Endangered and Threatened Species; Identification and Proposed Listing of Eleven Distinct Population Segments of Green Sea Turtles (Chelonia mydas) as Endangered or Threatened and Revision of Current Listings
A. Discussion of Population Parameters for the North Atlantic DPS
The range of the North Atlantic DPS extends from the boundary of South and Central America north along the coast to the northern extent of the green turtle’s range to include Panama, Costa Rica, Nicaragua, Honduras, Belize, Mexico, and the United States. It then extends due east across the Atlantic Ocean at 48° N.; follows the coast south to include the northern portion of the Islamic Republic of Mauritania (Mauritania; to 19° N.) on the African continent; and west along the 19° N. latitude to the Caribbean basin, turning south and west at 63.5° W., 19° N., and due south at 7.5° N., 77° W. to the boundary of South and Central to include Puerto Rico, the Bahamas, Cuba, Turks and Caicos Islands, Republic of Haiti (Haiti), Dominican Republic, Cayman Islands, and Jamaica. The North Atlantic DPS includes the Florida breeding population, which was originally listed as endangered (43 FR 32800, July 28, 1978). Critical habitat was previously designated for areas within the range of this DPS (i.e., coastal waters surrounding Culebra Island, Puerto Rico; 63 FR 46693, September 2, 1998).
Green turtle nesting sites in the North Atlantic are some of the most studied in the world, with time series exceeding 40 years in Costa Rica and 35 years in Florida. Seventy-three nesting sites were identified within the North Atlantic DPS, although some represent numerous individual beaches. For instance, Florida nesting beaches were listed by county with the numerous beaches in each county representing one site and, for other U.S. beaches (from Texas to North Carolina), each state’s nesting beaches were represented as one site. There are four regions that support high density nesting concentrations for which data were available: Tortuguero, Costa Rica; Mexico (Campeche, Yucatan, and Quintana Roo); Florida, United States; and Cuba. There is one nesting site with 100,000 nesting females (Tortuguero at 131,751; Chaloupka et al., 2008a; Sea Turtle Conservancy, 2013), one with 10,001-100,000 (Quintana Roo, Mexico at 18,257; Julio Zurita, pers. comm. 2012) and six with 1,001-5,000: Cayo Largo, Cuba; Campeche, Yucatan, and Veracruz, Mexico; and Brevard and Palm Beach Counties, FL, United States. There are four with 501-1,000; Tamaulipas, Mexico; Vieques, Puerto Rico; Martin and Indian River Counties, FL, United States; nine with 101-500; 26 with 50; and 26 with numbers unquantified. Seventy-nine percent of the nesting turtles in this DPS nest at Tortuguero.
Of the nesting sites with long-term data sets, both Tortuguero and the index beaches in Florida exhibit a strong positive trend in the PVAs that were conducted on them, as does Isla Aguada, Mexico (one beach in the Campeche group). Three beaches in Cuba (total of 489 nesting females) either showed no trend or a modest positive trend. One beach in Mexico (El Cuyo, Yucatan) exhibited no trend.
Genetic sampling in the North Atlantic DPS has been generally extensive with good coverage of large populations in this region; however, some smaller Caribbean nesting sites are absent and coastal nesting sites in the Gulf of Mexico are under-represented. Genetic differentiation based on mtDNA indicated that there are at least four independent nesting subpopulations in the North Atlantic DPS characterized by shallow regional substructuring: (1) Florida (Hutchinson Island; Lahanas et al., 1994), (2) Cuba (Guanahacabibes Península and Cayería San Felipe; Ruiz-Urquiola et al., 2010), (3) Mexico (Quintana Roo; Encalada et al., 1996), and (4) Costa Rica (Tortuguero; Lahanas et al., 1994). These nesting sites are characterized by common and widespread haplotypes dominated by CM-A1 and/or CM-A3. A relatively low level of spatial structure is detected due to shared common haplotypes, although there are some rare/unique haplotypes at some nesting sites. Connectivity may indicate recent shared common ancestry.
Green turtles nest on both continental and island beaches throughout the range of the DPS (Witherington et al., 2006). Major nesting
sites are primarily continental with hundreds of lower density sites scattered throughout the Caribbean. Green turtles nesting in Florida seem to prefer barrier island beaches that receive high wave energy and that have coarse sands, steep slopes, and prominent foredunes. The greatest nesting is on sparsely developed beaches that have minimal levels of artificial lighting. A high-low nesting pattern for Florida and Mexico occurs during the same years; however, nesting in Tortuguero, Costa Rica is not always in sync with Florida and Mexico (e.g., 2011 was a high nesting year in Florida, but for Tortuguero the high nesting year was 2010). The nesting season is similar throughout the range of the DPS, with green turtles nesting from June to November in Costa Rica (Bjorndal et al., 1999), and May through September in the United States, Mexico, and Cuba (Witherington et al., 2006).
