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Proposed Rule

Endangered and Threatened Wildlife and Plants; 12-Month Finding for the Eastern Taiwan Strait Indo-Pacific Humpback Dolphin, Dusky Sea Snake, Banggai Cardinalfish, Harrisson's Dogfish, and Three Corals Under the Endangered Species Act

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


Proposed rule; 12-month petition finding; request for comments.


We, NMFS, have completed comprehensive status reviews under the Endangered Species Act (ESA) for seven foreign marine species in response to a petition to list those species. These seven species are the Eastern Taiwan Strait population of Indo-Pacific humpback dolphin (Sousa chinensis), dusky sea snake (Aipysurus fuscus), Banggai cardinalfish (Pterapogon kauderni), Harrisson's dogfish (Centrophorus harrissoni), and the corals Cantharellus noumeae, Siderastrea glynni, and Tubastraea floreana. We have determined that the Eastern Taiwan Strait Indo-Pacific humpback dolphin is not a distinct population segment and therefore does not warrant listing. We have determined that, based on the best scientific and commercial data available, and after taking into account efforts being made to protect the species, Pterapogon kauderni, and Centrophorus harrissoni meet the definition of a threatened species; and Aipysurus fuscus, Cantharellus noumeae, Siderastrea glynni, and Tubastraea floreana meet the definition of an endangered species. Therefore, we propose to list these six species under the ESA. We are not proposing to designate critical habitat for any of the species proposed for listing, because the geographical areas occupied by these species are entirely outside U.S. jurisdiction, and we have not identified any unoccupied areas that are currently essential to the conservation of any of these species. We are soliciting comments on our proposals to list the six species. We are also proposing related administrative changes to our lists of threatened and endangered species.


Comments on our proposed rule to list eight species must be received by February 17, 2015. Public hearing requests must be made by January 30, 2015.


You may submit comments on this document, identified by NOAA-NMFS-2014-0083, by any of the following methods:

  • Electronic Submissions: Submit all electronic public comments via the Federal eRulemaking Portal. Go to​#!docketDetail;​D=​NOAA-NMFS-2014-0083. Click the “Comment Now” icon, complete the required fields, and enter or attach your comments.
  • Mail: Submit written comments to, Lisa Manning, NMFS Office of Protected Resources (F/PR3), 1315 East West Highway, Silver Spring, MD 20910, USA.

Instructions: You must submit comments by one of the above methods to ensure that we receive, document, and consider them. Comments sent by any other method, to any other address or individual, or received after the end of the comment period, may not be considered. All comments received are a part of the public record and will generally be posted for public viewing on without change. All personal identifying information (e.g., name, address, etc.), confidential business information, or otherwise sensitive information submitted voluntarily by the sender will be publicly accessible. We will accept anonymous comments (enter “N/A” in the required fields if you wish to remain anonymous). Attachments to electronic comments will be accepted in Microsoft Word, Excel, or Adobe PDF file formats only.

You can obtain the petition, status review reports, the proposed rule, and the list of references electronically on our NMFS Web site at​pr/​species/​petition81.htm.

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Lisa Manning, NMFS, Office of Protected Resources (OPR), (301) 427-8403.

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On July 15, 2013, we received a petition from WildEarth Guardians to list 81 marine species as threatened or endangered under the Endangered Species Act (ESA). This petition included species from many different taxonomic groups, and we prepared our 90-day findings in batches by taxonomic group. We found that the petitioned actions may be warranted for 27 of the 81 species and announced the initiation of status reviews for each of the 27 species (78 FR 63941, October 25, 2013; 78 FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79 FR 9880, February 21, 2014; and 79 FR 10104, February 24, 2014). This document addresses the findings for 7 of those 27 species: the Eastern Taiwan Strait population of Indo-Pacific humpback dolphin (Sousa chinensis), dusky sea snake (Aipysurus fuscus), Banggai cardinalfish (Pterapogon kauderni), Harrisson's dogfish (Centrophorus harrissoni), and the corals Cantharellus noumeae, Siderastrea glynni, and Tubastraea floreana. The remaining 20 species will be addressed in subsequent findings.

We are responsible for determining whether species are threatened or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this determination, we consider first whether a group of organisms constitutes a “species” under the ESA, then whether the status of the species qualifies it for listing as either threatened or endangered. Section 3 of the ESA defines a “species” 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, NMFS and the U.S. Fish and Wildlife Service (USFWS; together, the Services) adopted a policy describing what constitutes a distinct population segment (DPS) of a taxonomic species (the DPS Policy; 61 FR 4722). The 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 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.” We interpret an “endangered species” to be one that is presently in danger of extinction. A “threatened species,” on the other hand, is not presently in danger of extinction, but is likely to become so in the foreseeable future (that Start Printed Page 74955is, at a later time). In other words, the primary statutory difference between a threatened and endangered species is the timing of when a species may be in danger of extinction, either presently (endangered) or in the foreseeable future (threatened).

When we consider whether species might qualify as threatened under the ESA, we must consider the meaning of the term “foreseeable future.” It is appropriate to interpret “foreseeable future” as the horizon over which predictions about the conservation status of the species can be reasonably relied upon. The foreseeable future considers the life history of the species, habitat characteristics, availability of data, particular threats, ability to predict threats, and the reliability to forecast the effects of these threats and future events on the status of the species under consideration. Because a species may be susceptible to a variety of threats for which different data are available, or which operate across different time scales, the foreseeable future is not necessarily reducible to a particular number of years. Discussions of the considerations for each relevant species are in the species-specific sections below.

Section 4(a)(1) of the ESA requires us to determine whether any species is endangered or threatened due to any one or a combination of the following five threat factors: The present or threatened destruction, modification, or curtailment of its habitat or range; overutilization for commercial, recreational, scientific, or educational purposes; disease or predation; the inadequacy of existing regulatory mechanisms; or other natural or manmade factors affecting its continued existence. We are also required to make listing determinations based solely on the best scientific and commercial data available, after conducting a review of the species' status and after taking into account efforts being made by any state or foreign nation to protect the species.

