The Socioecology of the Ringtailed Lemur: Thirty-Five Years of Research

120 Evolutionary Anthropology

ARTICLES

MICHELLE L. SAUTHER, ROBERT W. SUSSMAN, AND LISA GOULD

Linnaeus’1 original scientific description of Lemur catta, the ringtailed lemur, was ters take place between less closely based on a living animal brought to England in 1749.1 Although there were many related individuals.18,20,21 However, un- brief descriptions of wild ringtailed lemurs,2–5 it was not until Jolly6 wrote her now like cercopithecine monkeys, ringtail classic book, Lemur Behavior, that we had our first detailed description of the natural lemurs rarely form third-party alli- history of these beautiful animals (Fig. 1). Since then, long-term field studies, mainly ances during agonistic encounters.20,21 from two study sites in Madagascar, Berenty and Beza Mahafaly (Fig. 2), as well as Furthermore, reconciliation after con- studies on forest-living groups in captivity at the Duke University Primate Center in flict, which is common among anthro- Durham, North Carolina, have greatly expanded our knowledge of the ecology and poid primates, has not been noted in behavior of this species (Table 1, Box 1). Thirty-five years of research on this species this species, indicating that this is not at these various sites indicates that Lemur catta is proving to be every bit as complex a necessary prerequisite for perma- in its behavior as are many anthropoid primates. This very complexity has been nent social group life in primates.22 reflected in the current controversies and questions concerning the ecology and In free-ranging populations, if a behavior of this species. group becomes too large fission may occur, with one matriline evicting another.8,14,17,18,23 Dividing along mat- SOCIAL ORGANIZATION Groups are centered around a core of rilineal lines is also common among adult females and their offspring.6 As female-bonded cercopithecine mon- Like many cercopithecine monkeys, keys.24–26 One important mechanism Lemur catta lives in multi-male female in Old World monkeys, ringtailed le- for facilitating such fission among ring- resident groups that usually contain mur groups characteristically contain tailed lemurs is episodic targeting ag- 10 to 20 animals.6–8,10 Sex ratios are more than one matriline, with some gression.27 When groups reach a criti- approximately 1:17,8,10,11 and sexual di- matrilines being dominant over oth- cal size, females repeatedly attack and morphism is slight.12 Females usually ers.17–19 More friendly social interac- chase individuals of another matri- remain in their natal group, (but see tions occur between close relatives line, sometimes resulting in the evic- below) whereas males migrate.13–16 and more serious aggressive encoun- tion of the latter.27,28 Although there are no documented cases of individual female transfer, there have been rare Michelle Sauther is assistant professor at the University of Colorado, Boulder. She received her cases of mother and adult daughter Ph.D. from Washington University in 1992. Her research focuses on the socioecology of pairs joining other groups.8,15 At Beza nonhuman primates, with special emphasis on how individual life-history factors contribute to variation in feeding and reproductive strategies. She has studied the ringtailed lemurs of Beza Mahafaly, such a pair entered an ex- Mahafaly since 1987. Her most recent work on this population involves a joint effort to help tant group that contained only four develop a genetic profile to address issues of paternity and conservation for ringtailed lemurs. adult females and became the two She has also done research in Guyana, Panama, Kenya, and Costa Rica. Sauther recently chaired a symposium on the feeding behavior of the Malagasy prosimians at the meetings of top-ranking females. This is not al- the American Society of Physical Anthropologists in 1996. [email protected]. ways the case, however. In another Robert W. Sussman is professor in the department of Anthropology at Washington University, case, the attempt of a mother-daugh- St. Louis. He also is Editor-in-Chief of the American Anthropologist. He received his Ph.D. from ter pair to join a group was repulsed. Duke University and has been conducting research on the lemurs of Madagascar since 1969. He also has done research on primates and conservation in Costa Rica, Panama, Guyana, and They eventually joined a different, Mauritius. Besides primate behavior, ecology and conservation, he is interested in the evolution smaller group that contained only two of primate and human behavior. [email protected] resident females.15 Lisa Gould is assistant professor at the University of Victoria, Victoria B.C. Her research interest In all groups studied at Beza Maha- focuses on ringtailed lemur socioecology, including field studies of infant development, the faly, the top-ranking male has been of structure of male social relationships, and sex differences in vigilance behavior. One goal of 8 these projects is to examine the effect of female dominance on the social system of this prime adult age. Peripheral males are species. Most recently, she has been examining the effect of a severe drought on the not a cohesive subgroup, but include population of ringtailed lemurs at the Beza-Mahafaly Reserve in southwestern Madagascar. lower-ranking males and males at- [email protected] tempting to immigrate into the group. Male migration is regular, with young Key words: Lemur catta; ringtailed lemur; socioecology; reproduction males first migrating from their natal ARTICLES Evolutionary Anthropology 121

