river populations have high diversity and many low frequency (and sometimes private) haplotypes. The information from Grunwald

et al.

(2008) indicates that each river population within a DPS makes unique contributions to the genetic diversity of the DPS as a whole and lends greater support to our determination that the loss of a DPS represents a significant loss of genetic diversity.

Comment 13:

Peer reviewer 3 asked if the statement in the proposed listing rule that “with the exception of the Waccamaw River population, all river populations sampled within each population segment along the entire East Coast were geographically adjacent” was intended to mean that, with one exception, the genetic results are consistent with geography. In reference to the statement that the sample size from the Waccamaw River population was small (21 fish), the reviewer asked what the sample size was for the remaining river populations utilized in the genetic analysis.

Response:

The peer reviewer interpreted the statement in the proposed listing rule correctly. In reference to the genetic sample sizes for rivers other than the Waccamaw, they ranged from 35 to 115. However, it is also important to note that genetic samples used in the analysis for the other river populations were taken from YOY and adult Atlantic sturgeon only to ensure that the fish were spawned in the river they were captured in. The genetic samples from Atlantic sturgeon captured in the Waccamaw River, in addition to being small in number, were taken from only juvenile Atlantic sturgeon, as those were the only samples available. As stated previously, juveniles may utilize multiple systems for foraging and nursery habitat, therefore the fish captured in the Waccamaw River and used in the genetic analysis were not necessarily spawned in that system. We are revising information in this final rule to indicate that the genetic samples from the Waccamaw River all came from juvenile Atlantic sturgeon.

Public Comments

Comments on the Delineation of the DPSs

Comment 14:

Multiple comments were received either disagreeing with the listing of DPSs or disagreeing with the way populations were grouped into DPSs. One commenter stated that DPS is not a scientific term and that the DPS policy is arbitrary. The commenter also stated that the decision to list five DPSs results from the lack of NMFS' scientific ability to support the listing of the species as a whole. Several comments were received, some citing Grunwald

et al.

(2008), that all riverine populations of Atlantic sturgeon are genetically distinct. Another commenter stated that populations should either be evaluated on a drainage-specific basis or as a single unit south of Cape Hatteras because current DPS delineations combine high abundance rivers with rivers that have low abundance or unknown population status, are extirpated, or exist at the margins of the historical range. Comments were received that the entire Carolina DPS does not warrant listing as a unit and that only populations from river systems that would be afforded further protection by an ESA listing should be listed. Multiple commenters were concerned that incorrect delineation of DPSs could result in negative impacts to Atlantic sturgeon.

Response:

The ESA, as amended in 1978, included in the definition of “species” “any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature.” On February 7, 1996, the USFWS and NMFS adopted a joint policy (61 FR 4722) regarding the recognition of distinct population segments (DPSs) under the ESA. We agree with the commenter that this is not a scientific term, which is acknowledged in the policy itself: “the authority to list a ‘species' as endangered or threatened is thus not restricted to species recognized in formal taxonomic terms, but extends to subspecies, and for vertebrate taxa, to distinct population segments (DPSs)” and “the term is not commonly used in scientific discourse, although ‘population' is an important term in a variety of contexts.” The DPS policy is not arbitrary, and has been upheld by numerous courts as a rational and permissible interpretation of the statute by the Services. The policy formalizes the criteria that must be met in order to consider a subset of a species a DPS, and those criteria are based on scientific principles. The Services determined that the listing, delisting, and reclassification of DPSs of vertebrate species would consider the discreteness and significance of the population segment in relation to the remainder of the species to which it belongs.

We did not delineate the DPSs based on population abundance information and lumping high and low abundance rivers. We do not agree that the best available scientific information supports listing other population segments in the Southeast, such as on a drainage-specific basis or as a single DPS south of Cape Hatteras. In accordance with the DPS policy, we determined that two DPSs of Atlantic sturgeon exist in the Southeast based on genetic information that indicates the DPSs as delineated constitute cohesive ecological and evolutionary units, on each DPS' persistence in unique ecological settings, and on the conclusion that the loss of either population segment would result in a significant gap in the range of the species as a whole. In the proposed rule, we stated that Atlantic sturgeon studies consistently demonstrated the species to be genetically diverse and that between seven and ten Atlantic sturgeon population groupings can be statistically differentiated range-wide (

e.g.,

King

et al.,

2001; Waldman

et al.,

2002; Wirgin

et al.,

2002; Wirgin

et al.,

2005; Grunwald

et al.,

2008).

Given a number of key differences among the studies (

e.g.,

the analytical and/or statistical methods used, the number of rivers sampled, and whether samples from subadults were included), it is not unexpected that each reached a somewhat different conclusion. In the proposed listing rule, we specifically evaluated and discussed the information

presented by Grunwald

et al.

(2008) and concluded that, though they used additional samples, some from fish in the size range (less than 130 cm) excluded in the analysis we relied on because they were smaller than fish considered to be mature adults, the results of the genetic analyses in Grunwald

et al.

(2008) and in the proposed listing were qualitatively the same and did not invalidate our DPS structure. We agree that Atlantic sturgeon from different riverine spawning populations can be distinguished genetically. However, genetic distances and statistical analyses (bootstrap values and assignment test values) used to investigate significant relationships among, and differences between, Atlantic sturgeon river populations, formed the basis of our judgment that the DPSs as proposed constitute cohesive ecological and evolutionary units that are appropriate for listing under the ESA and the DPS policy. In our judgment, the groupings of river populations into the DPSs as proposed, incorporates likely patterns of Atlantic sturgeon dispersal between drainages.

We believe all river populations within the DPSs will be afforded greater protection by an ESA listing, and listing the DPSs as proposed will not result in negative impacts to Atlantic sturgeon. Any action funded, authorized, or undertaken by a Federal agency that may affect Atlantic sturgeon from either DPS would require consultation with NMFS under section 7 of the ESA. Those analyses will focus initially on the impact of an action on the spawning population(s) to which affected sturgeon belong and then consider the significance of those impacts to the DPS(s).

Comment 15:

Several commenters said use of the genetic data that are available for the designation of DPSs may be unreliable due to limited sample sizes, spatial, temporal, and ontogenetic differences in collection, and lack of samples from all river systems. Commenters also said our review of the literature was based on techniques used rather than the samples used to derive the conclusions. A commenter stated (citing Grunwald

et al.,

2008) that genetic analyses should have been restricted to samples from spawning adults. The commenter cited several studies (Grunwald

et al.,

2008; Wirgin and King, 2006; Wirgin

et al.,

2005; Wirgin

et al.,

2000) as indicating that the north-to-south clustering of Atlantic sturgeon river populations into DPSs is not valid. The commenter believed NMFS relied on genetic studies to say that there are genetic differences among populations but then ignored the actual results of the studies. The commenter stated that the Wirgin and King data were not peer reviewed and should be given less consideration. The commenter also stated that genetic information needs to be integrated with ecological and behavioral data in order to draw appropriate conclusions. Commenters stated that more data are needed to list DPSs and that although the peer reviewed studies have described a high degree of genetic separation with good classification success, there are problems when the papers are reviewed and considered for management. Several commenters noted that genetic samples for adult sturgeon will be collected in upcoming years through federally funded projects along the Atlantic Coast.

Response:

We agree with commenters that sample sizes, spatial, temporal, and ontogenetic differences in collection, and lack of samples from all river systems create uncertainty in the Atlantic sturgeon genetic data. However, in our judgment the available data show genetic separation of the Carolina and South Atlantic DPSs from northern populations and from each other. Results showed 92 and 96 percent accuracy in correctly classifying a sturgeon from four sampled river populations (the Albemarle Sound, Savannah, Ogeechee, and Altamaha River populations) to two groupings of river populations (Albemarle Sound and Savannah/Ogeechee/Altamaha Rivers). Contrary to the commenters' assertion, in reviewing the literature and evaluating the available genetics data in our consideration of DPSs we looked at both technique and the samples used. As stated in Grunwald

et al.

