Below is the uncorrected machine-read text of this chapter, intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text of each book. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.
5 Techniques for Aging and Sexing Primates The amount of information that must be known about the in- dividuals of a population depends on the questions being posed. Simple distributional or density estimates, for example, can omit information concerning the age and sex of the animals. If we wish to ascertain whether a species has a monogamous or polygamous social organization, distinctions between adults and nonadults and between adult males and adult females will suffice. But if we seek to understand the dynamics of population growth and pat- terns of mortality and natality, as in life-history analyses, knowl- edge of the age and sex of all individuals in a large population sample is indispensable. Knowing a few easy-to-recognize "key" animals is useful for identification of a group for which most members are not identi- fied. The greater the number identified, the betterâbecause identifying a large number of individuals reduces the chances of counting the same individuals twice in a population census. Knowing the individual identities of animals is necessary for de- tailed studies involving individual life-history records; genealogi- 81
82 TECHNIQUES IN PRIMATE POPULATION ECOLOGY cal relationships among individuals in a group or population; and detailed behavioral, ecological, and genetic analyses. Methods for identifying and aging large numbers of primates individually from natural markings were developed by W. Dittus while study- ing a population of toque macaques Macaca sinica at Polon- naruwa, Sri Lanka. These methods, which have been refined over a period of 12 yr, are offered in this chapter in the hope that others may find them useful. The artificial marking techniques developed by R. W. Thorington and others are offered for use with those species and in those studies for which identification by natural markings is not feasible. Primate species vary greatly in the ease, or difficulty, with which the age, sex, and identity of individuals can be ascertained. Difficulties arise because of cryptic genitalia, invariable indivi- dual morphologies, small body size, and nocturnal habits. Among forest-dwelling primates there is the added problem of restricted observability, especially among arboreal primates dwelling in tall, dense rain forests. In areas where primates are hunted, the investigator may have difficulty in getting close enough to his sub- jects to observe them, and habituation of the animals to the ob- server may be impossible or vary tedious and time-consuming. The ease and reliability with which information concerning the age, sex, and identity of individuals can be obtained under natu- ral conditions might affect the type of questions being posed and determination of the species and habitat to be studied. A pilot study to ascertain the feasibility of obtaining the information rele- vant to the research aims is a valuable investment, especially if these aims require data concerning the age and sex of a large sample of animals, as in demographic analyses. A survey of morphological traits that are useful for aging, sex- ing, and identifying individuals belonging to all species of pri- mates is beyond the scope of this chapter. Indeed, establishing a key for aging wild primates is impossible because accurate age data for most species under natural conditions are lacking. In- stead, the aim of this chapter is to establish a methodology that can be adapted to a wide variety of primates. The following dis- cussion provides guidelines for sexing and aging primates by dif- ferent methods and with different degrees of accuracy.
Techniques for Sexing and Aging Primates 83 SEXING Among most sexually dimorphic primates, fully grown adult males may be distinguished from females by their larger body size, fuller musculature, larger canine teeth, and larger jaws and muzzle. Species vary in the expression of other secondary sexual characters. Adult male baboons, Papio and Theropithecus, de- velop long, thick mantles of hair around the shoulders. Adult male howler monkeys, Alouatta, have an enlarged hyoid and thick neck that may be accentuated by a beard. Adult male man- drils, Mandrillus sphinx, possess bright red and blue faces. Con- spicuous colors of the testes or of the perineal skin may be found in adult males among several primatesâfor example, vervet monkeys, Cercopithecus aethiops; mandrills and drills, M. sphinx and M. leucophaeus; and gray langurs, Presbytis entellus. Adult females of chimpanzees, Pan, baboons, and many ma- caques periodically exhibit large, red tumescent swellings of the perineum. The color and degree of swelling vary with the monthly reproductive cycle. Adult females of many macaques have red faces. In some species of gibbons, Hylobates, sexual dimorphism is expressed by marked differences in fur color, and this may vary geographically (Fooden, 1969). Failing such conspicuous sex dif- ferences, the adult females in many primates are distinguishable by their elongate teats, which in males are undeveloped. Geni- talia may be deceptive. The female spider monkey possesses a long, pendulous clitoris that is longer and more conspicuous than the male's penis. Although size differences by sex in adults generally favor the male, the importance of assigning sex on the basis of genitalia rather than on size alone is underscored by the fact that the adult fe- male may be slightly larger than the adult male in marmosets, Cal- litrichidae, and the black gibbon, Hylobates concolor (Rails, 1976). Distinguishing sex among infants and juveniles is difficult in some species because the genitalia or secondary sexual characters are insufficiently developed to be seen. Even congeneric species may differ in this regard; the genitalia of juveniles may be seen in the red howler monkey, Alouatta seniculus, but not in the man- tled howler monkey, A. palliata (Thorington et al., 1979).
84 TECHNIQUES IN PRIMATE POPULATION ECOLOGY In the Old World monkeys, the separation of the ischial callosi- ties may aid sex identification. In the toque macaque, for ex- ample, the callosities are separated in the female but fused in the male. The difference is most marked in adults. ESTIMATING RELATIVE AGE CLASSES FOR CENSUSES Because of the limited time available during broad surveys and many transect censuses, investigators have used the size-scaling methods of early primate field studies to develop general age clas- sifications and have assigned estimated chronological ages to these size classes on the basis of information from known-aged captive animals. In this method each animal is scaled against the largest animal in the group, usually an adult male, and is catego- rized as an adult, juvenile, or infant. Figure 5-1 illustrates the scaling technique for the arboreal howler monkey. With in- creased habituation, and thus improved visibility of the animals, investigators have subdivided relative-size classes into as many as eight classes, including adult males, adult females, subadult males, two or three juvenile classes, and often two infant classes. Body proportions change dramatically with growth. As the head becomes relatively smaller and the hind limbs, especially the thighs, relatively larger, the weight moves posteriorly, changing the center of gravity and the locomotor and postural capacities of the animal. The thighs of climbing species are smaller than those of running species, and the tails, especially prehensile ones, are larger. Both of these differences can be seen in contrasting the howlers with baboons and macaques. Grand (in press) described the changes in body proportions between infant and adult male rhesus macaques, and these are diagramed in Figure 5-2. Changes in the mass of body regions are more significant than those in their lengths. During growth, the head in relation to body weight decreases rapidly, from 26% in the newborn infant to 12% at 10-15 mo to 8% in the adult female and 6% in the adult male. The transformation for howlers between the head of the newborn (20%) and that of the adult male (8%) is less ex- treme than that for macaques, but the change in proportion of the tail (10%-5.5%) is more extreme. An appreciation of the de-
Techniques for Sexing and Aging Primates 85 FIGURE 5-1 Age and sex classes of howler monkeys. Top: A = adult male, B = adult female, C = subadult, D = juvenile, E = infant. Bottom: Size classes are superimposed on each other as a first step in scaling animals for estimating relative ages. Greater refinement is achieved by considering changes in body pro- portions. tails of these changes in body proportions over and above changes in stature greatly facilitates the aging and recognition of individ- ual animals. Commonly recognized classes are characterized below. ADULTS Adults are fully grown and reproductively mature. In males, adulthood is indicated by the full development of the genitalia and of the secondary sexual characters. Usually they are larger than those of adult females. As a practical starting point, adult females have given birth to at least one infant and often may be
86 TECHNIQUES IN PRIMATE POPULATION ECOLOGY 01 .0 .0 E - c => " 0 a â i_ o * -I 1- U- I Percent mass<l 16 46 12 46 l- I o Li- Newborn infant FIGURE 5-2 Changes in body proportions with age in macaques. seen carrying one (see p. 89). They are distinguishable from large nulliparous juvenile females by their teats (but see comment on p. 95). In the latter the nipples are small and unprotruding as in males, whereas in adult females they are elongated and often pen- dulous as a consequence of having been suckled. SUB ADULT MALES Subadult males are separately identified among sexually dimor- phic species in which the adult males are larger than the adult fe- males. They are intermediate in size between large juvenile males (or adult females) and adult males, and their secondary sexual characters are incompletely developed. A few primatologists (e.g., Neville, 1972) working with howler monkeys, Alouatta seniculus, also recognize a subadult female class. These are juvenile females that have started to develop but have not yet achieved the body size and genital configuration typi- cal of adult females. Most workers classify such females as juve- niles and restrict use of the term "subadult" to males between the size of adult females and adult males.
Techniques for Sexing and Aging Primates 87 JUVENILES Juveniles are young animals that are usually weaned and not car- ried by the mother but are not yet reproductively mature. The up- per size limit for juveniles corresponds to that of the average adult female, the lower limit to that of the largest infants. Several juve- niles of varying sizes and ages usually occur in any social group. It has been common in field studies to recognize several classes with each class encompassing a range of sizes that is distinct from other such classes. Thus, small juveniles are known as "juve- niles-1" and juveniles of the next larger size range are known as "juveniles-2" (see Figure 5-3 and Table 5-1). Generally not more than three juvenile size classes have been distinguished. INFANTS Infants are the smallest and youngest animals in a group. They are not yet weaned and are carried by the mother at least part of the time. The individual carrying an infant is not always its mother. For example, in tamarins, Callitrichidae, and squirrel monkeys, Saimiri, the fathers and other group members may carry infants; and in some colobines, juvenile females and adult Yr. 8 6-8 >5 Age/sex Am SAm Af J|m 12f FIGURE 5-3 Age and sex classes of baboons. Diagram of baboons traveling on the ground helps to scale identified, known-aged individuals. Table 5-1 sup- plements the figure. Redrawn from Altmann and Altmann (1970) and personal communication (1979).
