Fragmentation and Demography as Causes of Population Decline in Seychelles Freshwater Turtles (Genus Pelusios)
ABSTRACT
In the Seychelles islands, all 3 endemic freshwater turtle taxa are either extinct (Pelusios seychellensis) or critically endangered (Pelusios castanoides intergularis and Pelusios subniger parietalis). These turtles are threatened by habitat loss, and monitoring of populations since 1996 has identified significant ongoing population declines. Drainage of wetland sites has reduced the number of populations, but even surviving sites are mostly reduced in area and quality. Only 5 Pelusios subniger parietalis and 3 Pelusios castanoides intergularis populations showed evidence of reproduction within the last 10 years. Longevity records suggest that Pelusios species may live for at least 40 years, and captive breeding data indicate that sexual maturity may be comparatively early in these taxa (ca. 2 years). Populations can persist for decades after reproduction has ceased, resulting in effective population extinction, even when environmental conditions stabilized. This is a characteristic that is shared with other long-lived species, and demography should be an essential component of recovery plans for any such species. Conversely, improvement in habitat may allow rapid population recovery, as has been demonstrated in Pelusios subniger parietalis on Fregate Island.
The “extinction crisis” has recently been evaluated as threatening 41% of species that have been assessed (Baille et al. 2004). These are at risk of extinction from a wide range of factors, but general patterns have been identified based on particular threats that are faced by species with slow generation times and delayed maturity (Purvis et al. 2000; Dulvy et al. 2003; Fisher and Owens 2004), and also the presence on occupied islands where such vulnerability is magnified by high human pressures and intrinsically small population sizes (MacPhee and Flemming 1999). Taxa that combine these life history traits and insular distributions would be expected to show exceptionally high levels of threat, as is the case in freshwater turtles. Overall, 60% of the 159 freshwater turtle taxa are threatened, but, of those restricted to islands 71% are threatened (IUCN 2004). The highest proportion of threatened island turtles is found on the Seychelles islands, where all 3 endemic taxa are critically endangered or extinct.
The Seychelles islands support 3 species of freshwater turtles that belong to the Pelomedusidae. These comprise 2 endemic subspecies of African mud turtle, Pelusios subniger parietalis Bour, 1983, and Pelusios castanoides intergularis Bour, 1983, and an endemic species, Pelusios seychellensis (Siebenrock 1906) (Fig. 1). In addition, there have been records of the Nile softshell Trionyx triunguis (Forsskål 1770), red-eared slider Trachemys scripta elegans (Wied 1839), and Pelusios sinuatus (Smith 1836), all wild animals escaped or were released from captivity. The endemic taxa are biogeographically important as being the only Pelomedusidae found naturally on oceanic islands. Otherwise, the family is found in Africa and Madagascar, with introduced populations in the Chagos and Mauritius (both apparently extinct) and in Guadeloupe (Bour 1983). Of the 3 taxa, P. subniger parietalis and P. castanoides intergularis are representatives of southeastern African and Madagascan species (Bour, 1983) and may be of relatively recent origin, possibly dispersing from Africa during periods of lowered sea level during glaciations some 100,000 years ago. In contrast, P. seychellensis appears to be related to both the west African P. castaneus (Schweigger 1812) by its shell morphology and the east African P. castanoides Hewitt, 1931, by its skull features (Bour 1983), and may be a more ancient component of the fauna.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Pelusios subniger parietalis and P. castanoides intergularis are widespread in the granitic islands of Seychelles (Bour 1984; Gerlach and Canning 2001), although population densities are very low. In contrast, P. seychellensis is one of the least known species of Testudines: 3 specimens were collected in 1895 by August Brauer, and these remain the only definite evidence of the existence of the species. There are no locality data associated with the species, Brauer was in Seychelles when they were collected and visited the islands of Mahé, Praslin, and Silhouette, but which of these was the source of P. seychellensis is not known. However, in 1909, Siebenrock, referring to Brauer, informally restricted the type locality to Mahé. The specimens were initially described as Sternothaerus nigricans seychellensis by Siebenrock (1906) and were recognized as a distinct species by Bour (1983), who noted its close resemblance to P. castaneus.
