Sarcophilus harrisii ( Boitard, 1842 )

Rose, Robert K., Pemberton, David A., Mooney, Nick J. & Jones, Menna E., 2017, Sarcophilus harrisii (Dasyuromorphia: Dasyuridae), Mammalian Species 49 (942), pp. 1-17 : 1-13

Sarcophilus harrisii ( Boitard, 1842)

Tasmanian Devil

Didelphis ursina Harris, 1808:176 . Type locality “Van Diemen’s Land” (Tasmania).

Dasyurus laniarius Owen in Mitchell, 1838:363, plate 49, figures 3 and 4. Type locality “ Wellington Valley [New South

Wales], Australia;” fossil form from the Pleistocene. are 56% larger. Photograph by Christo Baars used with permission.

Ursinus Harrisii Boitard, 1842:290 . Type locality “la terre de Van-Diemen;” replacement name for Didelphis ursina Harris, 1808 vide Groves (2005).

Sarcophilus satanicus Thomas, 1903:289 . Type locality “ Tasmania.”

Sarcophilus harrisii Thomas, 1912:116 . First use of current name combination.

Sarcophilus. harrisii . dixonae, Werdelin 1987a:10. Type locality “Mt. Hamilton;” Victorian subfossil form vide Groves (2005).

CONTEXT AND CONTENT. Context as for genus. Sarcophilus har-risii has no living subspecies ( Werdelin 1987a; Groves 2005).

NOMENCLATURAL NOTES. Sarcophilus is from the Greek words sarx, meaning flesh, and philos, meaning loving or fond of ( Strahan 1981). The specific name harrisii is the Latin form of “harris.” Harris (1808), in his description of 2 new mammals from Van Diemen’s Land (at Australian independence in 1901, the state name was changed to “ Tasmania ”), gives the common name as “native devil.” Aboriginal names as recorded by early European settlers include “tarrabah,” “poirinnah,” and “parloo-mer-rer.” Werdelin (1987a), on the basis of priority and size comparisons, proposed the change in name from Sarcophilus harrisii to Sarcophilus laniarius (the butcherer); acceptance was brief ( Groves 1993) and S. harrisii is now widely accepted ( Groves 2005).

DIAGNOSIS

Restricted to Tasmania in recent times, Sarcophilus harrisii is distinctive among dasyurids by its large size (adults> 5 kg); black coat, usually with diamond-shaped markings on the chest, shoulders, or rump; massive neck and head; short broad snout; and robust bone-crunching dentition. No other living dasyurid can be confused with it on any of these criteria.

GENERAL CHARACTERS

Sarcophilus harrisii is the largest living carnivorous marsupial, under the assumption that the thylacine, Thylacinus cynocephalus , has been extinct since 1936. S. harrisii has short shiny black fur (30 mm long), with soft guard hairs and sparse soft underfur. Fur in the axillary regions is thin and that on the ears, if present, is short and fine. The hairs on the tail are about 60 mm long. In older animals, particularly males, the fur thins out on the face, tail, and rump. Some individuals have a distinct reddish tinge to their coat color, which can be almost ginger on the tail and around the ears. Diamond-shaped white marks, found most frequently on the chest, then rump, and least on shoulders and ribs, are highly variable and individually unique. About 13% of S. harrisii are all black ( Pemberton 1990).

The size of a small stocky dog, S. harrisii has short legs, tail one-half as long as the head and body, a wide head set on a thick neck, and roundish ears ( Fig. 1 ). Fat is stored in the tail, which may be more than 50 mm wide at the base in large males, and usually is thickest about 50–60 mm from its base. Wounds and scars are more prevalent in males than in females, probably the results of aggression in competition for food and when in conflict both with mates and other competing males during copulation. Muzzle wounds can be life-threatening, with jaw muscles ripped off and teeth exposed. The tail of older animals often is heavily scarred and sometimes shortened, as if bitten off.

The large and numerous backwardly swept black vibrissae of S. harrisii include some from the lower jaw and eyebrows. The genial vibrissae, usually about 12, arise from a nearly circular area and extend past the ears to the neck ( Pocock 1926). The mystacials are equally long and rigid, and sometimes sinuous. The rhinarium is large, wide, grooved, naked, and usually wet. The ear, higher than wide and attached by a broad base to the head, has numerous ridges and folds able to cover the auditory orifice, which lies at the base of the ventral-most cleft.

The entire plantar pad of the forefoot, covered with a coarse squamous tessellation, rests on the ground ( Pocock 1926). Digits 2, 3, and 4 of front feet are longer than 1 and 5; all digits are relatively long with long sharp claws that are not strongly recurved. Further, the forefoot is supple and capable of grasping. The hind foot has a less flexible plantar pad that extends to the heel. The heel, an important contact point when climbing, is sometimes placed on the ground while standing but when walking or loping S. harrisii is digitigrade. The hallux is extremely reduced and if visible is 0.5–1.0 mm long. The other digits of hind feet are long, strongly clawed, and of equal size, creating a distinctive square hind footprint. Foot pads and claws are commonly black, but are brown or even pink in those individuals with reddish “henna” fur.

Sexual size dimorphism in S. harrisii is moderate, with males 56% larger than females by weight (Jones 1997). Mean mass of 50 adult males was 8.2 kg and that of 50 females was 6.1 kg obtained from a 10-year study on the west coast of Tasmania ( Guiler 1978), although this sample of males probably included a mixture of fully mature and growing (2- to 3-year-old) males. Pemberton and Renouf (1993— n ≥ 100 of each sex) report males averaged 10.2 kg and females 7.1 kg from the drier northeast coast of Tasmania. S. harrisii living at high elevation or in subalpine areas is smaller; males are 8.43 kg (n = 56) and females are 5.4 kg (n = 130—Jones 1997). Healthy animals often have substantial amounts of body fat, especially in the skin, abdomen, and tail. Average and ranges of external measurements (mm) of 37 male and 32 female S. harrisii , respectively, were: total length, 824.1 (750–975), 780.7 (710–840); length of tail, 256.2 (220–285), 253.0 (215–265); length of hind foot, 91.2 (82–108), 86.7 (77–102); length of ear, 64.2 (47–80), 56.2 (44–73).

The skull is distinguished from that of other dasyurids by its massive bone thickness, relatively short rostrum, broad zygomatic arch, pronounced sagittal crest, and expansive zygoma to accommodate powerful masseter muscles ( Fig. 2 ). Canines are massive and molars are carnassial-like. The palatine is fenestrated. Average skull measurements (mm) for 18 male and 15 female S. harrisii , respectively, were: greatest length of skull, S. harrisii disappeared from the Australian mainland about 3,000 years ago, probably due to a convergence of extreme climate events (Brüniche-Olsen et al. 2014), competition with the dingo, Canis familiaris dingo (Jones et al. 2003a; Letnic et al. 2012), and an increase in the population density ( Prowse et al. 2014) of Aboriginal people, who also developed new hunting technologies around this time (Johnson and Wroe 2003).

137.9, 130.3; cranial breadth, 20.0, 20.8; zygomatic breadth, 110.7, 98.0; length of maxillary toothrow, 48.2, 49.0; length of molariform teeth in mandibular toothrow, 51.8, 53.5; maximal anterior-posterior diameter of upper canine, 10.03, 8.92.