In making a listing determination, we first determine whether a petitioned species meets the ESA definition of a “species.” Next, using the best available information gathered during the status review for the species, we complete a status and extinction risk assessment. In assessing extinction risk, we consider the demographic viability factors developed by McElhany et al. (2000) and the risk matrix approach developed by Wainwright and Kope (1999) to organize and summarize extinction risk considerations. The approach of considering demographic risk factors to help frame the consideration of extinction risk has been used in many of our status reviews, including for Pacific salmonids, Pacific hake, walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring, scalloped hammerhead sharks, and black abalone (see​pr/​species/​ for links to these reviews). In this approach, the collective condition of individual populations is considered at the species level according to four demographic viability factors: Abundance, growth rate/productivity, spatial structure/connectivity, and diversity. These viability factors reflect concepts that are well-founded in conservation biology and that individually and collectively provide strong indicators of extinction risk.

We then assess efforts being made to protect the species, to determine if these conservation efforts are adequate to mitigate the existing threats. Section 4(b)(1)(A) of the ESA requires the Secretary, when making a listing determination for a species, to take into consideration those efforts, if any, being made by any State or foreign nation to protect the species. We also evaluate conservation efforts that have not yet been fully implemented or shown to be effective using the criteria outlined in the joint NMFS/USFWS Policy for Evaluating Conservation Efforts (PECE; 68 FR 15100, March 28, 2003), to determine their certainty of implementation and effectiveness. The PECE is designed to ensure consistent and adequate evaluation of whether any conservation efforts that have been recently adopted or implemented, but not yet demonstrated to be effective, will result in recovering the species to the point at which listing is not warranted or contribute to forming the basis for listing a species as threatened rather than endangered. The two basic criteria established by the PECE are: (1) The certainty that the conservation efforts will be implemented; and (2) the certainty that the efforts will be effective. We consider these criteria in each species-specific section, as applicable, below. Finally, we re-assess the extinction risk of the species in light of the existing conservation efforts.

Status Reviews

Status reviews for the petitioned species addressed in this finding were conducted by NMFS OPR staff. Separate status reviews were done for the Eastern Taiwan Strait Indo-Pacific humpback dolphin (Whittaker, 2014), dusky sea snake (Manning, 2014), Banggai cardinalfish (Conant, 2014), Harrison's dogfish (Miller, 2014), and the three corals (Meadows, 2014). In order to complete the status reviews, we compiled information on the species' biology, ecology, life history, threats, and conservation status from information contained in the petition, our files, a comprehensive literature search, and consultation with experts. We also considered information submitted by the public in response to our petition findings. Draft status review reports were also submitted to independent peer reviewers; comments and information received from peer reviewers were addressed and incorporated as appropriate before finalizing the draft reports.

Each status review report provides a thorough discussion of demographic risks and threats to the particular species. We considered all identified threats, both individually and cumulatively, to determine whether the species responds in a way that causes actual impacts at the species level. The collective condition of individual populations was also considered at the species level, according to the four demographic viability factors discussed above.

The status review reports are available on our Web site (see ADDRESSES section). Below we summarize information from those reports and the status of each species.

Eastern Taiwan Strait Population of the Indo-Pacific Humpback Dolphin

The following section describes our analysis of the status of the Eastern Taiwan Strait (ETS) population of the Indo-Pacific Humpback dolphin, Sousa chinensis.

Species Description

The Indo-Pacific humpback dolphin, Sousa chinensis (Osbeck, 1765), within the genus Sousa, family Delphinidae, and order Cetacea, is broadly distributed. The taxonomy of the genus is unresolved and has historically been based on morphology, but genetic analyses have recently been used. Current taxonomic hypotheses identify Sousa chinensis as one of two (Jefferson et al., 2001), three (Rice, 1998), or four (Mendez et al., 2013) species within the genus. Each species is associated with a unique geographic range, though the species' defined ranges vary depending on how many species are recognized. Rice (1998) recognizes Sousa teuzii in the eastern Atlantic, Sousa plumbea in the western Indo-Pacific, and Sousa chinensis in the eastern Indo-Pacific. Mendez et al. (2013) recently identified an as-yet unnamed potential new species in waters off of northern Australia. Currently, the International Union for Conservation of Nature (IUCN) and International Whaling Commission (IWC) Scientific Committee Start Printed Page 74956recognize only two species, Sousa chinensis in the Indo-Pacific, and Sousa teuzii in the eastern Atlantic. Here, we follow a similar two-species taxonomy in our consideration of the genus and identification of the species Sousa chinensis. Under that taxonomy, Sousa chinensis' range includes nearshore tropical and subtropical habitats in southern Africa, the Indian Ocean, North Australia, southern mainland China, Hong Kong, and Taiwan (Jefferson et al., 2001; Mendez et al., 2013). We chose to follow a two-species taxonomy as it provides the clearest genetic, morphological, and geographic delineation of the species and is well supported by the current data available. While growing genetic and phylogeographic evidence suggests that Sousa chinensis is associated with further genetic subdivisions, more data are needed to clarify the taxonomy and delineate the geographic boundaries and ranges of these additional genetic units (Cockroft et al., 1997; Jefferson et al., 2004b; Frère et al., 2008; Frère et al., 2011; Lin et al., 2012; Mendez et al., 2013).

