Adapted From: Proc. 1st Intern. Symposium on Turtles & Tortoises: Conservation & Captive Husbandry. pp. 138-159, 1991. [Original includes 4 tables]

The Management and Breeding of the Asian Forest Tortoise (Manouria emys) in Captivity

by Sean McKeown, Duane E. Meier and James O. Juvik

Abstract

The Asian forest tortoise [Manouria emys (formerly Geochelone emys)] is the largest tortoise inhabiting tropical Asia. First captive bred at the Honolulu Zoo in 1978, reproduction has continued to occur there over a multi-year period and in several other collections in the United States and Europe as well. This paper summarizes the data from five separate captive populations as well as elaborates on the unique nesting behavior of this species which includes the construction of a large above ground leaf-litter/earth mound. Collection of nest building material is accomplished by the female "backsweeping" ground litter for several days before and after egg deposition. The nesting female assumes nest guarding behavior against potential predators for a period of 3-20 days. The female also continues to rework the external parts of the large nest during this time period. When incubated artificially at temperatures ranging between 25.6-28.9° C (78-84° F) the egg incubation period is relatively short varying from 63-84 days.

Introduction

Description and Taxonomy

The two Asiatic tortoises included in the genus Manouria, the Asian forest tortoise (Manouria emys) and the impressed tortoise (M. impressa) are considered the most primitive living tortoises (Pritchard, 1979; Moll, 1989). Their affinities to ancestral emydines is demonstrated by the broad, flattered carapace, the paired supracaudal scutes, posteriorly expanded nuchal scute and utilization of mesic, rather than xeric, habitat (Pritchard, 1979). The Asian brown tortoise is the largest terrestrial Asian chelonian. Specimens attaining a length of over 60 mm (2 ft) and a weight of 37 kg (84.4 lb) have been recorded (Moll, 1989). An enlarged patch of tubercular scales is present on each thigh and the species is sometimes referred to in the literature as the "six-legged" or "six footed" tortoise. Other common names include Asian brown tortoise, Burmese mountain tortoise and Burmese brown tortoise. Two subspecies are currently recognized Manouria e. emys (Schlegel and Muller, 1844) and M. e. phayrei (Blyth, 1853). Manouria emys phayrei is also referred to in much of the literature during the late 1970's and early to mid 1980's as Geochelone nutapundi based on the species account in Wirot, 1979. Each of the subspecies is characterized as follows:

Distribution and Habitat

This chelonian inhabits the temperate, moist, broadleaf forests of Southeast Asia that come under the influence of monsoon rains. It is most typically found in upland mesic habitats. During the warmer parts of the day these tortoises prefer to soak in pools or to remain in the shade, out of the sun's rays. Wirot (1979) reports that individuals may burrow in damp soil. They are primarily herbivorous. Manouria e. emys ranges from peninsular Thailand into Malaysia, Sumatra, and Borneo. Manouria e. phayrei occurs in India, Burma and western Thailand (Moll, 1989). This species is heavily exploited by man throughout its range for food. While little "hard data" exists, anecdotal accounts by indigenous peoples would indicate that these tortoises are becoming increasingly rare. They are mainly encountered in remaining forest habitat well away from human habitation. Collection for both food and for medicinal purposes and accelerated deforestation will only continue to make their survival more precarious. Although this tortoise receives nominal protection under Appendix II of CITES, it is moderately exploited in some areas for the exotic pet trade. Adult tortoises sell for over $500 each in Japan (Moll, 1989) and fetch $250-400 on American dealer price lists.

Methods

In 1975 four Asian brown tortoises were donated to the Honolulu Zoo by Fay Haserot, a member of the California Turtle and Tortoise Club. Fay selected the Honolulu Zoo as a place for her animals because of its subtropical climate which is ideal for managing tortoises outdoors year round and the track record of that institution in breeding other terrestrial chelonian species including Geochelone elephantopus (Galapagos tortoise) and Geochelone elegans (Indian star tortoise). During 1977 these four tortoises consisting of two (1.1) large adult Manouria e. phayrei, an adult female M. e. emys and a young adult M. e. emys were moved to a spacious grassed outdoor enclosure approximately 30 x 30 m. Several large trees afforded abundant shade. A mud wallow large enough for all four to soak in at the same time was created with a hose feed-in on one end. The Asian brown tortoises shared this yard with two species of Australian macropods, a pair of emus and one pair of Cape Barren geese.