DISTRIBUTION

Distribution is restricted to Tasmania, the island state off the southeast coast of mainland Australia ( Fig. 3 ). Within Tasmania, Sarcophilus harrisii is among the most widely distributed mammals, 3rd behind 2 macropods (Macropodidae—Rounsevell et al. 1991). Formerly widespread across southern Australia,

FOSSIL RECORD

The recent ancestry of Sarcophilus harrisii can be traced to several locations of Pleistocene age (Archer and Hand 1984), the oldest of which is from the early Pleistocene of Nelson Bay, Victoria (Gerdtz and Archbold 2003). Local faunas of 70,000 – 30,000 years ago with Sarcophilus fossils include Eastern Darling Downs (southeastern Queensland), Victoria Cave (southeastern South Australia), and Mammoth Cave (Western Australia). A late Quarternary record of Sarcophilus from the Mygoora Local Fauna, from Mygoora Lake in southern Northern Territory, is the 1st record from central Australia ( Megirian et al. 2002). More recent remains are from the Devil’s Lair Local Fauna (southwestern Western Australia, 35,000 – 2,000 years ago) and Fromm’s Landing Local Fauna (South Australia, <4,000 years ago). S. harrisii also is known (from one i3) from the upper layers of Pyramids Cave in eastern Victoria, a deposit of Holocene age ( Wakefield 1967a). Another Holocene (3,120 ± 100 years ago) record is from the Padypadiy archeological site in Northern Territory. A 2nd record from northern Australia (Calaby and White 1967) is a skull fragment from Cape York, Queensland, dated 11,000 –10,000 years ago ( Horton 1977). Subfossils are known from 4 sites on the Basalt Plains of western Victoria, 2 of which are from Aboriginal middens; another (cave) site yielded an estimated 60 individuals ( Wakefield 1964). Still other subfossils were found in McEachern’s Cave in extreme southwestern Victoria ( Wakefield 1967b). Although no S. harrisii survive on any island of Bass Strait north of Tasmania, subfossil remains from the Palana sand dunes on Flinders Island reveal that it lived there in the Holocene ( Hope 1973).

The type specimens (2 broken left maxillae) of the fossil subspecies laniarius , found among fossils from Wellington Caves ( Owen 1838; Dawson 1982) and later from other Pleistocene sites ( Marshall 1973), were determined by Werdelin (1987a) to be 16% larger than S. harrisii , but were not sufficiently distinct to merit a different species designation. S. harrisii survives only in Tasmania. Because subfossil specimens from Mt. Hamilton, Victoria, differ significantly in a number of dental and skull characteristics from the modern form, Werdelin (1987a) named these S. h. dixonae.

FORM AND FUNCTION

The dental formula is i 4/3, c 1/1, p 2/2, m 4/4, total 42 (Green and Rainbird 2015). The dentition reflects the carnivorous diet of Sarcophilus harrisii , but is fundamentally different from that of the Order Carnivora . The incisor row is transverse. The massive canine teeth are circular in cross-section, equivalent among the placental carnivores only to some ursids and large mustelids, and are immensely strong and well adapted for eating bone and perhaps grasping large prey (Jones 2003a). Premolar teeth are of modest size, but molar teeth are massive; tooth and cusp size increase from M1 to M4. Like all dasyuroids, S. harrisii lacks the specialized carnassial pair of the Carnivora . All 4 molars are similar in structure, because of phylogenetic constraints on tooth eruption and the resultant differences from other carnivorous marsupials in jaw geometry ( Archer 1976, 1978; Werdelin 1987b). All molar teeth have meat-slicing and grinding areas, functions performed by carnassial and post-carnassial molars, respectively, of the Carnivora . The functional equivalent of the carnassial blade and notch in molar teeth of S. harrisii is the paracristid crest, which is in a similar functional position, on the outer anterior face of the lower molar tooth, to the placental carnassial blade ( Archer 1976, 1978). Although the elongation and longitudinal orientation of the paracristid result in one long “carnassial” shearing unit ( Archer 1976), the equivalent tooth to the placental carnassial is M4, which is in a geometrically similar position ( Werdelin 1986). S. harrisii is equivalent to the thylacines in its adaptation to carnivory, and the grinding area of the tooth is almost absent in M4, which remains sharp throughout life (Jones 1997). Processing of bones in S. harrisii , for which hyenas ( Hyaenidae ) have a specialized conical 3rd premolar, is carried out on M2, which is biomechanically in an equivalent part of the jaw (Jones 2003a) and which becomes extremely worn in older animals ( Pemberton 1990).

All teeth have closed roots, and hence animals can be aged by degree of tooth wear, generally into yearling, 2, 3, 4, 5 and more than 5-year-old age classes. Canine teeth overerupt and this feature can also be used to age animals. Broken incisor and canine teeth are common in older animals, occurring twice as frequently as expected if all teeth have an equal chance of fracture (Jones and Stoddart 1998). Supernumerary teeth, including incisors, canines, and molars, occur occasionally: a 5th upper right molar in 4 of 33 skulls ( Green 1967) and supernumerary partially erupted lower molars (1 on each side) in a young female ( Doran 1975). Guiler and Heddle (1974b) describe the pattern of eruption and growth of teeth.

Sarcophilus harrisii has a narrow, flattened skull, like other dasyurids ( Werdelin 1986), but is remarkable for its tiny cranium (McNab and Eisenberg 1989) and short rostrum ( Werdelin 1986). Brain size is less than one-half (43%) that predicted by body mass allometry (McNab and Eisenberg 1989). The short rostrum combined with pronounced sagittal crest and expansive zygoma accommodating powerful masseter muscles result in a powerful bite force at the canines, which suits its crushing killing bite on large prey (Jones 1997). Also unusual in S. harrisii , although its functional significance is not known, is the postorbital process of the frontoparietal bone, which almost separates the orbit from the zygoma.

Sarcophilus harrisii has short metatarsals compared to the length of the femur, indicating it is not a particularly fast runner, and so is unlikely to indulge in long, fast pursuits of prey (Jones 2003a). The metacarpal-to-phalanx length ratio (associated with running speed), the ratio of olecranon process to ulna length (which affects rotational and thus tree-climbing ability), and the flattish profile of the claws (associated with tree-climbing ability) are all typical of terrestrial carnivores (Jones 2003a).

Females have a backward-directed abdominal pouch, formed when birth is imminent, with 2 pairs of teats surrounded in front and laterally by a horseshoe-shaped flap of skin. In males, the darkly pigmented scrotum is located in front of the penis in the inguinal region. The scrotum can be withdrawn by the action of cremaster muscles into a pseudo-pouch consisting of ventrolateral folds of abdominal skin ( Guiler 1970a; Hughes 1982). On relaxation of the cremaster muscles, such as when the male is resting or hot, the pseudo-pouch becomes shallow and scrotum pendulous. The penis normally is retracted within a pocket located ventro-anteriorly in the cloaca and the glans, although slightly furrowed, is not forked or bifid (MacKenzie and Owen 1919). Apart from their larger size and primary sexual characteristics, males are indistinguishable from females.

The wild S. harrisii often has a subcutaneous fat layer up to 3 cm thick ( Green 1967) and one of us (RKR) has observed visceral adipose that sometimes completely covers the intestines and kidneys with tallow-like deposits. The interscapular region is another area of fat stores.

The short digestive tract is typical of carnivores, as are the high apparent dry matter (79%) and apparent energy (87%) digestibilities (Green and Eberhard 1979). The digestible energy required for maintenance is 545 W (kg) −0.75 day−1 or 6.30 W (kg) −0.75, or about 2.5 times the calculated basal metabolic rate (Green and Eberhard 1979). Mean water turnover rates of S. harrisii , measured by tritiated water, were considerably higher than those predicted from other studies of marsupials ( Nicol 1978). Four adults averaging 5.25 ± 1.21 (SE) kg had a total body water of 3.48 ± 0.41 l, with turnover of 10–11% per day. Thus, the mean water turnover per day was 393 ± 98 ml/day, or 74.6 ± 2.6 ml kg−1 day−1 ( Nicol 1978).

Mean basal metabolic rate of S. harrisii , as measured in thermoneutrality, was 0.28 ml O 2 g−1 h−1 (MacMillen and Nelson 1969). Whereas its metabolic rate falls nearly on the line (0.90) predicted by body mass, its basal metabolic rate value lies on the line for 12 dasyurids as described by the equation: basal metabolic rate = 2.45 · W (kg) −0.261 (MacMillen and Nelson 1969). These basal metabolic rate values are 32.1% below those of placental mammals of comparable sizes, and close to the mean values for marsupials (Dawson and Hulbert 1970). The metabolic rate of free-living S. harrisii , determined in the field using doubly labeled water, was 2,591 kJ/day for a 7.9-kg summer animal and 2,890 kJ/day for a 7.1-kg winter animal ( Green 1997). Water fluxes for these 2 animals were 724 and 743 ml/day, respectively. Both field metabolic rate and water fluxes are independent of season for S. harrisii . Water fluxes of lactating females were comparable to those of 4 other dasyurids of varying sizes, and field metabolic rate was significantly raised during late-stage lactation but not in early lactation ( Green 1997).