(2008), due to the potential for subadult and adult Atlantic sturgeon to undertake extensive migration between systems, specimens certain to be spawned within a system (and candidates for use in genetic studies of spawning populations) include spawning adults or juveniles less than two-years-of-age. When possible, the genetic analyses we relied on in the 2007 status review report and in the proposed listing rule limited the samples utilized to those collected from spawning adults and YOY, which is consistent with (and more restrictive than) what Grunwald

et al

(2008) described. Where genetic samples from adult and YOY were missing, we reported the results of other analyses utilizing juvenile Atlantic sturgeon and clarified this in the proposed listing rule.

The commenter presented a comparison of river groupings (UPGMA trees) derived from genetic cluster analyses from the cited studies and asserted that the various groupings conflicted with the DPS structure proposed in the listing, stating that a north-to-south clustering of river populations is not valid. However, there is no difference in the river groupings resulting from the genetic analyses presented in Grunwald

et al.

(2008; Figure 3) and the river groupings resulting from genetic analyses presented in the 2007 status review report (Wirgin and King, 2006; Figure 16) for the southern populations. The river groupings presented in Wirgin

et al.

(2000) differ from our results, likely due to the inclusion of samples from subadults which may have originated from a system other than where they were collected. Wirgin

et al.

(2000) did find a pronounced latitudinal cline in the number of composite mtDNA haplotypes and in haplotypic diversity, which increased from north to south. The researchers ascribed the greater genetic diversity within and among southern populations to the persistence of these populations through the Pleistocene and to the faster mutation rates associated with their shorter generation times. The genetic results referred to by the commenter in Wirgin

et al.

(2005) were for shortnose sturgeon, not Atlantic sturgeon.

While the genetic analysis by Wirgin and King presented in the 2007 status review report was not previously published, it was peer reviewed as part of the status review and as part of the proposed rule. The status review report was peer reviewed by six experts from academia, and the proposed listing rule was peer reviewed by three experts, two from academia (including an Atlantic sturgeon genetics expert) and one from a Federal resource agency.

We agree with the comment that genetic information needs to be integrated with ecological and behavioral data in order to draw appropriate conclusions. We relied on behavioral information (

i.e.,

the migratory nature of subadults and non-spawning adults) to determine the appropriate life stages (

i.e.,

YOY and spawning adults) to use for the genetic analysis. We also used behavioral and ecological information in conducting our DPS analysis per the Services' joint DPS policy. We considered the species' behavior in that the majority of Atlantic sturgeon return to their natal rivers to spawn. We also considered ecological issues, such as the fact that the DPSs persist in unique ecological settings and that the loss of a DPS would represent a significant gap in the range of the species.

Additional genetic analyses will improve our understanding of Atlantic sturgeon and their population structure, and we eagerly await the results of upcoming and ongoing genetic analyses, some of which we are funding through our Species Recovery Grant Program under section 6 of the ESA. However, we believe that the currently available data support the discreteness and significance of the Carolina and South Atlantic DPSs. Because we have integrated the genetic data with other sources of Atlantic sturgeon information, such as the behavioral and ecological information noted above, we do not believe listing DPSs will create management problems.

Comment 16:

One commenter disagreed that the DPSs persist in unique ecological settings, citing a study by the Institute for Ocean Conservation (2010) that Atlantic sturgeon tagged in the Hudson traveled from Nova Scotia to Georgia. The commenter also disagreed that the loss of a DPS would result in the loss of important genetic diversity, citing Quattro

et al.

(2002) that dispersal is sufficient to prevent deep divergence over long evolutionary scales and Peterson

et al.

(2008) that Atlantic sturgeon are resilient to genetic bottlenecks.

Response:

The proposed listing rule states multiple times that Atlantic sturgeon mix extensively in the marine environment, which is consistent with the citation provided by the commenter. However, we disagree with the commenter that the Carolina and South Atlantic DPSs do not persist in unique ecological settings. The vast majority of Atlantic sturgeon return to their natal river to spawn, and the spawning habitat of each DPS is found in a separate and distinct ecoregion as identified by The Nature Conservancy (TNC) based on the habitat, climate, geology, and physiographic differences for terrestrial and marine ecosystems throughout the range of the Atlantic sturgeon.. The unique ecological characteristics of the ecoregions the Carolina and South Atlantic DPSs originate from are described in detail in the proposed listing rule.

We disagree with the comment that the loss of a DPS would not result in the loss of important genetic diversity. Grunwald

et al.

(2008) note that, while northern populations of Atlantic sturgeon have low genetic diversity, southern populations exhibit high genetic diversity with many low frequency haplotypes. The loss of genetic diversity associated with the loss of either the Carolina or South Atlantic DPS would reduce the ability of Atlantic sturgeon as a subspecies to adapt to new selective pressures, such as climate change or shifts in available resources. We also disagree with the commenter's assertion that Peterson

et al.

(2008) supports a conclusion that Atlantic sturgeon populations are resilient to bottlenecks. Peterson

et al.

(2008) reported “pronounced cropping” of genetic diversity in the Altamaha River Atlantic sturgeon population. The researchers expressed surprise over this result “given the resiliency to genetic bottlenecks previously reported in other studies of remnant Atlantic and shortnose sturgeon populations (Quattro

et al.,

2002; Waldman

et al.,

2002).” Grunwald

et al.

(2008) also stated that “current populations from the Hudson River northward represent step-wise recolonizations with a bottlenecking effect.”

Comment 17:

One commenter stated that the proposed listing rule suggested the number of Atlantic sturgeon spawning in locations other than their natal rivers (“outmigrants”) is not dependent on population size. The commenter believed the rate of outmigration is much higher than stated and should be presented as a percentage, but that some level of mixing should be considered. Another commenter stated that recolonization of a basin would be slow regardless of whether adjacent populations are low or robust due to the low rate of outmigration and genetic transfer between basins. The commenter noted that there are greater distances between rivers within the Carolina DPS than between the Carolina and South Atlantic DPSs. This commenter stated that if outmigration is limited and most likely occurs between adjacent populations, this refutes the DPS structure.

Response:

The number of Atlantic sturgeon outmigrants (less than 2 per generation) included in the proposed listing rule was estimated from genetic analyses by the studies we cited. We did not relate outmigration of Atlantic sturgeon to population size in the proposed listing rule, and we do not have available data to present outmigration as a percentage of population size; however, we agree with the commenter that rates of outmigration may increase with increasing population size. We agree that recolonization of a system from adjacent populations would be slow, which is consistent with statements in the 2007 status review report (page 97) and in the proposed listing rule (page 61912). The distances separating rivers within and between the Carolina and South Atlantic DPSs do not account for the extremely low level of outmigration in Atlantic sturgeon spawning populations. Adult (and subadult) Atlantic sturgeon are known to make extensive movements between systems along the East Coast range of the species. Though the exact cues are not known, it is a life history characteristic of Atlantic sturgeon that the vast majority spawn in their natal river system. The low level of outmigration does not refute the DPS structure; as we stated above, the groupings of river populations into the DPSs as proposed, incorporates patterns of Atlantic sturgeon dispersal among drainages. The evidence supporting the structure of the Carolina and South Atlantic DPSs is presented in the proposed listing rule and in our responses to comments 14-16 above.

Comment 18:

Several commenters stated that there were no specific geographic boundaries or coordinates listed to delineate the five DPSs and believed this should be addressed in the final rule, since conservation and other management measures will likely be implemented based on the delineation of the DPSs. The commenters also had concerns that the rivers and tributaries listed in each DPS are not all-inclusive and could potentially create loopholes for management and conservation measures. Another commenter stated that the extensive mixing of Atlantic sturgeon in the marine environment will make conservation and management of the DPSs difficult to impossible.

Response:

We do not believe additional geographic boundaries or coordinates delineating the DPSs are necessary or that there are any loopholes for management or conservation. As stated in the proposed rule text, each of the DPSs is defined to include fish that spawn in the range of watersheds encompassed by the DPS. Our intent was that all fish spawned in such watersheds would also be included in the listing throughout their life cycles. Thus, fish spawned in one river, but using an adjacent river as nursery or subadult feeding habitat, are included in the listing. We have refined the text descriptions of the Carolina and South Atlantic DPSs in the final listing rule to more clearly reflect this issue. The modifications to the text clarify the riverine ranges of the DPSs but do not change the populations making up each of the Southeast DPSs.