In addition to the abundant natural grasses, the four tortoises were offered a supplemental diet daily consisting of leafy vegetables, fruits, and small amounts of moistened dog chow as per the typical Honolulu Zoo diet for adult tortoises during the 1970's and early 1980's as noted in McKeown, 1982. Theralin or vionate vitamin/mineral supplements were lightly sprinkled on the food twice weekly. No additional calcium additive was used. When the tortoises were moved into this exhibit the male M. e. phayrei had a straight line shell length of 514 mm and a weight of 26 kg. The female M. e. phayrei measured 540 mm and weighed 30 kg.

Captive Behavior

Members of this species when housed in large, naturalistic enclosures, are highly gregarious. Most, but not all social interactions are involved with some aspect of courtship.

Head Bobbing

Fig. 2 Head Bobbing Head bobbing was utilized by all four tortoises. Head bobbing was employed both during non-sexual social interaction and during courtship. Two types were employed 1) horizontal bobbing and 2) elevated bobbing. Both sexes employed the same head bobbing techniques. These techniques were not varied whether directed towards a tortoise of the same or opposite sex. The most frequent individual to employ head bobbing was the large adult male M. e. phayrei. The individual that utilized this behavior the least was the female M. e. emys. Preliminary observations indicate that head bobbing is not typically reciprocated by the female during male courtship attempts. During other, non-sexual social interaction between these tortoises mutual head bobbing occasionally occurred.

Aberrant Sexual Behavior

Courtship of One Female Toward Another Female Female to female courtship was occasionally observed between 1975-1983, not only with Manouria emys, but also with radiated tortoises (Geochelone radiata) and red-footed tortoises (Geochelone carbonaria) at the Honolulu Zoo. Typically the entire male courtship routine (excluding penetration) or major portions of the routine were played out, including vocalization and mounting. A very typical sequence with Manouria emys was observed during April 1983 by University of Hawaii ethology student Cindy Kleh. The female Asian brown tortoise (Manouria e. emys) began courting the female Asian forest tortoise (Manouria e. phayrei). Initially the female M. e. emys emitted soft 1-2 second groans with long intervals of 2-7 minutes in between groans. This was followed by the female M. e. emys attempting to mount the female M. e. phayrei. She succeeded in mounting twice. In each instance the female M. e. phayrei aggressively overturned the female M. e. emys, a behavior she had never been employed with the males. After the second unsuccessful attempt, the female M. e. emys walked away leaving the other female alone. Typically, advances by one female tortoise to another in M. emys as well as in the G. radiata and G. carbonaria in which it was also observed, were not spurned. Whether female to female courtship occurs strictly for sexual gratification or whether it indicates one or more of the females is cycling or ready to be bred by a male is, for tortoises, unknown.

Male Fixation Behavior

Fig. 3 Male Fixation Behavior "Fixation" or "zeroing-in" behavior is occasionally employed by both males and is always directed towards a female. It is used either when a male is approaching a female or when she is moving in his direction. This behavior is characterized by a male fully extending his head and neck forward and pointing it directly at the female. The head is slowly rotated horizontally and adjusted to always fixate directly on the female as the position of each animal changes. This movement is not unlike that of a compass needle pointing true north. No head bobbing is associated with the behavior. Although sexually oriented, male fixation behavior does not always lead to further courtship activity.

Trailing

"Trailing" is frequently employed during courtship. Typically the trailing activity begins with the female moving, usually in a set direction and at an average pace. The male follows the female at a normal, or slightly more brisk pace. The head and neck of both the male and the female are held in normal forward positions. Often the male will initially move rapidly to close the distance between the two. Trailing continues with the male at a close distance behind the female.

Attempting to Mount

When the female slows her pace or stops, the male usually attempts to mount. He does so by moving close behind the female and raising one of his front limbs onto her carapace. He raises the other front leg and hauls himself onto the female's back. The female may either remain stationary during the process or moves forward which causes the male to unceremoniously drop to the ground.