Body temperature in free-ranging S. harrisii averages 36.5°C, with a daily range of 0.6°C that tracks the diel cycle ( Jones et al. 1997). Body temperature rises at dark as animals become active, remains high all night, and then is lowered during the day when S. harrisii is resting in an underground burrow. S. harrisii sometimes suns itself, with young animals basking with hind legs stretched backwards. Radiotracked animals have been observed to wade into water after long foraging trips, probably to cool down. Nighttime body temperature of 36.1°C and midday maximum body temperature of 37.7°C are reported in the laboratory for a single captive animal ( Morrison 1965); of the 7 dasyurids examined in captivity, only the 15-g Sminthopsis crassicaudatus had a diel amplitude lower than the 1.6°C of S. harrisii . Body temperatures of 34–35.5°C were reported for 10 experimental animals (Guiler and Heddle 1970), but were 2–3°C higher at night, when animals are most active, than during daytime rest (Guiler and Heddle 1974a).

When held for periods in constant temperatures ranging from −5°C to +35°C, S. harrisii is a good thermoregulator, usually at 35 ± 1°C. At ambient temperatures outside the thermoneutral zone of 28.5–32°C (Nicol and Maskrey 1980), S. harrisii produces heat by shivering or loses heat by panting, the usual mammalian responses. When held in the cold well below its thermoneutral zone, S. harrisii is homeothermic, maintaining a body temperature of 36.0°C rather than the 36.8°C in thermoneutrality (MacMillen and Nelson 1969). Despite snowy conditions through an alpine winter, 3 free-ranging male and female S. harrisii did not enter daily torpor ( Jones et al. 1997). After 2 weeks of acclimation to 2–3°C temperatures, S. harrisii exhibits a significant increase in metabolic rate after injection of norepinephrine compared to controls injected with isotonic saline ( Kabat et al. 2003). These authors interpret this response as evidence that S. harrisii produces heat by non-shivering thermogenesis, despite a presumed lack of brown adipose tissue and the absence of uncoupling protein-1, both prerequisites for nonshivering thermogenesis in eutherian mammals. A further study ( Kabat et al. 2004), which examined the presence of 2 other members of the mitochondrial anion-carrier protein superfamily, revealed the presence of uncoupling protein-2 but not uncoupling protein- 3 in muscle and white adipose tissues.

Hulbert and Rose (1972) concluded that S. harrisii does not sweat (confirmed by Bell et al. 1983), but loses heat via panting, when it raises its breathing rate 7-fold. At an ambient temperature of 40°C, body temperature is kept at 38.5°C but under exertion (running, up to 5.6 km /h) or application of external heat load (Hulbert and Rose 1972), body temperature may rise to 39°C or 40°C. In contrast to eutherians in which less than 10% of heat is stored and most heat is lost by convection, conduction, or radiation, S. harrisii stores about 40% of produced heat ( Bell et al. 1983) and dissipates about one-half the heat by evaporative means, the latter almost entirely through breathing rather than the skin. These features are consistent with the relatively low body temperature and high rates of water turnover in S. harrisii ( Baudinette 1982) . Although panting is the usual mechanism to dump heat in marsupials, S. harrisii may possess a carotid rete, a network to send cooler blood to the brain ( Shah et al. 1986). Taken together, these studies indicate that S. harrisii has a metabolic rate typical of marsupials, is a good thermoregulator, and often has a body temperature 2–3°C below the eutherian mean of 37°C.

Heart rate is somewhat variable, but averaged 102 ± 17 (SE) beats per min for 20 animals at thermoneutrality, whereas blood pressure readings of unanesthetized animals at thermoneutrality averaged 131 ± 26 mm Hg/98 ± 23 mm Hg ( Nicol 1982, who also summarizes hematological data). Parsons et al. (1970) recorded a mean aortic blood pressure (under anesthesia) of 94 mm Hg/ 42 mm Hg.

Numerous studies have been conducted on the blood, starting with Parsons et al. (1970), who found, among other features, high levels of acid phosphatase. Both serum and tissue levels (16 μg) are exceedingly high ( Parsons et al. 1971a); the enzyme has a molecular weight of 85,000 ( Sallis et al. 1973). S. harrisii and the next larger dasyurid, Dasyurus maculatus (spotted-tailed quoll), differ from other mammals in their high levels of acid phosphatase (Sallis and Guiler 1977). The values of 32.50 and 20.14 µ mol-p-nitrophenol formed per ml per min in plasma, respectively, are the highest recorded for any mammalian species, and are 1–2 orders of magnitude greater than those of other marsupials and of humans. Parsons et al. (1971b), who determined levels of serum and red blood cell electrolytes as well as those of several organic constituents and serum proteins, recorded pH and levels of gases in blood for S. harrisii below those of 5 marsupials and of humans for CO 2, HCO 3, and both percentage of O 2 and O 2 as a percentage of saturation. Benga et al. (1993) measured membrane permeability to water and other features of red blood cells. More detailed accounts of blood components ( Clark 2004) describe erythrocytes as eosinophilic discocytes with slight central pallor. Neutrophils have 3- to 7-lobed nuclei of clumped chromatin and colorless cytoplasm. Small- to medium-sized lymphocytes have round nuclei packed with dense chromatin and surrounded by little basophilic cytoplasm. The nucleus of monocytes is irregularly shaped and composed of lacy chromatin with a granular gray cytoplasm and each eosinophil has a 2- to 5-lobed nucleus and a pale basophilic granular cytoplasm.

The adrenal gland of S. harrisii is similar in size for both sexes, 171 mg /kg in males and 163 mg /kg in females. Cortisol is the major corticosteroid in the peripheral blood plasma ( McDonald 1977), which also contains a steroid tentatively identified as corticosterone (Weiss and Richards 1971). Plasmafree corticosteroid levels in free-ranging S. harrisii , 5.6 and 11.9 nM for adult males and females, were similar to values, 10.0 and 12.4 nM, for juvenile males and females, respectively ( Pemberton 1990). Females have high corticosteroid levels during the breeding season and when young are 1st deposited in nests, whereas males have constant levels, including those of testosterone, throughout the year ( Pemberton 1990). Males, when restrained for 5–10 min and lightly anesthetized, have peripheral plasma cortisol concentrations of 2.8–3.7 µg /100 ml, whereas females in the same conditions have a mean value of 7.5 (Weiss and Richards 1971). In males taken into captivity, plasma cortisol concentrations fall to basal levels after only 48 h in captivity ( Lockhart 2000). However, females have higher stressed secretion rates (190 µg kg−1 h−1) and higher stressed plasma concentrations (8 µg /100 ml) than males (111 and 3 µg, respec-tively—McDonald 1977). Neither sex shows seasonal patterns of corticosteroid levels nor are seasonal peaks of testosterone detected during the breeding season, as is typical of some smaller semelparous dasyurids. Testosterone levels in free-ranging adult and juvenile males were 0.66 and 0.78 ng /ml, respectively.

Both sexes show a neutrophil-to-lymphocyte shift over the mating season indicative of reproductive stress ( Burton 2002). An increase in the total number of neutrophils in males may relate to the extensive injuries they sometimes sustain during the mating season.

Like other dasyurids, S. harrisii is more tolerant to the poison Compound 1080, used to control some pest species, than are eutherian carnivores, likely because similar defensive molecules are found in a native plant, Gastrolobium . (Compound 1080, sodium monofluoroacetate, blocks enzymes that catalyze citrate and succinate metabolism, and thus inhibits the Krebs’ cycle, causing cardiac arrest.) On a mg per kg of body mass basis, S. harrisii is 38 times more tolerant of 1080 than is the dingo, a eutherian carnivore ( McIlroy 1982).