88 TECHNIQUES IN PRIMATE POPULATION ECOLOGY females other than the mothers may cany infants. In many pri- mates the youngest infants are set apart from older animals by skin color or fur color (or both). The youngest infants are some- times referred to as "infants-1," and those that have undergone a color change but are still being nursed and carried by their mothers are referred to as "infants-2." These color changes are il- lustrated in Figure 5-3 and Table 5-1 for baboons. DIRECT MEASUREMENT OF CHRONOLOGICAL AGE The most accurate measurement of age is direct, and the most convenient unit for measuring age is the year. The year is also a biologically meaningful unit of measurement for age because pri- mates in most habitats are subject to seasonal environmental changes that directly influence seasonal variations in their food TABLE 5-1 Physical Characteristics of Amboseli Baboons Class Physical Characteristics Estimates of Ages (years)" 1963-1971 1979 Infant-1 Infant-2 Juvenile-1 Hair completely or partially 0-1/2 0-2/3 black (natal coat). Black spots in tail and shoulders remain longest. Skin pink or red from skin vascularity; ears and nose retain pink longest. Hair brown to cream-colored, 1/2-1 2/3-2 often lighter (in Amboseli) than that of adults. Skin pigmented black, as in adults, except for pink scro- tum. Not sharply demarcated from 1-2 2-4 previous class. Light hair retained. Face wrinkles dis- appear. Scrotum changes from pink to gray at 3-4 yr of age.
Techniques for Sexing and Aging Primates 89 TABLE 5-1 (continued) Class Physical Characteristics Estimates of Ages (years)" 1963-1971 1979 Iuvenile-2 Not sharply demarcated from 2-4 4-5 for previous class. Hair often females darker, as in adult. Males' 4-6 for testes descend at 5'/2-6 yr males of age. Adult female Sexually mature; sexual skin Over 4 Over 5 swells periodically. Nipples buttonlike when nullipar- ous; elongated in more mature, multiparous fe- males. First pregnancy at about 6 yr of age; full size reached at about 7 yr of age. Subadult male Development of secondary 4-6 6-8 sexual characters: mantle, long canine teeth, large size, greater musculature than females. Scrotum (testes) larger than Juve- nile-2. White streaks on muzzle. Canine ridges. Adult male Secondary sexual characteris- Over 6 Over 8 tics fully developed. "Age estimates were revised as a result of increased field experience (see p. 95). Source: Altmann and Altmann (1970) and personal communication (1979). supply, reproductive and hormonal states, behavior, and sur- vival. Direct measurement of chronological age requires the identifi- cation of individuals at birth and the tracing of their identity through time. Since newborn infants may have few traits that set them apart as individuals, the identity of the mother is useful. By the age of weaning, the infant may have developed some of its own distinguishing features. Although direct measurement of age is costly in human effort and time, it is valuable, if not essential, in any serious study deal-
90 TECHNIQUES IN PRIMATE POPULATION ECOLOGY ing with life history or demographic processes. Ideally, one would like to assess the ages of all individuals in a population to the neatest year. Such accuracy is not always possible and may not be necessary. For example, if identified animals of known chrono- logical age are first used to establish morphological criteria that correlate with age, then morphology might be used in turn to esti- mate indirectly the chronological age of animals whose birth days are unknown. INDIRECT MEASUREMENT OF CHRONOLOGICAL AGE Estimating chronological age from established morphological criteria is a compromise between relative and direct measure- ments of age and serves to establish chronological ages between and within relative age classes. Several changes take place in vari- ous parts, of the body as individuals grow. If these changes occur in a regular sequence and show a high correlation with chronolog- ical age, they may be used as a basis for estimating age. Once the criteria for such estimates are established for a species, aging may be done without the long-term investment required by direct ag- ing. Among the criteria used for estimating ages in primates are changes in the number and sequence of erupted teeth, tooth wear, eye lens weight, allometric dimensions and weights of or- gans and skeletal segments, skin color, fur color, and body size (Gavan, 1953, 1971; Gavan and Hutchinson, 1973; Reed, 1973; Rosenthal, 1968; Stahl et al., 1968; Wagenen and Catchpole, 1956). For the field worker who does not capture his subjects, the number and type of criteria are restricted to those external mor- phological traits that can be seen with the aid of binoculars. Ex- amples include changes in the color of the skin and fur, size of the body or parts of the body, and the development of genitals and secondary sexual characters. Many observable morphological traits change gradually with age and are not useful for aging. Therefore, as an initial step in aging wild primates, one tries to find distinct morphological discontinuities or age markers that correlate well with a specific age. One such marker is the transi- tion from the typically natal pelage to the adult skin and fur col- ors at 2-5 mo of age in many Old World primates. Other markers
Techniques for Sexing and Aging Primates 91 are the onset of reproduction, especially in females, and the end point of physical growth. Anchoring such events to the correct age requires an initial direct measurement through long-term ob- servation. Some of the physical characteristics that help define age and sex classes for a particular species are illustrated in Figure 5-3, which relates to baboons. Table 5-1, which supplements Figure 5-3, gives an idea of the continuing process by which age esti- mates are refined during field studies. During more than a de- cade of studying Amboseli baboons, Altmann and Altmann (1970 and personal communication, 1979) have been able to replace es- timates that correspond only roughly to chronological age with improved estimates based on individuals of known ages within their study populations. A method for obtaining weights of macaques under field condi- tions has been used by W. P. J. Dittus to augment observational techniques for estimating growth. This technique makes it possi- ble to obtain more precise data on the growth of some species, thereby enabling an investigator to examine more closely the re- sponses of individuals to variations with age and the food supply. By suspending a scale from a branch and placing food in a tray that is attached to the scale, it is possible to attract macaques to sit on the tray and so to weigh them. Weights can be read, with the aid of binoculars, from several meters away. ESTIMATING CHRONOLOGICAL AGES OF INFANTS In species in which changes from a natal pelage and skin color to an adult type occur, these changes can be used to age infants. The following morphological correlates of age are abstracted from a key that was drawn up for the toque macaque (W. P. J. Dittus, unpublished data). They illustrate the type of information that may be used for aging. Day of Birth Skin is pink and wrinkled. Natal coat is fine and uniformly dark brown. Eyes are open but squinted. Umbilical cord is attached; thick and flexible.
92 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Day 2-3 Umbilical cord is generally thin, dry, and stiff or sometimes miss- ing by the second day. By the third, it is usually missing, the eyes are wide open and alert, and the skin is less wrinkled and pink. Week 1-3 Very slight melanin starts to occur on dorsal surfaces of hands, feet, and forelimbs during first week. By the third week, these areas are noticeably light gray. Otherwise the skin is white, but ears may flush in hot weather. WeekS Light gray melanin begins to appear at outer edges of pinnae. Week 9-10 Gray hair follicles begin to appear on the bare white forehead as two small patches to the left and right of the midline. This is the beginning of the pretoque (see p. 111). Month 4-5 Dorsal surface of hands and feet changes to black and acquires fur as in adults. Pretoque hair patches fuse across the midline and with the toque hair on the crown of the head. Adult-type pelage prevails. Month 9-12 Pinnae are fully or almost fully pigmented black. In the toque macaque, changes in the texture and color of the natal coat are variable between 2 and 5 mo of age and therefore are not very useful for aging within this age range. Useful age markers concern the onset of melanin deposits and the growth of hair on naked areas.
Techniques for Sexing and Aging Primates 93 The transition from natal coat to adult pelage is variable also in the yellow baboon, Papio cynocephalus, and the deposition of dark pigment in the skin is correlated better with age. The follow- ing changes occur in infant yellow baboons (Altmann et al., 1977). At Birth Skin is pink. 7 Mo All infants have gray hands and feet, primarily gray paracollosal skin, a little gray pigmentation on a primarily pink muzzle, and pink ears. 72-75 Mo Skin pigmentation is complete except for males' scrota, which re- main pink until about the fourth year of life. Most primate field studies are now of sufficient duration that similar keys might be established for infants of many species. "Infancy" can be variously definedâthe definition depending on purpose. In life-history studies the ability to identify infants about 1 yr old is useful. The size and morphology of 1-yr-old in- fants might be taken as the criteria defining the transition from infant to juvenile states. ESTIMATING CHRONOLOGICAL AGES OF JUVENILES The problem of aging juveniles is to assign chronological ages to a gradient of body sizes between 1-yr-old infants and adult females. Age estimates are aided if we know the duration of the juvenile phase (or the age at which it ends), the variation in body size or growth rate with age, and the factors that affect variations in growth. These topics, although interrelated, will be discussed in turn.