B. Summary of Factors Affecting the North Atlantic DPS
1. Factor A: The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range
a. Terrestrial Zone
Within the range of the North Atlantic DPS, nesting beaches continue to be degraded from a variety of activities. Destruction and modification of green turtle nesting habitat results from coastal development, coastal armoring, beachfront lighting, erosion, sand extraction, and vehicle and pedestrian traffic on nesting beaches (Witherington and Bjorndal, 1991; Witherington, 1992; Witherington et al., 1996; Lutcavage et al., 1997; Bouchard et al., 1998; Mosier, 1998; Witherington and Koeppel, 2000; Mosier and Witherington, 2002; Leong et al., 2003; Roberts and Ehrhart, 2007). In addition, sea level rise resulting from climate change poses a threat to all nesting beaches. Portions of the Southern United States and Caribbean are found be to highly vulnerable to sea level rise (Melillo et al., 2014). For instance, along the southern portion of the Florida coastline, one climate change model predicted one meter of sea level rise by 2060, resulting in the inundation of more than 50 percent of coastal wildlife refuges (Flaxman and Vargas-Moreno, 2011). Most green turtle nesting in the United States is concentrated along the southeastern coast of Florida with more than 90 percent of nesting occurring from Brevard to Broward counties (http://ocean.floridamarine.org/SeaTurtle/nesting/FlexViewer/). Loss of nesting habitat as a result of sea level rise poses a threat to the population. Sea level rise is exacerbated by coastal development and armoring, which prevents the beach from migrating and causes nesting green turtles to abandon their nesting attempts more frequently as a result of their encounter with such structures (Mosier, 1998; Mosier and Witherington, 2000; Rizkalla and Savage, 2011). Females might nest in sub-optimal habitats, where nests are more vulnerable to erosion or inundation (Rizkalla and Savage 2011). As a result, nests would be subject to more frequent inundation, exacerbated erosion, and increased moisture from tidal overwash, which can potentially alter thermal regimes, an important factor in determining the s*x ratio of hatchlings.
b. Neritic/Oceanic Zones
Green turtles in the post-hatchling and early-juvenile stages are closely associated with Sargassum algae in the Atlantic and Gulf of Mexico (Witherington et al., 2012), and vulnerable to ingesting contaminants such as tar balls and plastics that aggregate in convergent zones where Sargassum aggregates (Witherington, 2002). Juvenile and adult green turtles and their nearshore foraging habitats are also exposed to high levels of pollutants, such as agricultural and residential runoff, and sewage which result in degraded foraging habitat (Smith et al., 1992). Further, increased nutrient load in these coastal waters causes eutrophication. Eutrophication is linked to harmful algal blooms that result in the loss and degradation of seagrass beds, and possibly fibropapilloma tumors in green turtles (Milton and Lutz, 2003).
In Cuba, Jamaica, Puerto Rico, and Panama, water quality is also affected by sewage and industrial and agricultural runoff. Pollution remains a major threat in the waters of Jamaica. Major sources of pollution are industrial and agricultural effluent, garbage dumps and solid waste, and household sewage (Greenway, 1977; Green and Webber, 2003).
Nearshore foraging habitats such as seagrass beds are affected by propeller scarring, anchor damage, dredging, sand mining, and marina construction throughout the range of the DPS (Smith et al., 1992; Dow et al., 2007; Patrício et al., 2011). Sand placement projects along the Florida coastline affect nearshore reefs as a result of direct burial of portions of the reef habitat and loss of food sources available to green turtles (Lindeman and Snyder, 1999).
The SRT found, and we concur, that the North Atlantic DPS of the green turtle is negatively affected by ongoing changes in both its terrestrial and marine habitats as a result of land and water use practices as considered above in Factor A. The increasing threats to the terrestrial and marine habitats are not reflected in the current trend for the North Atlantic DPS, as it was based on nesting numbers and not on all current life stages. These increasing threats to the population will become apparent when those life stages affected by the threats return to nest, as the trend information is based solely on numbers of nests. This lag time was considered in our analysis. For example, a threat that affects the oceanic juvenile phase would not be detected until those turtles return to nest, approximately 15 to 20 years later. The SRT also found, and we concur, that coastal development, beachfront lighting, erosion, sand extraction, and sea level rise increasingly impact nesting beaches of this DPS and are increasing threats to the DPS.