Biting

Fig. 4 Biting Biting was attempted by the male M. e. phayrei when the female M. e. phayrei would not stop during trailing or initially stopped and then moved during mounting attempts. This behavior was not employed by the young adult male M. e. emys. Some males within a species employ biting as part of the courtship repertoire, others do not. This was noted by McKeown, et al., 1982 with Geochelone yniphora at the Honolulu Zoo. Biting behavior is utilized for the purpose of causing the female to cease moving so mounting can take place. Biting by the M. e. phayrei male took two forms, generalized and stylized. Biting was only observed when the male was facing the female. Generalized biting was directed to the front legs of the female. Biting to the face was done differently and had an increased level of intimidation. Initially the male bit at the female's nose while holding his own head in a partially raised arched "dominant" position. The female responded by fully withdrawing her head into her shell. In response to this behavior the male extended his head and neck horizontally and inserted his head between the partially drawn up front legs of the female and attempted to nip at her face. This was effective in causing her to cease movement. Mounting usually followed.

Mounting

Mounting typically took place along perimeter fence areas or less commonly in the open, and usually after trailing sequences. Mounting without much preliminary courtship also occurred while the tortoises were resting in their shaded shallow mud-bottomed waterhole. The greatest number of mountings in the wallow were between the young adult male M. e. emys and the female M. e. emys.

Vocalization

Vocalization appears unusually complex and well developed in this species. The most common vocalizations reported in the literature on tortoises are rhythmic grunts or bellows associated with abrupt exhalation during pelvic thrusting by mating male tortoises (e.g., Jackson and Awbrey, 1978; McKeown, et al. 1982). We have recorded similar, stereotyped mating vocalizations for both males of Manouria e. emys and Manouria e. phayrei in the Honolulu Zoo. Figure 5 illustrates a typical mating vocalization sequence for the Manouria e. phayrei male. In addition to these male mating vocalizations we have also recorded a range of separate and distinctive male and female calls associated with preliminary courtship. We believe these observations constitute the first record of a diverse and complex vocalization repertoire within a single tortoise species. Male and female courtship vocalization is generally associated with the head bobbing phase discussed earlier. During face-to-face head bobbing males typically emit low frequency, modulated "moans" of relatively long duration (continuous for 10-15 sec.). Female vocalization may also occur during such head bobbing episodes, and in contrast to the male calls, these were typically more infrequent, of shorter duration, and were characterized by somewhat greater frequency modulation. The range of Manouria e. emys vocalizations merely characterizes some of the call variety we have been able to document for this species. Much more work remains to be done in cataloging the full range and significance of vocalization in Manouria e. emys.

Our observations generally support the limited data from the literature indicating that auditory communication in tortoises (beyond the debatable significance of simple male mating grunts) may well be more widespread than previously recognized, and deserving of further study in both captive and wild tortoise populations. Campbell and Evans (1972) have provided other examples of tortoise vocalizations not directly associated with mating, including contact "chirping" in Geochelone carbonaria, and nighttime "chorus calling" by multiple individuals of Indotestudo (Geochelone) forsteni in southwestern India.

Figure 5. Time vs. frequency spectrographs of vocalization in Manouria emys. (A) Male M. e. phayrei mating vocalization associated with pelvic thrusting. (B) Male M. e. emys courtship vocalization during head bobbing. (C) female M. e. emys courtship vocalization during head bobbing approach by male.  Vocalization recordings were made between April 30 and May 7, 1993.

Pre-Nesting Behavior

Successful copulation was observed on a number of occasions between the two large Asian forest tortoises (M. e. phayrei). The female nested yearly during the month of either April or May. Two to three days prior to nesting she paced the perimeter of the large enclosure for much of the day. During this period she did not feed. She acted differently while in this pre-laying mode, ignoring both the other tortoises in the enclosure and zoo reptile staff as if each were inanimate objects. On occasion she would stop pacing and push against the perimeter chain link fencing and even bit the fencing itself in an attempt to push out. Occasionally while pacing she would sniff the ground at a number of locations. When sniffing she occasionally used a backsweeping motion with one of her front legs to move small amounts of leaves, debris and other surface litter.

Nesting Behavior

Figure 6. Female Manouria emys backsweeping debris onto nest mound.

Figure 7. Area cleared by female of leaf litter and debris for nest mound construction.

