The Khorat snail-eating turtle (Malayemys khoratensis) is a small freshwater turtle only recently described by Ihlow et al. (2016). Prior to the description of M. khoratensis, the Mekong snail-eating turtle (Malayemys subtrijuga) was thought to be the only member of the genus inhabiting the Mekong River Basin of Southeast Asia (Brophy 2004, 2005). Currently, the recognized distribution of M. khoratensis includes the Khorat Plateau of northeastern Thailand and a small area of adjacent Lao People's Democratic Republic (PDR; Turtle Taxonomy Working Group [TTWG] 2021). The occurrence of M. khoratensis (as M. isan, a name since synonymized with M. khoratensis; TTWG 2021) in the latter country was first suggested by Sumontha et al. (2016) based on 2 photographs (both published as Malayemys subtrijuga) taken in Vientiane that include 1) a turtle captured while crossing a city street (Stuart and Platt 2004), and 2) a group of turtles being sold at an urban wildlife market (Kubota et al. 2015). Due to the circumstances surrounding the collection of these records, Sumontha et al. (2016) were unable to conclusively establish the natural occurrence of M. khoratensis in the area of Vientiane. Furthermore, although presumably similar to its congeners (reviewed by Dawson et al. 2018, 2020), the natural history and ecology of M. khoratensis remains unstudied. This situation is lamentable because population status assessments and conservation measures are more likely to prove successful when based on a thorough understanding of the geographic distribution and natural history of an organism (Dodd and Franz 1993; Dayton 2003; Stuart and Thorbjarnarson 2003).

Herein we provide new information on the occurrence and natural history of M. khoratensis in Lao PDR. We first present specimen-based field records and traditional ecological knowledge (TEK) of M. khoratensis collected during recent biological assessments in central Lao. TEK is defined as the cumulative body of knowledge concerning the biology of organisms and their relationship to the environment, empirically acquired and passed down by oral tradition (Berkes et al. 2000; Huntington 2000), and as such, can provide insights into natural history and ecological relationships heretofore unrecognized by academic investigators (Goodman and Hobbs 1994; Platt et al. 2004). We then review available museum specimens, revisit previously published photographic records of Malayemys spp. from Lao, and tentatively reassess the geographic distribution of M. khoratensis within the country.

METHODS

Our specimen-based field records and data on TEK of M. khoratensis were obtained during fieldwork in the Xe Champhone Ramsar Site (XCRS; 12,400 ha) and adjacent Nong Louang Wetland Complex (NLWC; 32,000 ha) in Savannakhet Province (Fig. 1). This region is characterized by a tropical monsoonal climate with a wet season extending from mid-May through mid-October (peak rainfall in September and October). The XCRS and NLWC lie within the floodplain of the Champhone and Xangxoy rivers and as such, are subject to extensive overbank flooding during the wet season. Little precipitation occurs outside of the wet season and water levels fall dramatically during this period. Habitat in the XCRS and NLWC consists of a mosaic of natural and anthropogenic wetlands (reservoirs, oxbow lakes, swamps, sloughs, and creeks), agricultural ecosystems, scrublands, bamboo, and remnant forest patches. Oxbow lakes retain water throughout the dry season and serve as important refugia for many aquatic organisms. Most oxbow lakes are covered by extensive floating mats supporting graminoids, shrubs, and small trees rooted in a thick base of floating organic matter.

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At least 20 rural communities are located within or immediately adjacent to the XCRS and NLWC. Fishing is an important subsistence activity and rice agriculture is the principal livelihood with 2 crops being produced each year. Excessive extraction of water to irrigate rice during the dry season is considered a major threat to the ecological integrity of wetlands in both the XCRS and NLWC. The XCRS contains 2 core areas totaling 2550 ha that encompass habitat critical for the conservation of Siamese Crocodiles (Crocodylus siamensis). The physical environment, vegetation, and social setting of our study area are discussed in greater detail elsewhere (International Union for Conservation of Nature [IUCN] 2011; Brakels 2018; Platt et al. 2018a).

We conducted biological assessments of turtles, crocodiles, and wading birds in XCRS and NLWC from 4 to 11 January 2018 and from 12 to 26 November 2019. During these assessments we visited rural communities and conducted semistructured, open-ended interviews of knowledgeable persons to obtain information on taxa of interest. While recognizing the limits of indigenous knowledge (Huntington 2000), our experience (Platt et al. 2017, 2018b) and that of others (e.g., Thirakhupt and van Dijk 1994; Demaya et al. 2019) indicates such individuals can be reliable sources of information on local chelonians and their natural history. Focal groups of knowledgeable individuals were selected in advance by community leaders. Because our interviews were always conducted in public spaces (e.g., village school, community pavilion, domicile of the headman), other unsolicited villagers frequently joined the sessions and contributed to discussions.