As noted by commenters, Atlantic sturgeon from each riverine watershed and DPS may be found in multiple riverine, estuarine, and marine environments at various life stages. We agree that the extensive mixing of Atlantic sturgeon will make conservation and management of the

DPSs challenging. As we stated in the proposed listing rule, this extensive mixing of Atlantic sturgeon in the marine environment, as well as in multiple riverine and estuarine systems, can expose Atlantic sturgeon of a given DPS to a variety of threats at various life stages and in multiple locations. We discuss management challenges and potential strategies for dealing with them in the sections of the proposed and final listing rules entitled “Identifying the DPS(s) Potentially Affected by an Action During Section 7 Consultation.”

Species Data and Information Supplied by Commenters

Comment 19:

Commenters from North and South Carolina state agencies and other commenters supplied data and information for the Carolina DPS. One comment stated that there was an observed increase in abundance of Atlantic sturgeon in Albemarle Sound between 2005 and 2008. The commenter also stated there was a slight increase in abundance of juveniles and subadults in Pamlico Sound, while river surveys showed a slight decrease in abundance. Commenters also included data from late 2010 indicating there is a fall spawning run in the Roanoke River. Based on anecdotal angler reports from North Carolina, some commenters asserted that Atlantic sturgeon are persisting, though there has been little improvement in the size and age distributions of the Carolina DPS relative to historical levels. They also noted sampling efforts directed toward sturgeon have been sparse and limit ability to accurately characterize existing populations. Comments from South Carolina noted that Atlantic sturgeon were captured in most nets set in Winyah Bay from April to July in 2007 to 2009, including sites far upriver, and that sonar sampling indicated several hundred Atlantic sturgeon at the confluence of the Sampit River and Winyah Bay in 2009. A commenter stated that fishery surveys conducted as a requirement of the Federal Energy Regulatory Commission (FERC) license for the Yadkin-Pee Dee Hydroelectric Project resulted in the capture of a running ripe male in the Pee Dee River in October of 2003, indicating spawning activity. Large fish believed to be Atlantic sturgeon were sighted during electrofishing from 2002 to 2003. The commenter stated that this and other research (Collins and Smith, 1997; Collins

et al.,

2003; Gibbons and Post, 2009) suggest that there may be a sizeable Atlantic sturgeon population present in the Pee Dee River and the Winyah Bay system. State agency comments noted that there have been few encounters with Atlantic sturgeon in the Santee River and there are anecdotal reports of breaching sturgeon in the Cooper River.

Response:

We reviewed the specific information supplied for Atlantic sturgeon from the Carolina DPS and have added it to the “Distribution and Abundance” section of the final listing rule; however, this information does not require a change in our listing determination. The Independent Gill Net Survey (IGNS) data supplied by the North Carolina Department of Environment and Natural Resources (NCDENR) does show an increase in CPUE between 2005 and 2008 in Albemarle Sound. Based on Table 1 and Figure 2 included in NCDENR's comments, the CPUE in 2005 was 0.012, and increased in each successive year until 2008, when it reached 0.031. However, the data supplied by NCDENR for Albemarle Sound dates back to 1990 and continues to 2009. The 1990-2009 CPUE data as a whole shows a great deal of fluctuation, with no increasing trend, but rather periodic increases and decreases. In 2009, the CPUE dropped back down to 0.015, the level recorded in 2006. While 2008 was the highest CPUE observed since 2002, the CPUEs recorded for 1990 (0.081), as well as for 2000 and 2001 (0.032 both years), were actually the highest recorded in the 1990-2009 dataset for Albemarle Sound provided by NCDENR. The lowest CPUE levels recorded in the 1990s (0.005 to 0.010 in 1992, 1993, 1995, and 1996) were observed again in 2002, 2003, and 2004 (0.005 to 0.007). The commenter stated that there has been an increase in juveniles and subadults in Pamlico Sound since 2001. Based on IGNS data provided by NCDENR (Table 4, Figure 8), the CPUE for Pamlico Sound was 0 in 2001, and greater than 0 for 2002 through 2009. While all CPUEs for Pamlico Sound are greater than that recorded in 2001, there is no apparent increasing trend in the data. While the highest CPUEs were observed between 2004 and 2007 (0.016 to 0.066), the highest being recorded in 2005, the CPUE has decreased since 2005. The level observed in 2009 (0.003), the lowest CPUE in this dataset, was also observed in 2002 and 2003. Similarly, the river surveys of the Pamlico, Pungo, and Neuse Rivers showed a peak CPUE in 2005, with very low numbers observed in the other years within the survey period of 2000 to 2009. The information provided by the commenter on spawning in the Roanoke River supports information included in the proposed listing rule. While the Roanoke was determined to be an active spawning river within the Carolina DPS in the proposed listing rule, information supporting that a fall spawning run occurs there will greatly aid in the conservation and management of the species. We agree with the commenters' statement that Atlantic sturgeon are persisting, though there has been little improvement in the size and age distributions of the Carolina DPS relative to historical levels. The failure of Atlantic sturgeon populations to rebound, even with the moratorium on harvest and possession and other efforts to recover the species, is the primary reason we are proposing to list the species as endangered. In 1901, the Atlantic sturgeon fishery collapsed when less than 10 percent of the U.S. 1890 peak landings were reported. The landings continued to decline coastwide, reaching about 5 percent of the peak in 1920. Coastwide landings remained between 1 and 5 percent of the 1890 peak levels until the Atlantic sturgeon fishery was closed by ASMFC in 1998. Atlantic sturgeon populations, estimated to be 1 to 6 percent of their historical levels, have remained relatively unchanged since the initial collapse caused by the Atlantic sturgeon fishery of the late 19th century. We agree that sampling efforts need to be increased to effectively characterize populations and we are making efforts to see that it happens.

The South Carolina Department of Natural Resources provided information (SCDNR) for Winyah Bay that Atlantic sturgeon were encountered in most nets set from April to July (2007 to 2009) and that a researcher using sonar observed several hundred Atlantic sturgeon in Winyah Bay near the confluence of the Sampit River in 2009. We contacted Dr. Hightower, the researcher conducting the sonar work in Winyah Bay, to get further information on his observations. Dr. Hightower provided additional information via email on July 7, 2011, that he and fellow researchers were conducting “pilot trials without a specific survey protocol, so we have not tried to generate density estimates. One of the issues that must be resolved before using the side-scan files in a quantitative way is to estimate the probability of identifying (detecting) a sturgeon, given that it is present in the area surveyed by the side-scan sonar. We are still working on that question, but results to date suggest that the detection probability depends on fish size, position in the water column, and possibly orientation relative to the sonar. Thus, we could come up with a density estimate for fish above some

size threshold, but we would not be able to reliably estimate how many of those were Atlantic sturgeon. Some of the large fish on those images are clearly Atlantic sturgeon and many others are likely to be sturgeon. The statement that several hundred were in that area is a reasonable description of what the side-scan data show but we are not at the point of being able to estimate the density with confidence.” Dr. Hightower also remarked that “we have done pilot survey work in the Roanoke, Neuse, Cape Fear, and Pee Dee river systems. The side-scan images from the Pee Dee (Winyah Bay) suggest markedly higher densities than in the other rivers.” If all fish detected by Dr. Hightower were Atlantic sturgeon, the possibility that there were hundreds in Winyah Bay does not conflict with our estimate of less than 300 spawning adults per year in each spawning river. The sonar study was conducted in August 2009. Due to the time of year and location, it is unlikely this was a spawning aggregation and there is no way of knowing what age classes were present. It is possible that some of these fish were juvenile Atlantic sturgeon, which are known to utilize multiple riverine and estuarine systems other than their natal system. The information provided regarding the surveys conducted on the Yadkin-Pee Dee as a requirement of a FERC license is not new information, as it was included in the proposed listing rule. The information on the Santee-Cooper system is noted, and it is consistent with the proposed listing rule. The information for Atlantic sturgeon in the Carolina DPS presented by commenters, when considered as part of our listing determination, does not change our determination that the Carolina DPS warrants listing as endangered. In our judgment, none of the river populations in the DPS are large or stable enough to provide with any level of certainty for the continued existence of the DPS in the face of threats currently acting on the species. In our judgment, the Carolina and South Atlantic DPSs require multiple stable spawning populations.