2. Factor B: Overutilization for Commercial, Recreational, Scientific, or Educational Purposes
A partial list of the countries within the range of the North Atlantic DPS where ongoing intentional capture of green turtles occurs, includes Costa Rica (Mangel and Troëng, 2001; Gonzalez Prieto and Harrison, 2012), Mexico (Seminoff, 2000; Gardner and Nichols, 2001; Dirado et al., 2002; Guzmán-Hernández and García Alvarado, 2011), Cuba (Fleming, 2001; F. Moncado, Ministerio de la Industria Pesquera, pers. comm., 2013), Nicaragua (Lagueux, 1998; Humber et al., 2014), the Bahamas (Fleming, 2001), Jamaica (Haynes-Sutton et al., 2011), and the Cayman Islands (Fleming, 2001). Harvest remains legal in several of these countries (Humphrey and Salm, 1996; Wamukoya et al., 1996; Fleming, 2001; Fretey, 2001; Bräutigam and Eckert, 2006).
The commercial artisanal green turtle fishery in Nicaragua continues to be a threat to the Tortuguero nesting population, the largest remaining green turtle population in the Atlantic (Campbell and Lagueux, 2005). Local demand for turtle meat in coastal communities continues (Garland and Carthy, 2010). There is a legal turtle fishery on the Caribbean coast that is located in the most important developmental and foraging habitat for Caribbean green turtles (Fleming, 2001; Campbell and Lagueux, 2005). The hunting of juvenile and adult turtles continues both legally and illegally in many foraging areas where green turtles originating from Florida nesting beaches are known to occur (Chacón, 2002; Fleming, 2001).
Direct take of eggs is also an ongoing threat in Panama (Evans and Vargas, 1998). Green turtles nesting on Belize’s beaches and foraging along its coast are harvested in the Robinson Point area and sold in markets and restaurants (Searle, 2003). Large numbers of green turtles are captured in the area southeast of Belize, an area which may be an important migratory corridor (Searle, 2004). There are important feeding grounds in the Banc d’Arguin, Mauritania. While the frequency of green turtle nesting in Mauritania is not known, green turtle nests are reported as being harvested there (Fretey, 2001; Fretey and Hama, 2012).
Commercial harvest of green turtles was a factor that contributed to the historic decline of this DPS. Current harvest of green turtles and eggs, in a portion of this DPS, continues to be significant threat to the persistence of this DPS.
3. Factor C: Disease or Predation
Fibropapillomatosis (FP) has been found in green turtle populations in the United States (Hirama, 2001; Ene et al., 2005; Foley et al., 2005; Hirama and Ehrhart, 2007), the Bahamas, the Dominican Republic, Puerto Rico (Dow et al., 2007; Patrício et al., 2011), Cayman Islands (Wood and Wood, 1994; Dow et al., 2007), Costa Rica (Tortuguero; Mangel and Troëng, 2001), Cuba (Moncada and Prieto, 2000), Mexico (Yucatan Peninsula; K. Lopez, pers. comm., as cited in MTSG, 2004), and Nicaragua (Lagueux, 1998).
FP continues to be a major problem in some lagoon systems and along the nearshore reefs of Florida. It is a chronic, often lethal disease occurring predominantly in green turtles (Van Houtan et al., 2014). A correlation appeared to exist between these degraded habitats and the prevalence of FP in the green turtles that forage in these areas but no direct link was established (Aguirre and Lutz, 2004; Foley et al., 2005). Indeed, across green turtle populations, it is widely observed that FP occurs most frequently in eutrophied and otherwise impaired waterways (Herbst, 1994; Van Houtan et al., 2010). A recent study establishes that eutrophication substantially increases the nitrogen content of macroalgae, thereby promoting the latent herpes virus which causes FP tumors in green turtles (Van Houtan et al., 2014) although it is argued that there is no inferential framework to base this conclusion (Work et al., 2014). Despite the high incidence of FP among foraging populations, there is no conclusive evidence on the effect of FP on reproductive success (Chaloupka and Balazs, 2005).
Harmful algal blooms, such as a red tide, also affect green turtles in the North Atlantic DPS. In Florida, the species that causes most red tides is Karenia brevis, a dinoflagellate that produces a toxin (Redlow et al., 2002). Since 2007, there were two red tide events, one in 2007 along the east coast of Florida, and one in 2012 along the west coast of Florida. Sea turtle stranding trends indicated that these events were acting as a mortality factor (A. Foley, Florida Fish and Wildlife Conservation Commission, pers. comm., 2013). These events may impact a population’s present and future reproductive status.