94 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Duration of Juvenile Phase in Wild Populations The onset of reproduction in females is thought of as marking the end of the juvenile phase, but "onset of reproduction" has been variously defined. It has been defined as the onset of menarchy or puberty, the time of first conception, the time of first pregnancy, and the time of first birth. The ages differ for these events. Under field conditions the time of first birth is the most practical because it is an obvious event that can be dated. It can also be an- ticipated because pregnant females in late term are usually con- spicuous. If the period of gestation is known, the time of first con- ception can be estimated. The duration of the female juvenile phase will generally be set by the age at which reproduction begins. In some cases a female may attain full growth but be infertile. This will be an exceptional event and can only be determined by long-term monitoring. The relationship between age and the onset of reproduction is worth closer examination. Human studies (Frisch and Revelle, 1970) suggested that menarchy occurs over a range of ages and heights but at attainment of an invariable critical body weight. Peng et al. (1973) found that the female Taiwan macaque, Macaca cyl- copsis, cannot conceive unless she achieves a critical body weight in excess of 4 kg, and semen cannot be obtained from male Tai- wan macaques weighing less than 5 kg. Similar critical body weights have been established for female (5 kg) and male (6 kg) rhesus M. mulatta; for female (6.5 kg) and male (5-8 kg) Japa- nese macaques, M. fuscata (Mori, 1979); and for male (4.3 kg) cynomolgus macaques, M. fascicularis (Hartman, 1932; Valeric et al., 1971, quoted in Peng et al., 1973). Female howler monkeys, Alouatta caraya, weighing less than 4 kg did not con- ceive, and Gilbert and Gillman (1960) provide evidence from the chacma baboon, Papio ursinus, that is consistent with the finding in other primates and human beings that females below a critical weight do not conceive. The typically heavier species have higher critical weights for conception. If critical weight needs to be attained in order to reproduce, then any factor that may affect the rate of growth, such as food supply or social behavior, should influence the age at onset of re- production or the duration of the juvenile phase. For example,
Techniques for Sexing and Aging Primates 95 under extreme food shortage, the physical growth of female Japa- nese macaques was delayed and their average age at first birth in- creased from 6.2 to 6.8 yr, some not experiencing first birth until the age of 9 yr (Mori, 1979). Lacking long-term field data, primatologists have based their field estimates of age and of onset of reproduction on data from captive animals. However, captive primates usually receive liberal rations of well-balanced nutritious diets that maximize rates of growth and maturation. In nature, growth rates might be ex- pected to be less because of variations in the availability of food. Indeed, newborn rhesus monkeys whose mothers were caught in the wild weighed 14-19% less than those whose mothers were raised in the laboratory (Valerio et al., 1970). Recent long-term field studies in which the development of individuals was traced from birth to adulthood indicate that growth rate is slower than it was thought to be and that age at onset of reproduction is higher. For example, in his study of wild bonnet macaques, Macaca radiata, Simonds (1965) estimated the age of first birth in wild females to be the same as the age that had been established from studies of captive macaques: 3.5-4.5 yr. However, long-term field data for the slightly smaller toque macaque have shown that wild females of this closely related species do not experience their first birth until they are 5.5-6.5 yr old (Dittus, 1975, and unpublished data). Similarly, wild female baboons experience their first birth when about 6.5 yr old (Altmann et al., 1977), which is 2 yr later than the corresponding age of those raised in captivity. In light of these long-term field records, Dittus (1975) and Altmann et al. (1977) advanced their original estimates of age among juveniles. Thus, currently published estimates of age at onset of adult- hood in wild primates are probably considerably underestimated, particularly among the Cercopithecinae, if they are based on extrapolations of age from captive primates rather than on obser- vations of individuals in the field from birth to adulthood. Excep- tions to this might be the published estimates of age for Colobi- nae or others that are difficult to raise in captivity. Variations in the age at which the first birth in females occurs in a population may lead to uncertainty in determining age. To circumvent this difficulty, one may wish to distinguish between reproducing (primiparous and multiparous) females and those
96 at |3 i a 3 nt u i/i .Â§ & U .2? '3 g CO â¢o C at M lO ^j w c = 9(1 .= Â° 55 -H a *p il s I Â«â¢ -S Q Â£ <" Â« -H ll -H-H-H-H-H-H-H-H r*, ^ - ri m â ,c I-M <r> Â£ i/> oooooooo -H-H-H-H-H-H-H-H -H-H-H-H-H-H-H-H i/) OOOOOâ ââ¢ââ¢ -H-H-H-H-H-H-H-H oo o -" â Â»
Techniques for Sexing and Aging Primates 97 that are of the same age as the reproducing ones, but which are still nulliparous. Habitat, Social Rank, and Season of Birth as Factors in Growth Differences If body size is used to estimate chronological age, it is helpful to known how well age and body size correlate. Gavan and Hutchin- son (1973) provide some of the best data for such an assessment in their study of growth rates in rhesus macaques, Macaca mu- latta, raised under controlled colony conditions. Using animals of known ages, they measured the number of erupted teeth, the weight, and the sitting height (crown-to-rump length). A con- densed version of some of their data is given in Table 5-2. Using such data, Gavan and Hutchinson arrived at several regression equations for estimating age. Following are examples of equa- tions in which weight (WO is given in kg and sitting height (H) in cm: For males: Age = 0.537 X (W - 0.108) Age = (0.337 X W) + [0.058 X (H - 1.628)] For females: Age = 0.921 X (W - 0.646) Age = (1.021 X W) + [0.021 X (H - 0.152)] Testing these equations on a group of rhesus monkeys whose ages were known, the authors found their equations to have a maximum deviation of Â±0.4 yr. But this degree of accuracy is valid only for rhesus raised under ideal conditions. In wild popu- lations, growth rates are slower, but how do they vary? Wild toque macaques, Macaca sinica, living in good habitats weigh more than those living in marginal habitats, and socially high-ranking animals, which enjoy priority of access to resources, grow faster than low-ranking ones (W. P. J. Dittus, unpublished data). Whether such relations exist among other wild primates is unknown, but it is likely that habitat quality and social rank cause greater variation in growth in any wild, food-limited popu- lation (where such exist) than in captive animals that have access to a superabundant and invariable food supply. One would also expect year-to-year variations in the natural food supply to accen-
98 TECHNIQUES IN PRIMATE POPULATION ECOLOGY tuate or diminish size differences among growing animals born in different years. Primates subject to high year-to-year fluctuations in their food supply would be most affected. The traditional method of assigning ages to size classes as- sumes a fairly close relationship between body size and age. In light of the above, such methods might be scrutinized. Assigning ages to size classes is justified, however, where dis- continuities in size distribution are apparent and are the result of a birth pulse. A well-defined birth season is one in which births in a population are fairly well synchronized, so that most individuals of a given birth season are fairly close in body size and may be recognized as belonging to a distinct age class or cohort. How- ever, owing to the cumulative effects of differences in growth rates between individuals, these class distinctions become less de- marcated with increasing age. The effects of a birth pulse are most useful, therefore, in distinguishing the 1-yr-old juveniles from the newly born infants and from the juveniles 2 yr old or older. A breakdown of larger juveniles into distinct age classes pre- supposes an intimate knowledge of size differences by age. Given such knowledge of an average-sized juvenile of age "X," one might assume that in a large census sample the numbers of indi- viduals wrongly underestimated and overestimated in age for any one age class would cancel one another. Such errors, however, will only partly cancel one another as illustrated by the following example. Assume that the "true" age distribution in a hypothetical pop- ulation is like that in row 1 of Table 5-3. Assume further that 75% in each age class are estimated correctly (row 3) but that there is uncertainty as to the correct age for the 25% remaining individuals in each age class (row 2). The latter do, however, defi- nitely belong either to the age class under consideration or to one of the immediately adjoining age classes. If ages are assigned to the uncertain-aged individuals without bias into the age class in question or into one of the two adjoining classes, the numbers of uncertainly aged individuals are distributed evenly among adjoin- ing classes as in rows 4-7. These "best-guess" age distributions (rows 4-7) are added to the known (row 3) to arrive at a final esti- mate of age distributions (row 8). The percentage of error be-
