Female wanted for the world's rarest turtle: prioritizing areas where Rafetus swinhoei may persist in the wild

Abstract

The Yangtze giant softshell turtle Rafetus swinhoei is the rarest turtle species, with just two individuals known to be surviving, one male in a zoo in China and one individual recently identified as a female in the wild in Viet Nam. As the species is on the brink of extinction, it is an urgent priority to search for additional individuals in the wild, and for areas where it may still be present. Here, we analysed areas where the species may still occur, identified through interview surveys in Viet Nam. In addition, we introduced a novel system for evaluating the potential for occurrence of this rare and elusive freshwater turtle, using a conservation priority index. This index was based on three recorded variables: (1) probability of the species' presence based on interviews with local fishers, (2) degree of habitat alteration, and (3) fishing intensity, with the latter two based on experts’ evaluation of the sites where the species could potentially be present. There were at least 13 independent, reliable sightings in the 2010s, seven of which were in 2018–2019, indicating that R. swinhoei potentially persists in the wild. Although the species was confirmed at only one site, there are at least three more sites where it is likely to be present, and 13 sites of conservation interest. We provide a description of all sites where the species is potentially present, and a summary of relevant interviews. The Da River system has the highest number of recent sightings. We recommend that a research and conservation project be initiated urgently, and outline how such a project could be implemented.

Introduction

The Yangtze giant softshell turtle Rafetus swinhoei (Trionychidae; Gray, 1873) is one of the largest freshwater turtles, with some males weighing > 160 kg. The species occurs exclusively in the Red River basin in China and Viet Nam, and the lower Yangtze River floodplain in China (Pritchard, 2012; Wang et al., 2013) and is of particular cultural significance in Vietnamese mythology and folklore (Bettelheim, 2012). Until recently, R. swinhoei has been known primarily for cultural reasons (Pritchard, 2012), with few studies describing the species’ ecology and natural history (Gray, 1873; Heude, 1880; Meylan & Webb, 1988; Pritchard, 2001, 2005). Large dams have been constructed within the species’ range, and potential negative effects, including impacts on the nesting habitats of the species and effects caused by isolation and overfishing, were not considered (Le Duc et al., 2020b). Rafetus swinhoei is categorized as Critically Endangered on the IUCN Red List (Fong et al., 2021) and is one of the most threatened turtle species globally (Stanford et al., 2020). It began to decline in the 1980s, and became rare in the 1990s as a result of habitat alteration and intensive capture for local consumption (Le Duc et al., 2020a). Currently only one male individual remains in captivity, in China, and there is one known individual in the wild in Viet Nam, which was recently identified as a female (Le Duc et al., 2020a; Stanford et al., 2020, WCS, 2020). Intensive efforts to locate more individuals in both Viet Nam and China have failed (Wang et al., 2013; Kuchling et al., 2014; Pham et al., 2020). Most data available on the species is in unpublished reports and documents, or has been published in unverified reports in social media. In China, R. swinhoei has reportedly never been observed in the wild (Stanford et al., 2018). However, the species was historically reported to occur in the Red River, c. 300 km from Yuanjiang County (Wang et al., 2013). The species is also believed to have been present along the Yangtze River until a few decades ago (Pritchard, 2012), but there is no evidence confirming its current presence in this river (Wang et al., 2013). Trapping and observation surveys have been conducted in China (Wang et al., 2013; Kuchling et al., 2014), but only limited information from the surveys has been published.

Interview surveys have been carried out in both Viet Nam (Asian Turtle Program, 2008) and China (Kuchling et al., 2014). The results of these interviews (> 3,000 according to Timmins, 2016, unpubl. data) have not been published, the raw data are unavailable and the interview questions are unknown (Anadón et al., 2009; Turvey et al., 2015). However, information about the ecology and population biology of R. swinhoei has been obtained using local ecological knowledge, gathered in standardized interviews of former hunters of R. swinhoei in Viet Nam, raising the possibility that there may be more individuals in the wild (Le Duc et al., 2020a,b; Pham et al., 2020). Several priority sites have been identified where trapping/observational surveys are urgently needed to confirm the presence of the species (Le Duc et al., 2020a,b; Pham et al., 2020).

Here, we present the results of interview surveys with fishers on two river systems in Viet Nam where interviews have not previously been undertaken, categorize sites according to the likelihood that R. swinhoei is present, and recommend further research actions.

Study area

We conducted our survey in areas along the Da River (Black River), from Son La dam across the provinces of Son La, Lai Chau and Dien Bien, covering the entire 500 km of the Da River in Viet Nam (for interview data from areas along the Da River outside Viet Nam, see Le Duc et al., 2020a). The Da River (total length 910 km) originates in Yunnan province in China and flows through Viet Nam before joining the Red River in Hanoi (Dao, 2010; Vinh et al., 2014; Le Duc et al., 2020a).