The Indo-Pacific humpback dolphin is easy to distinguish from other dolphin species in its range, as it is characterized by a robust body, a long, distinct beak, a short dorsal fin atop a wide dorsal hump, and round-tipped, broad flippers and flukes (Jefferson et al., 2001). The Indo-Pacific humpback dolphin is medium-sized, up to 2.8 m in length, weighing 250-280 kg (Ross et al., 1994). Morphological plasticity exists among populations of the species and is correlated with their geographic distributions (Ross et al., 1994). For example, the Eastern Taiwan Strait population, which occurs at the eastern portion of the species' range, has a short dorsal fin with a wide base; the base of the fin measures 5-10 percent of the body length and slopes gradually into the surface of the body. This differs from individuals in the western portion of the range, which have a larger hump that comprises about 30 percent of body width, and forms the base of an even smaller dorsal fin (Ross et al., 1994). Males and females from the Pearl River Estuary population, and in other populations of Southeast Asia, do not exhibit sexual dimorphism in size, growth patterns, or morphology (Jefferson et al., 2001; Jefferson et al., 2012). In contrast, individuals from South Africa exhibit sexual dimorphism in terms of size and dorsal hump morphology (Ross et al., 1994; Karczmarski et al., 1997).

The species occurs in a range of nearshore habitats, including estuaries, mangroves, seagrass meadows, coastal lagoons, and sandy beaches (Ross et al., 1994). In Thailand, Malaysia, and Indonesia, nearshore ecosystems are associated with tropical seagrass, coral, and mangrove lagoons (Beasley et al., 1997; Smith et al., 2003; Adulyanukosol et al., 2006; Jaroensutasinee et al., 2011; Cherdsukai et al., 2013). In India, the species is associated with nearshore habitat consisting of mangroves, corals, and tidal mudflat, heavily influenced by monsoons that regulate the influx of freshwater to the system (Sutaria et al., 2004). The coast of mainland China is thought to host at least eight populations of the species, primarily occurring in estuarine systems at the mouths of large rivers (Jefferson et al., 2001; Jefferson et al., 2004a). Two coastal Chinese populations, in close proximity to the population in the Eastern Taiwan Strait, are relatively well-studied. These are the Pearl River Estuary/Hong Kong population and the Jiulong River Estuary/Xaimen population, both of which depend upon ecosystem productivity associated with the nutrient output supplied by large rivers (Chen et al., 2008; Chen et al., 2010).

The Eastern Taiwan Strait population of Sousa chinensis (henceforth referred to as the ETS humpback dolphin), for which we were petitioned, was first described in 2002 during an exploratory survey of coastal waters off of western Taiwan (Wang et al., 2004). Prior to these coastal surveys, there are few records mentioning the species in this region, save two strandings, a few photographs, and anecdotal reports (Wang, 2004), so their history in the region is unclear. Since the first survey in 2002, researchers have confirmed their year-round presence in the Eastern Taiwan Strait (Wang et al., 2011), inhabiting estuarine and coastal waters of central-western Taiwan.

The ETS humpback dolphin habitat is most similar to that of the populations located off the coast of mainland China. Individuals of the ETS humpback dolphin population are thought to be restricted to water less than 30 meters deep, and most observed sightings have occurred in estuarine habitat with significant freshwater input (Wang et al., 2007b). Across the ETS humpback dolphin habitat, bottom substrate consists of soft-sloping muddy sediment with elevated nutrient inputs, primarily influenced by river deposition (Sheehy, 2010). These nutrient inputs support high primary production, which fuels upper trophic levels, contributing to the dolphin's source of food (Jefferson, 2000).

The Indo-Pacific humpback dolphin is considered a generalist and opportunistic piscivore (Barros et al., 2004). As is common to the species as a whole, the ETS population uses echolocation and passive listening to find its prey. While little is known about the specific diet and feeding of the ETS population, diet can be inferred from that of other humpback dolphin populations (Barros et al., 2004; Chen et al., 2009). In Chinese waters off Hong Kong, the species consumes both bottom-dwelling and pelagic fish species, including croakers (Sciaenidae), mullets (Mugilidae), threadfins (Polynemidae), and herring (Clupeidae) (Barros et al., 2004). Part of the feeding strategy for this population may be to induce shoaling of fish by physically corralling them, allowing individuals to forage and feed successfully, even within murky nearshore waters (Sheehy, 2009). In general, the prey species of the humpback dolphin include small fish which are generally not commercially valuable to local fisheries (Barros et al., 2004; Sheehy, 2009).

Little is known about the life history and reproduction of ETS humpback dolphin. In some cases, comparison of the ETS population with other populations may be appropriate, but one needs to be cautious about making these comparisons, as environmental factors such as food availability and habitat status may affect important rates of reproduction and generation time in different populations. A recent analysis of life history patterns for individuals in the Pearl River Estuary (PRE) population is the best proxy for the ETS population. Like the ETS population, the PRE population inhabits estuarine and freshwater-influenced environments in similar proximity to anthropogenic activity (Jefferson et al., 2012). Maximum longevity for the PRE population is estimated to be greater than 38 years (Jefferson et al., 2012). Evidence from multi-year photo-analysis of the ETS population demonstrated that adult survivorship is high, 0.985, suggesting that this population also has a relatively long lifespan (Wang et al., 2012). In general, it is inferred that the population has long calving intervals, between 3 and 5 years (Jefferson et al., 2012). Gestation lasts 10-12 months (Jefferson et al., 2012). Weaning may take up to 2 years, and strong female-calf association may last 3-4 years (Karczmarski et al., 1997; Karczmarski, 1999). Peak calving activity most likely occurs in the warmer months, but exact peak of calving time may vary geographically (Jefferson et al., 2012). Age at sexual maturity is late, estimated at between 12 and 14 years (Jefferson et al., 2012).Start Printed Page 74957

DPS Analysis

The following section provides our analysis, based on the best available science and the DPS Policy, to determine whether the ETS humpback dolphin population qualifies as a DPS of the taxon.


The Services' joint DPS Policy states that a population segment of a vertebrate species may be considered discrete if it satisfies either one of the following conditions: (1) It is markedly separated from other populations of the same taxon as a consequence of physical, physiological, ecological, or behavioral factors (quantitative measures of genetic or morphological discontinuity may provide evidence of this separation); or (2) it is delimited by international governmental boundaries within which differences in control of exploitation, management of habitat, conservation status, or regulatory mechanisms exist that are significant in light of section 4(a)(1)(D) of the ESA (61 FR 4722; February 7, 1996).