Techniques for Sexing and Aging Primates 99 TABLE 5-3 Effect of Faulty Estimation of Ages and of Mutual Cancellation of Errors on Estimates of Age-Class Frequencies Number of Animals in a Hypothetical Population, by Age Classes (A, B, C, D) Row Number B D True age distribution 1 104 84 36 8 25% age uncertain 2 26 21 9 2 75% age correct 3 78 63 27 6 Number of individuals of ^\ f4 (26 H- 2) 13 13 uncertain age are as- / ) 5 (21 + 3) 7 7 7 signed equally among ( ) 6(9-5- 3) 3 3 3 adjoining age classes J L?(2 + 2) 1 1 Estimated age distribu- tion (sum of row 3 and rows 4-7) 8 98 86 38 10 % of error 9 6 2 6 25 tween the estimated (row 8) and true (row 1) age distributions is given in row 9. Although errors in aging are generally reduced for each age class by adjustments such as those illustrated in Table 5-3, it is evident that errors do not wholly cancel one another. The error is greatest in age classes with low frequencies. One way to reduce such errors is to combine two or more age classes and define the age limits of this combined class according to reliable age indicators. For example, in real census data, "young juveniles" might be readily distinguished as a distinct class as a result of a birth pulse and might be aged 1-2 yr old. "Old juveniles" might be those larger than "young juveniles" but smaller than adults; they would be 2-6 yr old. Sex as a Factor in Growth Differences Infant and juvenile males grow faster than their female peers among several primates studied in captivityâfor example, rhesus
100 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Macaca mulatta (Table 5-2), barbary macaques, M. sylvana (Roberts, 1978), squirrel monkeys, Saimiri sciureus (Kaak et al., 1979)âand in the wild population of toque macaques, M. sinica (Dittus, 1977a). Species differ in the degree of sexual dimorphism in size. If growth rates by sex under natural conditions are un- known, an attempt to adjust age classifications on the basis of sex differences in growth may assume a degree of accuracy in age determination that under field conditions is unjustified. Among infants and young juveniles especially, growth differences by sex are slight, and the task of making accurate estimates is made more difficult by size differences resulting from differences in date of birth relative to peers of the same birth season or cohort. That is, infants born early in the birth season will be larger than those born late, although both are classified as belonging to the same age class (e.g., 0-1 yr old). Among older juveniles, adjust- ment of age classification according to growth differences by sex may be justified if the effects of sex on growth are consistent and can be distinguished from other effects, such as social rank, and if the growth differences by sex are great enough to influence age estimates within the size-age categories chosen. For example, the error in age classification owing to growth differences by sex will be greater if fine distinctions in age are attempted than if several size-age classes are combined into one class spanning several sizes or years. Since growth differences by sex are cumulative, they will have their greatest effect among the oldest juveniles; therefore, they may need to be considered when establishing criteria for the up- per limits of the juvenile period in males. In females, this is marked by the first birth and poses no problem. For demographic analyses, one wishes to identify males that are of the same age as the females at first birth. Primiparous females often continue to grow for another year or so after their first birth until they reach full adult female size. In species where juvenile males grow faster than their female peers, a male the size of an average adult female may be fairly close in age to a smaller primipara at the time of her first birth. The de- gree of correspondence in these relationships needs to be estab- lished empirically for each species. Since first birth seems to occur at a constant critical weight, the sizes of primipara may vary less than the sizes of the average
Techniques for Sexing and Aging Primates 101 adult females. Hence, the size of a primiparous female may be an easier anchor for aging males of the same size. The age at which events such as first birth occur may vary ac- cording to the environmental conditions or according to whether the population is changing in size or is stable (Dittus, 1977a, 1980). Therefore, in using transitional stages such as first birth as indicators of age, one should be sure that the correlation between stage and age is established separately for each population under study. Traits other than body size can be used to supplement such age estimates. For example, during the later stages of the juvenile phase, the genitalia begin to change. Altmann et al. (1977) report that among yellow baboons, Papio cynocephalus, the scrotum of juvenile males turns from pink to gray at 3-4 yr of age. ESTIMATING CHRONOLOGICAL AGES OF SUBADULT MALES The criteria defining the upper limit of the juvenile male phase also define the lower limit of the subadult male phase. Examples of morphological changes in males of known ages are provided from the two primates for which such data are available from wild populations. Male toque macaques, Macaca sinica, by 5.5-6 yr of age are about the same size as multiparous adult females, and the canine teeth have erupted beyond the level of the incisors and molars. By the seventh year, the males are larger than adult females, and the testes have descended but are small. Males in their seventh and eighth year may appear lean owing to rapid skeletal growth that appears to have stretched their spare flesh. Full canine develop- ment, adult male size, and musculature are reached at over 8 yr of age. Male yellow baboons, Papio cynocephalus, are the size of adult females by 5 yr of age, are larger than all adult females by 6 yr, experience descent of the testes at 5.5-6 yr, and acquire full adult male development at over 10 yr of age (Altmann et al., 1977). In the toque macaque, the average weight of adult males is 5.35 kg, the standard deviation is 0.70 kg, and the range is 4.0-7.7 kg (N â 38 males weighed). Much variation in the body size of adult males may be true also of other primates. Therefore, definition of the criteria for the transition from subadult to adult
102 TECHNIQUES IN PRIMATE POPULATION ECOLOGY male could be problematic. In the toque macaque, some males in their prime (judged to be 10-15 yr old) weigh more than the "average" male owing to their well-developed musculature. Crite- ria for the transition to adulthood in males therefore might be taken as the attainment of canine teeth and body frame sizes, but not necessarily of body mass, as in prime males. AGING ADULT ANIMALS The onset of adulthood in males and females has been described in earlier sections. The end point of adulthood is defined by lon- gevity or maximum life span of a species under natural conditions. It has been assumed generally that primates and other animals maintained in captivity live longer than their wild counterparts. Although conditions in captivity may improve the probability that more animals will live to old age, it is questionable whether the chronological limits of longevity per se are advanced significantly in captivity. Long-term field studies of the toque macaque sug- gest that a few individuals live to be at least 30 yr old, a figure that agrees with longevity records of this species in captivity. Table 5-4 lists the longevity of several primates living in captivity. Age differences among adult primates seem to be registered best in the appearance of the skin and teeth. Therefore, it is more difficult to discern ages under field conditions in those species that are heavily furred and have deeply pigmented facial and other skin, since these conditions either hide or obscure changes in the skin with age. The experience of the investigator seems to be of little help in aging difficult species. Drs. Stuart and Jeanne Altmann have studied yellow baboons over many years and em- phasize their inability (and that of others) to discern age dif- ferences consistently among adult yellow baboons (personal com- munication). Although toque macaques may be exceptionally well suited for the identification of age-specific characters, adults were assigned ages only after the investigator had accumulated 3 yr of field con- tact with the macaques. Following Dittus' (1974, 1975) descrip- tion of characters that vary with age among adults, Hrdy (1977, Hrdy and Hrdy, 1976) attempted to classify adult gray langurs, Presbytis entellus, which are much more difficult to age than
Techniques for Sexing and Aging Primates 103 macaques. As observers increase their attention to the details of age changes in the skin, pelage, teeth, skeleton, and behavior of adults, it should become possible to distinguish ages among adults even in some of those species that have previously been thought to lack age-specific characters. This may be expected be- cause morphological changes are cumulative. Old age especially is marked by its own changes, such as weight loss, stiffness or lameness, and infrequent activityâfactors that can be recognized despite cryptic skin areas. The nature of the changes associated with aging vary with the species. Several changes are described here to illustrate charac- ters that were observed in toque macaques and can be seen by comparing the photographs in Figures 5-4 and 5-5. Gradual changes in the wrinkling and color of the skin become evident be- tween youth and old age. The facial and body skin of young adult animals usually is taut and smooth with few or no blemishes, whereas the facial skin of very old animals may appear pitted and creased, especially around the eyes and mouth. A loss of skin tonus may cause the lower lid to droop and produce "bags" under the eyes. The edges of the upper lips may be creased and drawn inward, giving a typically "toothless" appearance. Many small creases and wrinkles appear in the skin of the chest and abdo- men, and loose folds of skin appear at the juncture of the limbs and trunk and under the chin. In the Cercopithecinae, the empty cheek pouches may hang as large, loose folds of skin. Hanging teats and mammae and abdominal stretch folds may become prominent in old females. The degree of erythrization of the facial skin in some females also intensifies with age. The pale or slightly flushed complexion of young adult females may be intensified by middle age or old age to bright red and may deepen to bluish red in very old age. However, some young adult females also have bright red faces (but more even), and some old females have pale faces (but not unblemished), so that color is not a sole index of age. The num- ber and size of pigment spots and the prominence of facial hair, especially around the mouth, increase with age in both sexes. The number of scars and cuts in the ears accumulate with age, al- though by itself the amount of scarring is not a reliable index of age.