Figure 2. Formal field studies of Lemur catta Figure 1. Ringtailed lemurs live in large social groups in the dry and very seasonal forests of began in the 1960s at various sites in Mada- southern Madgascar. gascar. Information from long-term studies at Berenty and Beza Mahafaly are expanding our knowledge of the socioecology of this species. group when they are between 3 and 5 tionships are not invariably linear and years of age.14 On average, mature can change quite abruptly.20,29,33 ranks are actively maintained by females migrate every three-and-a-half There is also a developmental com- male agonistic intervention and daugh- years, with approximately 30% migrat- ponent in the establishment of domi- ters acquire ranks just below those of ing each year.14 Males form partner- nance relationships: Adolescent and their mothers through affiliative inter- ships while transferring, although young adult females may rank above actions and alliances among female these partnerships do not necessarily some adult females.20,32 Perhaps be- relatives.34 It thus appears that al- continue once group membership is cause alliances are rare and mothers though female ringtailed lemurs have attained.13,14,29,30 At Berenty, the major- dominance relationships, they do not ity of male migrations occur at the end maintain dominance hierarchies in the of the dry season and overlap, in part, manner of multi-male groups of cerco- with the birth season.13 In all cases of It thus appears that pithecine primates.32 male transfer, the males initially hold although female Unlike the males of many group- low-ranking and peripheral positions living anthropoid primates, male ring- upon entering a new group and are ringtailed lemurs have tailed lemurs appear to lack a consis- challenged by other group members of dominance tent linear hierarchy and rank reversals both sexes for many months.8,19,29,30 occur.16,18,22,29 This may relate to a lack A single top-ranking female appears relationships, they do not of the stable alliances and coalitions to be the focal point for the rest of the maintain dominance between migrating males that are group. She often initiates the direction found in some macaque and baboon of group progressions, although other hierarchies in the species, but have yet to be observed in individuals, including low-ranking manner of multi-male ringtailed lemurs.32 In most studies, a adult males, may lead the actual single, dominant male could be clearly 6,19 groups of cercopithecine travel. This female is also respon- identified and, at Beza Mahafaly, three sible for the greatest number of aggres- primates. males were able to maintain their domi- sive encounters overall, with the major- nance for six years, a pattern more simi- ity of these involving access to food.31 lar to that of male rhesus macaques than Females show strong, differentiated that of male baboons.8,35 Male ringtailed relationships within matrilines, as seldom support their daughters agonis- lemurs also develop preferred partner- measured by grooming and proxim- tically, female offspring do not invari- ships with one another, although these ity.18–20 Mothers are always dominant ably inherit their mother’s rank.20,32 usually do not persist through an entire over daughters.19,32,33 While female This is different from the relatively year.29,30 (However, see Nakamichi and dominance relationships in ringtailed stable linear dominance hierarchies Koyama.20) lemurs can be linear, transitive, and found among group-living baboons Intergroup encounters are common stable over long periods,19 these rela- and macaques. Among these species, at both field research sites.6,13,19,36–39 122 Evolutionary Anthropology ARTICLES

