Online sale of small turtles circumvents public health regulations in the United States

PLOS ONE RESEARCH ARTICLE Online sale of small turtles circumvents public health regulations in the United States Lauren E. Montague1, Juliana M. Marcotrigiano1, Niamh E. Keane1, Hannah E. Marquardt ID1, Jennifer A. Sevin2, Nancy E. Karraker ID1* 1 Department of Natural Resources Science, University of Rhode Island, Kingston, Rhode Island, United States of America, 2 Department of Biology, University of Richmond, Richmond, Virginia, United States of America * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Montague LE, Marcotrigiano JM, Keane NE, Marquardt HE, Sevin JA, Karraker NE (2022) Online sale of small turtles circumvents public health regulations in the United States. PLoS ONE 17(12): e0278443. https://doi.org/10.1371/journal. pone.0278443 Editor: Floyd W. Weckerly, Texas State University, UNITED STATES Received: April 7, 2022 Accepted: October 20, 2022 Published: December 21, 2022 Copyright: © 2022 Montague et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abstract In the United States (U.S.), pet turtles have been associated with outbreaks of salmonellosis, a serious and sometimes-fatal intestinal illness caused by Salmonella bacteria, with nearly 300,000 people being infected in some years. Children are particularly susceptible because of their propensity to put items, including small turtles, in their mouths. In 1975, a U.S. federal regulation prohibited the sale of turtles <4 inches (101.6 mm) in size, except for the purposes of export, scientific, or educational purposes. This regulation was established to reduce the incidence of salmonellosis, particularly in small children. Previous research has not evaluated the availability of turtles <4 inches in size on websites selling wildlife. We monitored 16 websites in 2021 and quantified listings of small turtles. We determined whether information on Salmonella, the 1975 federal regulation, or related state regulations were provided on the websites and determined legality of sales of small turtles by state regulations. We found that all 16 websites openly advertised and sold turtles <4 inches in size, but only half of these websites provided information about Salmonella and/or the federal regulation. These websites required buyers to confirm that they were not purchasing a turtle as a pet, thereby putting the onus on the consumer to adhere to the regulation. We documented 515 listings of turtles <4 inches in size, including 47 species and one hybrid. Our study has demonstrated that internet sales of small turtles currently represent part of the thriving online pet trade in the U.S. Enforcement of the federal regulation faces jurisdictional challenges in most states. Therefore, we recommend continued public education campaigns by public health agencies in the U.S. to help reduce the risk that pet turtle ownership presents. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: L.E.M., J.M.M., and N.E. Keane received an Undergraduate Research Grant from the University of Rhode Island (https://web.uri.edu/ undergraduate-research/). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. J.A.S. and N.E. Karraker received an award (#2018428) from the National Science Introduction In the 1960s and 1970s, hatchling turtles became increasingly popular pets in the United States. By the early 1970s, about 4% of households in the U.S. owned at least one turtle, and about 15 million hatchling turtles, primarily red-eared sliders (Trachemys scripta elegans), were being sold annually [1]. As hatchlings, red-eared sliders are about the size of a U.S. quarter (24.3 PLOS ONE | https://doi.org/10.1371/journal.pone.0278443 December 21, 2022 1 / 10 PLOS ONE Foundation - Research Coordination Networks in Undergraduate Biology (https://beta.nsf.gov/ funding/opportunities/research-coordinationnetworks-undergraduate-biology-education-rcnube). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Sale of turtles circumvents public health regulations mm), and their size, coupled with a lime green shell and red stripes on the sides of their heads, made them popular and highly desired as pets. During the same period, the Centers for Disease Control and Prevention was documenting salmonellosis, an intestinal disease caused by Salmonella bacteria, cases in the public, and it was estimated that approximately 280,000 cases per year were attributable to turtle ownership [1]. Small children, in particular, were contracting salmonellosis because of poor hygiene after handling turtles and putting small turtles in their mouths. Salmonellosis can cause severe illness and death, particularly in young children, the elderly, and those with compromised immune systems [2]. In the 1970s, a public health education program focused on turtle-associated salmonellosis was launched by the Centers for Disease Control and Prevention [3], but this apparently did little to stem the number of infections. As a result, the U.S. Food and Drug Administration formulated a regulation [4] that prohibited sale in the U.S. of live turtles with a carapace (upper shell) length of <4 inches (101.6 mm), with the exception of turtles “intended for bona fide scientific, educational, and exhibition purposes, other than use as pets.” This size restriction was included in the regulation as it was determined that because, “turtles with a carapace, i.e., upper shell, length of less than 4 inches are the more common pet varieties purchased for or by children, the ban should not be extended to include turtles whose carapace is larger than 4 inches [4].” The regulation permits export of turtles with a shell length of <4 inches in size from the U.S. Although no records on early enforcement of the regulation are available, the number of turtle-associated salmonellosis cases in children declined by 77% between 1972 and 1976 [3], reinforcing the combined value of education and regulation to protect public health. Up to the establishment of the regulation, the most popular turtles were red-eared sliders which were sold via brick-and-mortar pet stores and by mail-order [1]. The emergence of the internet, and subsequent ability to shop online, in the 2000s changed the nature of the pet trade [5]. Turtles and tortoises became more easily attainable by anyone using the internet, regardless of their proximity to the seller. Customers and sellers are also able to remain anonymous through transactions, providing protection and confidentiality by hiding locations and identiti (...truncated)