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8 Determinants of Population Density and Growth In the foregoing chapters, methods for measuring a variety of physical, floral, and faunal parameters of the habitat were dis- cussed. In this chapter the relationships between some of these variables are discussed in light of their influence in determining population size in relation to environmental factors. MEASURES OF POPULATION SIZE IN RELATION TO THE ENVIRONMENT ESTIMATES OF DENSITY AND BIOMASS In estimating the vital statistics of a population, knowledge of only the numbers of animals is relevant. Often, however, population size is expressed as a density, which is defined as the number of animals per unit area. Statements of density express an interest in the relationship between a population's numerical size and its en- vironment. Density is often converted to biomass by multiplying the number of individuals in the population by their average weight. Accurate 176
Determinants of Population Density and Growth 177 estimates of biomass should take into account differences in the numbers of animals of different body sizes (or ages) in the popula- tion. Thus, expressed mathematically, £ nxWx Biomass = â where «x and Wx are the number and average weight, respectively, of individuals in age class x, there being a total of7 age classes, oc- cupying an area of size A. The weight of inert gut contents may be subtracted in estimates of mean weights. The biomass of a species roughly represents the amount of resources or energy that it extracts from an environment. Since species vary in body size, such interspecific comparisons based on numbers alone would be inadequate. It is desirable to express den- sities in terms of biomass because it provides some measure of the importance or impact that a species has on an environment relative to other species. Comparisons of biomass can be made between different age classes within the same population (e.g., adults ver- sus juveniles or males versus females) or between species, higher taxonomic groupings, or ecological groupings (e.g., folivorous ver- sus frugivorous primates). Different methods for estimating densities and their correspon- ding biomasses are in use. The following definitions are useful: Crude density refers to the number of animals within a defined geographic area without regard to the suitability of the area for supporting the species in question. Estimates of crude density are useful only for reporting numbers of animals in a defined area, such as a game reserve or census plot. The area itself may encom- pass a diversity of habitats, some of which are totally unsuitable for the species in question. Ecological density refers to the number of animals per unit area of suitable habitat. Estimates of ecological density may be higher than those of crude density if the latter incorporates areas not in- habited by the species of interest.
178 TECHNIQUES IN PRIMATE POPULATION ECOLOGY The most accurate method for estimating ecological density in- volves charting the actual area of land or home ranges that a set of troops or a population has been observed to be using. UsuaHy this requires a long-term intensive survey of a relatively small area of land. Eisenberg (1979) reviewed density estimates for neotropical primates made by 24 different authors. For meaningful com- parisons he found it useful to separate density estimates according to the method of data collection. For example, for each of the following species the first and second values from each pair of den- sity estimates are based on the home range method and on a less intensive survey method, respectively: Callithrix torquatus, 20/km2 and 15/km2; Cebus capucinus, 130/km2 and 70-90/km2; Alouatta palliata, 60-80/km2; Alouatta seniculus, 160/km2 and 86/km2. In each case the estimate of ecological density based on the home range method was greater than that based on a broader, less- intensive survey method. Probably the latter method involves the risks of underestimating the number of animals occupying a large area and of incorporating habitats of variable suitability. Eisenberg (1979) called ecological densities based on the inten- sive home range method "K density," on the assumption that these densities are probably close to the mean equilibrium density (see below) for the species in question within the particular en- vironment where the measurements were carried out. It is evident from these considerations that the method used for estimating density should be clearly spelled out in reporting estimates of density. MEAN EQUILIBRIUM DENSITY (jc) Figure 8-1 illustrates the pattern of changes in a hypothetical population having an annual birth pulse. Observations of growing populations have indicated that they eventually reach an endpoint of no more growth. Although popu- lation density may fluctuate, the mean value of population den- sity remains fairly constant through time. This value has been called the asymptotic density, or the mean equilibrium density, and has been designated by the symbol K. K relates to the rate of population growth, r, and to any mea- sure of population density, n, as follows. In growing populations, r > 0, n < K. In declining populations, r < 0, n > K. In