TABLE 1. Main Study Sites of the individuals feeding at the same time 30% of their time feeding on the Ringtailed Lemur, Lemur catta when there is ample food. If a resource ground.10,19 Reproductive state affects (Studies of at Least One Year) is limited—for example, if there is feeding behavior. At Beza Mahafaly, Sites and Dates Main Researchers only a single drinking site—individu- lactating females focus more on low- als may queue up for access to that cost, predictable, high-protein plant Berenty, 1963–pre- A. Jolly, N. Budnitz, resource. Infants often smell or taste resources such as young leaves, sent K. (Dainis) Jones, food in their mothers’ mouths, and whereas during pregnancy they switch A.S. Mertl-Mill- 43 hollen, S. individual adults commonly smell each to flowers and seek out rare fruits. O’Conner, N. others’ mouths, perhaps to monitor Koyama, M. available food sources.19 In response Nakamichi to the seasonal nature of foods, L. REPRODUCTIVE ECOLOGY Beza Mahafaly, R.W. Sussman, M.L. catta are able to switch their dietary Ringtailed lemurs exhibit the basic 1987–present Sauther, L. Gould focus quickly as new foods become prosimian reproductive physiology. Antserananomby, R.W. Sussman available and often make long excur- They have a highly constrained breed- 1969–71 sions out of their normal home range ing period that lasts approximately 6 Duke University Pri- L. Taylor, M. Pereira, to monitor seasonal food sources.8,43,45 mate Center, P. Kappeler, J. to 24 hours per year.6,47,48 Among free- In addition, they can exploit water 1986–present Macedonia, J. ranging and captive L. catta, all fe- Ganzhorn males within a group experience estrus within 1 to 3 weeks of each other; Long-term studies at all females living within the same for- These primarily involve females, and Beza Mahafaly have est enter estrus during similar peri- 47,49 can escalate into serious physical con- revealed that ods. However, unlike nocturnal frontations resulting in injury.19,28,38 prosimians, they do not show periodic 50 Many of these encounters involve ac- reproduction in L. catta is closure of the vagina. Long-term cen- cess to food19 or appear to be designed tuned to the seasonal sus data at Beza Mahafaly indicate to keep others away from core areas of that 80% to 85% of females give birth 8 the home range.19,38–40 The peaks in nature of specific food annually. frequency of such encounters happen resources. Because Infants are weaned when they are when females are especially motivated about four to five months of age. In- to defend resources to provide food females all mate during fant mortality during the first year is for infants during weaning or for them- between 30 and 51%, depending on the same short period, 8,10,13-14,51 selves in preparation for the dry sea- the year and locality, although son, as well as during the costly peri- they move as a group during drought years infant mortality 15 ods of birth and early lactation.13,19,41 through different can be as high as 80%. As in many mammals, the survival of infant ring- reproductive states tailed lemurs at Beza Mahafaly is re- FEEDING ECOLOGY during which they lated to the age of the mothers, with Ringtailed lemurs can best be char- the infants of young-prime and prime- acterized as opportunistic omnivores depend on aged females having higher survival with a wide dietary regime that in- phenologically distinct rates than those of older females.8 cludes fruits, leaves, leaf stems, flow- Female ringtailed lemurs also show a ers, flower stems, spiders, spider webs, plant species. well-developed maternal affectional caterpillars, cicadas, insect cocoons, system paralleling that seen among birds, and even dirt.19 At Beza Maha- anthropoid primates.6,8,30,31,47,49,51–53 faly, daily consumption of soil from For example, female ringtailed lemurs sources such as tree hollows that are termite mounds has been observed will go to great lengths to care for sick unavailable to most other mammals. (Fig. 3).19 This has also been seen at or injured infants, even attempting to Drinking from tree hollows is a diffi- the Duke University Primate Center.42 carry infants in their arms while walk- Generally, L. catta spend 30% to 60% cult procedure because these hollows ing bipedally.51 In addition, male ring- of their time feeding on fruit, 30% to tend to be on the vertical face of a tree, tailed lemurs show an interest in in- 51% on leaves and herbs, 5% to 12% and often only one branch is available fants, behave in an affiliative manner on flowers, and less than 3% on in- to sit on (Fig. 4). A ringtailed lemur toward them, and occasionally engage sects.6,19,37,43 They display limited dex- inserts a hand into the hole and reaches in alloparental care.29 terity in the handling of food items as down, immersing the hand in the col- As in other placental mammals,54,55 compared to anthropoid primates,19 lected water, then withdraws the hand lactation is the most costly reproduc- although they do exhibit handedness.44 and licks the water from it. In captiv- tive period for prosiman primates.56,57 Food items are not manually manipu- ity, some ringtailed lemurs have even Ringtailed lemurs, along with other lated, but rather are simply grasped been observed immersing their tails in Eulemur sp., appear to produce dilute and held. water and then drinking water from milk more like that of anthropoid pri- Ringtailed lemurs are highly syn- the wet tail.46 Depending on the study mates and unlike those of lorises and chronous in their activities, with all site, ringtailed lemurs spend 18% to bushbabies, which contain high con- ARTICLES Evolutionary Anthropology 123