ONTOGENY AND REPRODUCTION

Ontogeny. —Neonates, like other marsupial young, must clamber from the birth canal into the pouch and find an unoccupied teat or die. Because neonates are numerous and the number of teats only 4, natural selection (and chance) determine which survive. Neonates weigh about 5 mg with a crownrump length of 6 mm, spend the first 90–105 days attached to teats, and a nearly equal time in the nest. Although weaned at 150–240 days ( Guiler 1970a reports 7 months, in November), or about 3–4 months later than other large dasyurids, maturity is not reached until nearly 2 years in most females. However, a fraction of females does breed as yearlings (immaturity confirmed by unfused tibial epiphyses) if they have achieved weights of 4–4.5 kg ( Hughes 1982). After the loss of adults in a diseased population, 1-year-old females with a mass of 6 kg entered the breeding population ( Lachish et al. 2009).

During early weeks of life, females are heavier than males, but by 18 months this pattern is reversed, and thereafter males can increase rapidly in mass ( Guiler 1978). Although males can be sexually mature at 3.5 kg and most complete growth by 24 months of age ( Pemberton 1990), some males continue to grow until they are 3–4 years old, by which age they may reach their final adult masses of 8–14 kg. Mass increased in 6 months from 2.28–7.27 kg to 3.5–9.4 kg for 2 males, an indication of growth potential in ideal conditions ( Guiler 1978).

Sarcophilus harrisii can live up to 8 years in the wild but in some populations few live past 3 years, an indication of variation in life span of recruits ( Guiler 1978). Juveniles have up to 80% mortality during their 1st year of independent life, with males outliving females, on average. Before weaned young enter the population, 61.5–91.0% (X = 76.2%) of the population is adult, a high value for carnivores ( Guiler 1978). Symptoms of physical deterioration due to age 1st appeared in zoo-held S. harrisii after 50 months of age (Holz and Little 1995). Gradual loss of balance leading to total hindquarter paralysis, interpreted as agerelated degeneration, is common; necropsies of aged animals revealed degenerative neurological disease consistent with these symptoms.

Although young are prey of wedge-tailed eagles ( Aquila audax ) or adult spotted-tailed quolls, adults have no predators, except dogs ( Canis familiaris ). Vehicular traffic can be a significant source of mortality for animals scavenging for roadkill (Jones 2000; Hobday and Minstrell 2008).

Reproduction. —Almost all dasyurids are seasonal breeders, with the period of pouch emergence and late lactation coinciding with spring and early summer in temperate Australia (Tyndale-Biscoe and Renfree 1987). Copulation in Sarcophilus harrisii is most common between mid-February and late March.

Gestation is 17.9 ± 1.0 days (SE: range 14–22 days—Hester-man et al. 2008a), with most births in April but some as late as July. Young are carried in the pouch for about 14–15 weeks, after which they are deposited in a den. They do not leave dens on their own until November and are weaned from mid-December to early February ( Guiler 1970a; Pemberton 1990).

Based on [22Na] and [3H] isotope-dilution techniques, females in late lactation have turnover rates per kg of body mass that were 90% and 60% (respectively) greater than those of males and non-lactating females, or of females carrying small young (Green and Eberhard 1979). The milk of S. harrisii is similar in 6 minerals to that of eutherian mammals, except for substantially higher levels of iron ( Green 1984).

All 3.5–9.8 kg males from April, May, and August exhibited spermatogenesis, and all males greater than 5.0 kg were judged to be fertile ( Hughes 1982). As in other marsupials, there is no evidence of either seminal vesicles or ampullary enlargement of the vas deferens, but a carrot-shaped prostate gland and 2 pairs of Cowper’s glands are present (MacKenzie and Owen 1919). The prostate gland contains glucose as a minor constituent but has substantial glycogen (400–500 mg %—Rodger and White 1977). Although the form in which the prostatic glycogen reaches the semen is unknown, glycogen is found in extremely high concentrations (4,000 mg %) in secretions recovered from the prostatic urethra and thus probably enters the semen intact ( Rodger 1978).

The scrotum, which is evident at birth ( Guiler 1970a), has a temperature at maturity of about 27.7°C, or 5.6°C lower than the body temperature of anesthetized animals ( Setchell 1977). By contrast, Guiler and Heddle (1970), using thermistors inside the scrotum, found testicular and body temperatures to be similar (34.5 ± 1°C). The diameter of the seminiferous tubules in the testes of S. harrisii is 360 µm, an average value for dasyurids ( Woolley 1975).

The sperm of S. harrisii , at 240 µm, is among the largest in mammals. Mature sperm in the proximal one-third of the epididymis show an unusual feature: the long axis of the head is held at an angle of 60–90° to the axis of the tail, supported by a conical cytoplasmic droplet ( Hughes 1982:60, figure 28). Identical in gross morphology and in ultrastructure to those of Dasyurus viverrinus (eastern quoll), a closely related dasyurid, the sperm also share some unusual features with the bandicoots (Peramelidae—Hughes 1982). Whether spermiogenesis is suspended during part of the year in adult males is moot. Among large dasyurids, only S. harrisii has sufficiently large testes to be a candidate for sperm competition ( Taggart et al. 2003).

The onset of breeding in females is marked by a conspicuous enlargement of the pouch to a moist, fist-sized structure with 4 well-developed mammary glands ( Hesterman et al. 2008b), with the uterus showing hypertrophy in association with preovulatory enlargement of Graafian follicles ( Hughes 1982; Keeley et al. 2012). Behavioral predictors of estrus in captive females include development of a fluid-filled neck roll, increased nesting behavior, loss of appetite, and lethargy ( Keeley et al. 2012). Ovulation is spontaneous, with large numbers of eggs released. Like other dasyurids, S. harrisii females produce more eggs and embryos (21 eggs—Flynn 1922; 15 embryos—Guiler 1970a; 11– 56 eggs and embryos in 6 females—Hughes 1982) than can be accommodated by the 4 teats. Although 4 is the maximum litter, usually only 2 or 3 survive to weaning age. Guiler (1978) found up to 80% of eligible females carrying pouch young; across his 10-year study 58.1% of females had young (X = 2.67 young). By contrast, Pemberton (1990 —2.30) and Lachish et al. (2009 — 3.40) recorded lower and greater mean numbers of pouch young per female.

The 14-day follicular phase of the estrous cycle is followed by an 18-day luteal phase leading to ovulation ( Hesterman et al. 2008a). In a zoo-study sample with 10 times more females, Keeley et al. (2012) report similar lengths of the luteal phases for both unsuccessful and successful matings (12.5 ± 1.4 (SE) days for the latter group). Pregnancy is accommodated within the luteal phase, and regression of the corpus luteum coincides with parturition. If lactation follows, the next follicular phase is suppressed and the corpus luteum of pregnancy slowly disappears or shrinks to a corpus albicans (Tyndale-Biscoe and Renfree 1987). An infertile cycle or loss of a litter is followed by another estrus after an interval of 33.7 ± 5.9 (SE) days ( Hesterman et al. 2008a). As many as 3 estrous cycles in a single year among females with unsuccessful matings are known ( Keeley et al. 2012). Hesterman et al. (2008a) documented female reproductive cycles between January and June, thus explaining the occasional presence of pouch young in late winter (July–September—Green 1967; Guiler 1970a) and 1-month-old young in August ( Pemberton 1990).

Eggs are about 435 µm in diameter ( Hughes 1982), including 3 egg membranes: zona pellucida (4 µm), mucoid coat (28 µm), and shell membrane (5 µm). All membranes and numerous trapped sperm remain intact while cleavages produce the cells of a unilaminar blastocyst (bypassing the morula stage of development). At least 20% of uterine zygotes fail to cleave and in some females less than one-half develop to the expanded blastocyst stage ( Hughes 1982).

The pouch, which develops from a circular fold of skin in the lower abdomen, expands as if to accommodate the growing young, opening backwards and downwards. The sex ratio of pouch young was unity in one study ( Pemberton 1990) but favored females (nearly double) in another ( Guiler 1970a), a pattern seen in another population ( Lachish et al. 2009), in which litters in diseased females had twice as many female pups as healthy females.

Young females average 2.0 young in the 1st litters ( Guiler 1978), but have 3.6 young per year during their 2nd–4th seasons, and 2.0 young in their last season, making a total of 14.8 young for the female that lives the longest in the wild. Pemberton (1990) also found that fertility decreased in older females, as indicated by increases in reproductive failure (no pouch young) as well as reductions in litter size from earlier years.