Comment 20:

Commenters from state agencies supplied data and information for the South Atlantic DPS. South Carolina Department of Natural Resources (SCDNR) supplied data from the Edisto, where 3,661 Atlantic sturgeon were captured between 1994 and the present; their population models estimate between 20,000 to 70,000 sturgeon. Between 1997 and 1999, SCDNR captured 118 adults in the Edisto River during spring and fall spawning runs, but netting ceased once that number was reached. They believed if they had continued netting activities, they would have captured more than 300 spawning adults. SCDNR also noted approximately 20 adults were captured in one to two months during surveys targeting other species. In 2010, four adults tagged in the 1990's as age 0+ were recaptured, which they believe indicates the moratorium is having the desired effect of allowing fish to recruit to the broodstock population. In the Savannah River, the SCDNR captured 369 Atlantic sturgeon between 1997 and 2010. SCDNR commented that there is not enough data to support the contention that the Altamaha has the largest population in the southeast and that other rivers have less than 300 spawning adults per year. The Georgia Department of Natural Resources (GADNR) commented that there is new information on the potential increase of Atlantic sturgeon in the Altamaha, and additionally, the Satilla River has been found to contain a substantial number of fish, where few to none were thought to exist in the past. Citing Peterson

et al.

(2008), GADNR stated the Altamaha may be recovering, though absence of adults older than age 17 suggests the effects of overfishing are still evident. According to Georgia's recent compliance reports to the ASMFC, the 2009 and 2010 estimates of age-1 Atlantic sturgeon in the Altamaha River were two and five times the estimates from the 2004-2008 period, respectively. In the most recent compliance report to ASMFC, University of Georgia (UGA) researchers collected more than 200 Atlantic sturgeon in the Satilla River in less than 2 years of sampling. They concluded that the presence of juvenile fish measuring less than 50 cm indicates this is likely a self-sustaining, spawning population.

Response:

We reviewed the specific information supplied by the states for Atlantic sturgeon from the South Atlantic DPS and have added it to the “Distribution and Abundance” section of the final listing rule. However, the additional information does not require a change in our listing determination. SCDNR stated that in the 16-year period since 1994, they captured 3,661 juvenile (one- to three-year-old) Atlantic sturgeon in the Edisto River. This updates information we included in the proposed listing rule that over 3,000 juvenile Atlantic sturgeon were collected in the ACE Basin between 1994 and 2001, including 1,331 YOY. SCDNR used Lincoln-Peterson and Schnabel models to derive Atlantic sturgeon population estimates from these data, which resulted in estimates of 70,000 and 20,000 Atlantic sturgeon in the Edisto River, respectively. SCDNR commented that the models' results suggest increasing trends in abundance. Both models rely on mark-recapture data and assume a closed population (there are no births, deaths, or immigration/emigration between the initial capture and the recapture period) and that all individuals have an equal chance of being captured (Nichols, 1992; Lindeman, 1990; Chao, 1987). We note that there is great uncertainty in the population estimates resulting from the two models, as evident in the great disparity between the two results (20,000 versus 70,000). The reliability of the population models used depends on the validity of the assumptions of those models. The primary assumption of these two models, that each individual has an equal probability of capture, is likely unattainable in natural populations (Chao, 1987; Carothers, 1973). The assumption of a closed population is probably violated for any estimate calculated using the Schnabel or Lincoln-Petersen method on data collected over several weeks or months, and it is surely violated when data from one or more active seasons are used (Lindeman, 1990). SCDNR indicated they are currently completing an open system model (which is based on survival probabilities, as well as capture probabilities) to better assess the Atlantic sturgeon population in the Edisto River. Because the closed system models used by SCDNR provide estimates of juvenile abundance only and do not account for other population dynamics (birth, mortality, immigration/emigration), the estimates provided by the models likely represent an overestimate of juvenile abundance, do not provide an estimate of how many juveniles likely mature into spawning adults, and do not provide any information that undermines our use of the estimate of less than 300 spawning adults per year in the system. Atlantic sturgeon do not reproduce every year; females reproduce on the order of once every 2 to 5 years, males every 1 to 5 years. Small numbers of fish spawning can reduce the likelihood of successful spawning and the amount of genetic variation introduced into the next generation.

SCDNR commented that we do not have enough data to support the belief that the Altamaha River has the largest spawning population in the Southeast and that all other rivers have less than that. However, we relied on the best available information in arriving at the

estimate, and the information supplied by commenters, including the data provided by SCDNR, actually supports the estimate. The Altamaha is believed to have the largest Atlantic sturgeon spawning population in the Southeast, based on the absence of dams impeding access to appropriate spawning habitat, the lack of heavy development in the watershed, and relatively good water quality. The information supplied by GADNR showed an increase in age-1 Atlantic sturgeon from the Altamaha River in 2009 and 2010 over 2004 to 2008 levels. This was also reported by peer reviewer 2 and discussed in our response to comment 2. The information provided for the Satilla River is consistent with information in the proposed listing rule that the Satilla River has a resident spawning population of Atlantic sturgeon. The information for Atlantic sturgeon in the South Atlantic DPS presented by commenters, when considered as part of our listing determination, does not change our determination that the South Atlantic DPS warrants listing as endangered. In our judgment all river populations in the DPS are too small to be stable and self-sustaining.

Comment 21:

In response to our request in the proposed listing rule for information on the mixing of Atlantic sturgeon populations, the petitioner cited Erickson

et al.

(2011) stating that out of 15 Atlantic sturgeon tagged in the Hudson River, one was relocated in Georgia, which supports extensive, long range mixing of sturgeon. The petitioner also cited Laney

et al.

(2007) that Atlantic sturgeon from the Hudson River represent approximately 44 percent of those in North Carolina overwintering habitat.

Response:

We appreciate the information provided by the petitioner. These studies support our assertion in the proposed listing rule that extensive mixing of the DPSs outside their natal rivers occurs during non-spawning phases. We are continuing to seek information on the degree of mixing of the different river populations, including through our funding of the project to determine seasonal and spawning migration patterns and incidences of inter-basin transfer for adult Atlantic (and shortnose) sturgeon in southeastern rivers in North Carolina, South Carolina, and Georgia.

Comments on Abundance and Trends

Comment 22:

Many comments were received stating that the abundance estimate of 300 spawning adults per year is not supported by data. Many of these comments stated that the proposed listing rule is not valid without stock assessments of Atlantic sturgeon populations. One commenter stated that the estimate of 300 spawning adults per year is misleading in regards to total population abundance since Atlantic sturgeon do not spawn every year and the total population abundance is likely much higher. Another commenter, citing Schueller and Peterson (2010), stated that we should consider juveniles rather than spawning adults. A comment was received that the statements on page 61920 of the proposed listing rule about spawning populations being less than the 500 recommended by Thompson (1991) conflict with the statement that total population abundances for the Carolina and South Atlantic DPSs are not available. Additionally, a comment was received that based on modeling, populations in the Winyah Bay system and the ACE Basin have more individuals than Thompson (1991) recommended as minimum viable population sizes for short-term and long-term population fitness.

Response:

In response to comments on lack of stock assessments being a bar to listing determinations, we note that section 4(b)(1)(A) of the ESA provides that the Secretary shall make required listing determinations solely on the basis of the best scientific and commercial data available to him at the time of the determination, after conducting a review of the status of the species and taking into account efforts to protect the species. Even if a formal stock assessment of the species has not been conducted, if the best available information indicates the species warrants listing, as it does for Atlantic sturgeon, then we are required to list the species. Lack of formal stock assessments is not an unusual circumstance for species that have drastically declined, are at very low population numbers, or whose ranges have constricted, such that they are the subject of petitions to list them as threatened or endangered. Though we do not have stock assessments, we believe the current body of information on the declines of Atlantic sturgeon, the failure of their population numbers to rebound despite harvest prohibitions, the small relative magnitude of riverine spawning populations, and the ongoing impacts and threats from bycatch and habitat modification, warrant listing the Carolina and South Atlantic DPSs as endangered.