Determinants of Population Density and Growth 179 Time FIGURE 8-1 Changes in population density, n, in a hypothetical population having an annual birth pulse and increasing in density until it reaches its mean equilibrium density, K. The carrying capacity of the environment is defined by K rather than by the maximal (n2) or minimal («() values fluctuating about the mean K. stationary populations at equilibrium, r = 0, n = K. It is evident that any measure of population density, n, is not necessarily equivalent to K. One may assume that « = K only if the average population density over several years remains constant; or, if calculations based on other demographic parameters indicate that the rate of population growth, r = 0 for some time. The value of r is determined by the sum of the rates of birth (b) and immigration (im) minus the sum of the rates of death (d) and emigration (em); i.e., r = (b + im) â (d + em); or, if im = em, r = b - d. Since K is in part a function of environmental stability (see below), it is sometimes assumed that n = K if all other evidence points to long-term environmental stability. Such an assumption is less satisfactory than estimates of « over several years. THE CONCEPT OF CARRYING CAPACITY The mean equilibrium density, K, varies both with the features of the species and of the environment. The fact that different values
180 TECHNIQUES IN PRIMATE POPULATION ECOLOGY of K may be reached by the same species in different en- vironments, or by the same population at different times, has em- phasized the importance of the environment in determining K. As a result the focus of interest often is the environment itself, which may be discussed in terms of its "carrying capacity" with respect to a particular population, species, or group of species. Thus, carrying capacity is often used in an abstract sense in com- paring the relative qualities of different environments. It must be recognized, however, that the many factors that determine the quality of the environment and, ultimately, the value of n or K are not always known or easy to measure. For example, the food supply has a major influence on population density. Yet it is doubtful whether absolute food availability can ever be mea- sured, except perhaps in very simple environments. In contrast, the measure of K either in numbers of individuals or in biomass is fairly straightforward. For convenience, therefore, carrying ca- pacity is defined in terms of K, or, as the maximum mean density of a species that an environment can support on a sustained basis without being degraded. In such assessments, carrying capacity is represented by the ac- tual mean equilibrium density, K, rather than by the temporary maximal or minimal fluctuations away from the mean, par- ticularly if such fluctuations are short term, as result, for exam- ple, from an annual birth pulse (Figure 8-1). One should also be aware that predation or disease may depress population density, n, below its potential maximal K. Or, a rare environmental event, such as a severe drought, may temporarily depress K below its usual maximal value. On the other hand, an environmental change may be more permanent and alter the long-term carrying capacity for a particular species. Thus a change in n may indeed reflect a real change in K. One might suspect a change in carry- ing capacity especially if n changes over the long term. It is evi- dent that the nature of such interrelationships is best understood through a close study of both the environment and the population and preferably over a long term. Despite the limitations in measuring some environmental fea- tures, one can often gain a fairly good appreciation of the nature of ecological interrelationships from correlated changes among measures of different environmental factors. Whether or not one
Determinants of Population Density and Growth 181 may assume that such correlations represent cause and effect events depends on the quality of the information. Because of the complexity of the relationships that determine carrying capacity, one generally does not prove, but assumes, that a population's constant size may represent its mean equilibrium density with respect to the carrying capacity of the environment. DETERMINANTS OF POPULATION SIZE The causes and mechanisms responsible for changes in popula- tion size are of central interest in ecology. They may be approached at four levels: (1) measurement of the demographic processes underlying changes in population size or density, (2) identifica- tion and measurement of the environmental factors that may cause demographic changes, (3) measurement of annual fluctua- tions in food, and (4) identification and measurement of the behavioral and physiological mechanisms through which en- vironmental factors affect demographic processes. The last two levels are discussed in detail later. DEMOGRAPHIC PROCESSES This method was discussed in Chapter 7, which deals with population analysis. In that chapter we identified the basic data required for measuring demographic events and formulated the manner in which demographic processes determine population growth rates (e.g., R0). ENVIRONMENTAL FACTORS We have noted that many environmental factors influence population size and that the observable mean equilibrium density (AT) for a species may vary between habitats or over time within the same population. Several of the physical and biological fac- tors that ultimately influence densities of a population (or the carry- ing capacity of the habitat to support that population) are dis- cussed below. A simplified hierarchy of interrelationships between these factors is given in Figure 8-2.