Throughout the 1900s, all Seychelles freshwater turtles were in decline because of drainage of coastal wetlands. In the 1960s, stuffed specimens were sold as curios to tourists (Honegger 1966), and according to High (ca. 1972), some turtles were eaten during celebrations. A survey of distributions was carried out in 1996, and a status assessment was published in 2001 (Gerlach and Canning 2001). Since 1996, population monitoring has been maintained and recent field research has updated the status assessment; the current conservation situation is described below.
METHODS
The current status of Seychelles freshwater turtles was determined by visual searches of marshes and rivers, and by trapping of all apparently suitable water bodies (Table 1); sites not trapped were considered unsuitable for turtles on the basis of regular sea incursion or residents reporting the absence of turtles. Trapping used baited hoop traps (described in Gerlach and Canning 2001) baited with tuna in vegetable oil; this has been successful for catching P. castanoides and P. subniger. Traps were emptied and rebaited every morning for at least 4 days, and all turtles caught were marked with marginal notches, sexed, measured, and released next to the trap. After the initial study in 1996, specific localities were studied in more detail on a semi-annual basis. These were localities occupied by comparatively large turtle populations (Rivière Mare Anglaise, Mahé, and Anse Kerlan, Praslin) or where observations suggested the possibility of the occurrence of P. seychellensis (Beau Vallon, Mahé).
For comparative purposes, population data are divided into 2 time periods: 1996–2000 and 2001–2005. This division is arbitrary, but 1999–2000 represents the time of greatest recent disturbance of Pelusios populations, with the drainage of Anse Kerlan on Praslin, modification of the marsh on Fregate island, and construction work around the Rivière Mare Anglaise population on Mahé. Thus, the first 5 years of data largely predate these disturbances, whereas the last 5 years represent the current situation.
RESULTS
Turtle presence was confirmed in 10 sites (of which 8 were occupied by P. castanoides and 5 by P. subniger) in 1996–2000, and in 2001–2005, 11 sites were located (9 P. castanoides, 8 P. subniger). No P. seychellensis populations were found. The results of surveys are summarized in Table 1 and Figs. 2 and 3.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Pelusios castanoides was located in lowland rivers (Fig. 4) and in some marshes, whereas P. subniger was located only in marshes. Pelusios castanoides population densities were higher in rivers than in marshes, and, in optimal habitats, both species occurred at similar densities (133–150/ha for P. castanoides in rivers, compared with 125/ha for P. subniger in marshes). Data from 2001–2005 show a notable decline in population density from 1996–2000 in both species and in both habitats where they occur (Fig. 5). This estimates population change within 5 to 10 years in P. castanoides from approximately 390 to 120 individuals and in P. subniger from 950 to 660, declines of 69% and 31%, respectively (Table 3).
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Pelusios castanoides intergularis
Mahé and Nearby Islands
Populations of P. castanoides (Fig. 1a) were confirmed in lowland rivers in the north of Mahé (Rivière Mare Anglaise and Beau Vallon) and the south (Anse Royale) (Fig. 2). There were isolated records from other localities, but these were identified as single individuals that represented relict populations (Anse La Mouche and Port Launay) or recently released captive individuals (Anse Aux Poules Bleus). The species is also present on Cerf Island. Population size could not be determined for Anse Royale, where turtles are recorded moving out of the degraded river habitat, but no resident population could be located by trapping. All the turtles observed in this area were very large adults; there is no evidence of recent reproduction. Trapping in the north of Mahé identified 14 individuals; mark-recapture studies recorded no unmarked turtles in the Rivière Mare Anglaise by 2000. Two unmarked turtles were caught at the Beau Vallon marsh in 2003, these have been observed subsequently, and it is believed that all individuals in this population have now been recorded. One subadult (carapace length 10.8 cm) and 1 juvenile (9.2 cm) were caught in 1996 and 1998, respectively. There is no further evidence of recent reproduction.
Silhouette
Only 3 wild P. castanoides have been recorded, all in the La Passe marsh. These comprise 1 large male, 1 small female, and a juvenile (8.0 cm, captured in 2000). Apparently suitable nesting areas are present, but the area of freshwater habitat is very small. Hotel construction in 2005–2006 caused significant disruption to the marsh, including pollution. No evidence has been found of turtle survival since 2005, although the habitat is now restored.