ECOLOGY

Population characteristics. —Both distribution and density of Sarcophilus harrisii correlate with low-to-medium mean annual rainfall (Jones and Rose 1996). Densities sometimes exceed 1 animal per km 2 in the eastern one-half of Tasmania, across the northern coastal region, and in a narrow strip down the west coast (Jones and Rose 1996). Population density varies across the landscape at a scale of tens of kilometers. S. harrisii was not always common, for Flynn (1939) describes the species as rare in his title. Earlier, Flynn (1922) had difficulty obtaining sufficient animals over 18 years of effort to study its reproduction. Numbers were thought to be low also in the 1860s, the early1900s, and the 1940s ( Guiler 1992). S. harrisii may have been most abundant in the 1970s–1990s, with estimates of 130,000 (Jones and Rose 1996). However, since the mid-1990s, an aggressive, rapidly progressing, and fatal disease, characterized by facial tumors, has resulted in massive population declines. The disease, 1st detected in 1996 in the dense populations of the northeast coast, has spread westward across the state at the rate of about 7 km per year, resulting in an estimated loss of one-third to one-half of the population by the end of 2003 (Jones 2003b) and perhaps 80% declines later ( McCallum et al. 2007). In 2016, the disease still was moving westward unabated but disease-free populations still remain in parts of the state.

Numbers also vary from year to year. A study population on the west coast ranged from 20 to 106 animals over 10 years ( Guiler 1978). Pemberton (1990), who trapped and radiotracked S. harrisii in the prime habitat of Mt. William National Park in northeastern Tasmania, estimated a maximum of 200 animals on his 16-km 2 study area, with mark-recapture estimates being nearly double that value.

After the large influx of weaned young into the population during January and February, the population was 72% young of the year, 7% juveniles (12–24 months of age), and 21% adults ( Pemberton 1990). Young females tend to be philopatric, whereas most young males disperse. In healthy populations, the number of transient S. harrisii decreases throughout the year, but the number of adult residents remains relatively constant.

Preweaning mortality was 27%, but far greater mortality (80%) was suffered by juveniles during their 1st year of independence ( Pemberton 1990). Annual adult mortality of 20% probably increases in older animals.

Space use. — Sarcophilus harrisii occupies overlapping home ranges that average 13.3 km 2 (range 4–26.7 km 2 for both sexes); the smallest are those of females with young in dens ( Pemberton 1990). Females attend denned young every night at 1st, but more sporadically later as the young approach weaning age.

Its widespread distribution within Tasmania suggests that S. harrisii has wide habitat tolerances. In general, S. harrisii is found in open forest and woodlands that are not too shrubby at ground level and so offer clear runs for hunting. It avoids open habitats, steep or rocky areas, and tall or dense wet forests, including rainforest (Jones and Rose 1996; Jones and Barmuta 2000), but is attracted to predictable point sources of food, such as roadkills (Jones 2000), garbage pits, “devil restaurants” for tourism, and carcass dumps on farms. S. harrisii reaches its highest population densities where prey is abundant, such as the short green sward of a sheep pasture that is attractive to macropods, its primary native prey in some locations (Jones and Barmuta 2000).

Diet. — Sarcophilus harrisii , a dweller of forest, woodland, and coastal scrub, is a generalist predator and scavenger, eating a variety of vertebrates, but mostly medium-to-large mammals. S. harrisii undoubtedly has benefited from the introduction of sheep in 1804; Tasmania had 2.4 million sheep in 2015, many of them under low-intensity “rangeland” management which results in many mortalities. S. harrisii can be a significant predator on young and moribund sheep if livestock husbandry practices are poor. Some breeds are better than others at protecting their lambs, but 1st borns of multiple births are particularly vulnerable while the 2nd is being born. The frequent presence of wool in feces indicates that sheep are often part of the diet of S. harrisii , especially in the drier eastern half of Tasmania where most of the sheep are raised.

Sarcophilus harrisii can consume food equal to as much as 40% of its body mass, making them noticeably plump ( Pemberton 1990). S. harrisii consumes hair and fragmented bones as well as the flesh of prey, leaving only parts of large skulls and the often still-filled colon. The scraps are strewn over an area of as much as 500 m 2. Dried chalky feces, often 20 by 150 mm and grayish from the remains of digested bone ( Jones 1995), usually contain bone fragments and large amounts of hair.

In the central highlands of Tasmania, lacking domestic animals, fecal analysis indicates adult S. harrisii consume large prey, such as common wombats, Vombatus ursinus , Bennett’s wallabies, Macropus rufigriseus , and Tasmanian pademelons, Thylogale billardierii (Jones and Barmuta 1998) , and rely less on smaller mammals and birds, the primary prey of subadults and juveniles. Diet overlap between adults and juveniles is less in summer, when adults shift toward the larger end of the prey spectrum, possibly because juveniles of their larger prey species are available then (Jones and Barmuta 1998). This dependence on large prey is reflected in stomach and fecal analyses from other parts of Tasmania, but a wide range of foods is eaten, including birds, rabbits, and sheep (review—Pemberton et al. 2008). In a study of 3 coastal and 3 inland sites from the western onehalf of Tasmania and using microscopic analysis of hairs from scats, Pemberton et al. (2008) report a remarkably catholic diet: scats had remains of birds (50%), wallaby or pademelon (36%), common ringtail possum ( Pseudocheirus peregrinus ) or brushtailed possum ( Trichosurus vulpecula —30%). Both possums are semiarboreal. Four of 44 scats had remains of the Tasmanian monotremes: platypus ( Ornithorhynchus anatinus ) or echidna ( Tachyglossus aculeatus ). Some of the identifiable bird remains were those of little penguin ( Eudyptula minor ) and short-tailed shearwater ( Puffinus tenuirostris ), both of which nest in cavities in coastal dunes. S. harrisii is the most carnivorous of the large dasyurids, consuming almost no plant material (Jones and Barmuta 1998).

All foods have a high content of protein, water, vitamins, and minerals, variable amounts of fat, but with small amounts of carbohydrates. Thus, S. harrisii obtains its hexoses largely from amino acids. With dentition and bite force to deal with every part of a carcass, S. harrisii scavenges more than the syntopic quolls ( Pemberton 1990; Jones 1995). When placed in small enclosures with 0.5 kg brown rats, Rattus norvegicus , S. harrisii is a clumsy killer ( Ewer 1969; Buchmann and Guiler 1977). Nevertheless, incidental (but no direct) observations show that they can be successful predators of 8 or 30 kg macropods. Whether they can attack and kill a common wombat, adults of which are twice the mass of an adult male S. harrisii , is uncertain.

Diseases and parasites. —An analysis of 100 years of disease and mortality for Australasian marsupials held at the London Zoo (Canfield and Cunningham 1993:165) revealed that “ill-defined dermatopathies” on the faces of S. harrisii , usually attributed to injuries related to fights, may have been “erosive squamous cell carcinomas.” The origin of these multiple proliferative lesions, previously reported for S. harrisii ( Griner 1979; Canfield et al. 1990), may not be due to traumatic wounds but to a genetic predisposition for tumor development in S. harrisii , as suggested by Griner. That work was prescient in light of the appearance in the 1990s of a facial cancer transmitted by bites (see details in the “Conservation” section).

Trichinella pseudospiralis , a nematode whose larvae encyst in muscle tissue, was detected in S. harrisii in 1988 ( Obendorf et al. 1990). A survey of 9 locations across Tasmania revealed infected S. harrisii at all sites, and an overall prevalence of 30% in 153 animals. At least 3 other Tasmanian mammals eaten by S. harrisii harbor this parasite, and cannibalism likely contributes to maintenance of the parasite in wildlife populations. When fed muscle from infected S. harrisii , laboratory rats, cats, 2 native raptorial birds, brush-tailed possum, eastern quoll, and other S. harrisii all became infected with T. pseudospiralis larvae ( Obendorf 1993).