182 TECHNIQUES IN PRIMATE POPULATION ECOLOGY POPULAT10N Species specific trophic adaptation CO* Availability of free water Floristic Environment * Plant species diversity, productivity and seasonally i \ Fauna! Environment Animal species diversity, trophic structure Physical Environment Geology and soil substrate ^=^ Climate: - temperature - amount and seasonal distribution of water > major influence â¢* secondary influence FIGURE 8-2 Interrelationships among physical and biological factors that in- fluence the population growth rate and mean equilibrium density of a species. Physical Factors Basically, the physical environment determines the diversity and abundance of plant life, on which all animals ultimately depend. Therefore, information concerning the physical world is useful for making predictions concerning the biological communities one might expect in a specific area.
Determinants of Population Density and Growth 183 On a global scale the warm lowland and tropical regions sup- port more diverse plant and animal communities than do the colder temperate or high montane areas. Areas of high rainfall that is evenly distributed throughout the year are richer in life than those of low or seasonal rainfall. On a local scale the loca- tion of oceans and mountain ranges in relation to prevailing wind currents affects temperature and rainfall patterns. For example, areas on the windward side of montane zones are generally drier and wanner than those on the leeward side. The effect of physical parameters can be more subtle, as in the Amazon rain forests where areas subject to nutrient-rich flood waters support a greater diversity and abundance of life forms than do areas that are not flooded, despite minor differences in rainfall or temperature between these areas. Similarly, in areas of equivalent rainfall and temperature, porous soils support less life than those that retain water. In classifying the world's vegetation into major types, such as savanna grassland, deciduous forest, semi-evergreen forest, and evergreen rain forest, Walter (1971) found the parameters of temperature, total rainfall, and the duration of drought in the an- nual cycle to be the most useful variables in predicting major vegetation types, despite variations in the taxonomic composition of the forest types. Biological Factors The density of a studied species may vary between habitats having similar physical characteristics but differing in species composi- tion. A biological community is composed of the vegetation that gives structure to it and the fauna that directly or indirectly depends on it for food and shelterâthe consumers, competitors, predators, and pathogens. The type of vegetation will in large part determine its depen- dent animal populations. For example, stable savanna grasslands support large and diverse populations of grazers and predators that prey on these grazers, whereas tall rain forests support fewer terrestrial animals. Instead, tropical forests support a larger biomass of arboreal browsing folivores and frugivores (Eisenberg and Thorington, 1973). Moist semi-evergreen forests support a higher density of primates than semi-deciduous dry forests
184 TECHNIQUES IN PRIMATE POPULATION ECOLOGY (Eisenberg et al., 1972), and even within small geographic areas, the diversity of the vegetation correlates with the diversity of primate species it supports (Struhsaker, 1975). The food supply is a major factor influencing the size of primate populations (Dittus, 1977a, 1980). The amount of food that is available to a species is determined by a variety of factors, including the species' trophic adaptations, the diversity and pro- ductivity of the vegetation in the habitat, and competition from other animals. These factors are not wholly independent of one another but interrelate in a complex fashion. These relationships and how they might be measured are examined more closely in the next section. The natural food supply for any primate is likely to fluctuate in abundance during the yearly cycle. Many vertebrates and in- vertebrates share the foods that are eaten by a particular primate species. If the food supply is limiting, competition from these animals is likely to have its greatest effect during the season of least food abundance. The extent of competition needs to be established empirically in each community. Indirectly, the vegetation will also influence the occurrence of predators for primates. The influence of predation can be estimated by making a faunal list of potential predators in an area and then making a rough estimate of mortality from preda- tion through long-term observation. The incidence of predation on a given primate species can also be assessed indirectly through examination of fecal scats of predators for remains of the primate of