104 ^ !".-- CT* o^ ^ ^o r-" r"- r^ S = S u" S _, *5 "O â, ^3"Â°^, r""O*^.^ QO fN \p j- fN rs â¢Â« 53 C iO C ^J ** ~ 9- o o c TT -^ ^ "X âÂ» "*? 5 y * 0^ â ^ ON O^ C^^QN^rto* â I â â ,c â â Â«ccâ , c â -5 h? V â¢* V u Â«ru 42 M" Â«r Â« -o Â»; iÂ« .2 -o -o <Â« S -o Â«i r ^ U u u e Bb V U 5, > > V C > V c 1 = =â Â§CS Â«oo = = &52 >, A 4^303^^ ZCOCO^SOB^U [> 8 D. u Â« *- -â¢-. U S) u < -5 Â« r^ 10 fN ''T i"^ i/} fN r^ r â 10 â¢-â¢ c*^ oo o Q o a a â¢o V .c "S '3 S 1 0 O ts ^ Â£ JS 2 3 5 â¢0 '; ,5- S3 & o 1 .2 1 1 1 t * 1 S "^ *O -^ "3 in flj oC |E Â£.2^5 S2 S jj S ^ Â§ .Â§& J> Common Nami ^ | -S 1 f |.gga-gsJS8. ^l-s.f-g I 1 M-g-l l-g-g -"' Â« caj o^E_c"o M S,oSÂ«^^ ilSjg.&JJ a, <UQ-OcoS of-zca^oDooj in 3 .s Â£ 1 9 C Â§ 1 .- '>< &o "S 1 Â£ IN lilL.Pl li Jiff lt*: ll*tl 1-i illi iliiillm |jilfll|li4ijil| -i & 2, w 3 S CQ I H
105 Â§ t*- II 1 1 1 S 8 i wT wÂ» S "i u Â§ g- II 1 C c *â¢ Â» z â¢o si o ,G i Â£ rs c g; â¢o -o c c â¢o 1| g; ^ PS 2 Â« C3 flj â ' * B B C ON E ^- S 2 . c â¢S o t/T V V "O T3 4J .i, iU u *o c â¢o c tfl S S 4 " o â 1> Sd, rt o^Â£ c: ~ c o C CQ z O 03 Q3 O3 DÂ« O 03 ~ s .. . a a S?S O fN ,s s Â§1 55 b O b 0 b b b b b c o B 3 O* 3 O1 1 6 Hamadryas baboo Chacma baboon 3 Japanese macaque Rhesus macaque Pigtailed macaque Toque macaque Stumptailed maca Grey langur White-handed gib c & Â§ u M Â£ Si ,* 3 JO Gorilla Chimpanzee S 1 1 ^B ao 8 ^ Orangutan etf Â§ 00 B JP Â« & S C ? | a I a s 1 a C ^ a â¢Â« :aca nemestri- â¢aca sinica :6^to cristata >bus polykomt :opithecus dia io hamadryas io ursinus :aca fuscata â¢aca mulatto â¢aca speciosa :bytis entellus ilia gorilla troglodytes go pygmaeus V 1 3 if 2 ^ o u ^ Sr â¢8 c II 1 II II II ia ll o 14 4 S 6 2 Q
106 TECHNIQUES IN PRIMATE POPULATION ECOLOGY FIGURE 5-4 An adult male toque macaque, "Stumpy." Left, in December 1971 when middle-aged; right, in February 1980 when "senile." The number of red spots on the face has increased, and the facial skin has lost some of its tonus. Photograph courtesy of Wolfgang P. J. Dittus. Changes in pelage are probably most evident in very old age. The pelage may become dull and without luster, and bald spots may appear, especially on the tail. Dunbar and Dunbar (1975) described changes in the length and color of the cape in adult male gelada baboons, Theropithecus gelada, that may be useful for distinguishing ages among them. With increasing age the teeth become worn and discolored through tartarization. The canine teeth of adult males are espe- cially useful for gauging these changes. The canines of adult male toque macaques in their prime (judged to 10-15 yr old) are fully erupted, sharply pointed, and clean ivory colored. With increas- ing age the canines become less pointed, shorter, and more stained.
Techniques for Sexing and Aging Primates 107 By old age the canines may be worn to the level of the incisors, and the teeth in general are worn and stained yellow-brown. These changes, like those of the skin, are graded and may be use- ful for judging ages intermediate between youth and old age. Very old animals often experience a loss in weight and appear scrawny. Lameness, gnarled fingers, stiffness and swelling of the joints (apparent arthritis), and difficulty in locomotion collec- tively are signs of very old age. When stiff fingers or awkwardly mended joints or bones are seen in young animals, they appear to be the result of injuries rather than a general syndrome of stiff- ness. In the toque macaque the voice changes from infancy to adult- hood, and very old adults may have a characteristically low- pitched, raspy, or quavery voice. Waser (1978) describes a similar "old voice" in an old female mangabey, Cercocebus albigena. A summary of morphological traits observed in very old ani- mals of several species is given in Table 5-5. The most useful characters for assessing ages intermediate between young adult and very old adult are those that change gradually and progres- FIGURE 5-5 An adult male toque macaque, "Harris." Left, in December 1971 when middle-aged; right, in April 1975 after he had acquired a new cut on his up- per lip. The red spot under the left eye has grown larger, and several new small red spots have appeared. Photograph courtesy of Wolfgang P. J. Dittus.
108 B 1 X X X X X "*.-, ll X (X5 "u -2 s E " 1 1 0 1 XX X 1 *i; <u CQ Â°0 1 O J X XX C S> 1%, ! S ^ rt "^c O ll "8 6 * X X 2 . a B j? 1 1 X XX a E- .a a M v, 3 C a a- la 0 E s JS 2 2 S XX XX Â£ o u 3 2 ^ U CT" H â¢o O II "2 X x X X X X 2 â S S2 sl > "â¢- C 3 -0 JC 3 5 o o o-.E OJ O z ? S o -S X X Â« 8 â¢a v a a "3 <- Â° O Â£ 1 i/5 X Is o +.. ll ll V B 4^ Â« <Â« 00 W "? S â¢o il'lit ! li ill .a â B C "O 8! n -S Q.S? 8Â«SÂ§|8|c g - J ^ II M .5 < s<< H C 1 1 1 f 1 1 i 1 s 1 1 ? ? K O (J O
109 X X X X XX X X X X X XXX X X X X Â£ Â£ '5' c X X .2 "3 i . c) c â¢8 e (/! V SH X 1 c. "(j . | *Â« 1 ^ ts X XXX c Â£ Â«> Â¥.'. 2 S wi 2- c 1 '* a % w? lX ^ f> . 3 1 3 e ca ^ X X X X XX S Â£ Q Is Q .. jjf P â¢o OJ . c CL ~~ ^H Q Q S2 -o ^ rt ?z 3 s . ^L 00 X X X OJ C (^ Â±j o " ? 0 C go Co w ^ e cf -s o s Â« Q c M* SP . i â¢il c > i ^ 1 M Si n .S 3 ^1 X X X ^ "a Q " Sifaka Propithecus verreauxi (Jc 'White-fronted capuchin Cebus c Toque macaque Macaco sinica t d Rhesus macaque Macaco mulat "Gelada baboon Theropithecus g ^Chacma baboon Papio ursinus ( * Gray langur Presbytis entellus ( ' Chimpanzee Pan troglodytes (va 'Orangutan Pongo pygmaeus (M; *Man (W. P. J. Dittus, personal Hair loss, or bare patches Change in timbre of voice Loss of weight, scrawniness Accumulation of scars and injuries Stiffness, or difficulty in locomotion Lethargic or inactive * Mangabey Cercocebus albegina â¢8
110 TECHNIQUES IN PRIMATE POPULATION ECOLOGY sively with ageâfor example, the skin and the teeth. Although it is difficult to quantify these changes with age, they are very simi- lar to those that occur in adult human beings. It has been useful in the toque macaque to establish five adult age classes: young, young to middle aged, middle aged, old, and very old (or senile). Adult animals are assigned to one of the adult age classes based on the investigator's subjective appraisal of the animal's overall morphology or set of age traits as outlined above. As a rough approximation of the chronological ages that might correspond to each of the adult age classes, the following proce- dure is adopted. The "Young Adult Female" class is assigned a duration of 5 yr from the sixth to the tenth year of life inclusively (slightly revised since Dittus, 1975). The "Subadult Male" class (sixth and seventh years) plus the "Young Adult Male" class (eighth to tenth years) together span the same 5 yr as the "Young Adult Female." The remaining 20 adult years (eleventh to thir- tieth years) are divided equally among the remaining four adult age classes for each sex, each class thus spanning 5 yr. IDENTIFYING INDIVIDUAL PRIMATES BY NATURAL MARKINGS Free-living primates can be identified individually if they possess recognizable natural or artificial markings that distinguish them from other individuals. Natural markings are discussed below. A discussion of artificial marking techniques begins on page 117. Distinguishing individuals by their natural markings is by far the most common method used by field primatologists. Its suc- cess depends on the existence of morphological variations among the individuals in the population under study, on the experience and perseverance of the investigator in learning to recognize and record individual differences, and on good observation condi- tions. The following guidelines for the establishment of keys for identi- fying individuals were developed from the study of toque macaques, Macaca sinica, at Polonnaruwa, where observation conditions are good and where 500 toque macaques have been in- dividually identified by their natural markings. About 60 animals are added and lost annually. Each monkey is observed at least once a month as part of a regular census schedule. The guidelines
Techniques for Sexing and Aging Primates 111 are suggested as a general approach to the problem of identifica- tion and may have merit when applied to other species. SELECTING AND DESCRIBING INDIVIDUALISTIC TRAITS The most important aid to identification is knowing the kinds of differences to look for. A morphological trait that is to be useful for distinguishing individuals should have the following proper- ties: â¢ Variable between individuals. â¢ Constant through time or changing slowly enough to permit a record of the change. â¢ Visible under normal working conditions. â¢ Recognizable by other investigators. Some of the obvious traits that meet these criteria are sex, body size, missing limbs, healed scars, and presence or absence and size of canine teeth. Traits that are least useful for identification are those that change seasonally with the reproductive condition (e.g., color or size of perineal swellings in female baboons and some macaques) and those that change rapidly with maturation (e.g., color of pelage or skin among infants or the body size of subadult males). The first task in identification therefore is the selection and compilation of a list of reliable "key traits." Such a list may in- clude pelage color (among juveniles and adults); color of skin (face or other areas); length and configuration of head hair or mane; and distribution of pigment in ears, face, or elsewhere. The second task is to determine the extent of variation in the traits. The third is to devise a standard vocabulary for describing the variations in each of the key traits. The following abridged list is an example from the toque ma- caque: Pelage The pelage (exclusive of the head hair) is described at two levels: first, the basic or overall coat color of light, medium, or dark brown; second, the tint or hue of the basic color. Thus, medium
112 TECHNIQUES IN PRIMATE POPULATION ECOLOGY or dark brown furs can be tinted either orange, gray, or simply brown. Light-brown furs are more variable and may be tinted orange, golden, yellow, sandy beige, agouti, or gray. In addition to color the pelage varies in distribution of color and in luster. Head Hair Toque macaques and their closest relatives, the bonnet ma- caques, Macaca radiata, possess a whorl of hair that radiates symmetrically outward from a central spot on top of the crown. In the toque macaque, three growths of hair (toque, pretoque, and overtoque) interrelate to form very variable "hairdos," which may require lengthy though standardized description. The toque, which varies in color and especially in structure, is the most char- acteristic trait for some individuals, and it is useful for distin- guishing young animals over 6 mo old. Face Color The face color of adult females can be described as follows: pale skin color, slight pink flush, light red, medium red, deep red, and deep red to slightly purple. The distribution of the color varies. The facial skin color of adult males and of juveniles of either sex may be pale, typical medium tones, beige, slightly flushed, or grayish. The lower lip may be unmelanized or mela- nized according to certain patterns. Ears The skin at the juncture of the pinnae and the head and also the tragus may be melanized totally or partially black, in varying pat- terns. Pigment patterns of juveniles change gradually. Dermal Pigment The skin on the ventral or inside surfaces of the body and upper limbs is sparsely haired so that the light-blue pigmented skin can be seen. In many animals the "ventrum" is entirely and evenly pigmented; in others, white depigmented areas occur. The con-