The following discussion represents a summary of observations made by the zoo reptile staff during successive nesting years and elaborates on the earlier descriptions of McKeown, et al. (1982). The female M. e. phayrei collected leaf litter, loose earth, and debris through the use of a "back sweeping" technique. The tortoise facing away from the nest area would extend her forelimbs and "sweep" litter material backward. She also periodically moved backward and gradually moved surface material to the nest site. In this way leaf litter from as distant as 10 m was relocated to the site of the nest mound. While tropical forest-dwelling species of tortoise such as Geochelone denticulata (yellow-footed tortoise) and G. carbonaria (red-footed tortoise) have been described as digging nest holes in leaf litter (Pritchard, 1979), the use of the front legs to back sweep, and mound building by a tortoise had never previously been described prior to our earlier observations (McKeown, Juvik and Meier, 1982). Additional backsweeping by the female at the base and sides of the mound creates the final shape and takes several days. Just prior to laying the female burrows into the mound headfirst and using her forelimbs, excavates and shapes a cavity for the eggs. Typically it takes her 10-30 minutes of work with the forelimbs to create a shallow, bowl-shaped depression at the base of the leaf litter and earth mound. Then the female reverts to a tail-down position, using her hind feet to make any last minute refinements to the nesting chamber. Rather than using her rear limbs to lift material out of the hole, she pushes the loosely consolidated debris to each side to increase the size and depth of the cavity. The entire process using first the front limbs and then the hind limbs takes about an hour.

Once the egg chamber is ready the female exits the mound and places her cloaca over the shallow depression in the earth at the bottom of the mound and begins to lay. Each of the large round eggs has a dime-sized dent which disappears within several days. During laying, the rear legs are held straight and the female rocks forward as she lays, typically emitting a low, "moaning" vocalization. A very large number of eggs (up to 51) are deposited in less than an hour. Upon completion of laying the female uses her rear feet to gently cover the eggs with a shallow layer of earth creating a small mound within the large mound of earth, leaves and debris. Next the female moves out of the nest cavity and through backsweeping with her forelegs, fills in the cavity with earth and leaf litter debris. Once this is completed she continues to increase the size of the nest mound and over a several day period adds to and shapes the nest mound collecting additional litter from adjacent areas, sometimes working night and day. In each of the nesting years, after egg laying the female Asian forest tortoise assumed aggressive guarding behavior with respect to the nest which lasted for 3-6 days with the M. e. phayrei (between the years 1978-1990) and 6-20 days with the M. e. emys (E2) - (1988-1990). If a Honolulu Zoo reptile staff member approached the nest during the guarding period, the female would either move to a position on top of the mound (over the eggs) or alternatively, advance toward the "intruder" and with the front of her shell and head, attempt to push the person away from the nest.

Figure 8a. Female Asian forest tortoise aggressively responding to monitor lizard "predator" digging in nest mound.

Figure 8b. Female M. emys biting monitor lizard while pushing away from nest mound.

Figure 9. Female M. emys pushing armadillo "predator" off nest mound.

Figure 10. Female in defensive nest guarding posture.

In order to further evaluate the characteristics of M. e. emys nest guarding behavior during the 1982 nesting period two simulated predators were introduced into the nest area and the response of the guarding female was recorded. The "predators" consisted of two deceased stuffed animals: an adult Bengal monitor lizard (Varanus bengalensis) and a nine-banded armadillo (Dasypus novemcinctus) (McKeown, et al., 1982). Monitor lizards are native to southeast Asia and are egg predators. The armadillo is similar in shape to a mongoose and other small to mid-sized Southeast Asian egg-predating mammals. It was for this reason, in addition to their immediate availability, that they were selected for the tests. First the monitor lizard and later the armadillo were pushed into position near the mound while the female tortoise was just a few meters away collecting leaf litter for nest enlargement. In each of the trials as soon as the tortoise noticed the predator she moved quickly to take up a position on top of the nest mound. In one of the trials the armadillo was pushed directly onto the nest mound and manipulated so as to appear to be digging up the eggs. At this point the female tortoise moved towards the armadillo from her position on top of the mound and proceeded to backsweep leaf litter into the cavity. As long as each moved slowly while in the immediate area of the nest, the tortoise came off the top of the mound and using the front of her shell aggressively pushed the perceived egg predator off the nest mound. In two other separate trials the predator was made to move at a rapid pace while on the lower part of the nest. The tortoise after initially moving towards the predator, instinctively realized the futility of trying to out maneuver the faster egg predator, and retreated to the top of the mound. In response to these quick movements, the female tortoise switched from an offensive guarding to defensive guarding behavior mode. She proceeded to lie flat on the nest curving her four legs down over the upper sides of the mound thus making any digging difficult due to her considerable bulk. Other evidence of agonistic maternal behavior in land tortoises has recently been reported for the desert tortoise (Gopherus [Xerobates] agassizii). Barrett and Humphery (1986) described two incidents in the wild where female desert tortoises aggressively defended (by pushing and blocking) nests and eggs from Gila monsters (Heloderma suspectum). Henen (in press) has also reported two occurrences of unusual agonistic behavior by female desert tortoises that had recently deposited eggs. In one case a female tortoise exited her burrow and advanced on Henen, ramming his leg repeatedly with her epiplastron. She also began ramming his camera case, pushing it one meter along the ground. After Henen replaced the tortoise in its burrow, it re-emerged and advanced ten meters toward him, this time attacking (ramming) his backpack which had been left on the ground. These comparable observations of agonistic maternal behavior in two quite divergent tortoise genera [Manouria and Gopherus (Xerobates)] suggest that the possibility of similar behavior in other tortoise species, and this may be worth investigating.