interest. Leopards, for example, exist primarily on prey species, such as deer, antelope, and pigs, that inhabit savanna and savanna woodlands. Although primates are not a major food item in the leopard's diet (Muckenhirn and Eisenberg, 1973), they nevertheless are subject to leopard predation in habitats that support the leopard's main prey animals. Most field studies of medium-to-large primates have indicated a low incidence of predation. It is generally assumed that most populations of large verte- brates have become adapted or fairly resistant to the pathogens natural to their populations, and large-scale reductions in their populations through disease have been thought to be rare. The widespread episodic heavy mortality observed among South Amer-
Determinants of Population Density and Growth 185 ican howler monkeys, Alouatta sp. (Collias and Southwick, 1952), may represent an unstable relationship between Alouatta and the yellow fever virus that was introduced from Africa more than 200 yr ago. The case exemplifies how an introduced patho- gen can decimate populations that have not fully adapted to its virulence. The proportion of mortality in natural populations that is attributable to pathogens can be assessed only through close studies directly addressing this problem. Morbidity and mortality statistics are unavailable for primate populations that may be af- fected by parasites and diseases such as yellow fever, malaria, tu- berculosis, Lassa fever, and Marburg virus. Since resistance to disease may be in part a function of other factors, such as nutri- tional state, wounding, or age, its effect on mortality is not easily isolated from that of other factors (Freeland, 1976). FOOD SUPPLY AS A MAJOR FACTOR DETERMINING POPULATION SIZE Consideration of food supply in relation to population size in- volves three aspects: (1) the dietary intake of a species, (2) the diversity and productivity of food plants relative to the food items consumed, and (3) the manner in which food supply influences demographic parameters. Methods for estimating the diet were described under "Feeding Ecology" in Chapter 6. Methods for estimating the diversity, productivity, and phenology of plants were described in Chapter 3. In addition to the productivity of food plants in the habitat, the amount of food that is available to a primate population depends on the primate's trophic adapta- tions and the abundance of competitors that feed on or otherwise destroy the same foods. TROPHIC ADAPTATIONS Trophic adaptations include all those morphological and behav- ioral traits that allow a species to collect, chew, and digest food. Trophic adaptations should not be confused with "trophic level," which defines a species' role in the flow of energy within an eco- logical community. Prehensile tails and modifications of denti- tion and the digestive tract are examples of trophic adaptations.
186 TECHNIQUES IN PRIMATE POPULATION ECOLOGY Prehensile tails, for example, allow South American cebids to hang from sturdy branches in order to reach plant food items at the ends of flimsy twigs that they would not be able to reach otherwise. The long hooklike arms and hands of gibbons and sia- mangs serve a similar purpose (Grand, 1972, 1978). Strong incisor teeth in savanna-dwelling baboons aid in the uprooting of tubers and roots, and modification of the molar teeth aid leaf-eating primates in chewing mature fibrous leaves (Kay, 1978). The most striking trophic adaptation may be the ruminantlike digestive system of leaf-eating primates. The fore- guts (in the Colobinae) or the caecum (in the Indridae and Alou- attinae) are highly specialized as fermentation chambers support- ing symbiotic microbes that break down the tough cellulose in mature leaves (Bauchop, 1978). Since leaves are much more abun- dant than flowers and fruits, leaf-eating primates have available to them a much greater store of food than do non-leaf-eating pri- mates. As a result, leaf-eating monkeys occur at much higher densities than non-leaf-eating primates sharing the same habitat (Eisenbergef a/., 1972; Struhsaker, 1975). Estimation of a species' trophic adaptations therefore includes documentation of anatomical adaptations or specializations rele- vant to the acquisition, processing, and digestion of food; behav- iors used in the acquisition and processing of various food items; and the diet. RELATIONSHIP BETWEEN THE DIVERSITY AND PRODUCTIVITY OF FOOD PLANTS AND POPULATION SIZE The diversity of primate species correlated positively with the diversity of tree species in the rain forests at Kibale, Uganda (Struhsaker, 1975), and New Indenau, Cameroun (Gartlan and Struhsaker, 1972). Conceivably, primate diversity is a function of the diversity of ecological niches. Thus, as floristic diversity decreases, the diversity of exploitable feeding niches decreases until at some point the carrying capacity of the habitat is reduced to zero for some species. To a large extent, climatic and edaphic (or local ecological) factors determine both the diversity and productivity of a forest type; in an undisturbed forest, diversity and productivity are likely