Individuals from the ETS population exhibit pigmentation that differs significantly from nearby populations along the mainland coast of China, and evidence suggests that pigmentation varies geographically across the species' range (Jefferson et al., 2001; Jefferson et al., 2004a; Wang et al., 2008). Across the species, pigmentation changes as individuals mature. When young, dolphins appear dark grey with no or few light-colored spots; as they age, they transform to mostly white (appearing pinkish), as dark spots decrease with age. In particular, the developmental transformation of pigment differs significantly between ETS and nearby Chinese humpback dolphin populations; specifically, the spotting intensity (density of spots) on the dorsal fin of the ETS population is significantly greater than that of four mainland Chinese populations, including the other nearby populations in the Pearl River Estuary and Jiulong River estuaries (Wang et al., 2008). Significantly greater spotting intensity on the dorsal fin of the ETS population is consistent, regardless of age (Wang et al., 2008). Further, the ETS humpback dolphin never loses the dark dorsal fin spots completely, as has been observed in older individuals of other humpback dolphin populations (Wang et al., 2008). In contrast, dorsal fins of Chinese populations are strikingly devoid of spots, compared to their bodies, throughout most of their lives, except when they are very young or very old (Wang et al., 2008). These differences in pigmentation can be used to reliably differentiate between the ETS humpback dolphin and nearby Chinese populations (Wang et al., 2008). Thus, we consider these significant differences in pigmentation of the ETS humpback dolphin as evidence of its discreteness.

Several researchers have suggested that the ETS population of the humpback dolphin is physically and geographically isolated from other populations, based on the fact that individuals have not been observed crossing or to have crossed the Strait of Taiwan, despite repeated surveys of Chinese and Taiwanese populations using photo-identification techniques (Wang et al., 2004; Wang et al., 2007b; Chen et al., 2010; Wang et al., 2011; Wang et al., 2012). For instance, a detailed analysis of more than 450 individually-recognizable dolphins catalogued for Taiwanese and Chinese populations revealed no matches among them (Wang et al., 2008). Movement of Sousa chinensis is thought to be limited to shallow water and nearshore habitat (Karczmarski et al., 1997; Hung et al., 2004). Water depth and fast-moving currents within the Eastern Taiwan Strait are thought to isolate the ETS population from Chinese populations, despite their relatively close geographic proximity (Wang et al., 2004; Wang et al., 2008; Wang et al., 2011; Wee et al., 2011; Wang et al., 2012). In fact, the ETS population has never been observed in waters greater than 30 meters depth (Wang et al., 2007b). Evidence suggests that the ETS population of the humpback dolphin has a narrow home range, and does not migrate seasonally or mix with Chinese populations (Wang et al., 2011). The population has been shown to inhabit the shallow, narrow habitat on the western coast of Taiwan throughout the year, and exhibits strong site fidelity (Wang et al., 2011).

The evidence for geographic isolation is based on limited survey data collected since 2002, which focused only on nearshore waters at certain times of year and did not survey the Strait waters between mainland China and Western Taiwan (Wang et al., 2004; Wang et al., 2011; Wang et al., 2012). Thus, the possibility for Indo-Pacific humpback dolphin migration or emigration across the Strait cannot be eliminated entirely. However, the best available scientific information indicates that the species is found primarily in shallow nearshore habitat, and the ETS population has never been observed in waters greater than 30 meters, and thus migration or emigration across the deeper Strait is thought to occur rarely, if ever.

The best available data suggest that the ETS humpback dolphin population is discrete from all other populations of the species based on its morphological differences. Although limited, the best available data also suggest that the ETS humpback dolphin population is geographically isolated from other populations. The morphological differences and geographic isolation set this population apart from other populations of the Indo-Pacific humpback dolphin, and thus, we conclude that the ETS humpback dolphin population meets the discreteness criterion of the DPS Policy.


When the discreteness criterion is met for a potential DPS, as it is for the ETS humpback dolphin population, the second element that must be considered under the DPS Policy is the significance of the DPS to the taxon as a whole. Significance is evaluated in terms of the importance of the population segment to the taxon to which it belongs, in this case the species Sousa chinensis. Some of the considerations that can be used under the DPS Policy to determine a discrete population segment's significance to the taxon as a whole include: (1) Persistence of the population segment in an unusual or unique ecological setting; (2) evidence that loss of the population segment would result in a significant gap in the range of the taxon; and (3) evidence that the population segment differs markedly from other populations of the species in its genetic characteristics.

The ETS humpback dolphin population occurs in an ecological setting similar to populations occurring along the coast of mainland China, and many features of its habitat and ecology are similar to those of populations throughout the range of the species, as discussed above. Throughout its range, the Indo-Pacific humpback dolphin is consistently associated with coastal river output and is found in shallow nearshore waters (Jefferson et al., 2001). It displays no apparent preference for clear or turbid waters (Karczmarski et al., 2000). The habitat and ecosystem use of the species differ in some ways geographically, but evidence suggests that the dolphin is an opportunistic piscivore, and thus does not exhibit unique or restricted feeding ecology across its range (Jefferson et al., 2001).

In Thailand, Malaysia, and Indonesia, the species occurs in tropical seagrass, coral, and mangrove lagoons not present in ETS humpback dolphin habitat (Beasley et al., 1997; Smith et al., 2003; Adulyanukosol et al., 2006; Jaroensutasinee et al., 2011; Chersukjai Start Printed Page 74958 et al., 2013). In India, the species is associated with nearshore habitat consisting of mangroves, corals, and tidal mudflat, heavily influenced by monsoons that regulate the influx of freshwater to the system (Sutaria et al., 2004). The ETS humpback dolphin habitat is most similar to that of coastal Chinese populations, with more temperate water, soft muddy substrate, and consistent input from river systems. The ETS humpback dolphin habitat differs from the habitat occupied by mainland Chinese populations in some ways, with nearby rivers generally smaller than those in mainland China, and with warmer waters in the winter due to the influence of the Kuroshio Current, which periodically moves into the Strait of Taiwan (Chern et al., 1990; Jan et al., 2002; Wang et al., 2008). However, feeding ecology, prey availability, and prey preference are thought to be similar in mainland China and Taiwan (Barros et al., 2004; Wang et al., 2007a), so these small differences in habitat do not seem to have significant effects on the species' ecology.

