Mortality of Adult Green Turtles (Chelonia mydas) at the Nesting Beaches of Aldabra Atoll, Seychelles
Abstract
Adult mortality at the nesting site is an important demographic parameter for green turtles (Chelonia mydas) at Aldabra Atoll, Seychelles, where, between 1995 and 2008, records were kept of adult green turtles found dead (n = 158) or so trapped or incapacitated in the vicinity of the nesting beaches as to be unable to return to the sea without human assistance (n = 50). The main cause of death (n = 121) was entrapment and/or incapacitation on beach rock (62.0%), and adjusted rates of mortality were twice as high on the windward south coast as on the north coast and 3 times that on the west coast. Annual natural mortality, conservatively reported at 16–30 females per year, claims an estimated 0.3%–1.0% of the annual adult female nesting population at Aldabra, which is otherwise healthy, increasing, and free of terrestrial predation.
Population models are a tool for species management and conservation that rely on accurate data to quantify survival probabilities at all life history stages (Troëng and Chaloupka 2007; Hamann et al. 2010). The life history traits of many long-lived marine species include slow growth and delayed sexual maturity, both of which necessitate high adult survival probabilities to maintain populations (Congdon et al. 1993; Musick 1999; Bjorndal et al. 2005). While human slaughter of adult turtles at nesting beaches has caused worldwide declines in sea turtle nesting populations (Wallace et al. 2011), natural land-based predation of adult turtles is apparently rare and limited to only a few sites with large cats (Troëng 2000) and crocodiles (Sutherland and Sutherland 2003; Whiting and Whiting 2011). Most reports of natural mortality in adult turtles at the nesting beach primarily involve accidental deaths caused by unfavorable features of the physical environment, i.e., entanglement in beach vegetation or entrapment in mud (Fretey 1977), rocks or crevices (Limpus et al. 2003; J.A. Mortimer, unpubl. data, 1977–1978), or heat exhaustion subsequent to having become disoriented and wandering too far inland during the night (Mortimer and Day 1999; Limpus et al. 2003). In this study, we documented rates of mortality in adult green turtles (Chelonia mydas) associated with the rugged physical features of nesting beaches at Aldabra Atoll, Seychelles, and compare the results with those from other sites. The aims of this article were to (1) determine the natural mortality rate of nesting female green turtles in a healthy and growing population and provide data for future population modeling of this population, (2) assign causes of death and ascertain the most serious threats to nesting females at a site with no terrestrial predation, and (3) compare these rates and causes to those from other turtle nesting sites. Aldabra Atoll is a UNESCO World Heritage Site managed by the Seychelles Islands Foundation since 1983, and hosts a major green turtle rookery that has been the subject of a long-term conservation and monitoring program (Frazier 1971; Gibson 1979; Mortimer 1984, 1985, 1988; Mortimer et al. 2011).
METHODS
Study Site
Aldabra Atoll is a raised limestone reef in the western Indian Ocean (lat 09°24′S, long 46°20′E), which consists of 4 main islands plus hundreds of smaller islets. It has a total land area of 155 km2 and an outer perimeter of 83 km. Much of its surface geomorphology comprises rugged champignon, a deeply pitted and irregular solution-fretted reef rock, and platin, a smooth-surfaced pavement-like cemented limestone (Stoddart et al. 1971). Along much of the seaward coastline of Aldabra are champignon limestone cliffs that rise 3.5–4.5 m above the level of the intertidal reef flat or platform (Stoddart et al. 1971). Dispersed along the outer rim of this treacherous coastal terrain are 52 turtle nesting beaches, with a combined total length of 5.2 km (Mortimer et al. 2011). These beaches cluster within 4 sections of coastline (Tables 1 and 2; Fig. 1): West Grand Terre (WGT), South, North, and Settlement (SETT) beaches. For much of the year, the South beaches are subject to rough seas caused by the southeast trade winds, which blow from April to November, and peak from May to September at 81%–100% constancy and wind speeds of 6–8 m/sec (Farrow 1971). Between 1968 and 2009, mean annual dry bulb temperature varied between 26.4°C and 27.5°C (Duhec et al. 2010). The entire outer perimeter of the atoll (except at the entrances of the 4 passes that separate the main islands) is bordered by a shallow intertidal reef flat that dries out at low tide and effectively bars reproductive females from nesting at low tide. At extreme low tides parts of the reef flat become completely dry.