In accordance with the format of a semistructured interview, informants were asked a series of questions that included standard questions prepared in advance and others that arose during the course of conversation (Martin 1995; Gilchrist et al. 2005). We guided the discussion, but the direction and scope of each interview was allowed to follow the participants' train of thought. Semistructured interviews are more of a conversation than a typical question-and-answer session, and rather than rigidly adhering to a set of prepared questions, the interview provides an opportunity for collecting and discussing unanticipated information (Gilchrist et al. 2005; Huntington 2000). Interviews were conducted in Lao by one of us (O.T.) and later transcribed into English.

During interviews, we asked informants the following standard questions: 1) What species of turtles are present in the area? 2) Are turtles harvested and if so, what harvesting strategies are employed, what period of year is harvesting conducted, and how many turtles are harvested per month or year? 3) How would you qualitatively characterize the abundance of each species of turtle (i.e., rare, uncommon, common, or abundant)? 4) What is TEK pertaining to turtles; specifically what information can you provide on habitat, reproduction, and diet? As part of these interviews, we also asked to examine any living turtles or shells that might be available in the village. Unlike trade specimens for which provenance can be difficult to reliably determine, shells obtained in villages are generally from turtles harvested nearby (Stuart and Platt 2004; Platt et al. 2018b).

We measured living turtles and shells (straight-line carapace length [CL; measured along the midline from the posterior marginals to the anterior edge of the nuchal scute], and plastron length [PL; measured along the midline from the base of the anal notch to the anterior edge of the gular scute]) with calipers and photographed most specimens. We also measured the width and length of the first vertebral scute of each carapace (see below). The sex of living turtles was determined according to tail morphology with males having longer and thicker tails than females (Brophy 2006; Platt et al. 2008). We often accompanied informants to areas where turtles were reportedly captured to inspect traps and fishing gear, and qualitatively assess habitat. Interview transcripts and field notes are archived in the Campbell Museum, Clemson University, Clemson, South Carolina.

In addition to our field records from XCRS and NLWC, we reviewed Malayemys material from localities across central and southern Lao. We examined 9 museum specimens (or photographs of these specimens) housed in the collections of the Field Museum of Natural History (FMNH), North Carolina Museum of Natural Sciences (NCSM), and Stuttgart State Museum of Natural History (SMNS). We examined 1 unpublished photograph (taken by P. Brakels) and photographs previously published as M. subtrijuga and Malayemys macrocephala (Stuart and Platt 2004; Teynié and David 2010; Kubota et al. 2015; Suzuki et al. 2015; Brakels 2018; Cranmer et al. 2018; Scott et al. 2018). We critically assessed the accuracy of the locality data accompanying this material and excluded any erroneous records from our analysis of the geographical distribution.

We assigned species identifications to our field records and museum specimens using diagnostic morphological characters presented in Ihlow et al. (2016). Specifically, the characters we considered were 1) the presence or absence of a postocular stripe; 2) the shape of the infraorbital stripe; 3) whether the infraorbital stripe reached the loreal seam; 4) whether the infraorbital stripe was connected to the supraorbital stripe; 5) the number of ocular rings; 6) the number of nasal stripes below the nostrils; and 7) the color pattern of the lower posterior marginal scutes. Additionally, for living turtles and shells, we measured the width along the posterior edge (VW) and length (VL) of the first vertebral scute of the carapace to determine the VW/VL ratio in accordance with Ihlow et al. (2016). While the VW/VL ratio is less reliable than the head pattern or color pattern of the lower marginals for identifying species of Malayemys due to high intraspecific variability (F.I., pers. obs.), this was the only character available for some incomplete shells lacking soft tissue. Whenever possible, we used a combination of characters to make identifications. However, some of the available material was partial or fragmentary in condition, thus limiting our ability to employ multiple characters for species identification. In cases of uncertainty, we indicated our identifications as being either tentative or unknown. Finally, our taxonomy is in accordance with the Turtle Taxonomy Working Group (TTWG 2021), which currently recognizes 3 species of Malayemys (M. subtrijuga, M. macrocephala, and M. khoratensis). That said, we acknowledge the taxonomic ambiguity surrounding the status of M. khoratensis and M. macrocephala as full species (TTWG 2021, pp. 402–403).