The presumed habitat of the ETS humpback dolphin is narrower in offshore width than that of other studied populations of the taxon. For instance, the ETS population is thought to inhabit a small area of coastal shallow waters within 3 km from the shore (Wang et al., 2007b). In contrast, Chinese populations inhabit a broader shallow area ranging tens of kilometers offshore, where dolphins can range farther from the coastline without moving into deeper water (Hung et al., 2004; Chen et al., 2011). While the ETS population exhibits some behavioral differences, such as increased cooperative calf-rearing and social connectivity, as compared to Chinese populations (Dungan et al., 2011), it is uncertain whether or not these differences are adaptive or facultative, and simply based on the population's low abundance. Thus, insufficient evidence exists to suggest significant differences in the dolphin's ecology or adaptation have derived from the differences in the physical parameters of its environment. Therefore, differences in the habitat and ecological setting of the ETS humpback dolphin do not set it apart from the rest of the taxon, and do not appear to relate to significant selection pressures affecting the population's foraging, behavior, or ecology.

There is no evidence to suggest that loss of the ETS humpback dolphin population would result in a significant gap in the range of the taxon. The ETS humpback dolphin population constitutes a small and peripheral portion of the entire range of the species, and its loss would not inhibit population movement or gene flow among other populations of the species (Lin et al., 2012). The ETS humpback dolphin is distributed throughout only 512 square kilometers of coastal waters off Western Taiwan; this small range is not geographically significant in comparison to the taxon's range throughout the coastal Indo-Pacific and Indian Oceans.

There are no data to show that the genetic characteristics of the ETS humpback dolphin population differ markedly from other populations in a significant way. While pigmentation of the ETS population is significantly different from other populations within the taxon (Wang et al., 2008), whether the pattern is adaptive or has genetic underpinnings is unknown. In other cetacean species, differences in pigmentation have been hypothesized to relate to several adaptive responses, allowing individuals to hide from predators, communicate with conspecifics (promoting group cohesion), and disorient and corral prey (Caro et al., 2011). However, the differences in ETS humpback dolphin pigmentation may be a result of a genetic bottleneck from the small size of this population (less than 100 individuals) and the possibility that it represents a single social and/or family group. Such small populations are more heavily influenced by genetic drift than large populations (Frankham, 1996). Insufficient data exist to determine whether significant differences in ETS humpback dolphin pigmentation relate to the functional divergence of the population, or are simply a product of genetic drift and a genetic bottleneck. The best data available thus lead us to conclude that loss of the ETS humpback dolphin population would not result in significant loss of overall genetic or ecological diversity of the taxon as a whole.

DPS Conclusion and Proposed Determination

According to our analysis, the ETS humpback dolphin population is considered discrete based on its unique pigmentation patterns, which set it apart morphologically from the rest of the taxon, and evidence for its geographic isolation. However, while discrete, the ETS humpback dolphin population does not meet any criteria for significance to the taxon as a whole. The ecological setting it occupies is similar to that of the rest of the species, loss of the population would not constitute a significant gap in the taxon's extensive range, and no genetic or other data have demonstrated that the population makes a significant contribution to the adaptive, ecological, or genetic diversity of the taxon. As such, based on the best available data, we conclude that the ETS humpback dolphin population is not a DPS and thus does not qualify for listing under the ESA. This is a final action, and, therefore, we do not solicit comments on it.

Dusky Sea Snake

The section below presents our analysis of the status of the dusky sea snake, Aipysurus fuscus. Further details can be found in Manning (2014).

Species Description

The dusky sea snake, Aipysurus fuscus, is a species within the family Elapidae, which is a very diverse family of venomous snakes. The genus Aipysurus contains seven species, six of which are restricted to Australasian waters. The dusky sea snake is brown, blackish-brown, or purplish-brown with wide ventral scales and diamond-shaped body scales that are smooth and imbricate (i.e., overlapping). There are generally 19 scale rows around the neck, 19 around the mid-body, and 155 to 180 ventral scales (Rasmussen, 2000). The dusky sea snake is completely aquatic and, like all sea snakes, has a paddle-like tail for swimming. Its maximum total length is about 90 cm (Rasmussen, 2000). Growth rates for the dusky sea snake have not been documented, but reported growth rates for other sea snakes range from 0.07-1.0 mm per day and decline with age (Heatwole, 1997). The maximum lifespan for dusky sea snakes has been assumed to be about 10 years, and age at first maturity has been assumed to be about 3-4 years (Lukoschek et al., 2010). Generation length is thought to be approximately 5 years (Lukoschek et al., 2010).

Despite its aquatic existence, and like all reptiles, the dusky sea snake lacks gills and must surface to breathe air. Dive durations vary by species, but most sea snakes typically stay submerged for about 30 minutes, and some for up to 1.5-2.5 hours (Heatwole and Seymour, 1975). Maximum dive depth for dusky sea snakes is unknown, but co-occurring members of this genus are considered “shallow” and “intermediate” depth species that dive no deeper than 20 m or 50 m, respectively (Heatwole and Seymour, 1975).

The dusky sea snake is viviparous, meaning embryos develop internally and young undergo live birth. Because this species never ventures on land, mating occurs at sea and young are born alive in the water. Within the genus Aipysurus, the number of young per Start Printed Page 74959brood is small, usually less than four, and young are relatively large at birth (Cogger, 1975). Timing and seasonality of the dusky sea snake's breeding cycles are unknown, and very little is known about the juvenile life stage.