In 1983 the female M. e. emys (E1) also built a large nest mound which eventually obtained a measured height of 45 cm. During the last week of August she did not feed, and backswept material from the earlier M. e. phayrei nest into a new mound adding additional earth and leaf litter. On 29 August she extended her head and neck and sniffed at the surface of the nest. Then the female lowered her head into the nest mound and continued to sniff in several places.

The mound was approximately 30 cm in height on 30 August when the female entered the nest. She began laying at 2:15 p.m. and finished at 3:38 p.m. after depositing 39 eggs. When she had completed covering the nest with her rear feet, she filled in the nest hole by backsweeping with her front limbs. This was followed by her using her plastron to push down and compact the top of the mound. Shortly after, a large gray kangaroo, one of the mammals that shared the large enclosure, approached the mound and sniffed at its base. The female tortoise moved quickly to the nest, climbed to the top and lay flat "guarding" with her legs extending down over the sides of the nest.

The following day, a reptile staff member entered the enclosure and proceeded to the nest. The tortoise moved to the mound. The staff person moved his hand in a digging motion at one side of the nest. The tortoise moved directly to that spot, looked intently at the hand and then stepped on it while continuing to watch intently. The keeper continued to move his hand and the tortoise extended her head, bit at the hand several times, and then moved to a guarding posture at the top of the mound. Later in the day when the male M. e. emys moved near the nest, the female approached, put a foot on his carapace and bit the front of his shell. The male retreated a short distance and the female continued her backsweeping activity. Additional efforts to produce guarding behavior were undertaken on 1 September employing the stuffed armadillo and monitor lizard used in 1982. Results were very similar to those elicited from the female G. e. phayrei the previous year.

Several new behaviors were observed during and after the 25 August 1988 nesting in a different area, by a second female M. e. emys (E2). While in the process of adding material to the nest after laying, the female pushed down and bit off 1.3 cm thick stocks of 1.5 m high cane grass (Panicum maximum) growing in clumps in the enclosure. She bit off the entire clump, about 20 individual stocks and backswept them to the base of the nest. Pushing off with her front feet and using her rear legs in a side-to-side motion while continuing to face away from the nest, she pushed the grass stems to the top of the mound. A short time later she bit off additional shoots of cane grass about 4 m from the nest and used the same procedure to move these grass stocks onto the upper portions of the mound. On August 29, 1988, she was observed backsweeping more freshly cut cane grass to the nest, adding it on in a similar manner as on 25 August. Later that day she lowered the front of her shell and pushed earth and leaf litter at the edge of the nest forward into the mound. Her head and neck were extended forward as she pushed in a "bulldozer-like" manner. During this 1988 nesting, the female M. e. emys (E2) actively nest guarded from 25 August through 13 September and nest tended through 16 September. When nest tending she typically sniffed at top sections of the large mound and moved and rearranged the top layer of material in what can only be interpreted as a directed effort to regulate temperature inside the mound, even 23 days after egg laying. The completed 1988 nest measured 0.67 mm in height.

The nest tending behavior routinely employed by Manouria emys compares in many respects with that utilized by mallee fowl and other mound nesting birds of Australia and New Guinea, that maintain proper egg incubation temperatures by constant adjustment of the mound covering.

