THE ESA AND TURTLE LISTINGS

With only 33 species listed (ECOS 2023), the ESA is currently underutilized for freshwater turtles and tortoises. The US government protected the first freshwater turtles and tortoises in the United States in 1970 under the Endangered Species Conservation Act, a precursor to the Endangered Species Act, when it listed 6 foreign (non-US) species as endangered (ECOS 2023). From 1973 to 1997, an additional 25 species were listed (ECOS 2023). Over the following 25 yrs, as threats to turtles have grown and the extinction crisis worsened, the US government has listed just 2 species of freshwater turtles and tortoises, Kinosternon sonoriense longifemorale (Sonoyta mud turtle) and Testudo kleinmanni (Egyptian tortoise) (Table 1).

Table 1. Species of freshwater turtles and tortoises listed under the Endangered Species Act (ECOS 2023) by year listed.

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The ESA mandates that species be listed as either threatened or endangered depending on the species’ extinction risk, and the listing determines the level of protections species receive, as described below. Of the 33 freshwater turtle and tortoise species listed under the ESA today, 7 are listed as threatened and 26 are listed as endangered (ECOS 2023). Ten of the listed species are US domestic species and 23 are foreign species (ECOS 2023). Scientists and conservationists have petitioned for 9 additional species to be listed under the act, but the petitions are currently pending a decision by the government (ECOS 2024). The pending petitions are all for species found in the United States, with 4 species’ ranges extending into Canada and 1 extending into Mexico. Species can be listed under the ESA throughout their entire range or as distinct population segments that offer protections to segmented portions of the population. Although 28 species of freshwater turtles and tortoises are currently listed wherever they are found, only a designated portion of the population is listed for 5 species: Sternotherus depressus (flattened musk turtle), Trachemys terrapen (Cat Island turtle), Gopherus polyphemus (gopher tortoise), Gopherus agassizii (desert tortoise), and Glyptemys muhlenbergi (bog turtle) (ECOS 2023). Additional populations of G. agassizii and G. muhlenbergi are also protected because of their similarity in appearance to other ESA-listed turtle populations to make enforcement of the law more consistent and effective (ECOS 2023).

PROTECTIONS AFFORDED UNDER THE ESA

Species listed under the ESA receive varying levels of protections depending on whether they are listed as threatened or endangered, the species’ range (domestic or foreign), and the agency’s decisions regarding the species’ requirements for recovery. As described above, the ESA defines an endangered species as one that is “in danger of extinction throughout all or a significant portion of its range” (16 USC §1532[6]). A threatened species is “any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range” (16 USC §1532[20]). To determine whether a terrestrial species is endangered or threatened, USFWS must consider 5 factors: (1) the present or threatened destruction, modification, or curtailment of its habitat or range; (2) overutilization for commercial, recreational, scientific, or educational purposes; (3) disease or predation; (4) the inadequacy of existing regulatory mechanisms; and (5) other natural or manmade factors affecting its continued existence (16 USC §1533[a][1]).

Once listed, species receive many important protections. Among the most impactful of these protections is a ban on take of endangered species within the United States under Section 9 of the ESA (16 USC §1538[a][1][B]). The term “take” includes collection from the wild, as well as killing, harming, and harassing a listed animal (16 USC §1532[19]). This is particularly important for freshwater turtles and tortoises because overcollection from the wild, particularly of adult turtles for the pet and meat trade, is one of the leading threats to species (Lovich et al. 2018; Rhodin et al. 2018). Any person subject to US jurisdiction who violates this or any other prohibition in the ESA can face a fine, imprisonment, or both (16 USC §1540[a], [b]), unless USFWS has issued a permit for the take, under narrow circumstances (16 USC §1539[a]).

In addition to take, commercial import and export of endangered species are prohibited under Section 9 of the ESA (16 USC §1538[a][1][A]). It is also unlawful to sell an endangered species or “possess, … transport, or ship” endangered species taken in violation of the law (16 USC §1538[a][1][D]). The United States is a major player in the trade of freshwater turtles and tortoises as both an importer and an exporter (Luiselli et al. 2016). Researchers analyzing trade data from the Convention on International Trade in Endangered Species (CITES) found that the United States was the leading importer of wild freshwater turtles and tortoises from 1990 to 2010 and one of the leading exporters, second only to Malaysia (Luiselli et al. 2016). More than 126 billion freshwater turtles were exported from the United States from 2000 to 2012, 19% of which were labeled as wild-caught (Mali et al. 2014). Given the sizeable role of the United States in the global market for freshwater turtles and tortoises, closing the US market for a species through an endangered listing may contribute significantly to the conservation of species that are in demand in the United States.