The dusky sea snake preys mainly on labrid (e.g., wrasses) and gobiid (e.g., gobies) fishes, and to a lesser extent, fish eggs (McCosker, 1975). Food competition among sympatric sea snakes is thought to be minimal, based on examinations of diet composition for sympatric sea snakes (McCosker, 1975; Voris and Voris, 1983). Feeding behavior of dusky sea snakes has not been thoroughly investigated; however, during surveys at Ashmore Reef, Australia, Guinea and Whiting (2005) commonly saw dusky sea snakes over sand bottom habitat and watched one snake actually force its head and about 15 percent of its body into the sand. However, because it emerged without a prey item (Guinea and Whiting, 2005), it is unclear whether this was foraging or some other behavior. Like their terrestrial relatives, sea snakes swallow their prey whole and therefore must have some strategy for subduing them. McCosker (1975) hypothesized that the highly toxic venom of sea snakes is probably more of a feeding adaptation than a defensive one.

The dusky sea snake is a benthic, coral reef-associated species endemic to several shallow emergent reefs of the Sahul Shelf off the coast of Western Australia in the Timor Sea, between Timor and Australia. These reefs are relatively isolated and lie at the edge of the continental shelf over several hundred kilometers from the mainland. The dusky sea snake has been reported to occur at Ashmore, Scott, Seringapatam, and Hibernia Reefs and Cartier Island; however, individual surveys have not consistently recorded dusky sea snakes at all of these locations. For example, in transect surveys conducted by Minton and Heatwole (1975) over several weeks during December 1972 and January 1973 at Ashmore, Scott, and Hibernia Reefs and Cartier Island, dusky sea snakes were recorded at Scott and Ashmore reefs only. Extensive surveys conducted more recently at Ashmore Reef, where dusky sea snakes were once relatively common, have located no specimens (Guinea, 2013; Lukoschek et al., 2013). Lukoschek et al. (2010) estimated that the area of occurrence of dusky sea snakes is probably less than 500 km2.

During their surveys, Minton and Heatwole (1975) observed dusky sea snakes in shallow water (<10 m) as well as in the 12 to 25 m depth-zone. They were observed in areas of moderate to heavy coral growth, but they were also observed to congregate in sandy-bottomed gullies and channels (Minton and Heatwole, 1975). Home-range size and site fidelity of individual dusky sea snakes has not been evaluated. However, a short-term (6-9 days), telemetry study on the sympatric olive sea snakes (A. laevis) and a long-term (8-year), mark-recapture study on the turtle-headed sea snake (Emydocephalus annulatus) suggest that home-ranges of sea snakes are small, movement of adults is very limited, and longer-distance dispersal may be due mainly to passive transport, such as by currents and storms (Burns and Heatwole, 1998; Lukoschek and Shine 2012). While it is very plausible that adult A. fuscus are similar to these other species, research to evaluate adult and juvenile A. fuscus habitat use and movement is needed.

Sea snakes typically have patchy distributions and can be found in very dense aggregations in certain locations within their ranges (Heatwole, 1997). This patchiness complicates efforts to understand habitat use patterns, as seemingly suitable habitat can remain unoccupied. On a smaller spatial scale, distributions of sea snake fauna on Australian reefs appear to be influenced by water depth, substrate type, and feeding strategies (McCosker, 1975; Heatwole, 1975b). Other biotic factors, such as limited juvenile dispersal, may also contribute to the observed patchy distributions (Lukoschek et al., 2007a). Overall, however, causative factors for observed distributions are not completely understood.

Population Abundance, Distribution, and Structure

There are no historical or current population estimates for the dusky sea snake. However, multiple reefs have been surveyed repeatedly, and although survey methodologies have varied, the data provide some indication of population trends for some locations. For Ashmore Reef in particular, the survey data provide a strong indication of severe population decline and possible extirpation. Older surveys dating from 1972 to 2002 by various researchers indicate that the relative abundance of A. fuscus was fairly consistent and represented about 10-23 percent of the sea snakes observed (see Table 1, Manning, 2014). A footnote in Smith (1926) also indicates that a sample of 27 dusky sea snakes (out of an ~100-specimen sea snake collection) had recently been collected for him at Ashmore Reef. The dusky sea snake, however, has not been recorded in a single survey conducted at Ashmore Reef after 2005, despite considerable effort (Lukoschek et al., 2013; Table 1, Manning, 2014). Based on reef area data reported in Skewes et al. (1999), Ashmore Reef represents about 40 percent of the dusky sea snake's historical reef habitat. Extirpation from this reef would represent a substantial change in the species' distribution and abundance.

A survey in 2005 at Hibernia Reef indicated a relatively low abundance of A. fuscus, and the most recent surveys, conducted in 2012 and 2013, have failed to detect any dusky sea snakes despite extensive survey effort (Guinea, 2005; Guinea, 2013). Dusky sea snakes were observed in surveys conducted at Scott Reef in 1972/73, 2006, 2012 and 2013; however, their relative abundance varies across the surveys, and no trends are detectable given the limited data (see Table 1, Manning, 2014). For example, Guinea (2012) visited Scott Reef in February, 2006, and reported that dusky sea snakes, as the third-most abundant species, made up 15 percent of the total sea snake sightings (Guinea, 2013). Portions of Scott Reef were surveyed again in 2012 and 2013, and dusky sea snakes made up only 3.2 percent and 7.4 percent of the total sightings respectively for each year (Guinea, 2013). At Seringapatam Reef and Cartier Island, A. fuscus is rare or potentially absent. Overall, while these limited abundance data are very difficult to interpret, they indicate that dusky sea snakes have not been present in high numbers in any recent reef surveys (Table 1, Manning, 2014).