RESULTS

We conducted interviews of 78 persons in 11 villages during fieldwork in XCRS and NLWC. During these interviews we examined 18 Malayemys spp. obtained from 5 villages (Table 1); these turtles were reportedly harvested from wetlands near the villages where we examined them. Our sample consisted of 4 living turtles (3 females and 1 small juvenile), 4 carapaces lacking an accompanying plastron, 1 plastron without an associated carapace, 2 shells (carapace and plastron) separated at the plastral bridge (during butchering to extract contents), and 7 intact shells. Excepting a small juvenile (CL = 42 mm; PL = 31 mm), the mean ± 1 SD CL (n = 15) and PL (n = 13) of our sample were 125 ± 38 mm SD (range = 78–209 mm) and 106 ± 37 mm SD (range = 13–186 mm), respectively. The first vertebral scute of the turtles in our sample was approximately square in shape and the mean VW/VL was 0.80 ± 0.05 SD (n = 15). This value is similar to the mean VN/VL ratio reported for both male (0.83 ± 0.12 SD) and female (0.83 ± 0.09 SD) M. khoratensis by Ihlow et al. (2016). Likewise, the head and neck coloration of the living turtles we examined was consistent with M. khoratensis, i.e., absence of a postocular stripe, relatively straight infraorbital stripe that never or seldom reached the loreal seam, single ocular ring (faint in most turtles), 2 nasal stripes, and first vertebral scute approximately square in shape (Fig. 2A–D).

Table 1. Geographic coordinates of villages in Xe Champhone Ramsar Site and Nong Louang Wetland Complex, Savannakhet Province, Lao PDR where specimens of Malayemys khoratensis were examined during a rapid biological assessment in November 2020.

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Our informants referred to M. khoratensis as Tao Sam Son, which translates as “turtle with 3 lines on its back”, an obvious descriptive reference to the tricarinate carapace of Malayemys. There was unanimous agreement among our informants that M. khoratensis was the most common of 4 hard-shelled aquatic species occurring in XCRS and NLWC (other species include Heosemys grandis, Heosemys annandalii, Cuora amboiensis; Brakels 2018; S.G.P. et al., unpubl. data, 2019). Our informants stated that M. khoratensis occurs widely throughout XCRS and NLWC and that every permanent wetland contained “at least a few turtles”. The capture sites we visited were heavily vegetated irrigation reservoirs, swamps, and oxbow lakes with water levels that fluctuated according to the season; however, at least some water was present throughout the year in these wetlands (Fig. 3A–B).

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Perceptions of abundance varied among different villages, ranging from common to uncommon; however, most persons we interviewed stated that M. khoratensis was less common now than in the past. Most of our informants were reluctant to estimate the annual harvest of M. khoratensis. However, focal groups in Nong Deun and Nong Boua Louang stated that about 30 M. khoratensis were annually harvested from local wetlands. Our informants indicated that M. khoratensis is rarely targeted for harvest but is instead mostly taken as bycatch incidental to other fisheries. Most turtles are captured in bamboo fish traps or on hooks deployed to catch snakehead (Channa sp.) and baited with earthworms (Annelida) and apple snails (Pomacea sp.). Bamboo fish traps are often used in conjunction with extended weirs that function as an aquatic drift fence to funnel fish and turtles into the trap. Malayemys khoratensis is also opportunistically harvested after becoming entangled in monofilament fishing nets, when exposed by fires ignited to clear wetlands of grass and reeds during the dry season, and when chanced upon by the ubiquitous dogs that accompany villagers into the rice fields. Our informants stated that M. khoratensis is especially active early in the wet season (June and July) and most captures occur during this period. A few turtles are released unharmed, and some persons believe that to do so will bring good fortune. However, most turtles are retained for domestic consumption or sold in nearby urban markets (e.g., Champhone and Savannakhet). In general, smaller and hence less valuable turtles are eaten by villagers, while larger, more valuable turtles are sold in local markets. Itinerant Vietnamese traders are said to exchange baubles and sweets for the dried plastrons of turtles consumed by villagers.

According to our informants, M. khoratensis deposits eggs from November to March–April, a period coinciding with the annual dry season. One informant stated that gravid females can be identified by an outward “bulging” of the plastron, which recedes after the eggs are laid. Clutches containing as many as 10 to 15 eggs were reported by our informants. Villagers typically find nests by noting the presence of eggshells that remain after hatching or destruction of the clutch by predators. Nests are described as shallow holes (ca. 12–15 cm deep) excavated near water in substrates ranging from sand to clay soil. Rodents (probably Rattus spp.) and 2 species of nonvenomous snakes are considered to be major predators of M. khoratensis nests. The 2 species of snakes are known locally as Ngou Ta He and Ngou Pa, and said to be largely piscivorous, frequently encountered in flooded rice fields, and most active during the wet season. However, given the diversity of piscivorous natricine and homalopsine snakes present in our study area, we are unable to confidently equate these folk species (sensu Berlin et al. 1966) with scientifically recognized taxa. Villagers consume turtle eggs but expend little effort in targeted searches owing to the difficulty of locating nests. Instead, most eggs are obtained when villagers butcher gravid female turtles. Our informants were uncertain when neonates emerge from the egg but reported encountering hatchling M. khoratensis in wetlands as early as July, suggesting that hatching occurs early in the wet season.