Praslin
In 1996, a small population of P. castanoides was recorded at Anse Kerlan (Fig. 6a). The loss of 90% of this site in 1999 (Gerlach 2004) reduced the population to a small number of individuals in a marsh of 400 m2 (Fig. 6b). Trapping at the site in 2003 failed to locate any surviving P. castanoides, a single old female was caught in 2004, and it is believed that this population is now functionally extinct. Although the small area of aquatic habitat is healthy, it is under threat from development and lacks any suitable nesting areas. Other degraded sites on the eastern side of Praslin support turtles: reports from Grande Anse were substantiated with the capture of a single large male. This area also lacks nesting areas and cannot support a reproductive population.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
La Digue
Pelusios castanoides is present in the Mare Soupape, and reproduction continues (a juvenile of 9.2 cm was caught in 2004). Conditions in the marsh have been unstable because of periodic smothering of aquatic habitat by water lettuce Pistia stratiotes (Fig. 7) and the level of recruitment is not known, although a healthy age structure is present in the population (Fig. 2). Population density has decreased since 2000, unlike other areas, this does not appear to be because of a loss of nesting habitat and is probably due to the unstable conditions.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
Fregate
The first P. castanoides was located on this island in 2002 (Gerlach 2004). Trapping by the island's conservation management since then has located a total of 5 individuals, 4 adults, and a single subadult (S. Hill, pers. comm., April 2005).
Pelusios subniger parietalis
Mahé and Nearby Islands
Pelusios subniger (Fig. 1b) is restricted to the stationary or slow flowing marshes. Five recent localities have been identified: Rivière Mare Anglaise, North-East Point, Anse Forbans, Anse Intendance, and Petit Police (Fig. 3). The former is represented by a single individual trapped in 2004. The area of suitable marsh has decreased from some 100 ha historically to 0.5 ha in 1996, less than 0.1 ha in 2004, and was completely drained by 2005. A similar decline has occurred at North-East Point, turtles are still occasionally reported from this site, but there has been no confirmation since 1996. The only substantial population in recent times was at Anse Forbans, where residents frequently encounter animals on the roads and collect them. These animals represent a wide range of sizes, including juveniles and approximately equal proportions of both sexes. Attempts to trap turtles at this site failed because of the lack of pools in the reed bed deep enough for proper siting of traps. In 2005–2006, this site was almost entirely drained. Only isolated records have been received from Anse Intendance and Petit Police, and the size of these populations remains unclear.
Pelusios subniger is extinct on St. Anne Island, where all marsh habitat was drained in the 1980s, but a small population survives on Cerf Island.
Silhouette
Pelusios subniger was reintroduced to Silhouette experimentally in 2001 (Gerlach 2002a, 2004). Five adults were released, and, in 2002–2003, juveniles were also released in the Grande Barbe marsh (Gerlach 2004). Radio tracking of the adults resulted in their location 6 months after release (Gerlach 2002a), trapping has relocated one of the adults 2 years after release and, subsequently, 3 have been observed; this represents adult survival of at least 60% over 3 years. At present, there are no data on juvenile survival.
Praslin
Pelusios subniger was located only at Anse Kerlan, where a very large population was recorded in 1996. The loss of most of this site in 1999 (Gerlach 2004) restricted the Praslin population to 2 relict sites. A dense population of P. subniger was located in the surviving 400 m2 of the Anse Kerlan marsh in 2004. These were all large individuals; there is no evidence of recent reproduction. In addition, some P. subniger survived in the drained areas and have been able to colonize the water features of the Lemuria golf course. A substantial population is present, and reports of small individuals suggest that successful breeding is occurring (E. Jeannevo, pers. comm., March 2005).
La Digue
As with P. castanoides, P. subniger persists on this island. Most of the Mare Soupape is too deep for occupation by P. subniger, the periodic smothering of aquatic habitat by water lettuce may be associated with recent declines in population density of this species on the island.
Fregate
In the 1980s, only a small area of marsh (a network of cleared ditches) existed on this island, and it was assumed that the 10 individuals found in 1983 (Bour 1983) represented the majority of this introduced population (R. Bour, pers. comm., May 2005). Drainage of the marsh and its replacement by a new marsh area in 1999 appears to have been beneficial to P. subniger, and trapping has identified 100 individuals on the island (Hill, pers. comm., May 2005).