Predators such as raccoons (Procyon lotor), feral hogs (Sus scrofa), foxes (Urocyon cinereoargenteus and Vulpes vulpes), and coyotes (Canis latrans) may take significant numbers of turtle eggs (Stancyk, 1982; Allen et al., 2001). Nest protection programs are in place at most of the major nesting beaches in the North Atlantic DPS, although they are managed at varying levels and degrees of effectiveness (Engeman et al., 2005). Predator species that are particularly difficult to manage include red fire ants (Solenopsis invicta) and jaguars (Panthera onca) (Wetterer, 2006; Prieto and Harrison, 2012).
Although FP disease is of major concern, with increasing levels in some green turtle populations in this DPS, it should be noted there is uncertainty of the long-term survivability and effect on the reproductive effort of the population. Predation is known to occur throughout this DPS, and we find it to be a significant threat to this DPS in the absence of well managed nest protection programs.
4. Factor D: Inadequacy of Existing Regulatory Mechanisms
At least 15 regulatory mechanisms that apply to green turtles regionally (e.g., U.S. Magnuson-Stevens Fishery Conservation and Management Act) or globally (e.g., Convention on International Trade in Endangered Species of Wild Fauna and Flora) apply to green turtles within the North Atlantic Ocean. The analysis of these existing regulatory mechanisms assumed that all would remain in place at their current levels.
In the United States, regulatory mechanisms that protect green turtles are in place and include State, Federal, and international laws. The green turtle was listed under the ESA in 1978, providing relatively comprehensive protection and recovery activities to minimize the threats to green turtles in the United States. Considering the dependence of the species on conservation efforts, significant concerns remain regarding the inadequacy of regulatory mechanisms. The development and implementation of Turtle Excluder Devices (TEDs) in the shrimp trawl fishery was likely the most significant conservation accomplishment for North Atlantic green turtles in the marine environment since their 1978 ESA listing. In the southeast United States and Gulf of Mexico, TEDs have been mandatory in shrimp and flounder trawls for over a decade. These regulations are implemented and enforced to varying degrees throughout the Gulf and U.S. Southeast Atlantic. For example, the State of Louisiana prohibits enforcement of TED regulations and tow time limits. In other States, enforcement of TED regulations depends on available resources, and illegal or improperly installed TEDs continue to contribute to mortality of green turtles. Further, TEDs are not required in all trawl fisheries, and green turtle mortality continues in the Gulf of Mexico, where shrimp trawling is the highest (Lewison et al., 2014). There are also regulatory mechanisms in place that address the loss of nesting habitat, such as the Florida Administrative Code Rule 62B-33.0155, which addresses threats from armoring structures. However, these regulatory mechanisms allow for variances and armoring permits continue to be issued along nesting beaches.
Other threats, such as light pollution on nesting beaches, marine debris, vessel strikes, and continued direct harvest of green turtles in places like Nicaragua, are being addressed to some extent by regulatory mechanisms, although they remain a problem. In addition, other regional and national legislation to conserve green turtles (often all sea turtles) exists throughout the range of the DPS. The extent to which threats have been reduced as a result of these efforts is difficult to ascertain. When the SRT assessed conservation efforts, it assumed that all conservation efforts would remain in place at their current levels. The following countries have laws to protect green turtles: The Bahamas, Belize, Bermuda, Canary Islands, Cayman Islands, Costa Rica, Cuba, Dominican Republic, Guatemala, Haiti, Honduras, Jamaica, Mauritania, Mexico, Nicaragua, Panama, and the United States (including the commonwealth of Puerto Rico).
With regard to the United States, the key law currently protecting green turtles is the ESA. This law has been instrumental in conserving sea turtles, eliminating directed take of turtles in U.S. waters unless authorized by permit and reducing indirect take. In addition, the Magnuson-Stevens Fishery Management and Conservation Act has been effective at mandating responsible fishing practices and bycatch mitigation within fleets that sell fisheries products to the United States, and the Marine Turtle Conservation Act authorizes a dedicated fund to support marine turtle conservation projects in foreign countries, with emphasis on protecting nesting populations and nesting habitat. In addition, at least 12 international treaties and/or regulatory mechanisms apply to the conservation of green turtles in the North Atlantic DPS.
Outside of the United States, there are some national regulations that address the harvest of green turtles as well as the import and export of turtle parts. These regulations allow for the harvest of green turtles of certain sizes, months, or for “traditional” use. Gear restrictions and TED requirements exist in a few countries, although the compliance level is unknown. Our Status Review did not reveal regulatory mechanisms in place to specifically address marine pollution, sea level rise, and other effects of climate change that continue to contribute to the extinction risk of this DPS.