The cestodes Anoplotaenia dasyure , up to 15,000, in the small intestine ( Gregory et al. 1975) and Dasyurotaenia robusta ( Beveridge 1984) , and a stomach nematode, Physaloptera sarcophili (Beveridge and Spratt 2003) , all infect S. harrisii . The filarioid nematode, Cercopithifilaria johnstoni , transmitted by the tick Ixodes trichosuri , sometimes is present in the subcutis of S. harrisii (Spratt and Haycock 1988) . Baylisascaris tasmaniensis is an ascaridoid nematode sometimes found in the intestines of S. harrisii ( Sprent 1970) . A new genus of mite that produced mange in a S. harrisii held in the London Zoo was reported by Fain and Laurance (1975) and the following 4 species of mites of 3 families were taken from S. harrisii in Tasmania: Diabolicoptes sarcophilus , Haemolaelaps flagellatus , Ornithonyssus (Trichonyssus) dasyuri , and Satanicoptes armatus ( Green 1989) .

Interspecific interactions. —The 3 largest (> 500 g) dasyurid carnivores, Sarcophilus harrisii , spotted-tailed quoll, and eastern quoll, are sympatric only in Tasmania. As the largest, S. harrisii dominates at a carcass, although an adult spottedtailed quoll can chase off a young S. harrisii ( Jones 1995) . S. harrisii overlaps in diet with spotted-tailed quolls, which in turn overlaps with and dominates eastern quolls (Jones and Barmuta 1998). Morphological patterning in trophic structures (canine tooth strength and masseter muscle strength) among the species and sexes of quolls in Tasmania, and character release among the same quolls on the adjacent Australian mainland where S. harrisii is absent, constitute evidence for competition among these carnivores at an evolutionary timescale (Jones 1997).

The role of S. harrisii in the community structure of carnivores is complex ( Dickman et al. 2014). For example, spottedtailed quolls adjust their activity to avoid S. harrisii where S. harrisii is at high density ( Hollings 2013). Further, S. harrisii seemingly suppresses the behavior and probably the abundance of feral cats ( Felis catus ), with increased detections observed in areas where the number of S. harrisii has declined from disease; 2 studies using different methods support this conjecture ( Hollings et al. 2014; Hollings et al. 2015). Even when S. harrisii is at low densities, cats still avoid them, both spatially (Lazenby and Dickman 2013) and temporally ( Fancourt et al. 2015a), indicating their strong suppressive influence. Also, S. harrisii may protect smaller carnivores such as eastern quolls through controlling cat numbers. Although severe weather may have contributed to the recent decline in eastern quoll populations ( Fancourt et al. 2013; Fancourt et al. 2015b), high cat densities now threaten the species ( Hollings et al. 2015), a further indication of the complex role of S. harrisii in the carnivore community in Tasmania. The disease-induced reduction in S. harrisii densities likely is triggering a complex trophic cascade, including an increase in invasive rodents and a decline in native small mammals in areas where cat detections are increasing ( Hollings et al. 2015).

HUSBANDRY

Sarcophilus harrisii has been reared successfully for a hundred years in Tasmania, initially using methods developed by Mary Roberts of Tasmania’s Beaumarais Zoo. In response to the threat of what is now called Devil Facial Tumor Disease (DFTD), quarantine protocols and breeding programs incorporating genetic variability have been developed to ensure substantial captive “insurance” populations. The pooled experience of zoo and wildlife park cooperators and of wildlife carers has led to standard guidelines, under the Australian Zoo and Aquarium Association, for use in the Tasmanian government’s Save the Tasmanian Devil Program (Hogg and Hockley 2013). In 2015, about 700 S. harrisii were held in captivity, including more than 500 in 40 institutions in Australia; others were in 3 locations in New Zealand and in 6 places in the United States.

Facilities to house S. harrisii under intensive management must be kept separated from other captive wildlife, have sufficient area for several animals, and be enclosed with non-climbable fencing. Environmental enrichment is vital, and includes hidden food, scats from others, natural vegetation including hollow logs, and substrate for digging. Less intensive facilities, known as “Free Range Enclosures,” in which other wildlife can mix with S. harrisii , also are permitted. Socialization of young animals is important both for developing competitive feeding behaviors at carcasses and for mate selection. Diet is almost entirely whole animal food including fur, feather, and bone, and occasionally a large carcass with offal and gut contents is presented. Water is provided for drinking, playing, bathing and, as needed, cooling; indeed, S. harrisii enjoys shallow water. The diet of captive females is more closely adjusted in preparation for the breeding season in February and early March.

BEHAVIOR

The behavior of Sarcophilus harrisii has been studied as much as that of any marsupial ( Croft 1982). In the wild, the major studies of behavior are those of Pemberton (1990), Pemberton and Renouf (1993), and Jones ( Lachish et al. 2007).

Sarcophilus harrisii spends the day in one of its well-hidden dens (X = 3.8 dens per adult—Pemberton 1990), often located in a wombat burrow or on the surface under a tussock. When the young become too large to be carried in the pouch, they are deposited in a den for a period of weeks ( Pemberton 1990). At least in captivity, females build a nest of dry vegetation in the dens, chewing and digging to create a thick bed.

A tireless runner, S. harrisii often runs a predictable transect, up to 20 km, to places where food was found in a recent night (Pemberton and Renouf 1993), the long-distance gait being a characteristic 1-1-2 pattern of right hind–left fore–left hind and right forefoot together has been observed by one of us (NJM). An average S. harrisii spends 7.7 h traveling 8.6 km per night while hunting ( Pemberton 1990). Animals from an alpine population ( Jones et al. 1997) spent an average of 8 active hours in both summer and winter (in snow). Continuous radiotracking revealed that travel was intermittent, perhaps indicating a dual foraging tactic, i.e., that of ambush predator (waiting to rush and overpower prey) while also covering large distances to maximize chances of finding a carcass. Nicol and Maskrey (1986) determined that a 5.2-kg S. harrisii had a maximal aerobic running speed of about 10 km /h, making such a dual strategy plausible.

As is typical of most dasyurids, S. harrisii catches and holds small prey with its forepaws. Dead prey is examined tactilely with nose, lips, and the numerous facial vibrissae. S. harrisii , which eats its own dead as willingly as those of other animals, consumes small prey head 1st but devours larger prey by working against the lie of the hairs toward the head (Eisenberg and Leyhausen 1972). With wallabies, the fatty tail often is eaten 1st (N. J. Mooney, pers. obs.). Isotope studies ( Pemberton 1990) show that S. harrisii , as gorge feeders, consumes one large meal every 4–8 days.

Once a carcass is located, consumption begins immediately unless another S. harrisii already has possession of the carcass; entry usually is through a wound, the cloaca, or the thin skin near the pouch or scrotum (Pemberton and Renouf 1993). Eating and tearing quickly, S. harrisii consumes the softer organs it can easily reach and then moves to limbs, completely consuming the bones as it does. The sounds of breaking bones, and the snuffling and other noises made by a feeding animal, usually are heard by others in the vicinity, and then the aggressive interactions at the carcass begin. Increasing amounts of time must be spent driving off intruders. Based on 47 nights (482 h) of direct observation at standardized carcasses at 7 sites of differing densities ( Hamede et al. 2008), the proportion of more than 1 S. harrisii at a carcass increased with density and, more importantly, so did the rate at which bites were inflicted. Nearly 90% of bites, and most puncture bites, were to the head.

Lone animals feeding on a carcass spend more time being vigilant than multiple feeders (Jones 1998). If the carcass is large, such as adult common wombat or sheep, feeding S. harrisii can take up positions at the ends and sides, but they usually do not feed shoulder to shoulder. The successful outcome of agonistic interactions ( Fig. 4 ) at carcasses depends on body size (larger), age (older), and the degree of hunger (hungrier— Jones 1995). Such interactions sometimes result in injury, particularly on the jowls and face, and wounds are common on older animals, often lightening the color of the face from the scars. Lactating females with denned young are especially aggressive. Young animals do not fare well in such feeding competitions and often obtain scraps only after larger animals depart. Young show higher levels of vigilance behavior at carcasses than adults, consistent with their smaller size and risk of injury from older animals (Jones 1998).

The eastern quoll, the smallest syntopic dasyurid, readily forages on mammal carcasses while maintaining higher levels of vigilance than S. harrisii does (Jones 1998). Once an S. harrisii arrives, the quoll moves to the sidelines and when a 2nd S. harrisii appears, the quoll departs.

