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.
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:
Manouria emys emys
Figure 1a. Pectoral scutes of Manouria e. emys
Manouria emys phayrei
Figure 1b. Pectoral scutes of Manouria e. phayrei
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.
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.
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.
Figure 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 femaleM. 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
Figure 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" 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.
Figure 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 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 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" inGeochelone 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.
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.
|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 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.