5. Factor E: Other Natural or Manmade Factors Affecting Its Continued Existence
a. Incidental Bycatch in Fishing Gear
Fisheries bycatch in artisanal and industrial fishing gear continues to be a major threat to green turtles in the North Atlantic DPS. The adverse impacts of bycatch on sea turtles has been documented in marine environments throughout the world (National Research Council, 1990b; Epperly, 2003; Lutcavage et al., 1997). The lack of comprehensive and effective monitoring and bycatch reduction efforts in many pelagic and near-shore fisheries operations throughout the range of the North Atlantic DPS still allows substantial direct and indirect mortality (NMFS and USFWS, 2007).
i. Gill Net and Trawl Fisheries
Gill net fisheries may be the most ubiquitous of fisheries operating in the neritic range of the North Atlantic DPS. In the United States, some states (e.g., South Carolina, Georgia, Florida, Louisiana, and Texas) have prohibited gill nets in their waters, but there remain active gill net fisheries in other U.S. states, in U.S. Federal waters, Mexican waters, Central and South America, and the Northeast Atlantic. Finfish fisheries accounted for the greatest proportion of turtle bycatch (53 percent) in Cuba. In Jamaica, fish traps and gill nets are the gear primarily identified in sea turtle bycatch. Purse seine and gill nets are used commonly in the waters of the Dominican Republic (Dow et al., 2007). In Costa Rica, gill nets, hook and line, and trawls are the main gear types deployed (Food and Agriculture Organization of the United Nations, 2004). Shark-netting operations in Panama are known to capture green turtles (Meylan et al., 2013).
The development and implementation of TEDs in the U.S. shrimp trawl fishery was likely the most significant conservation accomplishment for North Atlantic green turtles in the marine environment since their 1978 ESA listing. In the southeast United States and Gulf of Mexico, TEDs have been mandatory in shrimp and flounder trawls for over a decade. However, compliance varies throughout the States, and green turtle mortality continues in the Gulf of Mexico, where shrimp trawling is the highest (Lewison et al., 2014). With the current regulations in place, an estimated 3,000 green turtles are captured (1,400 killed) by shrimp trawls each year in the Gulf and U.S. Southeast Atlantic (http://sero.nmfs.noaa.gov/protected_resources/section_7/freq_biop/documents/fisheries_bo/shrimp_biop_2014.pdf). These regulations are implemented and enforced to varying degrees throughout the Gulf and U.S. Southeast Atlantic (see discussion in Factor D).
ii. Dredge Fishing
Dredge fishing gear is the predominant gear used to harvest sea scallops off the mid- and northeastern U.S. Atlantic coast. Sea scallop dredges are composed of a heavy steel frame and cutting bar located on the bottom part of the frame and a bag made of metal rings and mesh twine attached to the frame. Turtles can be struck and injured or killed by the dredge frame and/or captured in the bag, where they may drown or be further injured or killed when the catch and heavy gear are dumped on the vessel deck.
b. Channel Dredging
In addition to the destruction or degradation of habitat as described in Factor A above, periodic dredging of sediments from navigational channels can also result in incidental mortality of sea turtles. Direct injury or mortality of green turtles by dredges has been well documented in the southeastern and mid-Atlantic U.S. (National Research Council, 1990b). From 1980 to 2013, 105 green turtles were impacted as a result of dredging operations in the U.S Atlantic and Gulf of Mexico. Solutions, including modification of dredges, have been successfully implemented to reduce mortalities and injuries to sea turtles in the United States (73 FR 18984, April 8, 2008; 77 FR 20728, April 6, 2012), and NMFS imposes annual take limits based on the expected number of green turtles impacted that will not, directly or indirectly, appreciably reduce the likelihood of survival and recovery of the green turtle in the wild.
c. Vessel Strikes and Boat Traffic
Boat strikes have been shown to be a major mortality source in Florida (Singel et al., 2003). Vessel strikes are a growing concern and, as human populations increase in coastal areas, vessel strikes are likely to increase (NMFS and FWS, 2008). From 2005 to 2009, 18.2 percent of all stranded green turtles (695 of 3,818) in the U.S. Atlantic (Northeast, Southeast, and Gulf of Mexico) were documented as having sustained some type of propeller or collision injuries (L. Belskis, NMFS, pers. comm., 2013). It is quite likely that this is a chronic, albeit unreported, problem near developed coastlines in other areas as well, such as Panama (e.g., Orós et al., 2005).