Pemberton and Renouf (1993) examined the role of visual communication at dimly illuminated carcasses and recorded 20 postures observed during social interactions. Although physical damage seldom resulted, agonistic interactions led to wounds on the muzzle and rump, as supported by heavy scarring in those regions, particularly in males. There is no hierarchical structure to the sequence in which S. harrisii feeds, and feeding duration seems to be determined by satiety; feeding bouts of all individuals were similar in length except that some were longer because of interruptions caused by conflicts. Pemberton and Renouf (1993), who placed 20 kg of wombat and wallaby bait before making observations in controlled conditions, report that a mean of 7.5 devils consumed 90% of the carcasses (leaving vertebrae, skulls, and some long bones), each consuming about 2.7 kg. After a cow was shot in the study area, 22 S. harrisii were observed feeding simultaneously, but overall, 46.8% of observations involved 2–5 S. harrisii feeding simultaneously on smaller carcasses (Pemberton and Renouf 1993). Feeding duration averaged 34 min for both sexes; however, adult males fed much longer, 57.1 min. At a study site with a low population density of S. harrisii , 1.6 animals fed for an average of 33.4 min ( Jones 1995).

Social behavior is poorly developed in dasyurids, predation and scavenging being largely solitary activities. Pemberton and Renouf (1993), who observed more than 200 S. harrisii across a 46-km 2 area, never saw animals traveling in pairs or groups and never heard them vocalize except at carcasses. However, the overlapping home ranges indicate a tolerance among neighbors (a prerequisite to sociality), allowing Buchmann and Guiler (1977) to speculate that closed (family?) groups may feed communally on large carcasses. Play behaviors such as locomotory, mock attack, and wrestling are described for S. harrisii ( Fleay 1935) . In captivity, males dominate females except during pregnancy and when females are guarding young (Buchmann and Guiler 1977). The male often confines the female to her den for up to 12 days after mating ( Fleay 1935), a behavior confirmed in the wild by Pemberton (1990) and in zoo studies ( Keeley et al. 2012).

As in most nocturnal mammals, olfactory and auditory communication are most important, but S. harrisii also has well developed open-mouth (visual and olfactory) behaviors that can be a preliminary to such agonistic behaviors as chases, bites, wrestling, and, rarely, locking of jaws (Buchmann and Guiler 1977; Eisenberg and Golani 1977). S. harrisii also displays a lateral posture after “shouldering” against an opponent, including bumping and pushing with the rump.

Visual and olfactory behaviors are usually accompanied by vocalizations; 8 vocalizations and 2 non-vocal sounds are made by S. harrisii in captivity ( Eisenberg et al. 1975). The loud snorts and barks of a S. harrisii defending a food source can explode with the arrival of intruders into a loud cacophony of agonistic vocalizations, including growls, grunts, hisses, moans, footstamping, whines, and shrieks ( Eisenberg et al. 1975).

Of 11 vocalizations identified in the wild by Pemberton and Renouf (1993), the briefest was a snort lasting 162 ms and the longest a growl emitted for nearly 5.5 s. All were distinguishable by humans, and most had low frequencies of 9–12 kHz.

During courtship, the male makes a “huff” or “clap” sound while pursuing the female. Prolonged chases and thwarted mounting attempts usually are part of courtship. In captivity, a male marks its space with scent, either from a sternal rub, urine dribble, or a cloacal drag (Eisenberg and Golani 1977). The cloacal drag seemingly is important early in an interaction but once an animal has established dominance the frequency of marking behavior diminishes progressively in the subordinate animal (Buchmann and Guiler 1977).

In copulation, the typical neck-grip behavior of dasyurids sometimes is augmented by the male dragging the female. During copulation, which can last for several hours, the male grasps the female with his forelimbs, sometimes palpating her abdomen, especially when thrusting ( Croft 1982). Because males sometimes hold females in dens during a copulation period lasting more than 1 week, S. harrisii may be facultatively monogamous in response to high population density ( Pemberton 1990).

After the long period of pouch life, young are left behind in a vegetation-lined nesting chamber of a den while the mother goes out foraging. The female continues to nurse young for another 4 months and may bring food back to the den until the young are weaned, usually between mid-December and mid- January. About 2 months after permanent pouch vacation, usually in October, the young start to venture out from the den by themselves at night. The young are not taught to hunt nor do they accompany the mother at night. Although dispersal is malebiased, some young females do disperse.

GENETICS

Sarcophilus harrisii has a diploid number (2n) of 14 chromosomes, with 12 metacentric autosomes, a small metacentric X chromosome, and a tiny Y chromosome ( Sharman 1961). An analysis of population genetic structure using microsatellite ( Jones et al. 2003b; Jones et al. 2004), SNP, and mitochondrial ( Miller et al. 2011) and immune ( Siddle et al. 2010) loci revealed moderately low genetic variability (allelic diversity = 2.7–3.3; heterozygosity = 0.39–0.47— Jones et al. 2003b; Jones et al. 2004). S. harrisii has lost genetic diversity perhaps twice in its history: at the last glacial maximum (about 20,000 years ago) and more significantly about 3,000 years ago, at the end of prolonged and severe ENSO climatic events (Brüniche-Olsen 2014). Neighborhood size is about 100 km, similar to the postnatal dispersal distance from capture-recapture data of animals marked as juveniles ( Lachish et al. 2011). This movement distance is reflected in population structure, with extensive gene flow, which reduces at scales above 150 km, and with just 2 major genetic subpopulations in Tasmania, due to a band of less suitable natural and anthropogenic habitat (e.g., cleared land, urban development, tall wet forest or rainforest, and alpine habitat) that separates northwestern populations from central and eastern ones ( Jones et al. 2004).

The karyotype of cancer cells present in DFTD is distinctive and stable in diseased animals from geographic regions and has the following features (Pearse and Swift 2006): 13 autosomal chromosomes but no sex-determing chromosomes; no chromosome-2 pair; only 1 chromosome-6; the long arm of one chromosome-1 was deleted; and 4 unidentified marker chromosomes were present (designated as M 1 –M 4). Importantly, these anomalies were the same in tumors of all animals (n = 11). Thus, tumor cells are karyotypically distinctive from those of their hosts (Pearse and Swift 2006).

CONSERVATION

Fully protected by law since 1941, Sarcophilus harrisii received increased protection under the Wildlife Regulations of the Tasmanian National Parks and Wildlife Act of 1971. It is now listed under both Federal (Section 178 of the Environment Protection and Biodiversity Conservation Act of 1999 [40]) and Tasmanian (Threatened Species Protection Act of 1995) laws. Until about 2000, with estimated numbers as high as 130,000 (Jones and Rose 1996), S. harrisii was classified by the International Union for Conservation of Nature and Natural Resources at the category of “Lower Risk–Least Concern.” This status changed after the discovery in 1996 in a population in northeastern Tasmania of DFTD, a new, infectious, and always fatal cancer that has reduced some local populations by up to 90% in about 10 years, while overspreading much of Tasmania ( Mooney 2004; Hawkins et al. 2006; McCallum et al. 2007; Lachish et al. 2009; Jones et al. 2014).

Although population fluctuations have happened in the past ( Guiler 1970c; Bradshaw and Brook 2005), DFTD, if not controlled, clearly poses a threat of endangerment and even extinction in the wild ( Lachish et al. 2007). Soon after the consequences of DFTD became known (McCallum and Jones 2006), state and federal agencies mounted broad-scale efforts to diagnose, describe, and curb the spread of the disease (Owen and Pemberton 2005). Information was needed from a range of scientists: ecologists, geneticists, immunologists, modelers, pathologists, and veterinarians; even the general public provided many new records.

The 1st disease symptoms appear as patches in the mouth or on the cheeks, lips, and neck ( Fig. 5 ), then grow into large solid masses of soft tissue ( Fig. 6 ), usually circumscribed and flattened, and later progressing to tumors with ulcerative and exudative surfaces ( Loh et al. 2006a). The tumors, usually located in the dermis, are nodular aggregates of round- to spindle-shaped cells and often with a pseudocapsule divided by septae into lobules. Histologically, the cells are of one type and characterized by large nuclei. Tumors are locally aggressive and metastasize in 65% of cases ( Loh et al. 2006a), typical of undifferentiated softtissue neoplasms. As tumors grow, body condition deteriorates until death, usually within 6 months; causes of death vary but likely include starvation and secondary infections. Importantly, histological sections of tumors and related lymph nodes revealed a general absence of infiltrating T-lymphocytes, indicative of a failed immune response by the host ( Howson et al. 2014).