The Section 9 prohibitions on import, export, and trade apply automatically to endangered species. For threatened species, under Section 4(d) of the ESA, USFWS “shall issue” conservation rules that the agency “deems necessary and advisable” to ensure the species does not become endangered, and the agency may extend any or all of the Section 9 prohibitions to the threatened species (16 USC §1533[d]).

Section 7 of the ESA also affords critical protections to listed species. Under Section 7, federal agencies are required to “insure that any action authorized, funded, or carried out by such agency… is not likely to jeopardize the continued existence of any endangered species or threatened species” (16 USC §1536[a][2]). Federal agencies must determine whether their actions “may affect” any endangered or threatened species in the area (16 USC §1536[a][2]; 50 CFR §402.14) and engage in expert consultation, which can result in conservation measures (16 USC §1536[i]). The US federal government is frequently involved in major development and resource decisions, including those on the nation’s vast public federal lands. With habitat loss and degradation being major threats to turtles (Lovich et al. 2018; Rhodin et al. 2018), this consultation process is an important protection to help prevent development related to federal projects from jeopardizing threatened and endangered turtles.

Another ESA provision addresses the threats of habitat loss and degradation. When a species is listed, the ESA requires USFWS to designate critical habitat (16 USC §1536[a][3]), though the agency designates habitat only within the United States (50 CFR §424.12[g]). Critical habitat is defined as occupied areas with features “essential to the conservation of the species” and that “may require special management considerations or protection” or unoccupied areas “essential for the conservation of the species” (16 USC §1532[5]). Federal agencies must generally consult with USFWS before permitting, funding, or carrying out actions that “result in the destruction or adverse modification” of critical habitat (16 USC §1536[a][2]). Critical habitat has proven successful in the conservation of imperiled species. Species with critical habitat designated for 2 or more years are more than twice as likely to be recovering compared to species that do not have critical habitat (Taylor et al. 2005).

Under Section 4(f) of the ESA, recovery plans are developed for domestic listed species with the goal of increasing populations to the point that protections are no longer needed. When the USFWS drafts new recovery plans, it requests public comments to inform the plans. Of the 10 US turtles listed under the ESA, 6 currently have recovery plans written and 1 additional plan is being drafted (ECOS 2023). Recovery plans are not developed for foreign, ESA-listed species.

ESA-listed species also benefit from increased federal funding for conservation programs and population monitoring. Under Section 6 of the Endangered Species Act, USFWS is authorized to provide federal funding to support the “development of programs for the conservation of endangered and threatened species” (16 USC §1535[d][1]). The US government also has the authority to provide funds to any foreign country for programs “necessary or useful for the conservation of any endangered species or threatened species” (16 USC §1535[d][1]). As discussed below, federal funding can be used for a variety of conservation efforts that provide a lifeline to imperiled turtles. Finally, ESA listings can raise awareness about species and their conservation needs. They can help educate the public and may increase research interest and resources (USFWS 2023).

THE ESA’S POTENTIAL FOR TURTLE CONSERVATION

The ESA has considerable potential for freshwater turtle and tortoise conservation. Numerous conservation initiatives are currently underway for listed endangered and threatened species. For example, the northern population of G. muhlenbergii has been listed under the ESA as threatened since 1997. The species’ listing opened up funding for land conservation to protect and restore bog turtle habitat, which is helping to ease pressure from development near extant populations (USFWS 2022a). At the time the northern population of bog turtle was listed under the ESA, there were thought to be 191 populations in 7 states. Although the data are not directly comparable, there are currently 330 extant metapopulations (USFWS 2022a). Because of their slow life history, there may be a delay before the full impact of land conservation is reflected in turtle populations.