Determinants of Population Density and Growth 187 to be positively correlated. Thus, an attempt to distinguish the ef- fects of each factor on the density or biomass of a particular species may be difficult. An example taken from Sri Lanka shows that all tree species found in the forests at Wilpattu are also found in those at Polonnaruwa, but not vice versa, so that the Wilpattu forests have a lower diversity (Table 8-1). Forest pro- ductivity is also lower at Wilpattu than at Polonnaruwa. The biomass of primate species found at Wilpattu is less than in the more diverse and productive forests at Polonnaruwa, as is predicted by this correlation. Such a correlation does not hold, however, for comparisons of primate biomass between the forests at Polonnaruwa and Horton Plains. Although forest diversity and productivity are greater at Horton Plains than at Polonnaruwa, the biomass of all three primate species there is considerably less. In such cases, knowledge of the nutritional requirements of the TABLE 8-1 Differences in Biomass Among Species of Primates in Three Forest Habitats and Climatic Zones of Sri Lanka Climate Average annual rainfall 1,200mm 1,671 mm 2,000 mm No. months drought per annum 4-5 2-4 none Forest Type arid semi- montane scrub evergreen cloud Forest productivity in metric evergreen tons/ha/yr° 2 4.5 5 Tree species diversity* low moderate moderately Primate Biomass (kg/km2)*'' H'(ln) = 2.97' high Macaca sinica 1 300 <40 Presbytis entellus 19 730 0 Presbytis senex 0 1,430 630 Wilpattu Polonnaruwa Horton Plains "Hladik and Hladik, 1972. 'Dittus, 1977b. cSee Chapter 3 for derivation of Shannon Index. ^Eisenbergef al., 1972. 'Dittus, 1977c.
188 TECHNIQUES IN PRIMATE POPULATION ECOLOGY species in relation to the relative abundance of available foods in the different forest habitats may provide a clue for this apparent contradiction. For example, the macaque's preferred foods at Polonnaruwa are the fruits of seven species of fig trees (Ficus). In the montane forest at Horton Plains, figs are absent. Thus, despite the greater overall productivity of the montane forest, the productivity and diversity of the plants on which the macaques depend are less than at Polonnaruwa. This probably explains the lower biomass of macaques at Horton Plains. It is obvious from this example that a great deal of ecological information is re- quired to draw conclusions concerning ecological relationships. EFFECTS OF FOOD SUPPLY ON THE VITAL STATISTICS OF A POPULATION The relationship between food supply and the demographic parameters that determine K density are illustrated by the follow- ing examples: ⢠Natural populations of vervet monkeys, Cercopithecus aethiops, and of yellow baboons, Papio cynocephalus, decreased in size by over 40% and 90%, respectively, as a result of the destruction of their natural food plants through edaphic changes in the Masai-Amboseli Game Reserve in Kenya (Hausfater, 1975; Struhsaker, 1973, 1976). The natural population of toque ma- caques, Macaca sinica, decreased by 15% as a result of a drought; but during the same drought period, the population in- creased by 60% in an area where artificial feeding occurred (Dit- tus, 1977a). Declines in the populations of vervet monkeys and toque macaques were attributed to an increase in mortality among juveniles, especially the youngest juveniles (Dittus, 1977a; Struhsaker, 1976). In Nepal, rhesus macaque, M. mulatta, populations are food-limited in relatively undisturbed habitats. Although natality declines at high densities, mortality increases in the juvenile and adult age classes (Southwick et al., 1980). ⢠Populations of rhesus macaques, Macaca mulatta, and of Japanese macaques, M.fuscata, that have been provisioned with food by man have grown at annual rates of 16% (Koford, 1965) and 9% (Dittus, 1980, after Itani, 1975), respectively, and exist
