Part 19

Chiggers were ordinarily found only on the soft parts of the turtles' bodies. Early in the season infestations were chiefly on the head and neck. Favorite sites of attachment were the point where the skin of the neck joins the carapace and on the skin around the eyes. Later in the season some chiggers could be found on nearly every part of the body where soft skin was present; concealed areas of skin, such as the axillary and inguinal pockets, the anal region, and the inner rim of the carapace (where it joins the skin of the body), harbored concentrations of chiggers. Juveniles were relatively more heavily infested than adults and, even early in the season, had chiggers attached along many of the interlaminal seams of the shell. Broad areas of soft, newly-formed epidermis on the shells of juveniles probably afforded a better place of attachment to chiggers than did the interlaminal seams of adults. The interlaminal seams and transverse hinges of adults were not infested until the height of the season of chigger activity. Heavily infested adults, observed in early July, were literally covered with chiggers; red larvae outlined nearly all the scutes of the shell, the anus, the mouth, and the eyes. When turtles were picked up for examination, chiggers could be seen moving rapidly from one interlaminal seam to another.

Box turtles kept in outdoor pens and in the laboratory did not long maintain visible infestations of chiggers, even during the time in summer when turtles found in the field were heavily infested.

A four-year-old juvenile was found nearly immersed in the shallow water of a pond on July 4, 1955; its right eye had been damaged by an especially heavy concentration of chiggers. When I released the turtle, some 50 feet from the pond, it returned to the water and spent the next four days there. The turtle was probably in a period of quiescence induced by the eye injury and the heavy infestation of chiggers; immersion in water could be expected to help free the turtle of chiggers and to relieve trauma resulting from the injured eye. Richard B. Loomis told me that larval chiggers are able to survive under water for several days but that warm water will hasten their demise.

Infestations of larval bot flies (Sarcophaga cistudinis) were noted in several turtles at the Damm Farm and, upon closer scrutiny, were found to be common in preserved specimens from other areas. Larvae were always found in flask-shaped pockets (Pl. 27, Fig. 2) beneath the skin; the pockets opened to the outside by a small hole, the edges of which were dried and discolored. One larva sometimes protruded from the opening. The inside of the pocket is lined with smooth, skinlike tissue. Heavily infested box turtles may have four or five such pockets, each containing one to many larvae. The most frequent sites of the pockets are the skin of the axillary and inguinal regions, and the skin of the limbs and neck, especially near the bases of these members. Subadults were more heavily infested than older adults; no infestations of hatchlings or small juveniles were noted.

An adult female, infested with bot fly larvae when she was removed from her hibernaculum in late October, 1955, bore no trace of larvae or of the pocket that had contained them when she was recaptured the following June. According to Rokosky (1948), the larvae eventually fall to earth and pupate. The individuals of T. carolina studied by him were not re-infested by adult bot flies; one turtle ate some of the larvae that dropped from its body.

The manner in which box turtles are infested by bot fly larvae is uncertain. Possibly the eggs are picked up accidentally or laid on the skin while box turtles are foraging in dung. Belding (1952:841) classifies the genus Scarophaga as semi-host-specific, depositing eggs in open wounds.

McMullen (1940), Rodeck (1949), and Rainey (1953), described individuals of T. ornata parasitized by S. cistudinis. Rokosky (1948) and Peters (1948:473) reported infestations in T. carolina. Infestations were the cause of death in the instances noted by Rainey and Rokosky.

PREDATORS

Few first-hand observations on predators of T. ornata are available and I have found little direct evidence of predation in the course of this study. In general, adults of the species seem to have few natural enemies other than man. Several of my colleagues at the University of Kansas have observed dogs carrying box turtles in their mouths or chewing on them. Frank B. Cross told me his dog caught and ate young T. ornata in Payne County, Oklahoma, and A. B. Leonard once saw a badger carrying one in Dewy County, Oklahoma. At the Reservation, a freshly killed juvenile was found beneath the nest of a crow (Corvus brachyrhynchos) and remains of a hatchling were found in a scat of a copperhead (Agkistrodon contortrix).

Dr. Fred H. Dale, Director of the Patuxent Research Refuge, Laurel, Maryland, kindly furnished photostatic copies of cards, from the Division of Food Habits Research of the U. S. Fish and Wildlife Service, recording the instances in which Terrapene ornata was listed as a food-item. In one instance the stomach of each of two nestlings, in the same nest, of the White-necked Raven (Corvus cryptoleucus) in Terry County, Texas, contained remains of recently hatched ornate box turtles; the remains of one turtle made up 64 per cent of the contents of one stomach, and parts of three turtles made up 80 per cent of the contents of the other stomach. Each of two stomachs of the coyote (Canis latrans) from Quay County, New Mexico, contained a "trace" of ornate box turtle.