A Brief Synopsis Of Manouria emys In Other Collections

Fort Worth Zoo, Fort Worth, Texas

1983 4 (2.2) Manouria emys phayrei in their collection; 37 white, spherical eggs laid by one of the females on 15 June; 32 of these eggs were removed for artificial incubation at 23.3° C (83° F) and 5 eggs were left in the nest; 24 of the 32 artificially incubated eggs hatched between 17-24 August. Courtship consisted of frequent head bobbing and audible groaning both prior to and during mounting. Courtship was frequently observed. Nest mound building began on 6 June 1983. Each day the mound became larger. Keeper spread out hay near the mound which was utilized along with dried grass, leaves, peat moss, earth and 2 or 3 sticks. The female was observed to frequently stop and rest on top of the mound. While there she would sometimes smell the surface or lower her head one to two inches below the surface of the mound to "test" for something, (composition, temperature?). Female gathered nesting material for 9 days and from as far away as three meters. Maximum height of the mound was 10-12 inches.

After completing oviposition on 15 June, the female continued to collect hay and surface debris and add to the nest mound on 15-18 June. Nest guarding was not observed. On 19 June the female ceased collecting nesting material.

Eggs were described initially as translucent white in color and each with a small dent. By 19 June the dent had been inverted and the color of the eggs was more of an opaque white. Eggs had a diameter of 419-451 mm and a weight of 40.5-45.8 g.

Wassenaar Zoo, Wassenaar, Holland (J.W.W. Louwman)

2 (1.1) Manouria emys obtained in 1976 and housed in a large tropical greenhouse. The tortoises became inactive if summer temperatures were too hot and they were moved outdoors during warm weather. Mating was most vigorous in February and March. The pair were never separated to stimulate mating.

The female constructed a large nest mound of earth, grass and weeds. The first nest was begun on 1 July 1978. The female did not urinate into the nest cavity to loosen the soil as is frequently observed for other tortoise species. After laying, the female covered the depression housing the eggs using both hind feet. Her tail moved from side-to-side as she covered the eggs. Louwman speculates this might be for the purpose of "feeling the eggs" or "the height of the soil over them". The female employed backsweeping with her front legs to gather surface material. She continued to work on the compost "heap-like" mound day and night, for three or four days with only brief periods of rest. During this period the staff supplied her with extra leaves and twigs (Louwman, 1982).

In the 1978 nesting when approached by a sub-adult Aldabra tortoise (Geochelone gigantea), the female Manouria emys rose high on all legs and vigorously bumped the other tortoise in an attempt to defend the site. After this encounter the Aldabra tortoise was removed (Louwman, 1982).

Clutches of 40, 39, and 42 eggs were laid respectively in 1978-1980. Eggs were smooth, and varied in size from 48 x 50 to 53 x 53 mm and weighed from 52-62 g (Table 4). The eggs were artificially incubated in boxes of damp sand at 28° C with a relative humidity of about 90% (Louwman, 1982).

Initially the hard outer shell of the eggs cracked before hatching. The inner rubbery skin remained intact for between several hours and two days depending on each egg. The incubation period was 66-71 days, shorter than for most other tortoise species. Hatchlings remained in the shells until most of the yolk sac was absorbed, a period of 12-48 hours. The neonates ranged from 50-55 g in weight and had a s.l. carapace length of 51-55 mm. At hatching they were dull brown in color with spiny edges to their shell and a prominent egg tooth on their snouts. During the first few months the dull brown coloring changed to black. Seventeen tortoises hatched during these three years, five more eggs contained dead embryos. Excluding the many damaged eggs discarded before incubation, the fertility rate was 21% (Louwman, 1982).

Toledo Zoo, Toledo, Ohio 1989 and 1990 (Val Hornyak)

2 (1.1) Asian forest tortoises (Manouria emys Phayrei); size of enclosure is marginal for these large chelonians.

1989 Summary: 36 eggs laid on 24 April 1989. Each egg had a small dent. All of the eggs were artificially incubated in a soil/sand mix but proved to be infertile. Backsweeping of leaf litter with front legs began on 24 March 1989. Limited backsweeping was noted on 25 March 1989, heaviest activity began about 4:00 p.m. Backsweeping activities continued through 16 April 1989. The male was removed on 14 April as he repeatedly attempted to court and mount during the female's gathering activities. Nesting material, consisting of earth, leaves, straw and mulch, was formed into a mound on 20 April 1989. The female entered the mound head first on 21 April and 22 April and also continued to actively backsweep. 36 eggs were laid on 24 April. On 35 April 1989 at 9:30 a.m. the female was resting on top of the large mound. At 9:45 a.m. she was backsweeping. The male approached the female, headbobbing. The female extended her head and neck in a forward horizontal position and shoved the male away from the nest with her head and front of he shell. The male continued to try to court during the day and was shoved away from the nest mound by the female. At 3:20 p.m. the male was removed from the enclosure. The female then proceeded to add additional material to the nest. At 4:00 p.m. when Val Hornyak approached the female tortoise, she returned to the top of the mound and lowered her body and assumed a guarding position on top of the mound. The male was returned to the enclosure the following day and similar behavior was noted on the part of the female as during the previous day. Once again the male was aggressively driven off the nest mound. This activity continued from the 27th through the 29th of April. On 30 April the female lost interest in guarding the nest. The nest guarding toward the young male tortoise and towards keepers lasted five days.