Determinants of Population Density and Growth 189 at densities that are over 10-100 times higher than those in their natural habitats (Dittus, 1975). Compared with the wild non- provisioned population of M. sinica, where r = 0, in the growing populations of M. mulatta and M. fuscata, the mortality among juveniles was less and the natality was greater (Dittus, 1975). ⢠The Koshima colony of Japanese macaques was heavily pro- visioned with food for many years and increased in size. Then ar- tificial feeding was decreased, and the population declined. Com- parisons of vital statistics from the period of food surplus and population growth with statistics from the period of food scarcity and population decline indicated the following changes: infant mortality increased from 15 to 68%; the average natality decreased from 66 to 32%; and the average age at first birth in females in- creased from 6.2 to 6.8 yr, and in some females first birth was delayed until the ninth year of life (Mori, 1979). Together these data suggest that the food supply is of utmost importance in limiting the density of some if not all primate populations and that food supply has its effect on population growth rate by influencing mortality, natality, and age at onset of reproduction. These relationships have been examined in greater detail by Dittus (1977a, 1979, 1980), who presents evidence to suggest that social behavior, or competition for food and mates, in large part mediates mortality and natality in relation to the availability of limiting resources. In short, social behavior regu- lates the size and age-sex composition of many primate societies in relation to the food supply, in a fashion that maximizes the re- productive success of some of its members. POPULATION REGULATION BY BEHAVIORAL AND PHYSIOLOGICAL MECHANISMS This section deals with the manner in which environmental fac- tors can influence the vital statistics in a primate populationâits rates of mortality, fecundity, and maturation. A flow diagram (Figure 8-3) is presented to clarify important relationships be- tween environmental factors and behavioral and physiological factors that ultimately influence demography. The various rela- tionships are discussed in turn.
190 TECHNIQUES IN PRIMATE POPULATION ECOLOGY IL - K PREDATOR AVOlDANCE MANEUVERS, AND lNTRASPEClF1C COMPETlTlON FOR REFUGES FROM PREDATORS PHYSlOLOGY - RATE OF GROWTH I REPRODUCTlVE MATURATlON - ENDOCRlNE BALANCE - NUTRlTlONAL STATE - RESlSTANCE TO DlSEASE FIGURE 8-3 Flow diagram of hierarchical interrelationships among environ- mental, behavioral, and physiological factors that determine population growth rate and equilibrium density. IDENTIFYING AND MEASURING INTRASPECIFIC COMPETITION FOR RESOURCES Competition occurs when a number of individuals (or groups) utilize common resources that are in short supply or, regardless of whether the resources are in short supply, when animals (or groups) harm one another in utilizing the same resources (modi- fied after Krebs, 1972). Competition can be measured directly through observation and recording of behaviors. Prerequisites to such recording are good observation conditions and well-habituated animals that are not disturbed by the proximity of an observer.
Determinants of Population Density and Growth 191 The first step in measuring competitive behaviors is their iden- tification. The investigator should familiarize himself with gestures of communication used by the primate under study. In most primates, unequivocal competitive behaviors can be recognized in situations when (1) one individual removes food from the hands, mouth, or cheek pouches of another and con- sumes it while the exploited individual attempts to resist such robbing or (2) one individual displaces another engaged in feed- ing and consumes the abandoned food. Such displacements may involve the use of physical force, such as biting, hitting, or push- ing; more frequently it involves only a threat gesture or simply an approach. More subtle competitive behaviors involve the gradual en- croachment and displacement of another individual from the vi- cinity of a desired resource. Displacements need not involve only food items or water; they may involve, for example, priority of ac- cess to a safe perch when scrambling to avoid a predator or an ag- gressive conspecific or when selecting secure sleeping perches. Some competitive acts may involve more than two individuals, as in coalitions of two or more individuals against a target ani- mal. Similarly, whole groups may defend their feeding territories against other conspecific groups, or a group may simply defend or avoid a particular feeding site in areas of home range overlap. The type of hypothesis formulated concerning competitive behaviors will define the method used for its testing. As a general guide, the focal-animal sampling method, in which each in- dividual in the social group is identified and followed for a fixed duration, is suggested as one that can be modified to suit many needs. The observation period will be determined by the total time it takes to collect a sample of behavioral frequencies that is sufficiently large to test the hypothesis statistically. A minimum of 10 h of direct observation per individual is suggested. For species with low interaction rates, such as langurs, a longer dura- tion may be required. For each minute of observation the subject animal's activity (e.g., feeding, resting, grooming) and behavioral interactions with others are recorded. One might also record food type consumed and distance to other animals (nearest neighbors). Since data are specific to identified individuals, frequencies or durations of