Techniques for Sexing and Aging Primates 113 figurations of these white patches are evident a few days after birth and remain constant (allowing for allometric growth) through life. These ventral patches therefore are extremely useful for distinguishing infants and juveniles that may otherwise ap- pear similar. In addition to these traits and their variations, adult in- dividuals especially vary in the number, size, and distribution of black, gray, brown, and red spots on the face. To some extent, the time of their appearance and their size are age related (spots become more numerous and larger with age), but the locations remain fixed for life. Adults are also frequently scarred. RECORDING INDIVIDUAL IDENTIFICATIONS Having recognized the nature and extent of morphological varia- tion, one must decide how to record traits systematically in such a way that identification data are easily and quickly recorded, up- dated, and referred to under field conditions. Contrary to what one might expect, photography is not the most useful tool, chiefly because of difficulties in obtaining close-up photographs of small subjects (e.g., monkey heads) from various angles or profiles. In addition, one must contend with poor or varying lighting conditions in the forest, moving animals, delays in film development time, and the sensitivity of film to out- door tropical conditions. Photography is thus reduced to a sup- plemental method of recording. The preferred procedure is to observe the animals with binocu- lars, to write descriptions of the animals (and prepare drawings) while the observer is still in the field, and to record the descrip- tions on identification cards. (See Appendix C and Figure 5-6.) Morphological traits that are not easily and quickly drawn are de- scribed. Such traits include pelage, toque structure, ears, face color, ventrum, and "other," which may refer to crippling, scar- ring, odd behavioral traits, and gait. Characters that do not lend themselves to concise description are usually easiest to draw. These relate to the size, color, configuration, and distribution of spots or scars. In the toque macaque, such spots occur mainly on the face. Therefore, left and right profiles and a frontal view of a standardized macaque face are printed on one side of identifica-
114 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Stumpy Troop: B Stumpy Dec. 15, 1971 Adult male: middle-aged Pelage: mid-to-dark brown Toque: round; slightly projects beyond sides of head and to brows, thus hiding the pretoque Face color: normal beige, lip pigment thick and even Ears: both intact; tragus black Tail is cut; distal quarter missing Ventrum: light blue except for small white patches in left and right groins Harris b. __ Notches Troop: B Harris Dec. 15, 1971 Adult male: middle aged Pelage: mid-brown, tinted slightly orange Toque: round overtoque strands project beyond sides of head; pretoque small and V-shaped Face color: flesh color, lip pigment slight dip Ears: both cut; left tragus black, right blotched Ventrum: no white patches; all even light blue FIGURE 5-6 Sample identification cards (3" X 5") for the adult males whose photographs are seen in Figures 5-4 and 5-5. Red blotches are shown as circles, which are larger than actual size. Dark freckles are shown as dots. The sketch ap- pears on one side of a card, the description on the other.
Techniques for Sexing and Aging Primates 115 tion cards. The spots and scars are drawn on the faces at or near easily recognizable reference points, such as nostrils, lips, and corners of the eyes. Facial spots and scars, especially small ones, are frequently conveyed more clearly in a drawing than in a photograph. How- ever, photographs provide a better representation of a monkey's overall appearance or gestalt. As the sum total of a monkey's ap- pearance is memorized, its gestalt becomes more important to an experienced monkey observer, and progressively less reliance is placed on key identification traits. Identification cards are never- theless indispensable as mnemonic props because in making them an observer is required to learn to recognize individuals. Reliance on photographs alone may lead to unjustified confi- dence in one's identification ability. A combination of identifica- tion cards and photographs may be desirable, especially at the beginning of a study, as a check on one's accuracy in description. Additional information that can be written on the cards in- cludes the date of the description or redescription, the individual's social group, its identification code (name or num- ber), its sex, and date of birth or estimated age. For young ani- mals the mother's code may also be useful. The convenience of identification cards lies in the ease with which they are prepared and stored, and in their accessibility and reproducibility. The major investment in time occurs earlyâin learning the most use- ful traits and how to consistently recognize and describe their variations. With modification of key traits the card system has been ap- plied to the study of gray langurs, Presbytis entellus, at Polon- naruwa. As in the toque macaque, individual differences register best in the pelage color, configuration of the head hair, and in pigment patterns of the exposed skin. Gray langurs have darkly pigmented facial and body skin. Individual differences are mani- fested in small depigmented or "white" blotches of varying size and configuration that occur especially in the groin and inner up- per thighs. In addition, the skin immediately above and lateral to the ischial callosities may vary in extent, configuration, and color. Wrinkles, scars, and overall facial gestalt help to distin- guish individuals despite their generally all-black faces.
116 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Investigators working with other species or under less favorable observation conditions have relied on different traits. A charac- teristic that has provided a ready means for distinguishing indi- vidual capuchins, Cebus capucinus, has been forehead hair pat- terns. The patterns described by Oppenheimer (1969) during his study in Panama are illustrated in Figure 5-7. In tall closed-canopy forests the observation of primates is more limited, but investigators working in such habitats have found there a range of natural markings for recognizing in- dividuals. In some cases it has not been possible to identify in- dividual markings for all ages, and investigators have used marker individuals, location, and group affiliation to identify in- age sex 1 any age m/f m/f 1/J m/f J m/f J/SA A f A m FIGURE 5-7 Forehead patterns of Cebus capu- cinus. The faces have been drawn to the same size without regard to age or sex class to emphasize the variability in hair patterns. Redrawn from Oppen- heimer (1969). Symbols are: 7, infant; J, juvenile; SA, siibarinlt: /t. adult; m, male; and/, female.
Techniques for Sexing and Aging Primates 117 dividuals. The difficulties Struhsaker (1975) reported in identify- ing individual red colobus, Colobus badius, in Uganda are typical of those that have been faced by field workers in observing shy canopy primates. He reported: Among the red colobus, adult males were most easily distinguished as individuals. This was partly because they habituated faster and conse- quently, one could observe them for longer periods and thus pick out identifying marks. In addition, their appearance was more individualistic than that of the females. Invariably, I could pick out individual males on the basis of their facial and whisker characteristics. I did not need "natural" deformities such as ear notches or tail kinks to identify the males, because their faces all looked different. As an initial check on this means of identification I also kept notes on "natural" deformities. The most common natural mark was one or more stiff fingers. The digit number, combined with a notation of left versus right hand, provided a check against the identification based on facial appearance. Ear notches and tail kinks were notably absent from adult males, although some had tails that were 1/4 to 1/3 shorter than normal. In contrast, I found it quite difficult to identify adult females. For them I had to rely on tail kinks, whisker shape and extent of whisker development, and general tone of pelage coloration. Stiff fingers were not seen among the females, although some had pink tips on one or more digits. IDENTIFYING INDIVIDUAL PRIMATES BY ARTIFICIAL MARKING TECHNIQUES CAPTURING LIVE PRIMATES Usually it is expensive and time-consuming to capture live pri- mates. There is also a risk to the animal being captured. How- ever, there are many benefits to an ecological study when animals are caught, so in each study the benefits, risks, and costs should be carefully considered before a capture program is initiated (Thorington, in press). In using any technique for capturing primates, one should keep in mind the possibility of using decoy animals. A captured or tame primate will frequently attract others of the same species. A decoy can be placed in a separate compartment of a trap or in a cage where one wishes to dart or net animals. Since many pri- mates are likely to be abusive toward a strange animal in the ter-
118 TECHNIQUES IN PRIMATE POPULATION ECOLOGY ritory, it is important that a decoy be adequately protected. When used in a trap, decoys should be double-caged so they cannot be bitten. Trapping Trapping is the technique most commonly used for capturing pri- mates (Dawson, 1977; Neyman, 1977). Many kinds of live traps are commercially available (e.g., Tomahawk Live Trap Co., Box 323, Tomahawk, Wisconsin 54487, USA), but in most tropical countries they can probably be made less expensively than they can be bought (Neyman, 1977). A cage with a guillotine door can easily be fitted with a tripping mechanism that will cause the door to fall when an animal takes the bait. Such traps are made and used in most parts of the world. When several suitable live trapsâbig enough and strong enoughâhave been obtained, they should be placed where pri- mates are seen high in the trees or on the ground, as appropriate. The trap should be "prebaited" with a suitable food. Prebaiting involves propping up the door of the trap so that it cannot be sprung, putting food in it, and thus using the trap as a feeding station. The objective is to accustom the animals to feeding there without concern. The advantage to the trapper is that he need not check the traps regularly at a time when the animals are most wary of them and least likely to be caught. When the primates seem to be taking the bait the traps can be set. It is then important to check the traps regularly. Don't leave diurnal primates in the traps overnight or nocturnal primates during the day, and prevent them from being stressed by heat (es- pecially in the sun), cold weather, or rain. You will probably catch other kinds of animals, like birds and rodents, in your traps. If released, many of these will not enter the traps again, but some may enter repeatedly and become expert at stealing the bait. These will need to be dealt with in other ways. If the primates are social it may be possible to use a large trap to catch a whole troop or most members of one. Some persons have used a trap triggered by a string from a blind, in which case they could wait until several animals were in the trap before springing it.