Aside from protecting habitat, some turtles listed under the ESA receive a more hands-on approach to conservation. Pseudemys rubriventris was listed under the ESA in 1980. In 1985 the state wildlife agency in Massachusetts initiated a head start program funded partially with ESA grant money. The program raises wild hatchlings in captivity for 9 mo to increase growth and survival into adulthood (USFWS 2022b). As of 2021, 4400 hatchlings had been released. The population was estimated to be around 200 individuals in 1980 and is now estimated to be around 933 individuals (USFWS 2022b). Conservation programs like these may help stabilize and increase populations of other imperiled freshwater turtles and tortoises if they are listed under the ESA.

In many cases, it is difficult to quantify the ESA’s impact for long-lived species such as freshwater turtles and tortoises because most species have not been studied or protected long enough to meet their recovery goals. Just 1 turtle, Lissemys punctata punctata (Indian flap-shelled turtle), has been delisted (removed) from the ESA. The species was listed in 1976 and delisted in 1984 because of a data error in the original listing. To date, no turtles or tortoises have been deemed recovered under the ESA. Some ESA recovery plans issued by USFWS have estimated recovery time for some turtles and tortoises: species are expected to take at least 35–63 yrs to recover if the recovery plan is fully implemented (Pulliam and Bowker 1990; Amaral 1994; USFWS 2011; Godwin and LaClaire 2019). On average, freshwater turtles and tortoises have been listed under the ESA for about 39 yrs and require more time to meet recovery goals.

Although data are lacking for many freshwater turtles and species have generally not been protected long enough under the ESA to expect recovery, sea turtles, which tend to have more population data over time, are showing a positive response to conservation efforts under the ESA. Before being listed under the ESA in 1978, the Hawaii Chelonia mydas (green sea turtle) stock was severely depleted because of human exploitation and habitat destruction (Balazs and Chaloupka 2004; Hays 2004). Since being listed under the ESA, the stock has grown substantially and is close to reaching its foraging habitat carrying capacity (Balazs and Chaloupka 2004; Hays 2004). Valdivia et al. (2019) analyzed 8 populations of sea turtles that occur and reproduce in US waters and were listed under the ESA before 2012. They found that 6 populations significantly increased after listing, and none of the populations had declined following ESA protections, which reduced threats from harvest, bycatch, loss of habitat, predation, and trade (Valdivia et al. 2019). These trends suggest that protections initiated by ESA listings contribute to successful conservation by addressing threats to Testudines and helping populations improve.

PUBLIC PARTICIPATION IN THE ESA

The ESA welcomes and benefits from public participation. The first way that private citizens, scientists, nongovernmental organizations, and others can participate in the ESA is by petitioning to add species to the threatened or endangered lists. Submission of a petition prompts a legally binding timeline for USFWS and NMFS, the agency that implements the ESA for marine species, to decide whether to list species. The ESA states that the agencies “shall make a finding as to whether the petition presents substantial scientific or commercial information indicating that the petitioned action may be warranted” within 90 days of receiving the petition (16 USC §1533[b][3][A]). If an agency determines that the petitioned action may be warranted, the agency must then decide whether to propose the species’ listing within 12 mo of receiving the petition and generally decide whether to finally list the species 1 yr later (16 USC §1533[b][3][B], [6][A]). Of note, the listing process generally takes far longer than the act’s timeframes due primarily to government budgetary shortfalls for species listings (Eberhard et al. 2022).

Following the petition, the next opportunity for public engagement under the ESA is at the proposed rule stage. At this time, a public comment period is opened, and public hearings may be held. In practice and despite the legal deadlines, often significant time has passed between the agency’s review of a species and the publication of the proposed rule and comment period. For this reason, submission of comments with updated data or published literature can lead to species being granted higher levels of protections, when necessary. Participation by scientists and experts at this stage is key to ensuring that decisions are based on the best available information in the field.

CONCLUSION

The ESA is a powerful tool that can be used to protect freshwater turtles and tortoises from the growing threats they face. In discussing turtle extinction events, Pereira et al. (2022) state that “further extinctions in this group would constitute an irreparable loss.” With more than half of turtles threatened with extinction, it is critical that every possible tool be used to help stabilize and increase populations of these imperiled species. Currently, many more species are threatened with extinction than are listed under the ESA, and more listings are needed to close that gap and open opportunities for protection and funding for imperiled species. Scientists and conservationists can take an active role in using the ESA for freshwater turtle and tortoise conservation by petitioning the US government to list a species and commenting on government proposals to ensure that turtle species persist and thrive for generations to come.