The Toledo male is a young adult. He weighed 12.2 kg (27 lbs) in 8/1989 while the female weighed 21.6 kg (47.5 lbs) after egg laying during 4/1989. The more aggressive but less sophisticated courtship activities of the young male is typical of young adult male tortoises. During the 1989 egg laying Hornyak observed the female tortoise rock forward and stiffen her rear legs as she laid each egg. During the post-laying backsweeping, one of the objects pushed onto the nest was the empty water bowl.

In 1990 when nesting began more leaf litter was put out for the female and the 1990 nest mound was considerably larger than the 1989 mound. After the female had completed laying in 1990, the zoo vet insisted on having her taken on a cart down to the clinic to be x-rayed to be certain all the eggs had passed. This was against the wishes of the reptile staff. When the tortoise was returned to the enclosure about 20 minutes later, she went into an immediate depression, refused to backsweep leaf litter, to guard the nest mound or to feed. She moved to a corner of the enclosure and remained there for two weeks before resuming some level of activity.

Richard Fife, Phoenix, Arizona

Large private collection of tortoises including 2 (1.1) Manouria emys phayrei. Size of enclosure is marginal.

0.1 weighed 25 kg and measured 57 cm in June 1974 upon being purchased from a dealer. This same female weighed 32 kg and measured 63 cm in 1986. 1.0 purchased from a Florida dealer in 1986 weighed 16 kg and measured 48 cm. Both tortoises are housed in an outdoor enclosure 4 m x 10 m. Tortoises graze on grass and are fed vegetables and fruit.

The high temperatures in Phoenix make it necessary to mist the M. emys during the day. Soaking pools are also provided. Additionally, as a result of the heat, the two tortoises often burrow in mounds of moist leaf litter and straw during the day when they are not soaking in their pools. In 1977 40 eggs were laid over a four-week period and proved to be infertile. At that time in addition to the 0.1 M. e. phayrei Fife had a male M. e. emys. Since a number of successful matings were observed Fife believes the infertility might be due to mixing the two animals of different subspecies.

In 1981 Fife received a 47 cm M. e. phayrei which was supposed to be a male, but turned out to be a female. When introduced to his established female in October 1981, the original tortoise immediately began trailing the new animal. She thumped her chin on the rear of the new tortoise's carapace. The thumping noise could be heard from some distance away. This was followed by pushing, ramming and finally mounting, and included an audible grunting sound. Fife's established female continued this male-like behavior regularly until August 1983 when the newer female was found turned over and dead.

In May 1988 when Fife only had the pair of M. e. phayrei, the female began gathering leaf litter for nest building. The site was moved three times and finally abandoned. However, in June she laid individual eggs for several days and then laid a clutch of 30 eggs which were artificially incubated indoors at 29-33° C. Two of the eggs were fertile, went full term but did not hatch. Fife attributes these deaths to too high an incubation temperature. The eggs from his 1988 clutch were 43-45 mm in diameter and 50-55 g in weight, significantly smaller than the 51-54 mm and 67-80 g eggs laid during the late 1970's and 1980's by Asian forest tortoises at the Honolulu Zoo. Each of Fife's eggs initially had a small dent which later inverted.

CONCLUSIONS

1. Manouria emys although primitive evolutionarily, is a gregarious and highly social species which uses a variety of vocalizations, and head and neck movements for communication.

2. Clutch size in captive Manouria emys (maximum 51 eggs) far exceeds that reported for other tortoise species.

3. Nesting behavior in Manouria emys includes the construction of above ground leaf-litter nest mound. The forelimbs are used to "backsweep" surface leaf-litter and debris for nest mound construction.

4. The rear limbs may also be employed in a side-to-side motion to advance nesting material from the base to the top of the nest.

5. The modification of potential nesting material to add to the mound (pushing down and biting off large clumps of cane grass) is also unique for a tortoise species.