In addition to our specimen-based records from XCRS and NLWC, we examined 9 museum specimens and an unpublished photograph of Malayemys sp. from Vientiane, Khammouan, Savannakhet, and Champasak provinces of Lao (Table 2). Of these, 4 complete specimens from Vientiane (FMNH 258868; SMNS 5512 and 5513) and Savannakhet (NCSM 76498) provinces are clearly referable to M. khoratensis on the basis of head coloration (lack of postocular stripe, distinct shape and position of the infraorbital stripe, and twin yellowish stripes below the nares) and characteristics of the carapace (relatively square shape of the first vertebral scute and black blotches on the lower marginal scute). Likewise, the configuration of the first vertebral scute suggests that a carapace from Khammouan Province (FMNH 255269) is assignable to M. khoratensis. An unpublished photograph taken by one of us (P.B.) in Nong Bok, Khammouan Province, clearly shows the distinct infraorbital stripe and twin yellowish stripes below the nares that characterize M. khoratensis.

Table 2. Localities and identification of Malayemys material from Lao PDR examined during this study. Numbers for map locations correspond to Figure 1.

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We were unable to satisfactorily resolve the identity of a complete specimen (FMNH 255267) and carapace (FMNH 255268) from Champasak Province. FMNH 255267 is undoubtedly not M. khoratensis based on the presence of a postocular stripe extending to the tympanum and an infraorbital stripe extending beyond the loreal seam. This specimen also possesses 4 (rather than 2) nasal stripes, a character more typical of M. macrocephala, but also occasionally found in M. subtrijuga (Ihlow et al. 2016; Dawson et al. 2020). FMNH 255268 has a posteriorly tapered first vertebral scute, which is present in both M. subtrijuga and M. macrocephala, but typically not in M. khoratensis (Ihlow et al. 2016). Because M. macrocephala is known only from western Thailand and Peninsular Malaysia and appears absent from the Mekong River basin (Dawson et al. 2018), we tentatively designated both specimens (FMNH 255267 and 255268) as “likely M. subtrijuga” (Table 2). The remaining specimens (FMNH 258888, 259653) could not be reliably identified based on the fragmentary material available (i.e., separated plastrons).

We located 5 previously published photographs of Malayemys spp. in Lao (Teynié and David 2010; Suzuki et al. 2015; Brakels 2018; Cranmer et al. 2018; Scott et al. 2018). Teynié and David (2010, p. 22–23) present photographs of M. khoratensis (identified as M. subtrijuga) from Phou Khao Khouay National Biodiversity Conservation Area and Nam Lik Eco-Village Resort in Vientiane Province (Fig. 1). In both images the distinct shape and position of the infraorbital stripe, 2 yellowish vertical stripes below the nares, and a single, albeit faint yellowish orbital ring indicate these turtles are assignable to M. khoratensis rather than M. subtrijuga. Moreover, these turtles were apparently photographed in the wild, which should eliminate the ambiguity surrounding the provenance of earlier records of M. khoratensis from Vientiane (Sumontha et al. 2016). Suzuki et al. (2015, fig. 2C–D) reported M. macrocephala and M. subtrijuga from wildlife markets in Vientiane Province, and Vientiane and Champasak provinces, respectively, and present photographs of 2 representative turtles without stating the provenance of either image. We concur with the identifications of Suzuki et al. (2015), with the caveat that as market specimens, the actual provenance remains questionable owing to wide-ranging trafficking networks that often transport wildlife from distant areas. Brakels (2018, p. 34) identified 3 turtles photographed in Beung Kiat Ngong Ramsar Site in Champasak Province as M. subtrijuga (Fig. 1), and we concur based on the angle and length of the infraorbital stripe, presence of a postocular stripe, and what appear to be multiple stripes below the nares of one individual in the photograph (visible with enlargement), traits which are consistent with M. subtrijuga (reviewed by Dawson et al. 2020). Cranmer et al. (2018, p. 6, fig. 3) also report the occurrence of M. subtrijuga from Beung Kiat Ngong Ramsar Site but support their finding with a photograph of a juvenile M. khoratensis. However, this photograph was apparently taken at a different location (possibly XCRS) prior to the survey at Beung Kiat Ngong, presented in Scott et al. (2018, fig. 4), and then reused in Cranmer et al. (2018).