d. Effects of Climate Change and Natural Disasters
While sea turtles have survived past eras that have included significant temperature fluctuations, future climate change is expected to happen at unprecedented rates, and if turtles cannot adapt quickly, they may face local to widespread extirpations (Hawkes et al., 2009). Climate change and sea level rise have the potential to affect green turtles significantly in the North Atlantic DPS. North Atlantic turtle populations could be affected by the alteration of thermal sand characteristics of beaches (from warming temperatures), resulting in the reduction or cessation of male hatchling production (Hawkes et al., 2009; Poloczanska et al., 2009). Increased sea surface temperatures may alter the timing of nesting for some stocks (Weishampel et al., 2004), although the implications of changes in nesting timing are unclear. Changes in sea temperatures will also likely alter seagrass, macroalgae, and invertebrate populations in coastal habitats in many regions (Scavia et al., 2002). Further, a significant rise in sea level, as is projected for areas within the range of the North Atlantic DPS (Flaxman and Vargas-Moreno, 2011), could significantly restrict green turtle nesting habitat due to coastal development. Structures on the landward side of the beach can effectively prevent access to nesting habitat and reduce available nesting habitat (Mosier, 1998). The increasing interaction between the structures and the hydrodynamics of tide and current, due to sea level rise, often results in the alteration of the beach profile seaward and in the immediate vicinity of the structure (Pilkey and Wright, 1988; Terchunian, 1988; Tait and Griggs, 1990; Plant and Griggs, 1992), increased longshore currents that move sand away from the area, loss of interaction between the dune and the beach berm, and concentration of wave energy at the ends of the structure (Schroeder and Mosier, 1996). Impacts from global climate change induced by human activities are likely to become more apparent in future years (IPCC, 2007).
Periodic hurricanes and other weather events are generally localized and rarely result in whole-scale losses over multiple nesting seasons. However, storm intensity and frequency are predicted to increase as a result of climate change (Melillo et al., 2014). The negative effects of hurricanes on low-lying and/or developed shorelines may be longer-lasting and a greater threat to the DPS overall when combined with the effects of climate change, and particularly sea level rise.
e. Effects of Cold Stunning
Cold stunning is the hypothermic reaction that occurs when sea turtles are exposed to prolonged cold water temperatures. Cold stunning of green turtles regularly occurs at several locations in the United States, including Cape Cod Bay, Massachusetts (Still et al., 2002); Long Island Sound, New York (Meylan and Sadove, 1986; Morreale et al., 1992); the Indian River Lagoon system and the panhandle of Florida (Mendonça and Ehrhart, 1982; Witherington and Ehrhart, 1989; Foley et al., 2007); and Texas inshore waters (Hildebrand, 1982; Shaver, 1990). Cold-stunning events at these foraging areas (Witherington and Ehrhart, 1989; McMichael et al., 2006) leads to mortality of juvenile and adult green turtles, which may affect the present and future green turtle population trend.
f. Contaminants and Marine Debris
Several activities associated with offshore oil and gas production, including oil spills, operational discharge, seismic surveys, explosive platform removal, platform lighting, and drilling and production activities, are known to affect sea turtles (National Research Council, 1996; Davis et al., 2000; Viada et al., 2008; Conant et al., 2009; G. Gitschlag, NMFS, pers. comm., 2007, as cited in Conant et al., 2009). Oil spills near nesting beaches just prior to or during the nesting season place nesting females, incubating egg clutches, and hatchlings at significant risk from direct exposure to contaminants (Fritts and McGehee, 1982; Lutcavage et al., 1997; Witherington, 1999), and have negative impacts on nesting habitat. The Deepwater Horizon (Mississippi Canyon 252) oil spill, which started April 20, 2010, discharged oil into the Gulf of Mexico through July 15, 2010. Witherington et al. (2012) note that the Deepwater Horizon oil spill was particularly harmful to pelagic juvenile green turtles. Due to their size, turtles in these stages are more vulnerable as a result of ingesting contaminants (Witherington, 2002).
Green turtles are affected by anthropogenic marine debris (including discarded fishing gear) and plastics throughout the North Atlantic DPS. Juvenile green turtles in pelagic waters are particularly susceptible to these effects as they feed on Sargassum in which there is a high occurrence of debris (Wabnitz and Nichols, 2010; Witherington et al., 2012). In recent decades, there has been an increase in stranded green turtles reported as affected by discarded fishery gear throughout the southeastern United States (Teas and Witzell, 1996; Adimey et al., 2014).
C. Conservation Efforts for the North Atlantic DPS
In the North Atlantic, nest protection efforts have been implemented on two major green turtle nesting beaches, Tortuguero National Park in Costa Rica and Florida, and progress has been made in reducing mortality from human-related impacts on other nesting beaches. Tortuguero National Park was established in 1976 to protect the nesting turtles and habitat at this nesting beach, which is by far the largest in the DPS and the western hemisphere. Since that time, the harvest of nesting turtles on the beach has been reduced by an order of magnitude (Bjorndal et al., 1999). At Tortuguero, Sea Turtle Conservancy researchers and volunteers regularly monitor green turtle nesting trends, growth rates and reproductive success, and also conduct sea turtle lighting surveys, education, and community outreach.