The dusky sea snake has a restricted range, and structure and connectivity of populations is uncertain. Assuming that A. fuscus is extirpated from Ashmore Reef, Sanders et al. (2014) recently estimated that the dusky sea snake's range is now less than 262 sq km. Although structure and connectivity of reef populations of A. fuscus have not been studied directly, some information may be gleaned from several studies on the olive sea snake, A. laevis, a sympatric congener that is larger in size, more common, and more widely distributed than A. fuscus, but is very closely related to A. fuscus (Sanders et al., 2013b). As mentioned above, a short-term (6-9 days) tracking study on A. laevis suggests that adults of this species have small home ranges (1,500-1,800 sq m) and undergo limited active dispersal (Burns and Heatwole, 1998). Results of that study are somewhat supported by analyses by Lukoschek et al. (2007b) of mitochondrial DNA (mtDNA) from 354 olive sea snakes collected across its range, including some samples from Hibernia, Scott, and Start Printed Page 74960Ashmore reefs and Cartier Island. Based on their results, Lukoschek et al. (2007b) concluded that gene flow among the reefs of the Timor Sea is low, and that olive sea snakes at these reefs have been diverging for some time. A subsequent analysis of microsatellite DNA from the same specimens indicates that two of the most distant Timor reef populations of A. laevis are significantly diverged (Lukoschek et al., 2008). However, the degrees of divergence of other reef populations were not statistically significant, and there was no clear isolation-by-distance relationship (Lukoschek et al., 2008). Although not conclusive, the available information for the olive sea snake and the fact that dusky sea snakes also lack a dispersive larval phase, suggest connectivity of A. fuscus may be limited among some reefs within the region. Limited inter-population exchange would increase the extinction risk and reduce the recovery potential for local populations that have experienced severe declines or have been lost.

Summary of Factors Affecting the Dusky Sea Snake

Available information regarding current, historical, and potential threats to the dusky sea snake was thoroughly reviewed (Manning, 2014). Although causes for observed declines in dusky sea snake have not been conclusively determined, we found that the species is being threatened by hybridization. Other possible threats include vessels, pollution, climate change, and inadequate regulatory mechanisms. We summarize information regarding each of these threats below according to the factors specified in section 4(a)(1) of the ESA. Available information does not indicate that disease, predation, or overutilization (including bycatch) are operative threats on this species; therefore, we do not discuss those further here. See Manning (2014) for additional discussion of all ESA Section 4(a)(1) threat categories.

The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range

Aipysurus fuscus is dependent on coral reefs for prey and shelter, and loss of live coral is a possible mechanism contributing to the decline of A. fuscus at locations such as Ashmore Reef. Coral reefs of the Sahul Shelf experienced widespread bleaching in response to El Niño events in 1998 and 2003. Ashmore Reef experienced bleaching in 1998 and again, to an apparently greater extent, in 2003 (Lukoschek et al., 2013). However, because there are no estimates of coral coverage prior to 1998, the extent of coral loss following the 1998 event has not been quantified. Widespread mortality of corals was documented in response to the 2003 bleaching event, and average live coral coverage was reduced to 10 percent (Kospartov et al., 2006; as cited in Lukoschek et al., 2013). Surveys conducted in 2005 and 2009 indicated that recovery of corals at Ashmore Reef was rapid but delayed by about 7 years (Ceccarelli et al., 2011). Overall, there has been an eight-fold increase in hard coral coverage from 1998 to 2009 (Hale and Butcher, 2013), with all of the recorded recovery occurring after 2005. Meanwhile, survey data suggest complete loss of dusky sea snakes at Ashmore Reef after 2005. Existing survey data also show sharp declines in total sea snake abundance and species diversity at Ashmore Reef following both the 1998 and 2003 bleaching events (Lukoschek et al., 2013). These patterns are consistent with a hypothesis that loss of live corals affects reef-associated sea snakes.

The patterns at Ashmore Reef are contrasted, however, by those observed at Scott Reef. Following the 1998 bleaching event, a greater than 80 percent loss of hard and soft coral cover occurred, which translated into a reduction of live coral coverage to a total of roughly 10 percent (Smith et al., 2008). The 1998 El Niño event represents the most extreme temperature anomaly recorded for Scott Reef, and involved a rapid rise in water temperatures that remained above normal for two months (NOAA, 2013). Almost 6 years after the bleaching event (in 2004), the hard corals had partially recovered to 40 percent of their pre-bleaching cover, the soft corals showed no sign of recovery, and community composition of corals remained significantly altered (Smith et al., 2008). Within 12 years after the event (by 2010), coral cover, recruitment, community composition, and generic diversity were similar to pre-bleaching years (Gilmour et al., 2010). Several lesser disturbances, including two cyclones and the 2003 El Niño event, occurred during this time period and may have slowed the rate of recovery to some extent (Gilmour et al., 2013). Available sea snake survey data, spanning 1972-2013, with surveys in 1972-73, 2006, 2012, and 2013, do not appear to indicate a major decline in abundance of dusky sea snakes at Scott Reef, which were relatively common during the surveys conducted by Guinea (2012) in 2006. However, the temporal gaps in these survey data, especially from 1973 to 2006, could conceal shorter-term patterns.

A comprehensive understanding of the relationship between live coral cover and dusky sea snake abundance likely requires more detailed information regarding coral species composition, habitat complexity, and coral and prey fish resiliency relative to both the 1998 and 2003 bleaching events. Such an analysis might offer further insights into the differing response patterns at the two reefs, and an indication of whether sea snake abundance is driven by live coral coverage over timescales relevant to these disturbances. At this time, however, because a clear or consistent pattern does not emerge from the available data regarding dusky sea snake abundances at Ashmore and Scott reefs in relationship to these two bleaching events, we cannot conclude that loss of live coral is contributing to the decline of the dusky sea snake.

The reefs where dusky sea snakes are found lie more than several hundred kilometers offshore and thus enjoy a considerable degree of protection from human activities and land-based sources of pollution. Despite this remoteness, the reefs may experience some degradation as a result of vessel traffic. Anchor damage, pollution from contaminated bilge water, and marine debris are among the potential issues identified at Ashmore Reef, which experiences a relatively high level of traffic from Indonesian fishers, yachts, merchant ships, and illegal entry vessels (Whiting, 2000; Lukoschek et al., 2013). The mechanisms for and extent to which these boat-based habitat threats are impacting dusky or any other sea snake species of the Timor Sea reefs are unknown.