Citation: Chelonian Conservation and Biology 12, 1; 10.2744/CCB-0991.1
Data Recorded
Between 1995 and 2008, records were kept of adult turtles found dead in the vicinity of the nesting beaches along with those that had become so trapped or incapacitated as to be deemed unable to return to the sea without human assistance. The following information was recorded for both dead and rescued turtles: date(s) encountered; nesting beach identification number; apparent cause of mortality or imminent mortality; whether already dead or rescued from death; and sex of the turtle. Occasionally, turtles deemed capable of freeing themselves were also assisted to the sea; but these were not included in the data set.
The 4 sections of coastline were compared in terms of recorded causes of mortality, including “beach rock,” turtle trapped or incapacitated by beach rock, i.e., fallen into holes, wedged between rocks, or passage blocked by rock barriers; “upside down,” turtle upside down on the beach crest, having fallen off a ledge onto the sand above the high water mark; “vegetation,” turtle trapped or entangled by vegetation having wedged itself under roots or low branches and unable to use its flippers to either retreat or advance; “anthropogenic debris,” turtle trapped or entangled by man-made objects; “smashed,” turtle smashed onto rocks in shallow water and washed ashore; “internal,” no apparent cause of death, turtle having died on the beach without external injuries, possibly succumbing to an internal complication such as old age, heat exhaustion, disease, or asphyxiation (or possibly invisible injuries caused by falls or impacts associated with heavy surf); and “not recorded,” when field personnel simply neglected to record the cause of death.
Other types of accidental threat involved the low-tide stranding of postnesting females and of mating turtles stranded on dry sand or reef flat in full sun. Occasionally, when such stranded turtles appeared to be heat stressed, they were assisted either by herding, dragging, or carrying them to the water (Mortimer 1998), or by cooling them with buckets of water. But, these turtles were not included in the data set of our study because mortality did not seem imminent in most cases. Flipper tags were usually applied to both males and females stranded at low tide.
Data Analysis
By using figures for “total deaths” (TotDR) at each section of coastline, with TotDR defined as the sum of dead and rescued turtles recorded during 1995–2008, we derived a “mortality index” (Table 2) with which to assess the relative likelihood of mortality to individual turtles in each of the 4 sections (WGT, South, North, and SETT) by taking into account nesting density and beach length. First, “nesting density” (ND) was calculated for each of the 4 sections, as the ratio of “estimated mean annual tracks with digging (TrD)” for the period 2004–2008 (Mortimer et al. 2011) to “total beach length” (TBL) (Table 2). Given that nesting density differed between sections, each of the 4 NDs was then divided into 20.4 (the highest of the calculated NDs) to produce a conversion factor by which TotDR could be multiplied to produce “extrapolated deaths adjusted for nesting density” (ED) (Table 2). For each section, ED was then divided by TBL and multiplied by 100 to produce the mortality index for that beach section (i.e., an index of the relative likelihood that a turtle would die). To assess which beaches currently posed the greatest threat to nesting turtles, the 52 beaches were ranked according to the absolute number of TotDR recorded during 1995–2008.
RESULTS
The reported causes of mortality or potential mortality combined for 158 adult turtles found dead plus 50 rescued turtles that we assumed would have died without assistance along the 4 sections of Aldabra coastline between 1995 and 2008 are presented in Table 1. No cause was reported for 87 of the 208 turtles (42%), but, for the remaining 121 turtles, the causes were, in descending order of importance: beach rock (62.0% [n = 75]), upside down (20.7% [n = 25]), internal (7.4% [n = 9]), vegetation (6.6% [n = 8]), anthropogenic debris (1.7% [n = 2]), and smashed (1.7% [n = 2]). Where vegetation was involved, at least 5 of the 8 turtles had been trapped by tree roots of native plants (3 by Casuarina equisetifolia, 1 by Guettarda speciosa, 1 by Tournefortia argentea), and 3 were trapped by roots or branches of unidentified plant species. Two rescues involved entanglement in human-generated debris: a rope in 1 case (at North), and entrapment under a concrete grave marker (at SETT). What appeared to have been a mating couple (both male and female were found dead near each other a few meters from the high-tide line) was smashed onto the rocky shoreline on the South coast. This was the only male mortality reported. Beach rock accounted for 73.7% and 75.5% of all reported causes of mortality at the WGT and South beaches, respectively, whereas the predominant cause reported in the North (58.3%) was upside down (Table 1). Although strandings of postnesting females and mating pairs occurred regularly at low tide below the high water mark, sometimes leaving the animals exposed on dry sand, these were not included among our calculated TotDR.