6. "Nest guarding" by female Manouria emys lasts for 2 to 20 days following egg laying and is directed towards any potential predator including reptiles, mammals, including man, and occasionally other tortoises.

7. Nest guarding, even of limited duration may be viewed as an appropriate adoptive strategy in Manouria emys to decrease the probability of nest predation.

8. The adaptive significance of nest guarding in Manouria emys probably relates less to the actual sustained ability of the tortoise to fend off egg predators than to the benefit gained by visual distraction and the possible intermingling of the tortoise's scent with that of the freshly laid eggs. Nest guarding and adding additional materials to the mound during the first few critical days when the nest scent is strong may well help to confuse and distract predators. In Southeast Asia, after several good rainstorms, the nest may look and smell like any other large mound of leaf litter on the forest floor.

9. "Nest tending" for the purpose of adding additional material to the nest mound, and routine modifications to the top layer of the mound which may regulate temperature and humidity inside the nest, lasts for 3 to 23 days.

10. During the five year period of 1978-1982 at the Honolulu Zoo, a total of 155 Manouria emys phayrei eggs were artificially incubated in slightly moist vermiculite. A total of 103 live hatchlings were produced. The incubation period ranged from 63-84 days, depending on the incubation temperatures utilized. Clutch fertility rates were 78.4-84.4 %. Fifty-six additional hatchlings were produced during the 1983-85 nesting seasons.

11. Nest mounding by Manouria emys took place in four other collections, with successful captive hatchings occurring at the Wassanaar Zoo (Holland) in 1978-80 and at the Fort Worth Zoo in 1983.

Acknowledgements

The authors express their appreciation to Val Hornyak of the Toledo Zoo, Rick Hudson of the Fort Worth Zoo and Richard Fife of Phoenix, Arizona for sharing of data. The authors also wish to express their gratitude to Jane Bowden for her beautiful illustrations. Finally, we wish to thank Frances Amoruso, Senior Secretary of Chaffee Zoological Gardens of Fresno for typing the manuscript.

Literature Cited

Barrett, S. L. and Humphery, J. A. 1986. Agonistic interactions between Gopherus agassizii (Testudinidae) and Heloderma suspectum (Helodermatidae). Southwestern Naturalist 31(2): 261-263.
Campbell, H. W. and Evans, W. E. 1972. Observations on the vocal behavior of chelonians. Herpetologica 28(3): 277-280.
Fife, R. 1989. Captive behavior and reproduction of the Burmese mountain tortoise. pp. 135-138. In: M. J. Uricheck (ed.). 13th Inter. Herpetol. Symp. on Captive Propagation and Husbandry. Phoenix, Arizona.
Henen, B. (In press). Maternal Behavior in the desert tortoise (Xerobates agassizii) at Goffs, California. In: Proc. 1987 Desert Tortoise Council Symposium.
Hornyak, V. 1989, 1990. Personal communication.
Hudson, R. 1989, 1990. Personal communication.
Kleh, C. 1983. Personal communication.
Louwman, J. W. W. 1982. Breeding the six-footed tortoise (Geochelone emys) at Wassenaar Zoo. pp. 153-156. In: P. J. S. Olney, P. Ellis and B. Sommerfelt (eds.). International Zoo Yearbook No. 22. Zoological Society of London.
McKeown, S. 1982. Priorities and techniques of captive breeding reptiles at the Honolulu Zoo, with an emphasis on Testudinidae, Iguanidae, Scincidae and Gekkonidae. pp. 93-102. In: 5th Annual Reptile Symposium on Captive Propagation and Husbandry. Thurmont, Maryland.
McKeown, S. 1990. Asian brown tortoise (Manouria emys). Tortuga Gazette 26(6): 3-5.
McKeown, S., Juvik, J. O. and Meier, D. E. 1982. Observations on the Reproductive biology of the land tortoises Geochelone emys and Geochelone yniphora in the Honolulu Zoo. Zoo Biology 1: 223-235.
Moll, E. O. 1989. Manouria emys: Asian brown tortoise. pp. 119-120. In: I. R. Swingland and M. W. Klemens (eds.). The Conservation Biology of Tortoises. Occasional Papers of the IUCN Species Survival Commission (SSC) No. 5.
Pritchard, P. C. H. 1979. Encyclopedia of Turtles. T.F.H. Publications, Neptune, New Jersey.
Wirot, N. 1979. Turtles of Thailand. Bangkok. Privately Published.