Growth and physical development of captive-raised black-footed ferrets (Mustela nigripes).
Black-footed ferrets (Mustela nigripes) are one of the most imperiled extant carnivores [International Union for the Conservation of Nature (IUCN), 1988]. Because of their nocturnal, elusive and fossorial lifestyle, field studies of wild black-footed ferret populations are difficult. Consequently, morphological development of wild young has never been studied. Black-looted ferrets have been maintained in captivity on a few occasions (Aldous, 1940; Progulske, 1969), but the first attempt to begin a captive propagation program for the conservation of the species was not initiated until the 1970s at the Patuxent Wildlife Research Center, in Laurel, Maryland (Hillman and Carpenter, 1983). However, successful production of ferret litters in captivity did not occur until 1987 at the Sybille Wildlife Research Unit, under the auspices of the Wyoming Game and Fish Department (Thorne, 1987; Thorne and Williams, 1988; Williams et al., 1991).
Studies in ontogeny are critical to understanding various aspects of the biology of a species (Lehrman and Rosenblatt, 1971) and accurate developmental data are best collected in a controlled setting (Bekoff, 1989). Although extensive research has been carried out at the various captive colonies (Carpenter and Hillman, 1978; Hillman and Carpenter, 1983; Thorne and Williams, 1988; Miller and Anderson, 1990; Wildt and Goodrowe, 1989; Williams et al., 1991; Carvalho et al., 1991) systematic accounts of growth and development of black-footed ferrets have never been provided.
We describe postnatal growth and developmental stages of captive-raised, black-footed ferrets. Behavioral development of black-footed ferret young has been described elsewhere (Vargas, 1994). We fit growth data to a model that will provide predictions of normal black-footed ferret growth in captivity. This growth model can serve as a basis for comparison between captive ferrets raised under different environmental conditions, between healthy and sick kits, and between free-ranging and captive-raised kits. In addition to growth patterns, we describe the tooth eruption sequence of the black-footed ferret. This information will permit determination of age of black-footed ferret young found dead in the field, as well as aging skulls of juvenile black-footed ferrets housed in museums. Our data contribute to the understanding of the biology of a highly endangered carnivore, and provide a model for comparisons with closely related mustelids and with future generations of captive and wild black-footed ferrets.
MATERIALS AND METHODS
Animals and husbandry. - Black-footed ferrets at the Sybille Wildlife Research and Conservation Education Unit (Wyoming Game and Fish Department, Wheatland) were held in elevated cages (1.22 x 1.22 x 0.61 m) with a plywood floor and 1.27 cm vinyl-coated welded wire sides [ILLUSTRATION FOR FIGURE 1 OMITTED]. Each ferret had access to two nest boxes (0.39 x 0.51 x 0.31 m), one attached to the cage and another placed on the floor. The bottom nest box was linked to the cage floor with 1 m of plastic tunnel. Nest boxes were divided into two equal compartments; one was used as a nesting site whereas the other was a space for depositing body fluids. Two sliding partitions separated both nest box compartments as well as the nest box from the rest of the cage for both cleaning and observation. Animals were kept under simulated natural photoperiod and fed a daily diet of 40% ground rabbit (Oryctolagus cuniculus) or prairie dog (Cynomys leucurus) mixed with 60% commercial mink chow, plus freshly killed hamsters (Mesocricetus auratus) once per week.
After captive females whelped, food was made more fluid by adding water, and at kits' age 4 wk a food bowl was placed in the litter's nest box to encourage youngsters to consume this semisolid food. Throughout the study, each kit was kept with its litter-mates and mother.
Assessment of external development. - Growth data were collected from June to December 1990 and 1991. Nine black-footed ferret litters (average litter size = 3.5 kits) were used for this study. Growing animals (n = 32: 17[double male] and 15 [double female]) were observed daily by trained keepers who noted any newly visible morphological feature. During the initial 2 wk after whelping, disturbances to the litter were minimized; thus, kits were not weighed or otherwise handled. For closer monitoring of the young ferrets' development, a Panasonic WV 1850 TV video camera was attached to the top of the nest box providing round-the-clock images of the nesting site. At postnatal wk 3, each animal was marked with Nyanzol-D fur dye (Belmar Inc., P.O. Box 145, N. Andover, Mass. 01845) for individual identification. Individuals were trapped in a vinyl clad wire cage (12 x 12 x 46 cm) for rapid physical examination and weight measurement without direct contact with humans.