The calculated mortality indices show that the overall levels of mortality adjusted for nesting density and beach length were highest at the South (30.7), followed by the North (14.7), WGT (9.6), and SETT (8.8) beaches (Table 2). Of the 208 TotDR recorded, 72% occurred on only 14 (27%) of the beaches, with 32.3% on South (nos. 28, 32, 33, 34, 35, 36), 17.8% on North (nos. 40, 41, 42, 45), 15.4% on WGT (nos. 8, 19, 20), and 6.3% at SETT beaches (Fig. 1). The sum of the TBLs of those 14 beaches is 2928 m, of which SETT accounts for 1880 m. When excluding SETT, 65.7% of TotDR occurred on 20.1% of the TBL. Between 1995 and 2008, the total numbers of turtles reported as either dead or rescued ranged from 7 (in 2002) to 31 (in 2003) (mean = 16.1 ± 7.4 SD; n = 14).
DISCUSSION
The average number of annual mortalities recorded at Aldabra during 1995–2008 was 16, but record keeping was uneven from year to year, with the greatest effort in 2003 when 31 mortalities (including 1 male) were recorded. Based on these data, we conservatively estimated a minimum average of 16–30 land-based mortalities annually among adult females at Aldabra. Mortimer et al. (2011) estimate that, during 2004–2008, an average of 28,152 ± 4867 SD tracks with digging, and 15,700 ± 2776 SD egg clutches, were produced annually at Aldabra. If we assume that the average female laid 3–5 egg clutches per season (Mortimer et al. 2011), this would be equivalent to a population of 3140–5233 females nesting annually. It follows that land-based mortality that involves 16–30 females annually at Aldabra would have claimed a minimum average of 0.3%–1.0% of the annual nesting population.
The mortality indices that we used to adjust raw TotDR for nesting density and beach length indicate that the actual rate of turtle mortality at the South beaches is the highest on the atoll, being twice that in the North, and more than 3 times the rates measured at WGT and SETT (Table 2). Most of the land-based accidental mortality among adult turtles at Aldabra is caused by beach rock (75%), especially along the South coast (Table 1) where turtles are subject to both highly rugous champignon terrain and rough seas during most of the year. A high proportion of dead turtles in the North (58.3%) were found upside down. Rugged champignon characterizes much of the coastline of the atoll (especially along the WGT, South, and North sections of coastline), and the champignon cliffs in the North are particularly high (i.e., 3–4 m). In addition, the nesting density in the North is greater than that elsewhere on the atoll, and it is possible that the proximity of other turtles increases the tendency for a female to wander from the beach platform to an adjacent cliff ledge, fall, and land on her back. This likelihood may also be exacerbated by beach length. The average length of North coast beaches (33.2 ± 24.1 m SD; n = 9) is less than half that of the WGT (73.5 ± 55.0 m SD; n = 24), South coast (74.9 ± 40.8 m SD; n = 18), or SETT (1880 m; n = 1) beaches.
The ultimate cause of most mortality recorded at Aldabra was heat stress, which is also a problem at other rookeries. At Raine Island Australia, where thousands of nesting green turtles can succumb to heat stress during a single nesting season, Limpus et al. (2003) studied the limits of thermal tolerance in naturally stranded adult green turtles. They measured the core body temperature of moribund turtles by inserting a cannula through the inguinal pocket anteriodorsally to the movement arch of the hind leg. The body temperature of upside down turtles (with light-colored plastrons facing skyward) remained lower than that of turtles whose dark-colored carapaces were facing upward. Although the nighttime core body temperatures of nesting turtles at Raine Island ranged from 26°C to 30°C, that of moribund turtles on the beach platform increased from 35.8°C at 1040 hrs to as high as 40.4°C at 1230 hrs. All turtles died once the core body temperature exceeded 39°C. The time of death varied from 1230 hrs to 1640 hrs (mode = 1445 hrs). At Raine Island, the mean monthly daily air temperatures were above 25°C year round but did not exceed 35°C (Limpus et al. 2003). Similar temperatures were recorded at Aldabra between 1968 and 1991, where the range for annual mean maximum was between 29.0°C and 30.8°C (Duhec et al. 2010), with the highest monthly mean temperature of 36.3°C recorded in January 1968 (Farrow 1971). Mating and postnesting turtles stranded on the Aldabra reef flat at low tide would probably not be threatened by heat stress given enough shallow water remaining on the flat to keep them cool. For that reason, we did not include such stranded turtles among the TotDR in the present study. It is conceivable, however, for postnesting females stranded at low tide at midday on either dry sand or dry reef flat at Aldabra to occasionally die of heat stress and float out to sea undetected with the rising tide.