In the Southeast, the Altamaha is the only river where abundance has been directly surveyed. While traditional stock assessments from other Southeast rivers in the species' U.S. range are not available, we nevertheless relied on the best available data to produce a relative estimate of the number of Atlantic sturgeon in the remaining spawning populations. Based on a comprehensive review of the available data, the literature, and information provided by local, state, and Federal fishery management personnel (both documented in the 2007 status review report and in comments received on this rule), it is our judgment that the Altamaha River has the largest Atlantic sturgeon spawning population in the Southeast. The larger size of this population relative to the other river populations in the Southeast is likely due to the absence of dams that impede access to appropriate spawning habitat, the lack of heavy development in the watershed, and relatively good water quality, as Atlantic sturgeon populations in the other rivers in the Southeast have been affected by one or more of these factors. Though abundance estimates from stock assessments are not available for the other river populations, because the Altamaha spawning population is the largest, we believe it is reliable to estimate the size of other spawning populations in the Southeast Region as no more than 300 adults spawning per year. Further, data supplied by managers and researchers (and discussed in the previous section of responses to comments), support an estimate of less than 300 spawning adults per year in the other Southeast rivers.

The use of annually spawning adults is not intended to be misleading. We agree with the commenter that total riverine population numbers of Atlantic sturgeon are higher than the number of annually spawning adults. However, the only quantitative abundance estimate available to us when the proposed rule published was the number of annually spawning adults in the Altamaha River, not total population numbers or the total number of juveniles, as suggested by another commenter citing Schueller and Peterson (2010).

Schueller and Peterson (2010) stated that quantified methods of assessing sturgeon recruitment are essential for evaluating population trends, but that early life stages of most sturgeon species are notoriously difficult to sample, and their study on the Altamaha River provides the first quantified recruitment data describing a juvenile Atlantic sturgeon population in a southern river. They conducted their research during the summers of 2004 to 2007 and estimated that juvenile abundance ranges from 1,072 to 2,033 individuals in the Altamaha River, with age-1 and age-2 individuals comprising greater

than 87 percent of the population. Based on modeling, estimated apparent survival and per capita recruitment indicate that the juvenile population experiences high annual turnover: Apparent survival rates are low (less than 33 percent), and per capita recruitment is high (0.82-1.38). However, the authors noted that their mark-recapture methods were not capable of providing separate estimates of annual survival and out-migration, yet these rates are critical in understanding recruitment processes for the species. They noted future studies are needed to obtain quantified recruitment data using alternative methods, such as biotelemetry and known-fates modeling approaches. Schueller and Peterson (2010) concluded that future studies of subadult and adult life stages are needed, but quantified assessment of river resident juveniles can provide fisheries managers with the data necessary for evaluating population trends.

The statement in the proposed listing rule that spawning populations are less than the 500 recommended by Thompson (1991) as a minimum viable population size for long-term population fitness does not conflict with the statement that total population abundances for the Carolina and South Atlantic DPSs are not available. As we stated in this response, we do not have direct estimates of total population numbers for any of the Southeast spawning populations. Based on data from Schueller and Peterson (2006), we were able to present an estimate of the number of annually spawning adults in the Altamaha River. Although survey/stock assessment data on total population numbers or annually spawning adults are not available for the remaining Southeast river populations, based on information that the Altamaha is the largest population in the Southeast and data from the remaining rivers, we estimate in comparison that the other spawning populations have no more than 300 spawning adults per year.

In response to the comment that based on observations and modeling, the Winyah Bay system and ACE Basin have more individuals than Thomas (1990) recommended as minimum viable population sizes for short-term and long-term population fitness, we note that Thomas (1990) offered a population size of 5,500 as “a useful goal,” but suggested that where uncertainty regarding a species' population dynamics, changing environmental conditions, and the species' reaction to the changing environmental conditions is extreme (as it is for Atlantic sturgeon) “we should usually aim for population sizes from several thousand to ten thousand.” Information provided for the Winyah Bay and ACE Basin does not provide an estimate of total population size in either system. Because annual spawning adults was the only quantitative population metric we had for any southern river population at the time of the proposed listing, we looked at estimated annual spawning adult population sizes in comparison to various viable population sizes suggested in the literature. We now have additional information on juvenile abundance in the Altamaha River and some preliminary modeling of juvenile abundance in the Edisto River; however, this information is lacking for most river systems, and the population trends are not certain from the data we have. Although the Carolina and South Atlantic DPSs, made up of multiple river populations of Atlantic sturgeon, were determined to be interbreeding population units, the vast majority of Atlantic sturgeon return to their natal rivers to spawn, with fewer than two migrants per generation spawning outside their natal system. We looked at the number and size of each riverine spawning population within each DPS when considering the effects of a small population size on the extinction risk for the DPS as a whole. We do not believe that information presented by the commenters provides a basis to revise our evaluation of the status of the Carolina and South Atlantic DPSs of Atlantic sturgeon.

Comment 23:

Several commenters stated that historical commercial landings do not accurately reflect abundance and are not a good indicator of status. One commenter stated that Secor (2002) should not be used as the basis for estimating historical abundances of Atlantic sturgeon. The commenter stated that due to the nearshore location of the fisheries in the latter part of the 19th century, the data would include Atlantic sturgeon from multiple populations and represent a gross overestimate of historical abundance. A comment was received that population modeling should have been used to analyze the trajectory of the species.

Response:

Section 4(b)(1)(A) of the ESA states that the Secretary shall make listing determinations solely on the basis of the best scientific and commercial data available. Historical abundance data is not available. However, we believe that the historical landings data and the sharp downward decline observed in landings throughout the 20th century are a valid indicator of the declines in abundance experienced by Atlantic sturgeon. Secor (2002) represents the best available data on the estimated historical abundances of Atlantic sturgeon, as does the U.S. Fish Commission data on historical landings, which the Secor (2002) publication was based on and which we reviewed ourselves for clarification in preparing the making our listing determinations. We agree that it is impossible to conclusively determine whether historical landings data potentially represents Atlantic sturgeon from multiple river systems and multiple DPSs. In the proposed listing rule, we reported historical abundances of Atlantic sturgeon from Secor (2002) as state-wide estimates of spawning females for North Carolina, South Carolina, and Georgia. Though not stated directly in the proposed listing rule, this infers that multiple river populations and DPSs are represented in these estimates, since each state contains multiple river systems, both of the DPSs in the Southeast encompass multiple states, and in the case of South Carolina, both DPSs include river populations originating in that state. Therefore, our use and presentation of the data in the proposed listing rule was appropriate and not inconsistent with the commenter's statement. Due to the lack of data (

e.g.,

abundance, recruitment, natural mortality, bycatch mortality) on Atlantic sturgeon throughout most of the species' range, reliable population modeling at the species/DPS level is not possible. However, as detailed in the proposed listing rule, we believe that the trajectory observed in the commercial landings from the late 19th century through the 20th century, combined with information from recent and ongoing surveys of Atlantic sturgeon populations and information on threats to the species from habitat modification (

e.g.,

dams, dredging, water quality and quantity) and bycatch clearly demonstrates that Atlantic sturgeon population abundances have shown little improvement since their initial declines and continue to face a degree of threat that warrants listing the Carolina and South Atlantic DPSs of Atlantic sturgeon as endangered.

Comment 24:

A commenter stated that the 1990-2003 increasing trend in Atlantic sturgeon abundance in the Cape Fear River should not have been discounted in the status review.

Response:

We did not discount information in the proposed listing rule on trends in Atlantic sturgeon abundance in the Cape Fear River between 1990 and 2003, as reported by Moser

et al.