192 TECHNIQUES IN PRIMATE POPULATION ECOLOGY behaviors, foods consumed or "competed for," and the like can be analyzed according to individual attributes such as age, sex, reproductive state, and genealogy. For further details concerning the collection and analysis of such data, see Dittus (1977a). Socially dominant animals are those that have priority of access to food and other contested resources. Socially subordinate animals are ones that do not have such priority of access. In a detailed study of the effects of competitive behavior in the toque macaque, Macaca sinica, Dittus (1977a) showed that relative to socially subordinate animals, dominant ones have the following advantages: ⢠Dominant animals expend less time or energy in searching for food items because they frequently usurp food from subor- dinates who have expended time and energy in locating it. ⢠They feed at sites where food is most abundant and therefore feed at faster rates. ⢠They consume a greater proportion of foods that are high in caloric or nutritional content. ⢠They have a faster rate of growth or weight. In addition, dominant mothers have a higher fecundity than subordinate ones, and their offspring survive better than those of subordinates (Dittus, 1979; Drickamer, 1974). Dominance differs according to an individual's age, sex, and genealogy. Dittus (1977a) showed that mortality patterns by age and sex for toque macaques closely follow the differences by age and sex in successful food competition. Competition for resources was thought to be a major cause of mortality. The general pattern of mortality in most mammals is one of high mortality early in youth and decreasing mortality toward adulthood. Mortality curves differ between the sexes in several species (Rails et al., 1980). Individuals that survive to reproduc- tive age generally have a long life (Caughley, 1966). Most primates appear to adhere to this pattern, and it is likely that food competition is a major factor in adjusting primate population density to the food supply (Dittus, 1980). When the food supply changes, food competition affects survivorship among infants, young juveniles, and old individuals the most
Determinants of Population Density and Growth 193 (Dittus, 1977a; Struhsaker, 1976). Such competition is exhibited within social groups but may also occur between them, as in in- tergroup dominance hierarchies or in territorial behavior. MATE COMPETITION The different reproductive roles of males and females subject them to different life histories. Although both males and females compete for food resources, males may also compete for mates. Mate competition occurs when males fight or otherwise vie over mating access to estrous females. The frequency of such behaviors can be documented through focal-animal sampling techniques similar to those outlined above. Primate studies that have investigated mate competition (Dittus, 1977a; Lindburg, 1971; Vandenbergh and Vessey, 1968; Wilson and Boelkins, 1970) indicate that males are frequently wounded and die as a result of wounds incurred in fights with other males. The life history of young males may involve their emigration from the natal troop at adolescence. Such emigrant adolescent males attempt to attach themselves to other social groups. In these attempts they are frequently forced to assume a subordinate position peripheral to the troop. As a result of food competition and of fighting with other, often stronger, adult males over female mates, they are frequently wounded and die. Male mor- tality reaches a peak during the adolescent phase and decreases with the attainment of adulthood. In adulthood, males continue to transfer between social groups, albeit at a lower rate than dur- ing adolescence (Boelkins and Wilson, 1972; Dittus, 1975; Kawai and Yoshiba, 1968). Because of such emigrations and the intense mate competition in their adult lives, adult males suffer higher mortality than adult females. The latter generally do not fight for mates, nor do they emigrate from their natal troop (for excep- tions, see Chapter 5). Male-male competitive behavior in some speciesâfor example, many colobinesâmay involve the killing of infants fathered by other males (Hrdy, 1974; Rudran, 1973b; Struhsaker, 1977; Sugiyama, 1967). Such infanticide has two benefits for males. First, females whose nursing infants die come into estrous sooner than if their infants had lived and continued to nurse. Therefore,