Pelusios seychellensis
In November 1994, a female turtle was found on Mahé Island and photographed; it was released in the Beau Vallon marsh. The photographs were examined and suggested to be of a P. seychellensis (Gerlach and Canning 1996). However, a number of the supposedly P. seychellensis characters were subsequently found in P. castanoides intergularis individuals, and the identity of the 1994 photographs remains uncertain. In 1997, it was suggested that P. seychellensis was extinct or had hybridized with P. castanoides to the extent that no pure P. seychellensis remained (Gerlach 1997). In October 2002, a turtle was observed in the Beau Vallon marsh on Mahé, which appeared to show the coloration and general outline of P. seychellensis in contrast to 2 readily identifiable P. castanoides at the same site (Gerlach 2004). This unusual individual was very dark, appearing black; the plastron could not be seen properly but also appeared to be black; the outline was rounded rather than the usual elongate shape of P. castanoides, and the skin was notably brighter yellow than in P. castanoides. This raised the possibility that P. seychellensis might survive in this locality. In December 2002, trapping resulted in the capture of 3 turtles. Two were female P. castanoides, and the third individual was also identifiable as P. castanoides but bore some resemblance to the “P. seychellensis” released in 1994 and also to the October 2002 sighting. Whether or not these were all the same individual cannot be determined.
DISCUSSION
Pelusios castanoides intergularis was located in lowland marshes and slow-flowing rivers; population densities were highest in rivers with woodland cover and abundant fresh-water mollusc populations. P. subniger parietalis was only located in lowland marshes. These marshes varied in characteristics, sharing very slow water movement and shallow water.
Historically, one of the most significant turtle populations in Seychelles was on Praslin Island. The drainage of the last coastal marsh on the island in 1999 resulted in the loss of 90% of the habitat. This area is now covered by an airport, housing, and a golf course. The remnant area of marsh (400 m2) does not contain any suitable nesting habitat and is adjacent to areas of housing; the small terrapin population remaining in this area has no long-term future. The golf course contains large water features with good-quality habitats, including reed beds. These support a diverse aquatic fauna and have attracted populations of bitterns and migratory ducks. Of the turtles, P. subniger parietalis has colonized the area and has a secure population at the site, but P. castanoides intergularis is more strictly aquatic and has not been able to cross unsuitable habitat and colonize the area.
Only 5 P. subniger populations showed evidence of reproduction within the last 10 years: Mare Soupape on La Digue, Fregate, Lemuria on Praslin, Cerf, and Anse Forbans on Mahé. Recent reproduction of P. castanoides was recorded only on Cerf, at Mare Soupape on La Digue, and La Passe on Silhouette, but after the disturbance in 2005–2006, this latter population is now thought to be extinct. From the growth rates of captive bred turtles, it is estimated that P. subniger can reach adult size at 21 months (males) to 2 years (females) (Fig. 8a). This is for juveniles kept in aquaria and fed daily. In the wild, this species spends long periods of time buried on dry land, and growth rates would be expected to be much lower. It is not known if this behavior is shown by juveniles; the estimates, therefore, must be considered minimum possible ages for maturity. To date, no P. castanoides have been reared to maturity, extrapolation of growth rates suggests attainment of adult size after approximately 2 years (Fig. 8b). If these estimates are related to field data, it would appear that the juvenile P. castanoides caught in Rivière Mare Anglaise in 1996 and 1998 were about 2 years old, indicating that the most recent evidence of reproduction in this site was in 1996. Conversely, the Fregate population would be expected to show signs of expansion shortly after habitat restoration, with the possibility of rapid growth after 2 years, from about 2001, as has been reported for P. subniger (S. Hill, pers. comm., May 2005). Reproduction appears to have ceased at 3 sites where populations still existed in 2005 (Rivière Mare Anglaise, Beau Vallon, and Anse Royale). At 2 sites on Praslin, total extinction appears to have occurred in 2004–2005.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0635.1
There are no data on the longevity of wild Pelusios. In captivity wild-caught adults have been kept for a large number of years: 6–14 years for P. sinuatus, 7–14.5 for P. niger, 15.5 for P. gabonensis, 24.5–40.5 for P. castaneus, 4.5–40.5 for P. adansoni (Flower 1925; Bowler 1975; Goin et al. 1978; Slavens and Slavens 2003). There are no data for P. castanoides, but for Pelusios subniger there are records of 24–29 years (Bowler 1975), with a maximum record of a female kept for at least 47 years (Slavens and Slavens 2003). From this, it would appear that populations are likely to persist for at least a decade after reproduction has ceased. Population decline is likely to be further exacerbated by adults migrating away from the deteriorating sites, as appears to have occurred on Praslin and at Rivière Mare Anglaise. The recent extinction of P. subniger on Cousin Island may be a consequence of this longevity. The Cousin population was introduced from La Digue in the 1940s (Bour 1984); although no significant changes occurred to the small seasonal marsh, turtles disappeared from the island in the 1990s. It is possible that this was the result of the habitat being suitable for a small number of adults but not suitable for reproduction. Recruitment failure would lead to the loss of an introduced population some 40–50 years after introduction. In this context, it is important that the success of future reintroductions be evaluated by investigation of recruitment and not just adult survival or breeding.