The extensive oil and gas industry activity in this region may also be a possible source of disturbance affecting dusky sea snakes and their habitat. Exploration and extraction activities within the Ashmore Platform began in 1968 (Geoscience Australia, 2012) and are expected to continue for some time, given the significant resources within this region. Ashmore Reef and Cartier Islands lie about 50-80 km west of the main offshore wells in the Timor Sea, and the closest exploration wells are 36 km away (Russell et al., 2004). However, Scott Reef lies directly above a significant portion of the Torosa Reservoir, where drilling for natural gas is expected to start by 2017. The development of the natural gas facility in this area will mean increased vessel traffic and potentially light, sound, and chemical pollution. The area is also expected to experience minor subsidence or compaction as the gas is removed (Woodside Energy LTD, 2013). Start Printed Page 74961Whether, and the degree to which, any of these threats or a combination of these threats will impact dusky sea snakes is not yet known.

Unfortunately, extremely limited information also exists regarding the toxic effects of oil exposure on sea snakes. Oil spills, which occur more frequently as a result of vessel or pipeline incidents rather than exploration and drilling activities (, have also not occurred very often in this region. Some information is available from the August 2009 explosion of the West Atlas oil rig on the Montara Well, which leaked oil and gas uncontrollably into the Timor Sea for 74 days until the well was finally capped in November 2009. Considered one of the worst oil-related spills to have ever occurred in Australia, the Montara leak was analogous in nature to the Deepwater Horizon disaster of April 2010 in the Gulf of Mexico. In an effort to rapidly assess impacts to multiple taxa, Watson et al. (2009) conducted ship-based transect surveys in areas around the Atlas drilling platform in September 2009. They did not observe or identify any dusky sea snakes; however, they did observe “lethargic sea snakes lying in thick oil (i.e., not moving much when approached, unable to dive)” and collected a dead horned sea snake (Acalyptophis peronii) from oil-affected waters for further analysis (Watson et al., 2009). The necropsy report indicated that this snake was in good physical condition, with no visible external or internal pathologies, and no oil was detected in swab samples of the skin (Gagnon and Rawson, 2010). Chemical analysis of tissues clearly indicated that exposure to crude oil occurred through ingestion of prey and not through inhalation (Gagnon and Rawson, 2010). Acalyptophis peronii is considered more of a diet specialist than the dusky sea snake and primarily consumes burrowing gobies (McCosker, 1975; Voris and Voris, 1983). Because they saw no physical damage to the gut structure and no contamination of the tissues, Gagnon and Rawson (2010) concluded it was unlikely that oil ingestion was the primary cause of death. Tests for presence of chemical dispersants used during the spill-response were not conducted.

A necropsy was also performed on a dead sea snake landed by a commercial fisherman operating in the vicinity of the West Atlas spill on September 14, 2009 (Gagnon, 2009). This specimen was identified as Hydrophis elegans, which is a relatively widespread and abundant species that preys on eels and other fishes (McCosker, 1975; Voris and Voris, 1983). The necropsy indicated that the snake had fed recently and that the stomach contents were contaminated with oil (Gagnon, 2009). Relatively high levels of polycyclic aromatic hydrocarbons were also detected in the lungs, trachea, and muscle tissue (Gagnon, 2009). Neither of two dispersant chemicals used to treat the spill were detected in lung samples (Gagnon, 2009). The necropsy report concluded that the likely cause of death for this specimen was exposure to petroleum hydrocarbons (Gagnon, 2009).

In 2012 and 2013, Guinea (2013) conducted surveys to evaluate the potential impacts of the Montara leak on species of marine reptiles. Potentially impacted areas surveyed included Ashmore Reef, Cartier Island, and Hibernia Reef; Scott and Seringapatam reefs were surveyed as control reefs (Guinea, 2013). Ashmore Reef and Cartier Island are 167 km west-north-west and 108 km west from the Montara well, respectively. Seringapatam and Scott reefs are several hundred km south-east of the Montara well and far from modeled oil trajectories (Guinea, 2013). The extensive survey efforts of Guinea (2013) did not indicate any impact of the hydrocarbon release on marine reptiles (sea turtles and sea snakes) of the potentially affected reefs. Of the reefs surveyed, Hibernia Reef and Cartier Island had the highest sea snake density; however, no sea snakes were observed at Ashmore Reef, where sea snake abundance and diversity had already declined to very low levels prior to the 2009 incident (Guinea, 2013). Overall, these data suggest that while there are likely to be acute impacts to sea snakes in response to major spills, it is unlikely that pollution stemming from oil and gas industry activities has contributed to the observed declines of the dusky sea snake.

Overall, based on the existing information, we conclude that there is a low likelihood that these habitat-related threats have contributed to the observed decline of the dusky sea snake. At this time, there is insufficient information to indicate whether and how the dusky sea snake will be affected by these habitat issues in the future. We do expect that each of the various habitat-related issues summarized above will continue well into the future, and some may worsen. Given that El Niño and its associated warming of equatorial Pacific Ocean waters is a natural and reoccurring climate phenomenon, coral bleaching in response to sufficiently strong El Niño events will continue. Furthermore, because climate warming as a consequence of carbon dioxide emissions is expected to continue (IPCC, 2013), and elevated sea surface temperatures are expected to rise at an accelerated rate (Lough et al., 2012), loss of corals through bleaching events is expected to increase. The expansion of Australia's oil and gas exploration and extraction in the Timor Sea may also result in an increased risk of oil spills and additional habitat threats for dusky sea snakes.

Inadequacy of Existing Regulatory Mechanisms

The dusky sea snake and its habitat receive a significant degree of regulatory protections. The largest potential gap in existing regulatory mechanism may be for threats related to climate change. Oil spills, while rare and unpredictable, and other oil and gas industry activities may also pose threats to the species as a consequence of inadequate management and regulation. We summarize the avail