Box 1. Ringtailed Lemur Study Sites

The Berenty Nature Reserve (A)isa Reserve in 1986. This reserve is the ter (C) was originally conceived by J. private, independent forest reserve set ﬁeld site for a cooperative interuniversity Buettner-Janusch while he was at the aside by the de Heaulme family in the project developed to promote conserva- Department of Anthropology at Yale 1940s, located in the extreme south of tion, education, research, and develop- University. In 1966, Dr. Buettner-Ja- Madagascar. It consists of 100 ha of ment in southern Madagascar. It con- nusch moved his prosimian colony of riverine gallery forest, as well as 140 ha sists of two parcels, one of 500 ha 80 bushbadies, plus a small number of of open-canopy scrub and dry spiny de- containing desert-like didierea forest and captive lemurs obtained from Parc sert forest. Bordered on the north by the the other of approximately 80 ha of river- Tsimbazaza in Madagascar, to Mandrare´ river, it is almost completely ine gallery forest bordered on the east by Durham. In 1971, the current facility surrounded by sisal plantations. Cur- the Sakamena River. Reserve bound- was opened in the Duke Forest. At rently, the forest contains approximately aries are within a much larger tract of that time the colony consisted of ap- 400 ringtailed lemurs, which have been continuous forest. Studies of ringtailed proximately 180 prosimians, including studied and counted at intervals since lemur socioecology have been carried 14 ringtailed lemurs. In October 1981, 19637. out since 1987. At least nine troops of a group of 15 ringtailed lemurs was The Beza Mahafaly Special Re- ringtailed lemurs live within the riverine moved into a 1.2-square-acre outdoor serve (B) located in southwestern gallery forest; their total population was natural enclosure. Today the Primate Madagascar, was established in 1978 124 individuals in 1987-1988.8 Center’s total enclosures include more and decreed a Special Government The Duke University Primate Cen- than 30 contiguous hectares of forest.9

B. The forest at Beza Mahafalay Special Reserve in southwestern Madagascar.

A. The Berenty Nature Reserve in southern Madagascar. C. Forests of the southeastern United States at the Duke University Primate Center. 124 Evolutionary Anthropology ARTICLES

Figure 4. Lemur catta are able to exploit sources of water not readily available to other animals. Here a female inserts her hand into a tree hollow filled with water, then pulls it out and licks the water from her wet hand. Figure 3. Ringtailed lemurs are opportunistic omnivores, their diet even in- the beginning of the wet season, with cludes daily consumption its concomitant increase in resource of the soil from termite nests. availability, while eight months later there is a dramatic drop in food resources. Thus, infant ringtailed le- centrations of fat, protein, and en- weaning period corresponds with mur’s pattern of growth allows maxi- ergy.57 This may reflect differences in greater availability of young leaves. mum velocity when mothers, and later patterns of maternal care. Nocturnal Pregnancy in ringtailed lemurs coin- their weaning infants, have access to lorises and bushbabies leave their in- cides with relatively low food availabil- more resources but, even in captivity, fants unattended for long periods while ity. During this period, L. catta at Beza slows when, under natural conditions they forage, which means that infants Mahafaly must focus on a few key- in Madagascar, resource availability must be sustained during long inter- stone fruit species. The birth season drops precipitously. vals between nursing.57 Ringtailed le- corresponds to a short burst of flow- During estrus, females characteristi- murs, like most other diurnal lemurs ers. Given the seasonality of their envi- cally mate with more than one male, (with the exception of Varecia sp.) and ronment, female ringtailed lemurs are including group males, transferring anthropoid primates carry their in- thus on a tight schedule in that they males, and males from adjacent fants with them, and suckle them on must not only nurse their infants but groups.6,14,29,47 Despite the basic mam- demand. also wean them during the wet season malian pattern of seasonal estrus, fe- Long-term studies at Beza Mahafaly (Fig. 6). An extensive and unique longi- male mate choice does occur. During have revealed that reproduction in L. tudinal study of growth and body behavioral estrus, females reject re- catta is tuned to the seasonal nature of weights among ringtailed lemurs liv- peated mating attempts by sons and specific food resources (Fig. 5).58 Be- ing within forest enclosures at the closely related males,17,47 an observa- cause females all mate during the same Duke University Primate Center indi- tion that is supported by genetic evi- short period, they move as a group cates that several ringtailed lemur life- dence.61 Similar behavior has been through different reproductive states history traits reflect this stress of re- noted for many free-ranging anthro- during which they depend on pheno- source seasonality.60 For example, poid species.62,63 Female mate choice logically distinct plant species.58 For infants grew quickly during the first also affects mating order, insuring that ringtailed lemurs at Beza Mahafaly, seven months of life, and then showed most females mate with more than early lactation coincides with an ini- dramatic reduction in growth rates in one male, and that some of these tial peak in fruit availability, although the eighth month despite being provi- mates are either from another group this timing is more variable at Ber- sioned. Remarkably, this fits extremely or are transferring males.14,47,64 Part- enty.59 Late lactation and weaning oc- well with the phenological and repro- ner preferences have also been ob- cur during a second peak in fruit avail- ductive data from Beza Mahafaly. served among captive L. catta fe- ability, and the entire lactation and Here, the birth peak occurs in October, males.18,48 ARTICLES Evolutionary Anthropology 125