The present study has not confirmed or refuted the survival of “P. seychellensis” turtles. The status of P. seychellensis and its morphological distinction from P. castanoides are being reviewed (Gerlach, in prep.).
Conservation of Seychelles turtles requires the effective protection of the existing reproductive populations (Anse Forbans, Cerf, La Passe, Mare Soupape) as an urgent first measure. The declining sites could also be protected and the nesting areas restored, but this is a more difficult proposition, because these conservation requirements conflict with the development pressures that caused the deterioration. Further secure reproductive populations need to be established, the proposals made in the Seychelles Terrapin Action Plan (Gerlach 2002b) would result in the establishment of secure populations in improved habitat at La Passe on Silhouette (150–200 P. castanoides and 75 P. subniger), Grande Barbe on Silhouette (475–600 P. castanoides and 125 P. subniger), North Island (25–75 P. castanoides and 125 P. subniger), Lemuria on Praslin (25–50 P. castanoides in addition to the 60–75 P. subniger already present) and Aride island (25 P. subniger). This would require the release of approximately 36 P. subniger and 40 P. castanoides either from captive breeding or translocation from nonreproductive populations.
All Seychelles freshwater turtles are protected by the Wild Animals (Seychelles Pond Turtle) Protection Regulations of 1966. The turtles occur only in one protected area (parts of the Mare Soupape on La Digue). Specific conservation action for Seychelles terrapins has been implemented by the Nature Protection Trust of Seychelles in a research and captive breeding program aimed at fulfilling the Seychelles Terrapin Action Plan.
Pelusios subniger was first bred in captivity in 2001, since then, 18 juveniles have been reared and released in the Grande Barbe marsh system on Silhouette. Incubation of this species has been successful at a range of temperatures, and hatchling embryonic sex ratios indicate that genetic sex determination occurs in this species. Pelusios castanoides was first bred in 2004. Only 3 hatchlings have been produced as a result of over 70% mortality during hatching. Premature hatching may be the result of excessively high incubation temperatures; this species may require lower temperatures than have been used to date, this is currently being investigated.
The persistence of turtle populations long after reproduction has ceased has effectively masked the precarious status of such populations. This may be a situation shared by many long-lived species, which could undergo sudden declines to extinction in the absence of any significant external threat factor in the recent past. Accordingly, it is essential that evaluations of species status and conservation prioritization take account of historical threats that shape the current demography of such species. The Seychelles Pelusios turtles combine this longevity with the potential for rapid population growth. This provides hope that, with remedial action to restore breeding sites and establish secure populations, these critically endangered taxa can be saved in the near future.
Seychelles freshwater turtles. a. Pelsuios castanoides intergularis. b. Pelusios subniger parietalis. c. Pelusios seychellensis (photograph R. Bour).
Size distributions of Pelusios castanoides intergularis populations. Black bars: 1996–2000 data; gray bars: 2001–2005 data. Size categories (in mm): < 40 mm, 40–59, 60–79, 80–99, 100–119, 120–139, 140–159, 160–179, 180–199, > 200.
Size distributions of Pelusios subniger parietalis populations. Black bars: 1996–2000 data (except for Fregate 1983 from R. Bour pers. comm., 22 May 2005); gray bars: 2001–2005 data. Size categories as in Fig. 2.
Pelusios castanoides habitat at the Rivière Mare Anglaise, Mahé.
Population density changes in Seychelles turtles between 1996–2000 and 2001–2005. Mean densities are shown with standard errors of estimates.
Anse Kerlan marsh on Praslin, the undisturbed marsh in 1996 (a), the remnant area in 2004 (b)
Marsh habitat at Mare Soupape, La Digue smothered by water lettuce Pistia stratiotes in 1996.
Growth rates in captive Pelusios subniger parietalis (a) and P. castanoides intergularis (b). Adult size ranges are shown at the right.