To evaluate black-footed ferret growth, 17 kits (7[double male] and 10 [double female]) from five different litters were weighed at weekly intervals, from the 3rd through the 27th wk of life. Two sigmoidal models (Gompertz and Michaelis-Menten equations; Zullinger et al., 1984; Bates and Watts, 1988, respectively) were examined for their efficacy at fitting male and female black-footed ferret growth curves (NONLIN, SAS Institute, 1987). Both equations estimated growth rate, asymptotic body mass, and age at which kits attain 50% of the adult weight. We used a modified form of the Michaelis-Menten equation that also estimates body mass at birth (M. Gillingham, pers. comm.). Our evaluation of the data is based on the modified Michaelis-Menten's model, although we will refer to the more popular Gompertz equation for comparisons with other species of Mustela.
Examination of black-footed ferret carcasses. - Because of the potential risks involved in handling an endangered species, colony husbandry was as noninteractive as possible. To obtain information on the development of black-footed ferret dentition, we examined all available carcasses of young black-footed ferrets at the Wyoming State Veterinary Laboratory. Among the 21 carcasses examined, there were nine different age classes: 11 days (n = 1), 16 days (n = 2), 4 wk [+ or -] 2 days (n = 3), 6 wk [+ or -] 2 days (n = 5), 7 wk [+ or -] 1 day (n = 3), 8 wk (n = 1), 9 wk [+ or -] 2 days (n = 3), 11 wk (n = 1), and 12 wk (n = 2). Frozen carcasses were partially thawed so we could examine teeth without damage to the specimen.
External development. - Black-footed ferret neonates were pink, with wrinkled skin and a fine coat of sparse white hair covering their bodies. Footpads and snout appeared naked, and the muzzle was darker than the rest of the skin. Black-footed ferrets' silky white fur became fuller and more apparent within a week. As in other species of Mustela, neonates were altricial and born completely helpless with ears folded over and closed eyes. Newborns had characteristic long thin bodies with an elongated neck and short legs. Nurslings were relatively active and managed to move themselves with the help of their strong forelimbs, although the posterior half of their bodies seemed weak and fairly immobile.
At birth black-footed ferrets had a dark line along their eyelids, as well as a darker snout. The latter characteristic enables rapid discrimination between newborn black-footed ferrets and domestic ferrets (Mustela putorius), which are born with pink footpads and pink snouts (Shump and Shump, 1978). Black-footed ferret feet and tail pigmentation was faint but already visible at 2-3 postnatal days. Typical face mask in the 32 observed kits was visible at 16-18 days, turned gradually darker, and became fully prominent at 32-35 days [ILLUSTRATION FOR FIGURE 2 OMITTED]. No differences were observed between males and females.
Black-footed ferret ears are flat and rounded, sitting perpendicularly above the zygomatic arch. Although ears were folded during the 1st few wk of life, they started opening at approximately 33 days (range: 28-36 days), acquiring the characteristic flat upright position [TABULAR DATA FOR TABLE 1 OMITTED] within 2-3 days [ILLUSTRATION FOR FIGURE 2 OMITTED]. Young kits began opening their eyes between 34-37 days after birth, and both eyes were wide open by day 39 [ILLUSTRATION FOR FIGURE 2 OMITTED]. Generally, one eye opened several hours to a day before the other. Upon opening, ferrets' eyes were dark marine blue but after a couple of days they turned brown, remaining so for the rest of their lives.
Following eye opening, ferrets became increasingly active. Within a couple of days, kits shifted from crawling to walking on all four legs. Walking was rapidly followed by sporadic play bouts (Vargas, 1994). Up until this time, the young frequently emitted a soft squeaking sound, but their vocal repertoire became increasingly complex (including the typical chatter, barking and hissing; Miller, 1988) shortly after their eyes opened [ILLUSTRATION FOR FIGURE 2 OMITTED]. Soon after eye opening ferret mothers began bringing their reluctant kits up to the surface of the cage, after which new motor actions gradually followed (Vargas, 1994).
Changes in body mass. - Mean adult body weight (g [+ or -] SE, weight range) for seven males and 10 females was: [double male] = 1035 [+ or -] 34.1, 832.1-1086.28; [double female] = 756 [+ or -] 20.5, 671.8-886.21. Although both the Gompertz and the modified Michaelis-Menten sigmoidal growth models generated identical residual plots and high correlation coefficients ([R.sup.2] = 0.99 for both sexes in both curves; Table 1), plots of both curves against data revealed that Gompertz equation tended to overestimate female growth during the 1st 8 postnatal wk.