Methods

We conducted 80 interviews during 13–24 November 2019, using the same questionnaire (Supplementary Material 1) and methodology as Le Duc et al. (2020a). Based on interviews with former hunters, fishers and local people during two periods in four areas (this study and Le Duc et al., 2020a), we assigned a presence score to each site: score = 1: confirmed presence of R. swinhoei, based on shells, skulls or photographic evidence; score = 2: high probability of presence, where > 3 independent interviewees accurately described the species' morphological characteristics, there had been multiple sightings within the previous 10 years, the precise location of these sightings was known and the sighting was confirmed by multiple household members; score = 3: medium probability of presence, where only one interviewee described morphological characteristics accurately, and any sightings had occurred > 10 years ago; score = 4: low or no probability of presence, where interviewees did not know the species, or their comments were contradictory and/or unreliable.

We categorized the sites where R. swinhoei may be present according to the level of habitat modification that had occurred during the past 30 years: score = 1: no or little habitat alteration, where habitat has been modified by human activities, but still retains large patches of natural vegetation cover in the waterbody and on banks, and the size and shape of the site have not changed significantly; score = 2: moderate habitat alteration, where habitat has been modified by dams and/or land conversion, water level, area and/or shape have been changed, vegetation cover has declined, but patches of natural vegetation remain; score = 3: severe habitat alteration, where habitat has been completely modified by dams and/or land conversion, water level, shape, and/or size of the site have changed significantly, and natural vegetation has largely disappeared.

We assigned a score to estimate fishing intensity at each site: score = 1: no fishing or low fishing intensity, where < 20 fishers were active at the site; score = 2: medium fishing intensity, where 21–40 fishers were active; score = 3: high fishing intensity, with > 40 fishers. The scores for habitat alteration and fishing intensity were assigned by three authors (OLD, TVP, LL), who together had > 45 years of experience in field surveys.

Our analyses included four sites newly surveyed in this study, in addition to the sites previously described by Le Duc et al. (2020a) and Pham et al. (2020). For each site, we calculated an overall conservation priority score that combined the presence, habitat alteration and fishing intensity scores, whereby a low overall score indicates a site of high conservation priority. The conservation priority score was calculated with the formula: presence score + habitat modification score + fishing intensity score. The highest possible priority would thus be a score of 3 (1 + 1 + 1), and the lowest possible priority would be a score of 10 (4 + 3 + 3). We analysed correlations between presence, habitat alteration, fishing intensity and overall priority scores using a Spearman's rank correlation coefficient (r _s). We used PAST 3.0 (Hammer et al., 2001) for all analyses, with alpha set at 5%.

Results

Interviewees in Son La and Lai Chau provinces reported 13 reliable sightings from 2010–2019, seven of which were in 2018–2019 (Table 1; see Supplementary Material 1 for a full summary of interview responses). Overall, we identified 13 sites where R. swinhoei may be present in the Da, Ma, Chu, and Red River systems, at a mean altitude of 98.6 ± SD 80.4 m (Table 2). One site had a presence score of 1, with one individual confirmed and possibly two others present, three sites a score of 2 (high probability of turtle presence), and nine sites a score of 3 (Fig. 1). If we combine the findings from our surveys with those from areas along the Da River and in Thanh Hoa province (Le Duc et al., 2020a), there is a total of 13 sites where R. swinhoei could potentially be present (Fig. 1), with sites 1 and 2 having the highest probability of presence based on the degree of habitat alteration and fishing intensity (Table 2), and sites 10, 11, 12 and 13 with multiple sightings reported over the last decade. Several of these reported sightings were in 2018 and 2019, predominantly at sites with more severe habitat alteration and higher fishing intensity (Table 1). In addition, these surveys combined provide evidence of 25 sites where R. swinhoei probably occurred until a few decades ago (Fig. 1). The assigned conservation priority scores for the different localities, with all variables, are shown in Table 2.

Fig. 1 Study area in northern Viet Nam, showing (a) the 13 sites where Rafetus swinhoei may be present, and (b) the sites where it was present before the 2000s (based on interviews with reliable descriptions of the species). For numbers of the various sites, see Table 2. To protect the sites, the precise locations are not shown; the circles indicate only the approximate locations. Scores for probability of the species' presence: 1: confirmed presence of R. swinhoei; 2: high probability of presence; 3: medium probability of presence (see Methods).

Table 1 Recent sightings (2010–2019) of Rafetus swinhoei that were reported in November 2019 by fishers from Son La and Lai Chau provinces, Viet Nam, along the Da River (only reliable reports were included; see Methods for details).

¹ For site numbers, see Table 2.

² A dash between two months (e.g. July–Aug.) indicates that the interviewee was unable to remember exactly the month of their observation, whereas an ampersand between two months (e.g. Apr. & Nov.) indicates that the interviewee reported distinct observations in different months.

Table 2 Details of the 13 sites with potential presence of Rafetus swinhoei, including the attributed scores for species presence, habitat alteration and fishing intensity (see Methods).

The scores for habitat alteration and fishing intensity were not significantly correlated (r _s = 0.472, n = 13, P = 0.103), and neither were those for fishing intensity and species presence (r _s = 0.068, n = 13, P = 0.827), nor for habitat alteration and species presence (r _s = −0.058, n = 13, P = 0.851). To protect the sites, their geographical coordinates are not reported here, but can be obtained from the authors on request. The general landscape of these sites is shown in Plate 1.