In Florida, a key effort was the acquisition of the Archie Carr National Wildlife Refuge in Florida in 1991 by Federal, State, Brevard and Indian River counties, and a non-governmental organization, where nesting densities range from 36 nests/km (22 nests/mi) to 262 nests/km (419 nests/mi) (D. Bagley, University of Central Florida, pers. comm., 2014; K. Kneifl, USFWS, pers. comm., 2014). Over 60 percent of the available beachfront acquisitions for the Refuge have been completed as the result of a multi-agency land acquisition effort. In addition, Hobe Sound National Wildlife Refuge, as well as coastal national seashores such as the Dry Tortugas National Park and Canaveral National Seashore, military installations such as Patrick Air Force Base and Canaveral Air Force Station, and State parks where green turtles regularly nest, provide protection for nesting turtles. However, despite these efforts, alteration of the coastline continues and, outside of publicly-owned lands, coastal development and associated coastal armoring remain serious threats.
Considerable effort has been expended since the 1980s to document and reduce commercial fishing bycatch mortality. In the Atlantic and Gulf of Mexico, measures (such as gear modifications, changes to fishing practices, and time/area closures) are required to reduce sea turtle bycatch in pelagic longline, mid-Atlantic gill net, Virginia pound net, scallop dredge, and southeast shrimp and flounder trawl fisheries. However, enforcement of regulations depends on available resources, and bycatch continues to contribute to mortality. Since 1989, the United States has prohibited the importation of shrimp harvested in a manner that adversely affects sea turtles.
As a result of conservation efforts, many of the intentional impacts directed at sea turtles have been lessened. For example, harvest of eggs and adults has been reduced at several nesting areas, including Tortuguero, and an increasing number of community-based initiatives are in place to reduce the take of turtles in foraging areas. However, despite these advances, human impacts continue throughout the North Atlantic. The lack of effective monitoring in pelagic and near-shore fisheries operations still allows substantial direct and indirect mortality, and the uncontrolled development of coastal and marine habitats threatens to destroy the supporting ecosystems of long-lived green turtles.
D. Extinction Risk Assessment and Findings for the North Atlantic DPS
In the North Atlantic DPS, there are several regions that support high density nesting concentrations, including possibly the largest in the world at Tortuguero, Costa Rica. Green turtle nesting population trends have been encouraging, exhibiting long-term increases at all major nesting sites, including Tortuguero (Troëng, 1998; Campbell and Lagueux, 2005; Troëng and Rankin, 2005) and Florida (Chaloupka et al., 2008; B. Witherington, Florida Fish and Wildlife Conservation Commission, pers. comm., 2013). The North Atlantic DPS is characterized by geographically widespread nesting at a diversity of sites, both mainland and insular. The increasing threats are not reflected in the current trend for the North Atlantic DPS as it was based on nesting numbers and not all current life stages. These increasing threats to the population will become apparent when those life stages affected by the threats return to nest as the trend information is based solely on numbers of nests. This lag time was considered in our analysis. However, the 5-factor (section 4(a)(1) of the ESA) analysis revealed continuing threats to green turtles and their habitat that affect all life stages.
On nesting beaches, many portions of the DPS continue to be exposed to, and are negatively impacted by, coastal development and associated beachfront lighting, coastal armoring, and erosion as described in Factor A above. Impacts from such development are further exacerbated by existing and planned shoreline development and shoreline engineering. The current and anticipated increase in armored shoreline along high density nesting beaches, particularly in Florida, is a substantial unresolved threat to the recovery and stability of this DPS as it will result in the permanent loss of nesting habitat.
Nests and hatchlings are susceptible to predation which is prevalent throughout the beaches within the range of the North Atlantic DPS. Predation would be an increasing threat without nest protection and predatory control programs in place.
Nesting beaches are also extremely susceptible to sea level rise, which will exacerbate some of the issues described above in addition to leading to the potential loss of nesting beaches. Along the southeastern United States, one climate change model predicted a 1-meter sea level rise by 2060, resulting in the inundation of more than 50 percent of coastal wildlife refuges (Flaxman and Vargas-Moreno, 2011). Green turtle nesting in Florida is concentrated along coastal wildlife refuges in southern Florida such as Hobe Sound National Wildlife Refuge and the Archie Carr National Wildlife Refuge, with more than 90 percent of nesting occurring along southeast Florida. This increase in sea level will result in the permanent loss of current green turtle nesting habitat. Loss of beach is expected to be worse as a result of the increase in hurricane frequency and intensity (Flaxman and Vargas-Moreno, 2011). The increasing threat of coastal erosion due to climate change and sea level rise is expected to be exacerbated by increasing human-induced pressures on coastal areas (IPCC, 2007).