Because we lacked black-footed ferret weights during the 1st 2 postnatal wk, the modified Michaelis Menten sigmoidal equation could not provide an accurate prediction of ferret body mass at birth. Parameter A in the modified Michaelis-Menten's model (Table 1) is, therefore, an overestimate of black-footed ferret's actual birth weights. In spite of the low adult weight attained by one of the males, asymptotic body mass (parameter C, Table 1) was notably greater for males than for females. Females reached 50% of their adult body weight (parameter D, Table 1) approximately 1 wk earlier than males. Although rate of increase in body mass (parameter N, Table 1) was higher for females than for males, 95% confidence intervals for this estimate overlapped in the two sexes, indicating that the difference [TABULAR DATA FOR TABLE 2 OMITTED] was not statistically significant. Females attained 95% of adult body mass at approximately 15 wk, whereas males did not reach this body mass until 18 wk after birth (Table 2).
Development of deciduous and permanent dentition. - Like most mammals, black-footed ferret dentition consists of two sets of teeth (Ewer, 1973). Deciduous dentition consists of 28 teeth: DI, 3/3; DC, 1/1; DP, 3/3, and the permanent set comprises 34 teeth: I, 3/3; C, 1/1; P,3/3; M, 1/2. Black-footed ferrets, like all other members of the genus Mustela (Ewer, 1973; King, 1989), lack the first premolars in both jaws. Deciduous dentition erupts between 16 days and 7 wk, and emergence of permanent teeth begins at 8 wk, leading to the complete replacement of the deciduous set by postnatal wk 12 [ILLUSTRATION FOR FIGURE 2 OMITTED].
The youngest carcass examined was that of an 11-day-old ferret, and at this age no teeth were present. Although we could not obtain the exact tooth eruption sequence, the two 16-day-old specimens already had incipient deciduous canines and shearing premolars. The second upper premolar, P3, was the largest carnassial-like milk tooth, shearing against the labial surface of p4 when the jaws closed. Both teeth had completely erupted in the three ferrets examined at postnatal wk 4. Except for I2, which was present at 4 wk in all three carcasses, the rest of the incisors were the last milk teeth to erupt (between 6 and 7 wk of age).
Replacement of the deciduous dentition began at 8 postnatal wk. Permanent I2 and i2 were present in the only 8-wk-old carcass available, and this ferret had other incipient incisors emerging through its gums. Canines and upper and lower first molars were the first permanent teeth we observed on the 8-wk-old ferret. All four canines emerged slightly in front of their milk precursors, and both deciduous and permanent sets remained together for at least 3 more wk (i.e., the three 9-wk-old and the only 11-wk-old carcasses had double sets of canines). Similarly, permanent ml erupted before replacement of deciduous p4, leading to a double set of functional carnassial-like teeth until permanent m1 was sufficiently developed. At 12 wk, the two black-footed ferrets we examined had complete adult dentition.
Young black-footed ferrets followed developmental schedules similar to those of other mustelids. Newborns of the long-tailed weasel (Mustala frenata), ermine (M. erminea), domestic ferret and Siberian polecat (M. eversmanni) are also altricial (East and Lockie, 1964, 1965; Shump, 1975; Shump and Shump, 1978; Rowe-Rowe, 1978; Powell, 1982; King, 1989). Least weasels (M. nivalis) are born naked, but develop a coat of fine hair within a few days (Heidt, 1972; King, 1989). During the 1st few postnatal wk, young members of the genus Mustela are incapable of regulating their body temperature (Segal, 1975). They channel much of their energy into growth and behaviorally thermoregulate by cuddling up to their mother and siblings (Segal, 1975). This behavior was also observed in captive-raised black-footed ferret young.
Anatomically, all previously mentioned mustelids possess long cylindrical bodies with elongated necks and short limbs. Although such body shape compromises metabolic efficiency (Brown and Lasiewski, 1972; Iversen, 1972), it offers these small carnivores the advantage of exploiting a fossorial niche space to which few other predators have access. The long, flattened and narrow skull is probably another adaptation to pursue prey through burrows (Ewer, 1973). An anatomical attribute in both juvenile and adult black-footed ferrets is the presence of 2-3 vibrissae (approximately 1.5 cm long) on the base of the elbow (D. Kwiatkowski, pers. comm.). Elbow vibrissae were occasionally observed in captive Siberian ferrets kept at Sybille (D. Kwiatkowski, pers. comm.). Black-footed ferrets and Siberian polecats are closely related mustelids (O'Brien et al., 1989) whose ecology is tied to the burrows of medium-sized rodents (Stroganov, 1962; Hillman and Linder, 1973). Perhaps elbow vibrissae are an adaptive feature to help orientation and navigation through the dark rodent burrows.