194 TECHNIQUES IN PRIMATE POPULATION ECOLOGY such a female is "freed" to conceive the infant of the infanticidal male sooner than if her first infant had continued to live. That is, the male increases the number of infants he can sire, or he enhances his fitness (Hrdy, 1974; Struhsaker, 1977). Second, males generally practice infanticide only at the time of first taking over a troop and displacing the resident male from it. If food resources are limiting, the new male leader who kills the infants sired by the deposed male eliminates food competitors for himself and especially for his own young. Because his own offspring would be younger, and therefore subordinate to the infants of the deposed male leader, they would stand to lose the most in food competition with the older, dominant infants. The infanticidal male therefore enhances the survivorship of his own infants by eliminating the most likely food competitors for his own offspring (Dittus, 1979; Rudran, 1979). Regardless of the source of mortality, be it resource competi- tion, mate competition, or the outright killing of individuals as in infanticide, such behaviors have a direct effect on the vital statistics of the population and on its growth rate and density. To test whether such behaviors are truly regulatory would involve documenting behaviors and their different effects on demography under different environmental conditions or under different phases of population growth (Dittus, 1977a). POPULATION REGULATION IN RELATION TO LIFE HISTORY The regulatory factors or behaviors one might expect a primate species to exhibit are predisposed by its life history. Although food competition is likely to affect all age and sex classes in most primate species, mate competition, as outlined above, appears to be most prevalent among sexually dimorphic species where males are larger than females. With the exception of the study of the toque macaque that directly addressed the question of population regulation (Dittus, 1977a), documentation of such regulation is fragmentary. The evidence for population regulation in other primates has been reviewed (Dittus, 1980). Among monomorphic species where male-male competition for mates is less prevalent, and where both males and females may emigrate from their natal troops, one might expect male mortal-
Determinants of Population Density and Growth 195 ity through mate competition to be minimal, and females might be subject to mortality resulting from troop transfer behaviors. Studies addressing these problems would be highly desirable, for only then can the phenomena underlying population regulation in primates be better understood. PREDATION IN RELATION TO POPULATION REGULATION Primates living in open savannal habitats are subject to predation from large mammalian predators. Both the body and canine teeth of adult males among savanna-living primates (e.g., ba- boons, Papio sp., Theropithecus, and patas monkeys, Erythro- cebus patas) are believed to have evolved to their characteristic large size at least partly owing to their advantage in the defense against predators. If the incidence of predation on a primate population is very high, its density might be kept lower than it would be in the absence of predation. Except for some primate populations that are hunted or trapped by man, such a population among the medium-to-large primates has yet to be discovered in undisturbed situations. If refuges from predators, such as tall trees in open savannah, are scarce, they might constitute a limiting resource. Access to such refuges is likely to be determined by differences in social dominance relations so that the effect of predation on vital sta- tistics would be determined at least in part by social behavior. THE INFLUENCE OF BEHAVIOR ON PHYSIOLOGY THAT MEDIATES SURVIVORSHIP AND REPRODUCTIVE PERFORMANCE Except for the outright killing of individuals, behavior exerts its influence on survivorship and fecundity through physiological changes. Physiological mechanisms are obviously involved in mediating behaviorally determined access to food into nutritional state and rates of growth and reproductive maturation. Social behavior also determines the hormonal balance of individuals. Laboratory and field experiments with other animals have in- dicated that behaviorally subordinate and harrassed individuals may die from stress. The typically lethal stress syndrome involves
196 TECHNIQUES IN PRIMATE POPULATION ECOLOGY marked changes in the endocrine systems. Such mortality may occur quite independently of food deprivation. Starvation is simply an intense form of physiological stress. Generally, animals that are in poor physical condition because of nutritional and en- docrine stress also have lower resistance to disease organisms and parasites. Thus, death or lowered reproductive performance may be mediated by a variety of endocrine changes that are brought about by behavior (see reviews by Christian, 1963, 1970).