The rates of natural adult mortality at Aldabra (0.3%–1.0%) are compared with those documented at 4 other sea turtle rookeries in Table 3. The rates at Aldabra are lower than those recorded at 4 beaches in French Guiana (> 3.14%; Fretey 1977) and Raine Island and Moulter Cay on the Northern Great Barrier Reef (2.3%) (Limpus et al. 2003) but higher than those recorded at Ascension Island (0.07%–0.12%) (J.A. Mortimer, unpubl. data, 1977–1978), and Tortuguero, Costa Rica (0.04%–0.06%; Emma Harrison and Sea Turtle Conservancy, unpubl. data, 2006–2010). The green turtle rookery of Ascension Island (South Atlantic Ocean) is characterized by rugged volcanic terrain similar in texture to that at Aldabra. But, during the combined 1976–1977 and 1977–1978 nesting seasons, when an estimated combined total of 3300–5980 females nested at Ascension (Mortimer and Carr 1987), only 3 turtles were rescued from rock crevices and a fourth was found dead on the beach with her trachea full of sand (J.A. Mortimer, unpubl. data, 1978). Even lower mortality was recorded at Tortuguero, Costa Rica, site of the largest green turtle nesting population in the Atlantic Ocean (Bjorndal et al. 1999). There, along the 8-km study beach, during 5 nesting seasons an estimated combined total of 109,521 egg clutches were laid; but only 13 accidental natural mortalities were recorded (including 12 deaths and 1 rescue) (Emma Harrison and Sea Turtle Conservancy, unpubl. data, 2006–2010). Given that regular nesting beach surveys were conducted throughout the seasons in question, search effort for dead turtles at both Tortuguero and Ascension Island would have been comparable to that at Aldabra.
Limpus et al. (2003) estimated that, at Raine Island and Moulter Cay, during a high-density nesting season with up to 131,000 nesting females (Limpus 2008), approximately 3000 died from heat exhaustion, primarily as a result of disorientation induced by a combination of sparse vegetation, flat terrain, and a depression in the interior of the island, which, together, obscured the orientation cues needed by turtles to distinguish between the seaward and landward directions. This caused some turtles to travel too far inland during the night and then to be unable to reach the sea before being overcome by heat exhaustion (Limpus et al. 2003). Similar disorientation and mortality was documented by Mortimer and Day (1999) at Nelson Island in the Chagos Islands, but its impact on that population was not quantified. At Raine Island, the mortality rate increased with nesting density (Limpus et al. 2003) because females were forced inland by the crowding of thousands of nesting turtles up on the beach of an island with a circumference of only 1800 m. Rates of accidental mortality at Aldabra may also be density dependent, in which case, they can be expected to increase in coming years as the nesting population continues to rise, it having already increased by 500%–800% during the 4 decades since 1968 when the population had reached critically low levels in response to overexploitation (Mortimer et al. 2011). To promote continued population growth, and also to minimize suffering of the animals, we recommend that the Seychelles Islands Foundation field personnel continue to rescue trapped turtles and also maintain records of all dead and rescued turtles. Mortality rates may change in this growing population and data on this will be important for future population models. To that end, a special effort should be made to routinely check those 14 beaches that our study shows to be particularly hazardous to nesting turtles (Fig. 1). In more general terms, quantifying rates of adult mortality at the nesting beach, particularly at a site with a healthy and growing population and few local anthropogenic threats, provides an important demographic parameter needed to produce accurate population models. Such baseline information is relevant to a better understanding of the effects of other mortality factors (such as those induced by fisheries) that pertain to sea turtle population dynamics.
Maps showing locations of: (a) Aldabra in the Western Indian Ocean; and (b) Turtle nesting beaches and 4 major beach groups on Aldabra Atoll considered in the present study: West Grande Terre beaches nos. 1–22 (WGT); South beaches nos. 23–39; North beaches nos. 40–46, 55; and Settlement beach no. 47 (SETT). The highest mortality (total turtle deaths plus imminent deaths recorded) was recorded at the following beaches: WGT (nos. 8, 19, 20), South (nos. 28, 32, 33, 34, 35, 36), and North (nos. 40, 41, 42, 45).