Wild carnivores known to occur on the Damm Farm were raccoons (Procyon lotor), striped skunks (Mephitis mephitis), badgers (Taxidea taxus), and coyotes (Canis latrans); all were suspect as predators of ornate box turtles.

On December 10, 1953, ten dead box turtles (eight adults and two juveniles) were discovered at the top of a cut bank on the Damm Farm, within a few feet of a burrow that was used at least part of the time by a striped skunk. The condition of the turtles suggested that they had lain in the open for several weeks. The heads and legs were missing from most of the turtles and tooth marks were discernible on several of the shells. A logical explanation of this occurrence is that the turtles, using the burrow as a hibernaculum, were ousted by a predator that also inhabited the burrow. Turtles moving about sporadically in late autumn may be quickly chilled by a sudden drop in temperature and therefore be more susceptible to predation than at other times of the year. Two of my colleagues at the Museum of Natural History informed me that they had observed similar concentrations of dead T. ornata in winter.

In July, 1952, H. B. Tordoff collected eight shells of juvenile T. ornata in a dry creek bed near Sharon, Barber County, Kansas. Some of the shells had small tooth-punctures. The stream bed habitat and the appearance of the tooth punctures tended to incriminate raccoons as predators. Raccoons, more than any other carnivore mentioned above, possess the manual dexterity necessary to pry open the shell of a box turtle and bite away the soft parts. Badgers and possibly coyotes are probably the only local carnivores (excluding large dogs) that could crack open the shell of an adult turtle by sheer force.

Adults of T. ornata, since they occasionally molest small juveniles, must be considered in the category of predators. When captive adults and juveniles were fed from the same container in the laboratory, the turtles occasionally bit one another accidently. Serious injury to the young was prevented by watching the adults closely and moving them away when they caught a smaller turtle by the leg or head. Similar accidents presumably occur in nature; juveniles and adults were sometimes found feeding side by side. William R. Brecheisen told me that adults kept in a stock tank at his farm in the summer of 1955 regularly and purposefully chased and bit small juveniles in the same tank. Brecheisen gave me a juvenile that had been so bitten; the right side of its head was badly damaged (the eye gone and a portion of the bony orbit broken) but was partly healed. Ralph J. Donahue told me that he saw an adult T. ornata attack a juvenal T. carolina, and provided a photograph of the incident. The juvenile was not injured.

Although small box turtles may occasionally be caught and killed by adults in nature, this seems not to constitute a major source of predation on the young.

Other animals that may prey upon young box turtles occasionally (and that were known to occur at the Damm Farm) are bullsnakes (Pituophis catenifer), red-tailed hawks (Buteo jamaicensis), marsh hawks (Circus cyaneus), crows (Corvus brachyrhynchos), and opossums (Didelphis marsupialis), and domestic cats.

Nest predators probably have greater effect on populations of T. ornata than do predators of hatchlings, juveniles, and adults. Four robbed nests were found at the Damm Farm; in each instance, striped skunks were thought to be the predators. E. H. Taylor told me that he once saw a bullsnake swallow an entire clutch of newly laid eggs before the female turtle could cover the nest.

DEFENSE

Box turtles rely for protection on the closable shell and on inconspicuousness; defense reactions, except in the rare instances that biting is provoked, are purely passive.

Box turtles handled in the course of field work varied widely in their reactions. Many struggled violently when being measured or marked whereas others were completely passive, closing the shell tightly and making it difficult for me to examine the soft parts of the body. These differences in behavior did not seem to be correlated either with sex or with age; generally lessened activity was associated with suboptimum body temperatures. All box turtles found in the field were extremely wary. As soon as one sighted me (sometimes at a distance of 200 feet or more), it became motionless with shell raised from the ground and neck extended (Pl. 28, Fig. 5). Some turtles remained in this motionless stance for half an hour or more, finally moving slowly away if I remained motionless. Turtles made no attempt to escape until I approached them closely or until they were in danger of being trampled by my horse; they would then move away with remarkable rapidity. Box turtles seemed unaware of an intruder until he could be seen or until he touched the turtle. When a turtle was approached from the rear, whistling, finger snapping, and normal footfalls did not attract its attention. Latham (1917:16) observed corresponding behavior in T. carolina. Wever and Vernon (1956) found the ear of T. carolina to be keenly sensitive to sounds in the range of 100-600 cycles per second but progressively less sensitive to sounds of higher and lower frequencies. Surely a predator as stealthy as a coyote could approach a box turtle unseen and could quickly bite off at least one of the turtle's legs. Many of the mutilated box turtles that I observed may have survived such encounters with carnivores. The tendency of some individuals, when handled, to over-extend the limbs and neck (rather than closing the shell) in an attempt to escape, would make them easy victims for any predator.