(1998) and Williams and

Lankford (2003). We presented different interpretations of the data that the researchers noted themselves in their research publications. In the proposed listing rule, we stated “abundance of Atlantic sturgeon below Lock and Dam #1 in the Cape Fear River seemed to have increased dramatically during the 1990-1997 surveys (Moser

et al.,

1998), as the CPUE of Atlantic sturgeon was up to eight times greater during 1997 than in the earlier survey years. Since 1997, Atlantic sturgeon CPUE doubled between the years of 1997 and 2003 (Williams and Lankford, 2003). However, it is unknown whether this is an actual population increase reflecting the effects of North Carolina's ban on Atlantic sturgeon fishing that began in 1991, or whether the results were skewed by one outlier year. There was a large increase observed in 2002, though the estimates were similar among all other years of the 1997 to 2003 study.” The commenter stated that the 2007 status review report should not have discounted the increase in sturgeon abundance in 2002 as an outlier year for the reason that it was a flood year. Williams and Lankford (2003) stated that CPUE is used to indicate a population size, but if environmental conditions affect the susceptibility of fish to being captured in gillnets, then the data may show a change in population size when environmental conditions actually caused the change in CPUE. Williams and Lankford (2003) further stated that, “although previous years have documented relatively similar catch-per-unit-efforts, the summer of 2002 yielded twice the CPUE of any season since 1997. This also happens to be the lowest flow conditions experienced during this survey. Although catch-per-unit-effort increased greatly during these low flow conditions, previous years with low flow summers did not have the same resulting increases in CPUE. Future surveys should investigate river flow and other environmental conditions that may impact the Atlantic sturgeon's use of the Lower Cape Fear River.” The researchers acknowledged ambiguity in whether these results represent increases in Atlantic sturgeon abundance or whether environmental conditions affected CPUE. Therefore, the information we presented in the proposed listing rule on trends in the Cape Fear River is consistent with what the researchers presented. Further, even if the data in the Cape Fear River do represent an actual increase in Atlantic sturgeon, data provided by NCDENR during the public comment period on the proposed listing rule did not show increasing trends in Atlantic sturgeon populations in other North Carolina rivers.

Comment 25:

A commenter asked if the historical data on pounds of Atlantic sturgeon landed in South Carolina (page 61907 of the proposed listing rule) can be converted to CPUE.

Response:

The majority of the landings data for South Carolina referred to by the commenter cannot be converted into CPUE. However, the data were taken from Smith

et al.

(1984), which did provide CPUE for the time period 1973 to 1982, and provided anecdotal data about the level of fishing effort for earlier time periods. The objective of the research conducted by Smith

et al.

(1984) was to obtain baseline information on the Atlantic sturgeon fishery in South Carolina. At the time their research commenced, South Carolina accounted for 55 percent of the total U.S. landings of Atlantic sturgeon, but little information on the characteristics of the fishery was available. Figure 2 in Smith

et al.

(1984) shows license data for the Atlantic sturgeon fishery in South Carolina. From 1960 to 1982, the number of fishermen licensed for sturgeon remained relatively constant, averaging 21 individuals (ranging between 15 and 30) per year. Smith

et al.

(1984) noted that fishermen possessing certain other types of fishing licenses (

e.g.,

a shrimp fishing license) were permitted to fish for Atlantic sturgeon without having a specific sturgeon license. Based on field observations, they estimated that there were two to three times the number of recorded licensed sturgeon fishermen active in these fisheries. No data on the amount of gear fished were available for the period of most active exploitation of the fishery (pre 1910), but from 1925 to 1970, the number of licensed units of fishing gear was also relatively constant and averaged 17.8 (ranging between 11 and 26). This suggests that landings data are representative of relative abundance, since fishing pressure remained constant.

There was a dramatic increase in fishing effort in the 1970 to 1982 time period, with the number of licensed nets at record levels for the time. The number of licensed nets in 1970 was less than 30, but by 1982, it was around 140. Smith

et al.

(1984) calculated CPUE data for 1973 to 1982 based on reported total landings and number of net licenses, as well as field observations and verbal information provided by fisherman. They noted several limitations of the license and landings data for calculating CPUE: (1) Though individual gear were required to be licensed, the license was not based on type or length; (2) the license data included gear fished in the northern (Winyah Bay) and southern (Edisto, Coosawhatchie, and Combahee Rivers) fisheries, whereas the landings data only included fish from the northern fisheries; (3) field observations indicated that not all nets were licensed, nor landings reported; and, (4) pre-1973 data included landings of shortnose sturgeon in addition to Atlantic sturgeon. Figures 6 and 7 in Smith

et al.

(1984) show landings, effort, and CPUE. Landings rose from about 20,000 to 42,000 kilograms (kg) between 1973 and 1982, while the number of licensed nets increased from 36 to 133 during the same time period, resulting in a slight declining trend in CPUE (Figure 6). Observations of fishermen on the Winyah Bay jetties between 1978 and 1982 (Figure 7) also showed a decline in CPUE during the time period, with Atlantic sturgeon landings declining even with effort increasing. Smith

et al.

(1984) concluded that a definitive analysis of the fishery was not possible because of the limitations of the data, but they stated that “fishing effort has substantially increased without a concomitant increase in landings”, and though “the fate of this fishery in South Carolina is not clear, it appears likely that intensive fishing effort will adversely affect local populations of these long-lived fish.”

Comments on the 2007 Status Review, the 1998 Status Review, and Difference Between the Status Reviews and the Proposed Listing Rule

Comment 26:

Commenters disagreed with NMFS' proposal to list both of the DPSs in the Southeast as endangered, when the 2007 status review report concluded that the Carolina DPS should be listed as threatened and did not make a listing conclusion for the South Atlantic DPS due to lack of information to allow a full assessment of subpopulations within the DPS. Several of these commenters stated that there was no new scientific information presented justifying the proposed listing of the Carolina and South Atlantic DPSs differently from the conclusions reached in the 2007 status review report. Similar comments were received that no new data has been collected, and no changes in the level of threats have been documented, since the 1998 status review, which concluded that listing was not warranted at that time. One commenter said the proposed listing rule does not sufficiently explain why the conclusion in the 1998 status review report that the existing moratorium on fishing for Atlantic sturgeon and the

listing of the shortnose sturgeon was adequate to protect Atlantic sturgeon is no longer valid.

Response:

Regarding comments about divergence from the 2007 status review report's listing conclusions for the Carolina and South Atlantic DPSs, see our response to peer reviewer comment 1 above.

In 1998, NMFS and USFWS (Services) determined that an ESA listing of Atlantic sturgeon throughout its range was not warranted at that time (63 FR 50187, September 21, 1998). The Services cited eight reasons for the negative determination: (1) Evidence that the historical range of the species has not been substantially reduced and that its current range is not likely to be significantly reduced in the foreseeable future; (2) persistence of at least 14 spawning populations; (3) the expected efficacy of existing prohibitions on harvest and possession in all 15 states comprising the species' U.S. range; (4) detailed evaluation of current habitat conditions and threats to habitat showing that conditions are adequate to sustain the species and are likely to remain so in the foreseeable future; (5) lack of substantial information indicating that overutilization for commercial, recreational, scientific or educational purposes is currently significantly affecting the species; (6) lack of information indicating that disease or predation are causing significant losses of individuals of the species; (7) existing regulatory mechanisms which provide adequate protection and further the conservation of the species; and, (8) lack of information indicating that artificial propagation is currently posing a threat to the species.

Section 4(b)(1)(A) of the ESA requires that listing decisions be made using the best available scientific and commercial information at the time of the decision, after conducting a review of the status of the species and considering the conservation efforts of states and foreign nations.

Information provided in the 2007 status review report and the 2010 proposed listing rule explain why we no longer believe all of the eight conclusions in the 1998 status review report are valid, particularly as applied to DPSs of Atlantic sturgeon. Specifically: (1) Reductions in the historical range of Atlantic sturgeon have occurred, as evidenced by extirpations of several spawning populations in both Southeast DPSs and limited access to historical river reaches and habitats above dams (detailed in the “Distribution and Abundance” and “Conservation Status” sections of the proposed and final listing rules); (2) no spawning populations in the DPSs are large or stable enough to provide with any level of certainty for the continued existence of the DPS in the face of threats currently acting on the species; (3) existing prohibitions on harvest and possession of Atlantic sturgeon in all East Coast states do not alleviate other significant threats to Atlantic sturgeon (

i.e.,

bycatch and habitat destruction/modification, a point discussed in further detail in the discussion on those threats); (4) habitat destruction and modification (from dams, dredging, degraded water quality and quantity,

etc.

) is a significant threat to Atlantic sturgeon river populations and DPSs, as discussed below and in our responses to comments 39-45; (5) information on overutilization of Atlantic sturgeon as bycatch suggests that this is also a significant threat to Atlantic sturgeon populations, as discussed below and in our responses to comments 46 and 47; and, (7) existing regulatory mechanisms have proven inadequate at controlling the threats to Atlantic sturgeon from habitat modification/destruction and bycatch, as discussed in our responses to comments 49 and 50. Evidence for these conclusions and detailed responses to the comments received on these conclusions is presented in the following text.