Despite S. harrisii having a functionally competent immune system ( Woods et al. 2007), the cells introduced by bites are not recognized as foreign, are not attacked by the immune system, and consequently are not rejected. The failure of the immune system to mount a proper response, while not well understood, is due in part to low genetic diversity, including in the major histocompatibility complex, the most variable part of the mammalian genome and important in recognition of self and non-self ( Loh et al. 2006b; Cheng et al. 2012). Recent genetic analysis of complete mitochondrial genomes from current and museum specimens indicates that low genetic diversity in extant populations predates DFTD by at least 100 years ( Miller et al. 2011).

Evidence that DFTD is a transmissible neoplasm, transmitted as a clonal cell line by injurious bites between animals at carcasses or inflicted during courtship and mating ( Hamede et al. 2008; Hamede et al. 2013), includes identical chromosomal rearrangements in all clones within each identified morphotype and the successful induction of the disease in healthy S. harrisii using cells from both natural tumors and cultured cell lines ( Pyecroft et al. 2007). DFTD arose in a female, as evidenced by X chromosome but no Y chromosome ( Tovar et al. 2011), in cells of neuroendocrine origin ( Loh et al. 2006b), more specifically Schwann cells ( Murchison et al. 2010). One Schwann cell protein, periaxin, was identified as being diagnostic for DFTD ( Tovar et al. 2011). This same research group ( Kreiss et al. 2011) also developed a mouse model that reproduces DFTD with fidelity: mouse cells are similar histologically and karyotypically, and xenografted DFTD tumors expressed periaxin, the marker protein that diagnoses DFTD.

Cells of all tumors have identical genotypes at multiple microsatellite and histocompatibility complex loci ( Siddle et al. 2007), further indication that all tumors are a single clone derived from one S. harrisii , an opinion also supported by Murchison et al. (2010). Thus, tumor cells are genetically different from host cells. Furthermore, the karyotypes of cells taken from tumors of animals of different sexes, ages, and regions are consistently similar in the high degree of aneuploidy and chromosomal rearrangement, indicating that cytogenetically, DFTD is relatively stable, leading Pearse and Swift (2006) to hypothesize that the cancer is acting as a transmissible allograft, with infectious cells introduced by bites.

The best early evidence of the local impact of the disease is from a longitudinal study, initiated in 1999 by M. Jones, of a S. harrisii population at Freycinet National Park, also on the east coast ( Lachish et al. 2007). Annual adult survival was about 0.5 and adults comprised 51–53% of the population until 2001, when the 1st diseased animal was detected. As DFTD moved southward, adult survival dropped to near zero within 3 years. By contrast, apparent survival of subadults, although more variable among years, was relatively constant across the 7-year study, declining slightly at the end. During the 1st two years of the decline in adult numbers, population size of subadults increased substantially, as if in response to release from competition from adults ( Lachish et al. 2007; Fig. 5 ). But this effect was shortlived and after adult population size fell to near zero, subadult numbers dipped to one-third of former levels. Documenting population declines is difficult but spotlight surveys of this population indicate reductions of 69–90% ( McCallum et al. 2007).

The outbreak and spread of DFTD through a population is characterized by a change in age structure, due to the loss of breeding adults (≥ 2 years). The average age of diseased animals in the Freycinet population was 2.27 years, but after 6 years adults comprised only 20% of the population and only one older animal had survived ( Lachish et al. 2009). Death (or disappearance) usually follows within 6 months of the appearance of DFTD symptoms. The higher growth rates of young animals at low density are attributable to greater feeding success because of fewer adults at carcasses or less competition for resources in other ways. In response to higher growth rates, some large 1-year-old females have become precocial breeders; thresholds were related to greater head width and heavy (6 kg) body mass ( Lachish et al. 2009). Precocial breeding increased in diseased populations by an average of 16-fold (range 13–83%—Jones et al. 2008). Another population response was that diseased females, although having similar litter sizes as healthy females (3.40 versus 3.42), had twice as many female pups compared to healthy females ( Lachish et al. 2009).

Besides documenting the progression of DFTD across the island, researchers and agencies have formulated plans to preserve disease-free isolated populations, such as those that might be established on nearby islands or on the mainland, i.e., places where healthy S. harrisii might be bred and held for later reintroduction after the disease has run its course ( Jones et al. 2007; McCallum and Jones 2010). By 2015, captive breeding populations were being studied at 7 secure sites on mainland Australia and also on Maria Island, Tasmania, and on the Forestier Peninsula through removal of the original population and introduction of healthy animals, at a time when disease-free populations were still present in the northwest and southwest of the state, and in pockets elsewhere ( Huxtable et al. 2015). Also, in September 2015, 20 S. harrisii injected with a vaccine derived from heatkilled tumor cells ( Kreiss et al. 2015) were released in a trial conducted at Narawntapu National Park in northern Tasmania, and a month later 40 unvaccinated animals raised in captivity were released on the Tasman Peninsula in southeastern Tasmania.

If S. harrisii is reduced to extremely low densities as a result of DFTD, other sources of mortality, which otherwise are not significant, might become important to survival (McCallum and Jones 2006). In such circumstances, mortality factors such as roadkill and persecution for alleged and actual livestock depredations gain additional importance ( Guiler 1970b; Jones et al. 2014). Although S. harrisii comprises only a small proportion of the overall roadkilled wildlife in Tasmania (<1%— Shaw 2003, and 8%—Hobday and Minstrell 2008), local mortality can be significant (e.g., the 50% population decline in 18 months after the paving of a road—Jones 2000). S. harrisii , in its nightly forays, moves easily along or is attracted to the roadway to scavenge on roadkilled wildlife. When dazzled by headlights of oncoming vehicles, S. harrisii often reacts unpredictably and so is among the most difficult wildlife for drivers to detect and avoid ( Hobday 2010).

With almost 100% adult mortality, S. harrisii is under extreme selection pressure to develop resistance to DFTD, to reduce transmission through behavioral mechanisms ( Dewar 2013), or to make such life-history adjustments as breeding at a younger age or producing more female than male offspring. The tumor also is evolving ( Murchison et al. 2010; Pearse et al. 2012), with tumor lineages being associated with epidemic and demographic effects ( Hamede et al. 2015). Rapid evolution of animal and tumor is expected, with DFTD eventually becoming an endemic disease and populations recovering.

Figures

Fig. 1.—An alert young Sarcophilus harrisii showing black coat with white marking on chest, prominent vibrissae, wet nose, and nearly naked ears. About 13% are all black. The sexes are similar except that males

Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of Sarcophilus harrisii (adult male, United States National Museum, USNM 252733) collected 4 June 1928; locality unknown.The specimen exhibits the tiny cranium, typical of marsupials. Photograph by Sam Hughes used with permission.

Fig. 3.—The distribution of Sarcophilus harrisii has been restricted to the island state of Tasmania, Australia, in historic times. The land area of the larger island of Tasmania, 64,519 km2, is approximately equivalent to that of the states of West Virginia or South Carolina, United States. Note the temperate location, 41–42°S.

Fig. 4.—Typical aggression between adult Sarcophilus harrisii, whether at a carcass or in contention for mates. Note the massive head, the postures during threat displays, the differential placement of white markings, and the pale cheeks of the older animal on the right, the result of scars from past conflicts. Photograph by Christo Baars used with permission.

Fig. 5.—The 1st symptoms of the fatal disease, Devil Facial Tumor Disease, often are patches of redness on the palate, lips, and snout. Note the relatively unscarred cheeks of this young adult Sarcophilus harrisii. Photograph by Christo Baars used with permission.

Fig. 6.—Adult Sarcophilus harrisii (photographed prior to 1996) with what is now called Devil Facial Tumor Disease. Such gross deformities of the advanced stages of the disease prevent normal feeding behavior, leading to death by starvation or secondary infections. At the time this photograph was taken by Christo Baars, Devil Facial Tumor Disease was undocumented in the literature.