Ornate box turtles were kept in my home, along with several cats. Initial behavior was characterized by mutual wariness; subsequently the cats would follow a turtle about the house for a time, occasionally pawing at an exposed limb. The turtles withdrew only when touched or when approached from the front. After a day or two the cats and turtles ignored each other, often eating and drinking from the same dishes without incident. Under these circumstances the cats, I believe, could easily have killed or injured the turtles. A turtle would occasionally gain the respect of a cat by biting it.

The strong odor sometimes given off by box turtles is produced by the secretions of four musk glands, two situated anteriorly on each side and opening by small, nearly invisible apertures beneath the fourth marginal scute. According to Hoffman (1890:9), two other musk glands, opening beneath the eighth marginal scute on each side, are also present in Terrapene; these posterior glands were not found in the several specimens of T. ornata that I dissected.

Strong odors were produced by nearly all small juveniles until they became accustomed to being handled. Older juveniles and adults produced strong odors only in response to pain or injury, as, for example, when they were killed in the laboratory prior to preservation or when they were being marked in the field. Young box turtles were capable of producing strong odors as soon as they hatched.

Norris and Zweifel (1950:3) considered the odor produced by T. o. luteola to issue from the "... concentrated, highly pungent urine...." voided by individuals when they were disturbed, and thought the production of odor to be a defense mechanism. Neill (1948b:130) reported that hatchlings of T. carolina with unhealed umbilical scars emitted a musky odor comparable to that of the stinkpot, Sternotherus odoratus; he thought the capacity to produce this odor was lost at about the time that the plastral hinge became functional.

The function of musk glands in Terrapene and, in all other turtles, is unknown. Since biting and nuzzling of the edges of the shell is an integral part of the courtship of many turtles, odor produced by the musk glands may well be a means of social recognition or of sexual stimulation. Repellant odor may have a protective value in young box turtles but it is unlikely that larger predators would be frightened away or even discouraged by odor alone. In this respect Neill (loc. cit.) and I concur.

DISCUSSION OF ADAPTATIONS

Most of the morphological characteristics distinguishing box turtles from other North American emyid turtles, the most notable of which is the movable plastron, are modifications that have evolved as a result of selectional pressures favoring adaptation to more or less terrestrial existence. Similar adaptations have arisen independently in several branches of the emyid stock (see introduction). The genus Terrapene seems to have departed farther from a generalized emyid form than have other kinds of box-turtle-like chelonians. In a morphological sense, Terrapene ornata is clearly the most specialized member of its genus now occurring in the United States (my own studies have revealed that populations in western Mexico now referred to as T. klauberi and T. nelsoni are as specialized as T. ornata in some respects but more generalized in others). The present ecological study has demonstrated that T. ornata is specialized in habits as well as in structure. It is concluded that these specializations (of more generalized and perhaps more primitive conditions as, for example in T. carolina) constitute adaptation for terrestrial existence in open, semiarid habitats. These adaptations in T. ornata have resulted, in a few instances, in unique habits and structures; however, in most instances the adaptations have produced slight but recognizable changes that are definable only by degree of difference from other species of box turtles.

The closable shell of box turtles is of obvious survival value in providing protection for the soft parts of the body. In most of the species of Terrapene, the lobes of the plastron completely close the openings of the shell; closure is so tightly effected in some individuals that it is difficult to insert the blade of a knife between the adpressed margins of carapace and plastron. In T. ornata nevertheless, both lobes of the plastron are deficient on their lateral margins; four narrow openings remain when the lobes are drawn shut. Emargination of the plastron has occurred at the places where the limbs rub against it during locomotion. This reduction of the plastron permits the body to be held off the ground during forward locomotion and seemingly permits a generally freer range of movement for the limbs. The possible disadvantages of an imperfectly closable shell seem to be compensated for by increased mobility. Reduction of the plastron is correlated with a general lightening of the shell, probably associated with the increased vagility of this species. Lightening of the shell is evident also in the relatively thin, loosely articulated bony elements. Shells of adult T. ornata that are old and weathered, or macerated (unless they are partly co-ossified because of injury), can nearly always be disarticulated with ease, whereas the bony elements in the shells of adult T. carolina (all races) are nearly always co-ossified or separable only after prolonged maceration.