Comments stated that no new data has been collected and no changes in the level of threats have been documented since the 1998 status review. However, studies not available at the time of the 1998 status review report on bycatch (discussed here) and habitat quality (discussed later in this section) have been reviewed by NMFS as part of our current listing determination. The 1998 status review report determined that estimated levels of mortality associated with bycatch on the Delaware and Hudson Rivers indicated that bycatch was not a significant threat to the species survival but could impede recovery, and recommended that efforts be made to better quantify data on bycatch levels, fishing effort, and river population levels to ensure that assumptions made using Hudson and Delaware River information are valid for other river populations. Since 1998, the ASMFC (2007) produced a bycatch report providing estimates of Atlantic sturgeon bycatch, as did Stein

et al.

(2004), a bycatch report used by the 2007 ASSRT. The reports documented mean bycatch mortality rates of 13.8 percent and 22 percent, respectively. However, the ASMFC (2007) report noted that the estimates of bycatch utilized in the analysis are likely to be underestimates of true bycatch and mortality levels, since they rely only on reported bycatch from the observer program (there is limited observer coverage in fisheries potentially capturing Atlantic sturgeon in Federal waters from North Carolina to Florida), and delayed mortality is not accounted for in their estimates. Further, the 1998 status review report did not consider the effects of bycatch and degraded habitat working in combination on greatly reduced Atlantic sturgeon populations, which are at 1 to 6 percent of historical levels.

In response to the comments that the proposed listing rule does not sufficiently explain why the conclusion in the 1998 status review report that the existing moratorium on fishing was adequate to protect Atlantic sturgeon is no longer valid, at the time of the 1998 determination, we note that the ASMFC moratorium on retention of Atlantic sturgeon had recently gone into effect. Because this eliminated directed fishing for Atlantic sturgeon (NMFS followed this with a 1999 closure of the EEZ to fishing for Atlantic sturgeon), which was considered the primary threat to the continued existence of the species at the time, the moratorium factored heavily in the Services' decision not to list the species at the time. However, since implementation of the moratorium, additional bycatch information (Stein

et al.,

2004; ASMFC, 2007) has become available and indicates that Atlantic sturgeon are vulnerable to bycatch in commercial fisheries, and that the current rate of bycatch is unsustainable in the long term (ASMFC, 2007). Further, the proposed listing rule described in detail why the existing moratorium on directed capture of Atlantic sturgeon has not eliminated the incidence of sturgeon bycatch in other fisheries and also does not address threats associated with the destruction and modification of their habitat. Comments were also received that the proposed listing rule does not sufficiently explain why the conclusion in the 1998 status review report that the listing of the shortnose sturgeon was adequate to protect Atlantic sturgeon is no longer valid. While Atlantic sturgeon have benefited from some of the protections afforded the endangered shortnose sturgeon due to their shared presence in some rivers, shortnose sturgeon do not coexist in all rivers within the Atlantic sturgeon's range and shortnose sturgeon do not use the coastal and marine environments used extensively by Atlantic sturgeon. Additionally, there is often spatial and temporal separation of riverine habitat

use by the Atlantic and shortnose sturgeon. Adults of both species use similar habitats for spawning in the riverine environment, but they are known to use them at slightly different times of the year. As stated in the 1998 recovery plan for the shortnose sturgeon, spawning begins in freshwater from late winter/early spring in southern rivers. The 2007 Atlantic sturgeon status review report stated that spawning adults generally migrate upriver in the spring/early summer (February to March in southern systems). Further, the 2007 Atlantic sturgeon status review report noted that other life stages of Atlantic and shortnose sturgeon may use different sections and/or different depths within the same river system. Therefore, the threats facing each species are not identical and protections for shortnose sturgeon cannot be expected to fully alleviate threats to Atlantic sturgeon.

Comment 27:

Several comments were received on differences in the 1998 and 2007 status reviews in the evaluations of the threat to Atlantic sturgeon from habitat modification. A commenter noted that the 1998 status review report denied the petitioner's claims that dam blockages, degraded water quality, and dredging significantly contributed to low Atlantic sturgeon abundances, but NMFS has not provided any evidence supporting a reversal of this conclusion. Another commenter specifically asked what changed between the 1998 and 2007 status reviews to warrant the “moderately high (4)” ranking of threats from dams on the Cape Fear River in the 2007 status review. The commenter also asked if the recommendations on page 91 of the 1998 status review report have been followed. The commenter requested we provide the baseline data on spawning and nursery habitat, including locations, depths, flows, substrates, carrying capacity or optimal population, that was recommended as “contributing to and accelerating the ongoing recovery or enhancement of Atlantic sturgeon” in the 1998 status review. Several commenters also cited the 1998 status review's statements that water quality has been improving since the 1970s, dredging activities are increasingly rare and have minimal effects on sturgeon, and successful shortnose restoration is indicative of future rebounding of Atlantic sturgeon stocks. One of the commenters referenced Table 9 in the 2007 Status Review, which shows a 2004 U.S. Environmental Protection Agency (USEPA) water quality grade in the Southeast as “B”, then questioned the extinction risk ratings in Table 13 of the 2007 Status Review, which rates water quality in most of the Southeast rivers as having a moderate risk of causing extinction.

Response:

In reaching our 1998 not warranted determination, we did not consider the loss of habitat due to dams to be a significant threat. Page 31 of the status review report states, “In the southern region of the U.S. Atlantic coast, the fall line is commonly much farther inland (322 river kilometers or rkm on the Savannah River, South Carolina-Georgia border) or almost nonexistent (St. Johns River, Florida). This potentially provided more freshwater (spawning) habitat than in many northern rivers. However, historical records of the amount of habitat actually used by Atlantic sturgeon are lacking. Thus, for most rivers, it is not possible to determine how much habitat was lost due to dam construction for southern rivers.” As stated above, the 1998 analysis included the amount of spawning habitat available to the species across its range. Since that time, we have determined the amount of habitat lost on each of the rivers due to dams (see Table 7 of the 2007 status review). We also have additional information on spawning locations for some rivers. The 1998 status review report cited the Savannah River as an example of a river with a fall line far inland and the 2007 status review report also stated that 92 percent of the habitat on the Savannah is unimpeded by dams. While both of these facts are true, the historical primary spawning habitat for Atlantic sturgeon (and only shoal habitat on the Savannah River), the Augusta Shoals, is not accessible to Atlantic sturgeon because it lies above the New Savannah Bluff Lock and Dam (Wrona

et al.,

2007; Marcy

et al.,

2005; Duncan

et al.,

2003; USFWS, 2003). Regarding the comment on the ranking for the Cape Fear River, the 1998 status review report did not have an estimate for how much spawning habitat was blocked by Lock and Dam #1. The 2007 status review report included the following information and provides insight into the “moderately high” ranking for the threat of dams on that river (page 51): “Historical spawning locations are unknown in the Cape Fear River; therefore, it is assumed that the fall line is the upper limit of spawning habitat. Using the fall line as guide, only 33 percent of the historical habitat is available to Atlantic sturgeon (96 km of 292 km). In some years, the salt water interface reaches the first lock and dam; therefore, spawning adults in the Cape Fear River either do not spawn in such years or spawn in the major tributaries of the Cape Fear River (

i.e.,

Black River or Northeast Cape Fear rivers) that are not obstructed by dams.”

Dredging activities are far from rare. NMFS routinely conducts section 7 consultations on listed species for dredging projects within the range of Atlantic sturgeon. Statistics on hopper dredging, the form of dredging most likely to take aquatic species (such as sea turtles and Atlantic sturgeon), can be found on the U.S. Army Corps of Engineers' (USACE) “Sea Turtle Data Warehouse” Web site (

http://el.erdc.usace.army.mil/seaturtles/index.cfm

). The Charleston, Jacksonville, Savannah, and Wilmington Districts have completed 307 hopper dredging projects, removing over 220 million cubic yards of material from federally maintained navigation channels in 307 projects since 1991. The number of private dredging projects permitted by USACE would increase that number considerably. Further, these numbers do not include other dredging methods (

e.g.,

cutterhead and mechanical) used by Federal and private entities that are less likely to directly interact with sturgeon species, but can modify and degrade sturgeon habitat.