Body mass is the best criterion for determining growth in an organism (Heidt, 1970; Case, 1978). Although black-footed ferret weights at birth could not be recorded in this study, Hillman and Carpenter (1983) reported neonatal body masses ranging between 5.19.7 g for 10 captive-born, black-footed ferrets. Birth weights of 51 domestic ferret neonates ranged between 5.8 and 14.1 g, with no significant differences between males and females (Shump, 1975). Black-footed ferret growth curves resembled those of domestic ferrets (Shump, 1975; Shump and Shump, 1978) in that males and females parallelled each other during approximately the 1st 7 postnatal wk. In both ferret species, females appeared to grow faster and attained adult body mass earlier than males. Similar growth patterns have been reported for other mustelids such as striped polecats (Ictonyx striatus), African weasels (Poecilogale albinucha), American mink (Mustela vison) and least weasels (Heidt, 1970; Rowe-Rowe, 1978). Black-footed ferret growth rates, as estimated by the Gompertz sigmoidal model, are similar to those of mustelids of comparable body mass, such as European and striped polecats (Zullinger et al., 1984).
Adult body mass values reported in this study are similar to those attained by wild black-footed ferrets at Meeteetse, Wyoming (Anderson et al., 1986), in which males and females weighed an average of 1034 g (range = 915-1125) and 704 g (range = 645-850), respectively. Captive-raised male and female black-footed ferrets reached approximately 95% of their adult body mass by early autumn. At this time of the year, free-ranging ferrets increased activity and began to live independently from their mothers and littermates (Biggins et al., 1985; Richardson et al., 1987). Because growth rate is adapted to different features of an animal's environment, it is possible that rapid growth at an early age may confer greater survivorship at later ages (Case, 1978). If black-footed ferrets grew slower, they would reach adult weight later in the season. By then, harsher weather conditions could compromise their ability to disperse and establish themselves in a new area.
Although this and other studies (Anderson et al., 1986) strongly indicate that black-footed ferrets are sexually dimorphic, the smallest male examined in this study attained an adult body mass similar to that of females [ILLUSTRATION FOR FIGURE 3 OMITTED]. Causes for the smaller size of this male could include genotype, pathological conditions and environmental factors (e.g., less access to available food because of more aggressive littermates). Nevertheless, adult body mass of male and female black-footed ferrets differ, with males being approximately 25-30% larger than females (Anderson et al., 1986; data presented above).
Adult dental formulas are identical for all species of the genus Mustela, although developmental schedules for eruption of deciduous and permanent dentition vary among species (Aulerich and Swindler, 1968; Berkowitz, 1968; Heidt et al., 1968; Ewer, 1973; An and Evans, 1988). Between their 4th and 5th postnatal wk, captive black-footed ferrets begin consuming solid food, and at this time they have a functional set of deciduous shearing teeth. The deciduous dentition remains for a short period of time and is totally replaced by the permanent set during the ferret's 2nd mo of life. As Ewer (1973) pointed out, the milk teeth perform a different function than their permanent counterparts. Deciduous P3 and p4 function as carnassials, resembling permanent P4 and m1, respectively. The tooth replacement sequence ensures that black-footed ferrets possess functional slicing and shearing sets of teeth from the time they begin eating solid food. By the time black-footed ferrets have developed complete adult dentition, young are already capable of killing live prey, although predatory efficiency greatly improves with experience (Vargas, 1994).
Knowledge of black-footed ferret tooth eruption sequence will be valuable to identify ages of ferret carcasses and skulls found in the field and of specimens housed in museums. Growth curves and other developmental information provide representative baseline data for all facilities that raise black-footed ferrets in captivity. These data will be useful to identify growth anomalies in captive-raised or free-ranging ferret kits, therefore contributing to the overall captive breeding and recovery efforts for this endangered and remarkable carnivore.
Acknowledgments. - Our studies were supported with grants from the U.S. Fish and Wildlife Service, Wyoming Game and Fish Department, National Fish and Wildlife Foundation, and Wildlife Preservation Trust International. We are grateful to Tom Thorne and the Wyoming Game and Fish Department for providing access to the black-footed ferret captive breeding facility at the Sybille Wildlife and Conservation Research Unit. The National Zoo's Conservation and Research Center, Front Royal, Virginia and The Henry Doorly Zoo, Omaha, Nebraska, generously provided some of their black-footed ferret developmental information. We thank Dr. Beth Williams, Sandy Anderson, Don Kwiatkowski, Kyla Borghi, Donna Zyler and Debbie Colgan for assisting with the data collection. Drs. Ken Gerow and Mike Gillingham offered valuable statistical guidance and we greatly appreciate their input. Thanks to Dr. John Goodrich, Dr. Brian Miller and Dr. Gordon Kirkland Jr. for critically reviewing the manuscript.
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|Author:||Vargas, Astrid; Anderson, Stanley H.|
|Publication:||The American Midland Naturalist|
|Date:||Jan 1, 1996|
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