Figure 5. The relationships of rainfall and resource availability to reproductive state in ringtailed lemurs at Beza Mahafaly, Madagascar, 1987–1988.58 Given the seasonality of resource availability in ringtailed lemur habitats in southern Madagascar, mothers are on a tight schedule in that they must nurse and wean their infants when resources are abundant.

Figure 6. Due to the highly seasonal nature of resources, female dominance in this species In extensive studies of collared ring- Second, paternity data from captive may function to reduce feeding competition tailed lemurs at Beza Mahafaly, we groups suggest a ﬁrst-mate advantage during stressful reproductive periods such as found that high-ranking males often in this species,61 although this has yet lactation and weaning. exhibited sexual consortships that to be tested in the wild. were reminiscent of those among There is increasing evidence that group-living cercopithecine primates.34 sperm competition is a viable repro- ing this time a male can mount as 47 Such consortships were maintained ductive strategy for male ringtailed many as 25 times before ejaculation. solely by the male, who basically shad- lemurs.47,65 Male L. catta have the larg- Postejaculatory guarding is commonly 47–48 owed the female’s movements.47 Dur- observed. At Beza Mahafaly, the ing the mating season, the month of top-ranked males guarded the longest, May, these males approached, sat near, and group males guarded longer than 47 and even rested or slept in contact Male L. catta have the nongroup males. Postejaculatory guarding may increase the male’s with females during the midday rests.47 largest relative testes of chances for paternity. Because copula- High-ranking males also curtailed tory plugs are common to this species, close contact between females nearing all strepsirhines. Also, as and form within minutes in the vagi- estrus and other males by ‘‘stink fights’’ noted earlier, in most nal canal,52 the longer after ejacula- and aggressive displacements6,47 and tion a male can guard a female, the were therefore nearest when receptiv- cases receptive females greater the possibility that a plug may ity occurred. This behavior was exhib- are approached by and form and block or at least impede ited only toward females who had not mate with more than subsequent sperm. The possibility that yet mated, and began one or two days further copulations might interfere 47 before the female became receptive. one male. with plug formation may also explain Although factors such as female why males at Beza Mahafaly ceased to choice, length of male tenure, and mount females after a single ejacula- inbreeding avoidance create some vari- tion, even though they continued to ability, there is a tendency for top- est relative testes of all strepsi- guard the female for up to 62 min- ranking males to be receptive females’ rhines.65,66 Also, as noted earlier, in utes.47 A comparative study of penile ﬁrst mating partners at both Beza most cases receptive females are ap- morphology and testicular volume in Mahafaly and Berenty.47,64 Mating or- proached by and mate with more than nonhuman primates has shown that der may affect male reproductive suc- one male. Males continuously harrass these reproductive organs are more cess in this species. First, there is most mating couples so that a male specialized in species with multimale evidence that mating with ejaculation will mount, then quickly dismount to mating systems.67 L. catta possess pe- may lead to a loss of receptivity.48,52 chase away approaching males. Dur- nile spines and a complex distal penis 126 Evolutionary Anthropology ARTICLES