While water quality has generally improved since the 1970s due to numerous Federal, state, and local laws, including the Clean Water Act of 1972, water quality continues to be an issue for Atlantic sturgeon due to human population expansion and a variety of agricultural, industrial, and commercial activities in the coastal zone. Table 9 in the 2007 status review report cites the USEPA's National Coastal Condition Report (NCCR) II (2005) in grading the Southeast water quality as a B. The NCCR II also assigned water quality a numerical score of 4 (where 1 is poor and 5 is good), ranking it as “good to fair.” It is important to note that the water quality index in the NCCR II was based on a combination of several parameters, the most important of which to Atlantic sturgeon is dissolved oxygen (DO). The DO range considered “good” in the NCCR II was greater than 5 mg/L while a DO range of 2 to 5 mg/L was considered “fair.” As stated in the proposed listing rule, sturgeon are more highly sensitive to low DO than other fish species and “low” DO was defined as less than 5 mg/L (Niklitschek and Secor, 2009a, 2009b). A DO of 2 mg/L (the lower end of the “fair” scale in the NCCR II report) would be considered very poor for an Atlantic sturgeon, likely lethal to early life stages (Niklitschek and Secor, 2009a, 2009b; Niklitschek and Secor, 2005; Secor and Gunderson, 1998). The USEPA

published the NCCR III in 2008 and downgraded water quality in the Southeast from a 4 to a 3, ranking it as “fair” rather than “good to fair.” It also showed that the portion of the Southeast that had a “poor” water quality index ranking increased slightly from 5 percent to 6 percent. While other condition indicators for the Southeast in the NCCR III showed improvement over the NCCR II levels (the benthic index was upgraded from a 3 to a 5 in the Southeast) or remained the same (the coastal habitat index remained a 3), the sediment quality index was downgraded from a 4 to a 3, and the fish tissue contaminant index was downgraded from a 5 to a 4. This resulted in a decrease from 3.8 to 3.6 in the overall condition of the Southeast. The results of the NCCR III report do not support the commenters' assertion that water quality has continually improved since the 1970's. Water quality was downgraded to “fair”, and DO levels included under a “fair” rating may be less than adequate for Atlantic sturgeon, particularly early life stages. Further, the percentage of geographic areas in the Southeast with “poor” water quality increased between NCCR II and III.

NMFS and other partners involved in the conservation of Atlantic sturgeon (such as the ASMFC, USFWS, and state agencies) continue to work on monitoring, research, and other activities, including those outlined in the 1998 status review, to recover Atlantic sturgeon. However, these are long-term, ongoing efforts, and the objectives outlined in the 1998 status review report are not complete. We do not have all of the data requested by the commenter, but what is available is included in the 2007 status review, the proposed listing rule, and the references cited therein. Once Atlantic sturgeon are listed, NMFS will have a greater opportunity to prioritize and standardize Atlantic sturgeon research, as recommended for recovery and conservation of Atlantic sturgeon in the 1998 status review.

Comment 28:

Several comments stated that the 2007 status review report was developed with little or no input from state agency experts and that state agency comments should be weighed heavily. One commenter stated that the results of the 2003 workshop that preceded the 2007 status review report were not publicly available.

Response:

Eight state and regional experts from six state agencies provided their individual expert opinions on the information contained in the 2007 status review report and provided additional data to ensure the status review report included the best available. Many of the comments, data, and information presented in this document originated from state agencies. As stated in the status review report and the proposed listing rule, information obtained at the 2003 workshop prompted the initiation of the status review. Information from the workshop was incorporated into the 2007 status review. In addition, the 2003 workshop was held in conjunction with a meeting of the ASMFC Atlantic Sturgeon Technical Committee and some of the proceedings of the workshop are published in various meeting summaries, reports, and documents on the ASMFC's Atlantic sturgeon Web site (

http://www.asmfc.org

).

Comments on the Need To List Atlantic Sturgeon Under the ESA

Comment 29:

Comments were received stating that Atlantic sturgeon should not be listed because their populations are stable, sufficiently large, and/or increasing. Commenters cited to Grunwald

et al.

(2008) for statements that the Altamaha and Edisto appear to have large, multiple year class populations that exhibit high annual reproductive success. The State of Georgia commented that, in order to list as threatened or endangered under the ESA, the condition must exist in “all or a significant portion of its range.” The commenter stated the Altamaha River represents a significant portion of the South Atlantic DPS's range due to the large population of Atlantic sturgeon in that river and the area of the watershed. They also stated populations are persisting in other systems, and therefore, they do not believe Atlantic sturgeon are threatened or endangered throughout a significant portion of their range. Other commenters stated that Atlantic sturgeon have been observed in most South Carolina coastal rivers during the last two decades, although it is not known if all rivers support a spawning population. Currently, the only long term data set available for Atlantic sturgeon in South Carolina is on the Edisto River, where the Atlantic sturgeon population seem to be relatively stable based on fishery independent sampling efforts by the South Carolina Department of Natural Resources. A commenter stated that abundance and distribution presented in the proposed listing rule is inconclusive, citing increasing incidental take in Albemarle Sound gill nets, increases in average length of Atlantic sturgeon captured off North Carolina between 1986 and 2003, suspected spawning activity on the Pee Dee River during the Fall of 2003, and the doubling of CPUE of Atlantic sturgeon from annual surveys conducted in the Cape Fear River between 1997 and 2003. One commenter stated that for the Savannah River, conclusions were incorrectly drawn in the proposed listing rule that the greater catch of shortnose sturgeon than Atlantic sturgeon, as cited in Collins

et al.

(1996), was not a reflection of lower than expected catch of Atlantic sturgeon, but rather that they were fishing in areas/habitat not preferred by juvenile Atlantic sturgeon.

Response:

The information presented by commenters stating that Atlantic sturgeon should not be listed does not provide a basis for revising our proposed listing rule determination of endangered for the Carolina and South Atlantic DPSs of Atlantic sturgeon. Grunwald

et al.

(2008) stated that “among southeastern populations, those in the Altamaha (Peterson

et al.

in press) and Edisto appear to be large, with multiple year classes and high annual reproductive success.” Grunwald

et al.

(2008) continued that “others range from small (Ogeechee and Savannah) to possibly extirpated (Satilla).” This is consistent with information we presented in the proposed listing rule that, at the 2003 workshop, we determined some populations seemed to be recovering while others were declining, prompting our initiation of the 2007 status review. This comment is also consistent with our description in proposed listing rule of the Altamaha population as larger and more robust than other populations in the Southeast. We received information from SCDNR (presented in the previous section of comments) that they have captured 3,661 Atlantic sturgeon in the Edisto since 1994. If all of these were spawning adults, then this represents an average of approximately 230 spawning adults per year since 1994, which is consistent with our estimate of less than 300 spawning adults per year for this system. The low number of annually spawning adults estimated for Atlantic sturgeon in the Southeast (343 for the Altamaha River and less than 300 for the remaining spawning populations) factored heavily in our determination that the Carolina and South Atlantic DPSs warranted listing as endangered. In the proposed listing rule, we did not define which rivers constitute a significant portion of the species' range because we concluded that the Carolina and South Atlantic DPSs are endangered throughout their entire ranges. The presence of multiple spawning populations does not negate the need for listing. As discussed above, we do not believe that any of the riverine

populations within either DPS, alone or in combination, are viable and stable enough to constitute a significant portion of either DPS's range.

We acknowledged uncertainty in the abundance and distribution information we presented. However, we believe that a conservative evaluation of the information the commenter referred to as “inconclusive” supports our endangered listing determination. As the commenter noted, we stated that catch records for Albemarle Sound, as well as the Roanoke River, indicate that this population seemed to be increasing until 2000, when recruitment began to decline. We also indicated the existence of catch records and observations from other river systems in North Carolina (

e.g.,

the Tar, Neuse, and Cape Fear Rivers), but, based on the relatively low numbers of fish caught, we stated it was difficult to determine whether the populations in those systems are declining, rebounding, or remaining static. However, the fact alone that low numbers of fish were caught does not logically lead to a conclusion that populations are increasing. The commenter's interpretation of data on increases in average length of Atlantic sturgeon caught

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