DISCUSSION

We identified the 18 turtles obtained from villages in the XCRS and NLWC as M. khoratensis rather than M. subtrijuga, which was previously assumed to occur in this region (Brakels 2018; Dawson et al. 2020). The habitat preferences of M. khoratensis as described by our informants (permanent water bodies including vegetated reservoirs, swamps, and oxbow lakes) appear to be similar to those reported for M. macrocephala (Dawson et al. 2018) and M. subtrijuga (Dawson et al. 2020). The clutch size of M. khoratensis given by our informants (10–15 eggs), greatly exceeds the maximum clutch size of either congener (mean clutch size = 5–6 eggs, maximum to 10 eggs; Dawson et al. 2018, 2020), appears to be largely based on counts of yolked ova found in females butchered during the reproductive season, and probably represents multiple clutches (see also Platt et al. 2008). The phenological reproductive pattern of dry-season nesting followed by hatchling emergence at the onset of the wet season reported for M. khoratensis by our informants is typical of both M. macrocephala (Dawson et al. 2018) and M. subtrijuga (Dawson et al. 2020). Emergence during the wet season allows hatchlings to access flooded vegetation, which harbors an abundance of prey (e.g., invertebrates and small fish) and also serves as escape cover.

Similar to our findings regarding perceptions of abundance and exploitation of M. khoratensis in XCRS and NLWC, Brakels (2018) reported that most respondents interviewed in XCRS regarded M. subtrijuga [khoratensis] as uncommon and the majority believed populations had declined in recent years as a result of overharvesting. Based on interviews, Brakels (2018) estimated that individual fisherman in XCRS harvested 4–6 M. subtrijuga [khoratensis] per year, with one individual reporting a catch of 50 turtles during a single year. Given the demographic sensitivity of turtle populations to even low levels of harvest (Congdon et al. 1993, 1994), exploitation of this magnitude is clearly a cause for concern and could potentially jeopardize the continued survival of M. khoratensis in XCRS and NLWC.

Collectively, our field records, museum specimens, and unpublished and published photographs from Savannakhet, Khammouan, and Vientiane provinces suggest the distribution of M. khoratensis within Lao is more widespread than previously assumed (TTWG 2021). Our results extend the geographic distribution of K. khoratensis by > 300 km from previously reported localities (Ihlow et al. 2016; Sumontha et al. 2016). Furthermore, our findings strongly suggest M. khoratensis occurs throughout the Khorat Plateau (Cota 2021) with the population in Lao being located along the eastern periphery of this distribution. Additionally, the confirmed occurrence of M. subtrijuga in Champasak Province suggests the presence of a biogeographic barrier south of Savannakhet separating the 2 species. While the Khone Falls on the Mekong River forms the boundary between the upper and lower stretches of the river, and functions as a complete or partial dispersal barrier for many freshwater taxa (Adamson et al. 2009; Lukoschek et al. 2011), the Beung Kiat Ngong Ramsar Site where a population of M. subtrijuga occurs is located above the falls.

Given this observed pattern of distribution, we instead posit that an upland area located along the borders of Savannakhet and Salavan provinces in Lao PDR and in Ubon Ratchathani Province, Thailand, serves as a barrier to geographically isolate M. khoratensis and M. subtrijuga (Fig. 1). Along the western edge of these uplands, a canyon-like defile is created where the Mekong River cuts through the sandstone plateau, just upstream from the confluence of the Mun and Mekong rivers. Although discontinuous in places, this upland area spans a gap between the Dangrek and Annamite mountain ranges, separating the lowlands on either side that are allopatrically inhabited by the 2 species of Malayemys (Dawson et al. 2018, 2020).

Finally, in the absence of baseline population data, predicting demographic trends among M. khoratensis in Lao is difficult. That said, the life history traits of turtles severely constrain the ability of populations to respond to overharvesting (Congdon et al. 1993), and even low-intensity subsistence harvesting is known to cause long-term declines (Thirakhupt and van Dijk 1994; Thorbjarnarson et al. 2000). Although M. khoratensis is globally ranked as a species of Least Concern by the International Union for Conservation of Nature (Rhodin et al. 2018) and probably secure in Thailand (Cota 2021), in light of the widespread harvest pressure and population declines that appear to be underway in Lao (Brakels 2018; this study), we believe the conservation status of this species warrants re-evaluation at the national level.