Techniques for Sexing and Aging Primates 119 Once the animals are in the trap the job is to get them out with- out traumatizing them or the investigator. It may be possible to chase small primates out of the trap into a cloth or string bag, but it is desirable to anesthetize larger primates before removing them from the trap. For this it may be necessary to have a stick with a syringe on the end, arranged so that the syringe injects the anesthetic when the animal is poked. Use a short needle and poke him in a nonvital area, like the muscles of the thigh or the back. The safest anesthetic for nonhuman primates seems to be Keta- mine HC1 (Domino, 1964; Martin, 1972). It is probable that 10 mg/kg is a safe dose or an underdose for all primates. For ner- vous animals it may be better to use a combination of Ketamine and Ace Promazine. Add enough Ace Promazine to the Ketamine bottle so that the animal will get 1 mg of Ace Promazine for every 9 mg of Ketamine. Darting Darting techniques are useful for capturing animals under many circumstances when trapping is difficult or impossible, such as trapping species that are trap-shy or spend most of their time high in the trees (Scott et al., 1976a; Thorington, in press). These techniques are laborious, however, and there is more risk to the animal. A variety of darts and projecting weapons are available. Most commonly used are dartguns, blowguns, and crossbows. Dartguns are usually pumpguns or are powered by CO2 car- tridges. Generally, the CO2 guns are preferable. A pumpgun must be pumped up between shots, which is a noisy and time- consuming procedure. If one misses his first shot, he cannot quickly and quietly take a second shot with a pumpgun. To be accurate and effective a dartgun must fire straight; there must be an easy way to modify muzzle velocity so that one can shoot at animals at different distances; the darts must have de- pendable trajectories and must not tumble in flight; and the darts must not penetrate deeply but must discharge the anesthetic reli- ably. (Effective systems are sold by Pneu Dart, Inc., 406 Bridge Street, Williamsport, Pennsylvania 17701, USA, and by Telinject, Veterinarmedizinische Specialgerate GmbH, Hohenzollern- strasse 92, D-6700 Ludwigshaffen am Rhein, Federal Republic of
120 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Germany. Zoo veterinarians frequently have need of such equip- ment and may be able to advise you about its use.) A blowgun is as good as the person using it. With practice, a person can become accurate and develop a good range. A blow- gun is much quieter than a CO2 gun. It must have the attributes named in the preceding paragraph. The critical factor is the dart, which must be very light. Darts can be made from tuberculin sy- ringes with the plungers weighted so that they inject upon impact (Brockelman and Kobayashi, 1971; Dewey and Rudnick, 1973). Another kind of dart, which uses air pressure to inject the fluid, and a blowgun are also available from Telinject in Germany. A crossbow can combine the accuracy and range of a CO2 gun with the quietness of a blowgun. Most are a bit noisier than blow- guns, however, and they do not allow one to modify the "muzzle velocity" easily when shooting at animals at different distances. With an increase in distance, one must unstring the bow, give the bowstring a few more twists, and restring it, but when darting distances are fairly constant, this would not be a problem. (Cross- bows especially designed for capturing primates can be obtained from Mr. Thad Martin, Route 5, Box 65, Huntsville, Arkansas 72740, USA. They shoot tuberculin syringes on the end of short bolts. On impact, the momentum of the bolt pushes the plunger of the syringe, causing it to inject the anesthetic.) The drug is a crucial part of the darting system. It should have a high ratio of lethal-to-effective dose. It must be concentrated enough to ensure that an effective dose will fit into a small dart. Sernylan, a phencyclidine, is such a drug, but it may be difficult to obtain. Ketamine is safer, but is is not so strong; two to four times as much fluid needs to be injected from the dart. These drugs do not work instantaneously, and the animal may flee the immediate area after it has been darted. If adequately dosed, however, the animal will stop in a minute or two. In many forest situations, one must follow the animal closely during this time or risk losing it. When animals are darted in trees it is desirable to catch them, lest they injure themselves in the fall. A large animal is more likely to be injured in a fall than a small oneâand the larger the animal, the harder the task of catching it. Two persons holding the corners of a blanket can catch a 10-kg monkey falling from a
Techniques for Sexing and Aging Primates 121 tall tree. If the forest floor is open so that persons can easily posi- tion themselves under the animal, a bigger "net" is desirable. If the understory is dense and positioning is difficult, a smaller net may be necessary. When the animal is being caught and while it is being maintained in captivity, it is important to follow humane practices. Netting Netting is one of many other techniques that has been used in capturing primates. It has been used successfully in capturing some of the smallest primates and some of the largest. Large ter- restrial primates, like gorillas and chimpanzees, have been chased into lines of strong nets, where they have been physically overcome. This would appear to be hazardous for both the apes and the people involved. At the small end, bird nets have been used to capture tarsiers (Fogden, 1974). Presumably, mist nets of appropriate size could be used to capture a variety of species of primates that regularly leap from one tree to another. It is probable that mist nets would be most effective for capturing small nocturnal primates, like tar- siers and bushbabies, but it is possible that they could be used ef- fectively for animals like talapoins, squirrel monkeys, and mar- mosets. MARKING LIVE PRIMATES In some studies it is desirable to have animals individually marked so that they can be recognized from a distance or when they are recaptured. A variety of systems has been used, no one of which seems to be best in all circumstances (Thorington et al., 1979). Investigators frequently use redundant identifications as a pre- caution against the loss of one of them. If the animals do not need to be identified individually at a dis- tance, they may be marked with ear notches, with ear tags, or with tattoos. If the animals do need to be identified at a distance, they may be marked by clipping and dyeing hair, using collars and freeze branding.