Figure 8. The percentage of encounters between Lemur catta and the Madagascar harrier Figure 7. Ringtailed lemurs combine the basic hawk at Beza Mahafaly, Madagascar, 1987–1988. Encounters peak during the period when prosimian emphasis on olfaction with visual the raptors have increased food requirements (nesting and fledging periods). These are times signals more common to anthropoid pri- when infant ringtailed lemurs are especially vulnerable to predation.47 mates. Here a male marks a tree with both scent and a visual mark. In addition, they use the spur to scratch tion.75–77 Ringtailed lemurs have nu- the surface of trees which, in tandem merous contact calls as well as a male morphology, including an enlarged with the wrist glands, leaves both an loud call that can be heard one kilome- 6,68 glans penis. Because male L. catta olfactory and a visual mark (Fig. 7). ter away and somewhat resembles the mating involves repeated brief intro- Investigations of the role of scent- song of Indri.6 Of particular interest is missions with thrusting prior to ejacu- marking behavior indicates that these the documentation of alarm calls in lation,47,52,64 such morphology could this species. L. catta are semi-terres- facilitate displacement or break-up of trial and are therefore exposed to many previously formed copulatory plugs, of terrestrial as well as arboreal preda- but little is known about this in pri- L. catta, like many tors.6,37,78 Antipredator defense in this mates.66,67 anthropoid primates, species involves vigilance and mobbing behaviors as well as alarm calls, have differentiated 6,78 COMMUNICATION once potential predators are sighted. alarm calls in response Recent field and captive work indi- Ringtailed lemurs show a combina- cates that representational signaling is tion of olfactory, visual, and vocal to different potential present in ringtailed lemur alarm modes of communication. Although predators, with avian calls,79,80 but may be absent from the they exhibit the basic prosimian pat- alarm calls of some other lemur spe- tern in that they use olfactory commu- predators evoking a cies.79 L. catta, like many anthropoid nication to a greater degree than do separate repertoire of primates,81,82 have differentiated alarm most anthropoid primates, they also have adaptations to a diurnal and vocalizations and calls in response to different potential group-living existence. Both males and behaviors than do predators, with avian predators evok- females have genital scent glands. In ing a separate repertoire of vocaliza- addition, males have wrist glands asso- mammalian and tions and behaviors than do mamma- 33,36,78,79 ciated with a hard, sharp, horny spur reptilian predators. lian and reptilian predators. and a well-developed brachial gland Such alarm calls may function, in just above the clavicle.52,68 Ringtailed part, to protect infants. At Beza Maha- lemurs also have trichromatic color faly, predation on infant ringtailed le- vision, although it is not as sensitive as lemurs may use olfaction in spatial, murs by the Madagascar harrier hawk that in catarrhine primates.69,70 An sexual, and social contexts.71–74 has been observed.83 Furthermore, example of this combination of visual Relatively speaking, the vocaliza- bones of adult and juvenile ringtailed and olfactory communication can be tions of ringtailed lemurs are similar lemurs have been found below roost- seen in male marking behavior. Males to those of Old World monkeys in both ing sites of this raptor.84 Encounters use both wrist and brachial glands to structural diversity and repertoire size, with avian predators, including vocal- mark their tails, which they then wave although comprising more discrete izations and mobbing, peak during the at another male during ‘‘stink fights.’’6 calls without so much intergrada- birth season and when infants are ARTICLES Evolutionary Anthropology 127 being weaned. These peaks in encoun- social contexts.31 At the Duke Univer- are other factors that may increase ters coincide with previously observed sity Primate Center, adult males began reproductive costs, but which have yet periods of greater food requirements spontaneously (not as a response to to be documented for lemurs as well for the harrier hawk and the Madagas- female aggression) showing submis- as most other primates. These include, car buzzard, for example, during their sive signals to maturing females, and but are not limited to, larger body size nesting and fledging periods (Fig. 8).78 they did this before the mating sea- in diurnal forms, infant carrying, Both of these are times when L. catta son.89 Thus, along with a developmen- greater potential feeding competition infants are especially vulnerable to tal component, males appear predis- in large social groups, seasonal re- predation. posed to retreat or exhibit other source availability, and reproductive submissive behaviors either spontane- seasonality.58,62,90 Of these, the last two ously or in direct response to female factors appear to be especially impor- 19,31,89 FEMALE DOMINANCE aggression. tant to understanding female domi- Why and how female dominance While female dominance was once nance among ringtailed lemurs.31,58,90 evolved among some Malagasy lemurs thought to characterize all the Mala- As noted, at Beza Mahafaly strict have been long standing ques- gasy primates, recent field and captive breeding seasonality is