In the water, fisheries bycatch, habitat degradation, direct harvest, and FP are major threats to green turtles in the North Atlantic DPS. Artisanal and industrial fishing gear, including drift nets, set nets, pound nets, and trawls, still cause substantial direct and indirect mortality of green turtles (NMFS and USFWS, 2007). In addition, degradation and loss of foraging habitat due to pollution, including agricultural and residential runoff, anchor damage, dredging, channelization, and marina construction remains a threat to both juvenile and adult green turtles. Many green turtles in this DPS remain susceptible to direct harvesting. Current legal and illegal harvest of green turtles and eggs for human consumption continues in the eastern Atlantic and the Caribbean. A remaining threat is the directed harvest of turtles in Nicaragua that nest at Tortuguero and thus belong to the largest and arguably the most important population within the DPS (although this population continues to increase in spite of the harvest). However, potential degradation or loss of other, smaller populations is also of concern, as these contribute to the diversity and resilience of the DPS. Finally, the prevalence of FP has reached epidemic proportions in some parts of the North Atlantic DPS. The extent to which this will affect the long-term outlook for green turtles in the North Atlantic DPS is unknown. Nesting trends across the DPS continue to increase despite the high incidence of the disease.
While the Status Review indicates that the DPS shows strength in many of the critical population parameters (abundance, population trends, spatial structure, and diversity/resilience), as indicated above, numerous threats continue to act on the DPS, including habitat degradation (coastal development and armoring, loss of foraging habitat, and pollution), bycatch in fishing gear, continued turtle and egg harvesting, FP, and climate change. Importantly, the analysis of threats in the Status Review was conducted assuming current management regimes would continue.
Many of the gains made by the species over the past few decades are a direct result of ESA protections in the United States, as well as protections by U.S. States and local jurisdictions and other countries within the DPS range that are influenced by the species’ ESA status.
Because the green turtle is currently listed under the ESA, take can only be authorized in the United States through the processes provided in sections 7 and 10 of the ESA and their implementing regulations. In the southeastern United States, threats to nesting beaches and nearshore waters include: Sand placement on nesting beaches and associated impacts to nearshore hardbottom habitat; groin, jetty and dock construction; and other activities. Any such activities that are currently funded, permitted and/or authorized by Federal agencies are subject to consultation with USFWS and NMFS, and therefore are subject to reasonable and prudent measures to minimize effects of these activities as well as conservation recommendations associated with those consultations. Federally-managed fisheries are also subject to interagency consultation under section 7 of the ESA. During the consultation process NMFS and USFWS have an opportunity to work with the action agency to design practices to minimize effects on green turtles, such as when the activity occurs in areas or habitats used mostly by green turtles (i.e., seagrass beds and nesting beaches). Activities that affect green turtles and do not involve Federal agencies, such as beach driving, some beach armoring, and research, must comply with section 10 of the ESA to avoid violating the statute. Section 10 permits require avoiding, minimizing, and mitigating impacts to green turtles to the extent possible. In addition to the above requirements, the requirement for use of TEDs in fisheries within the United States and in fisheries outside of the United States that export wild-caught shrimp to the United States is tied to listing under the ESA.
This DPS has exhibited increases at major nesting sites, and has several stronghold populations. Green turtles in the U.S. Atlantic have increased steadily since being protected by the ESA (Suckling et al., 2006). ESA driven programs such as land acquisition, nest protection, development of the TEDs, and educational programs provide a conservation benefit to green turtles. The species is conservation dependent or conservation-reliant in that even when biological recovery goals are achieved, maintenance of viable populations will require continuing, species-specific intervention (Scott et al., 2010). Without alternate mechanisms in place to continue certain existing conservation efforts and protections, threats would be expected to increase and population trends may be curtailed or reversed. Considering the conservation dependence of the species, significant concerns remain regarding the inadequacy of regulatory mechanisms (one of the five section 4(a)(1) factors (Factor D), especially when we evaluate the status of the DPS absent the protections of the ESA.
For the above reasons, we propose to list the North Atlantic DPS as threatened. We do not find the DPS to be in danger of extinction presently because of the increasing nesting population trends and geographically widespread nesting at a diversity of sites; however, continued threats are likely to endanger the DPS within the foreseeable future.