122 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Ear Notches and Ear Tags To make ear notches one needs only a pair of scissors. By notch- ing the pinnae of the two ears in different ways one can make a variety of distinctly different patterns by which individuals can be recognized. Under some circumstances these notches will be dis- tinguishable at a distance. The only problem with ear notches is that animals sometimes notch their own ears or their neighbors' in fights. Before deciding to use a system of ear notches, look at some of your animals and determine if there are many that al- ready have notched ears from natural causes. If so. it is probably not a good system for that species. Ear tags are easily applied and are unambiguous marks. They can frequently be seen at a distance, although the number itself cannot be read. The only problem is that animals will occasion- ally pull them out. Some investigators have reduced this problem by placing one ear tag in each ear on the theory that it would be unlikely for an animal to lose both tags. Ear tags can be used for individual recognition at a distance. The simplest system is to use several tags on each animal. A small number of individuals can be coded by the number of tags they have in each ear. Another system is to paint the ear tags. An enamel paint will last some- times for several years, and while it does the individuals can be recognized by their color codes (Thorington et al., 1979). Simi- larly, a small bit of plastic surveyor's tape may be looped through the tag, and the color of the tape may be used to distinguish in- dividuals. For a species that is hard to sex in the field, a useful trick is to tag the right ear of one sex and the left ear of the other. In this way one can quickly ascertain the sex of individuals at a distance. (Monel self-piercing ear tags can be purchased from the Gey Band and Tag Co., P.O. Box 363, Norristown, Pennsylvania 19404, USA, or the National Band and Tag Co., 721 York Street, Newport, Kentucky 41071, USA.) Tattoos To tattoo an animal one must make small holes in the skin and rub a permanent ink into the holes. This can be done crudely with
Techniques for Sexing and Aging Primates 123 a needle and india ink. More desirably, one can obtain a tattoo kit for small animals, consisting of a set of small numbers and let- ters, a pair of applicator pliers, and some tattoo ink. (A small- animal tattoo kit is available from Nasco, 901 Janesville Avenue, Fort Atkinson, Wisconsin 53538, USA.) The numbers or letters desired are put in place in the applicator. One holds up a flap of the animal's skin, squeezes the skin between the jaws of the ap- plicator, which makes the chosen pattern of perforations in the skin, and then rubs the ink into the holes. It is best to tattoo a relatively hairless place that is lightly pigmented. The skin under the arm or in the axila is frequently good. In macaques the chest or sternal area is often light in color and sporadically furred, making it ideal for tattooing. If the skin is light in color one can use a black tattoo ink. If it is dark one should use green or white ink. Clipping and Dyeing Hair For temporary marks that can be seen at a distance, one can sim- ply cut the animal's hair in unusual patterns. Bands of hair can be shaved off the tail, for example, to provide a distinctive code, or patches of hair can be removed from other areas. One can also use hair dyes or bleaches. Nyanzol is a particularly good dye for this purpose. (It is available from Nyanza, Inc., 49 Blanchard Street, Lawrence, Massachusetts 01842, USA.) It is mixed with equal parts of hydrogen peroxide and water and painted on the animal to make dark patches in the hair (Fitzwater, 1943). Such dyes will last until the animal next molts its hair. It should not be overlooked that such dyes can therefore be used to determine when animals molt their hair in the wild. Collars For more permanent marking that can be distinguished at a dis- tance, collars and freeze brands seem to be the most successful. Leather collars are suitable in some circumstances (Scott et al., 1976a), but they should be held together with rivets rather than with stitching if they are to survive for long periods of time. Col- lars can also be made of ball chain. They can be cut to size easily,
124 TECHNIQUES IN PRIMATE POPULATION ECOLOGY and they may survive better than leather collars on animals that have claws. Ball-chain collars made of nickel-coated brass will not last as long as ball-chain collars of stainless steel. Use the thickest gauge ball chain that seems reasonable for the size of the animal being studied if you wish to obtain a "maximum life span" for the collar. Collars should not be too tight around the neck, but they should not be so loose that an animal can get its forearm caught in the collar. Both kinds of collars can be coded for recognition of individuals. Round, numbered metal or plastic disks can be hung from the collar; the numbers should be large enough to be read with binoculars at a distance. Plastic disks can be color-coded. The ball-chain collars can have colored beads on them, arranged so that each animal has its own color pattern. If four beads are used one can usually see two adjacent ones easily; it is frequently difficult to see all four. Thus, it is best to use only one or two colors, alternating the colors when there are two. The animal can then be recognized whenever two adjacent beads are seen. Freeze Branding Freeze branding is accomplished by freezing the skin for a short period of time. This kills the melanocytes in the skin and causes the hair to subsequently grow in white. By freezing selectively one can give each animal a distinctive pattern of white patchesâ white bands on the tail, for example. When liquid nitrogen is available one can do the freezing with a piece of metal that has been cooled to the temperature of the liquid nitrogen. The metal should be attached to a wooden handle. Do not try to hold one end of the metal piece while freezing the other end. The metal may be cooled in a bath of dry ice in alcohol if liquid nitrogen is not available. Another way to freeze the skin is to use a spray of Freon (Lazarus and Rowe, 1975), frequently available in radio stores under the name of "Component Cooler." Be careful to spray only the desired area. It is usually best to use a mask over the area being sprayed so that only a small part of the animal is frozen. For thin-skinned, small primates, the skin freezes in about 10 s; for big, thick-skinned monkeys, it takes about 30 s. Freeze branding does not hurt at the time it is done, but it does
Techniques for Sexing and Aging Primates 125 hurt later. In the interest of animal welfare, use as little skin as possible in branding. Since freeze brands are not distinctive until the new hair grows in, it is best to combine this technique with a more temporary one, like cutting the hair distinctively or dyeing it. TOOTH CASTS AND AGING Tooth casts provide a permanent record of the teeth of the ani- mals. They can be studied after the animals have been released, and they can be studied in greater detail than is possible in the live animal. From tooth casts one can estimate the ages of the ani- mals, obtain dental measurements, and study dental anomalies and orthodontic problems. It is argued that asymmetries indicate stress (Siegel and Doyle, 1975a,b). Dental asymmetries can easily be studied on tooth casts and could be used to study nutritional stress during development. Discrete and metric variations of teeth have strong genetic components. Thus, tooth casts can be used to determine how closely related different troops or popula- tions of animals are, and from them inferences can be made about the amount of genetic exchange between troops or popula- tions (Froehlich and Thorington, in press). To make tooth casts one needs plastic to make dental trays of the right size and shape, alginate for obtaining the molds, and dental stone to make the casts. Since these supplies are used by many dentists, they can be bought at any dental supply store or directly from dentists. The dental trays must be shaped to the dental arcades of the animals being studied, but they must be slightly larger. The up- per tray can extend straight across the rear molars, but the lower tray must be U-shaped so as to leave room for the tongue. If one has access to skulls of the species, one can pad the teeth with wet paper and then form the plastic over this before it hardens. Be sure to make the tray deep enough for the canines. If you do not have access to skulls, you will have to make your first casts with- out a permanent tray. Make temporary trays of cardboard, which you can shape to the animal you catch. When you have a cast of the teeth you can use it to make a permanent tray. If you are catching animals of different ages, you will need trays of different
126 TECHNIQUES IN PRIMATE POPULATION ECOLOGY sizes. With heavy paper or cardboard you should be able to make a tray for any dental arcade you encounter. The trays should have holes in them so that the alginate will ooze through, thereby fix- ing the mold to the tray. The tray then serves to hold the flexible aliginate rigidly in the shape in which it sets. To make a mold of the teeth, mix the alginate with water; you will probably find instructions on the container. Use a spatula for mixing, then transfer the alginate to the dental tray. Put the tray in the mouth of the animal, pressing the alginate firmly over the teeth. Hold it in place until the alginate sets, then carefully pop it loose from the teeth. Immediately examine the impression in the alginate. Be sure that you have good impressions of all the tooth crowns. Air bubbles in the alginate can obscure important de- tails. If the animal's tongue is in the wrong place, a whole tooth row can be concealed. If the animal's teeth were not clean, you may have a beautiful impression of a leaf or of a piece of fruit, rather than what you are seeking. If you have a good impression, set the mold aside wrapped in damp paper or cloth until you have time to make the cast. If the mold dries, all is lost. It is better to keep it in water than to risk having it dry out. The cast is made from the dental stone. Mix the powdered stone with water until it is a paste in consistency; follow the in- structions on the box. Then carefully fill up the mold with it. You will find it easier to avoid air bubbles if you first immerse the mold in water, pull it out, and shake off the excess water before filling it with the dental stone. The dental stone will displace or mix with the water deep in the cusps, whereas it will not mix with air bubbles that get trapped in the cusps in the mold. Be sure to build up a good thickness of dental stone above the teeth, for this will be the base of the cast when you turn it out. If the base of the cast is weak, the cast will be easily broken. Let the dental stone set and dry, but you will have an easier time removing it from the mold if you do not allow the mold to dry. When the stone has set fairly hard, you can immerse the cast and the mold in water for an hour or two before removing the cast from the mold. If you separate them under water, you may be able to pour a second cast in the same mold. With practice you will be able to pull a cast from a mold without damaging either, even though there may be long canines to worry about. Have some glue available so that you
Techniques for Sexing and Aging Primates 127 can glue any broken canines back onto the cast right away. Be sure to number your cast as soon as possible, either by scratching the number into the base as the dental stone hardens, or by writ- ing with india ink on the cast as soon as it hardens. Note the ani- mal number and the date so that you will not confuse the cast with any you may make later of the same animal, if you recapture it. New dental materials for tooth casts are becoming available. Molding compounds like silicone rubber provide a more detailed mold than does alginate. In fact, the detail provided by some is good enough for studies with the scanning electron microscope. These materials have the disadvantage of not mixing with water the way alginate does. Therefore, the teeth must be dry when the impression is obtained or the detail is lost. They have the advan- tage that the mold is permanent and will not dry out and lose its shape as alginate does. Therefore, one does not need to make the casts as quickly from the silicone mold as one must from the algi- nate mold. The casts may be made from dental stone with algi- nate molds, or for more detail the casts can be made with an epoxy plastic. Because most dentists know and use these procedures, it is generally easy to get a demonstration of tooth-casting techniques. It is also relatively easy to obtain the necessary supplies in tropical countries as well as in Europe and North America. You will need the following materials or substitutes for them: plastic for dental trays (e.g., "Coe" tray plastic), alginate for the molds, dental stone for the casts, "flexibowls" for mixing alginate and dental stone, spatulas, a toothbrush, glue, and small plastic bags for keeping the molds damp before casting. (For epoxy casts one can obtain the molding material Xantopran from Unitek Corpora- tion, 2724 South Peck Road, Monrovia, California 91016, USA.) A recommended epoxy for the casts is Ciba-Geigy Araldite Epoxy 6005 with hardener #956. It is desirable to store the molds in zip- lock plastic bags. For cleaning and drying the animal's teeth it is useful to have a small portable water-pick and canned Freon or dust-free air. In making the casts it is useful to have a vibrator to remove the bubbles from the epoxy.