Plate 1 Landscape of some of the sites with potential presence of R. swinhoei in northern Viet Nam. (a) De lake, Thanh Hoa province; (b) Dap Nai dam, Buoi River, Hoa Binh province; (c) Dat hydro dam, Chu River, Thanh Hoa province; (d) Suoi Bung stream, Da River, Son La province; (e) Suoi Mu stream, near Hoa Binh dam, Da River, Hoa Binh province; (f) Dong Mo lake, Hanoi; (g) Suoi Hai lake, Hanoi; (h) Mu stream, Da River, Son La province; (i) Muong Sai section, Da River, Son La province.

The overall conservation priority score was statistically more affected by fishing intensity (r _s = 0.682, n = 13, P < 0.01) than by habitat alteration (r _s = 0.600, n = 13, P < 0.05) and species presence (r _s = 0.608, n = 13, P < 0.05), but overall the three variables had a similar weight.

Discussion

Our surveys provide new information about the potential presence of R. swinhoei in addition to the single location where the species is currently known, supporting the evidence previously reported by Le Duc et al. (2020a) and Pham et al. (2020). At least two sites (sites 1 and 3; Table 2) appear to be potentially suitable, and there have been reliable reports of occasional, recent sightings of the species at several other sites. We therefore consider it likely that R. swinhoei persists in additional sites in northern Viet Nam.

Several recent sightings were at sites with a relatively high density of fishers, perhaps because the probability of sightings increases when there are more observers. Sightings reported from sites with highly altered habitat cannot, however, be explained by collinearity effects between habitat alteration and density of fishers, as these two variables were not significantly correlated. The most likely interpretation is that R. swinhoei is an elusive, shy species that is rarely detected in the wild. It is therefore possible that the population of R. swinhoei is larger than believed and that the species can persist in remote areas where habitat alteration is low and fishing intensity moderate.

All sites with multiple recent sightings (10, 11, 12 and 13) were clustered along the northern course of the Da River system, far from other sites where the species could occur (Fig. 1). This suggests that R. swinhoei may persist throughout the area, but has gone undetected because of the remoteness of the areas and limited survey efforts. Further research needs to focus on the northern course of the Da River system.

Our evaluation of the conservation priority of sites where this rare and elusive freshwater turtle may occur was based on an assessment of the likelihood that the species was present, the degree of habitat alteration and fishing intensity. This method could also be applied elsewhere. It requires the acquisition of interview-based data and a general inspection of habitat features and densities of fishers, variables that are relatively easy to obtain. Our approach could be applied in other areas where field surveys of chelonians are logistically difficult or time-consuming. For example, our method could be used to study species such as Erymnochelys madagascariensis in Madagascar, Cyclanorbis elegans in continental Africa (Demaya et al., 2019a,b), and Chitra chitra, Chitra vandjiki, Chitra indica, Nilssonia formosa, Nilssonia nigricans, Pelochelys cantorii, Batagur affinis, Batagur kachuga and Batagur borneoensis in Asia. The method could also be used to study other threatened freshwater animals for which habitat loss and overfishing/overhunting are drivers of population declines (e.g. freshwater dolphins and large freshwater fishes).

However, there are also potential limitations of our method. Firstly, it is based on a combination of local ecological knowledge (interviews) and expert-based assessment of scores for habitat alteration and fishing intensity. As expert-based scores are influenced by researchers’ field experience, we recommend that only experts with > 5 years’ experience conduct field surveys and that the cumulative number of years of field experience of the surveyors is specified when publishing results. Averaging the scores independently assigned by multiple experts (three in our case) could also increase reliability. Seasonality can have a marked effect on perceived habitat characteristics and the density of fishers, and thus for highly seasonal environments we recommend that surveys are made in both dry and wet seasons or, if it is logistically difficult to survey in both seasons, to survey only in the wet season.

Based on the current knowledge of the species' distribution and population size, R. swinhoei is on the brink of extinction, with just two known living individuals. Further research should focus on locating additional live individuals in the wild and developing a robust conservation strategy. With respect to the sites we surveyed, site 1 has dense aquatic vegetation, hampering observational surveys. The remaining 12 sites have clear water surfaces, but sites 6, 7, 8 and 9 present logistical difficulties for observational surveys because of their complex spatial structure, with a number of islands present within the lakes. We recommend using trapping surveys at sites 1, 6, 7, 8 and 9, and observational surveys at other sites. Drones could facilitate sightings (Oliveira-da-Costa et al., 2020) and complement riverbank transects and visual searches by boat. In addition, we recommend monitoring fishers' catches, as newborn and juvenile R. swinhoei that can be mistaken for Pelodiscus sinensis because of the morphological similarities between the two species. Environmental DNA could also be used to survey for R. swinhoei (Rees et al., 2014; Davy et al., 2015; Kundu et al., 2018), but the efficiency of this method to detect freshwater turtles has been questioned (Raemy & Ursenbacher, 2018), and its applicability requires further investigation.