tied to the avail- tions.21,90,91 The main hypothesis ar- studies have revealed that this is not ability of resources. Females lactate gues that female dominance is a neces- the case.85–87 The ringtailed lemur is, during the period of food abundance, sary behavior for successful female in fact, one of only a few group-living gestate during the period of relatively reproduction because lemurs have un- lemur species documented as exhibiting low food availability, and give birth usually high energetic costs associated true female dominance, including both during peaks of important food re- with reproduction.90,91 However, sev- feeding priority and social dominance in sources such as flowers.58 Given the eral recent studies have not supported nonfeeding contexts.12,18,19,85–87 Female close reproductive synchrony in this this view. An analysis of strepsirhine dominance in this species appears to species,6,37,47,49 reproducing females have both a developmental and a neu- will experience identical reproductive rophysiological component. From a events and undergo similar reproduc- developmental perspective, it is impor- . . . males appear tive stresses, leading to high levels of tant to note there are no apparent sex predisposed to retreat or interindividual resource competition. differences with regard to rough-and- This can be mediated somewhat by 53 tumble play among ringtailed lemurs. exhibit other submissive behaviors that reduce energy costs.43,58 In this respect, they differ from most behaviors either Under such conditions, extra feeding male-dominant group-living anthro- competition from group males would poids, among which young males show spontaneously or in be a distinct disadvantage not only to 88 higher levels of such play. Infant females, but also to their infants, un- ringtailed lemurs exhibit dominance- direct response to less adult females had feeding priority. related behaviors as early as four female aggression. At Beza Mahafaly, males provide con- months of age. In the one study of stant direct and indirect feeding com- infant behavior in the wild, female petition for females throughout the infants initiated nearly all fights with year. This feeding competition is espe- other infants.53 life-history variation comparing le- cially acute during the physiologically Adult males do not inherently avoid murs with lorises, which do not ex- stressful periods of late lactation and females and, in fact, subadult females hibit female dominance, found that who have not yet bred can be nonag- while lemurs do have greater prenatal weaning, during which female-male 31 gressively displaced by adult males in maternal investment rates than lor- feeding agonism peaks. There is no all contexts, albeit most often over sises do, this was not a consequence of indication that males are simply defer- food.31 At Beza Mahafaly, this was constraints on basal metabolic rates.92 ring to females in naturally occurring 85,94 observed to change during the fe- In this analysis, lemurs and lorises groups, at least with regard to feed- males’ first mating season, when these showed no significant differences in ing priority, as most feeding agonism same females began aggressively cuff- postnatal litter growth rates, one mea- between males and females involves a ing and biting males that attempted to sure of maternal investment during female aggressively displacing the mate with them outside their estrus reproduction. Moreover, a study that male. period. Males reacted to such rebuffs compared lemurs (Eulemur sp.) and True female dominance in this spe- by retreating without physical counter- lorises (Otolemur sp.) with regard to cies may function, at least in part, as a aggression and by submissive vocaliza- energy transfer during gestation and reproductive strategy to minimize tions. What is especially significant is lactation found that for these particu- male feeding competition within a that after this change in the relation- lar species, the lemurs actually had the highly seasonal environment. In this ship between young females and adult lower prenatal and postnatal maternal regard, ringtailed lemurs are similar males, males could no longer directly investment.93 These results indicate to polygamous but sexually dimorphic supplant these females, and the nor- that we cannot make a special case for anthropoids such as the vervet and mal dominant female behavioral pat- the Malagasy lemurs with regard to patas monkey among which smaller tern ensued: These females began ac- energetic costs of reproduction as mea- females cannot easily displace males tively displacing males in feeding and sured in these studies. However, there individually, but instead use female- 128 Evolutionary Anthropology ARTICLES female coalitions to affect male behav- ity is ‘‘the active defense of individual of Berenty troops in richer zones was ior.95–98 Female vervets commonly form or group home range boundaries by noted as long ago as 1975,16 and under- aggressive coalitions against males in actual or ritualized agonistic encoun- scores L. catta’s adaptability. both feeding and nonfeeding con- ters, thereby maintaining essentially Another area of contention contexts.98 Patas monkey females can at- exclusive use of the home range,’’105 cerns the role of infant-killing. Ring- tack males both in coalitions and then ringtailed lemurs are not territo- tailed lemurs suffer high annual infant- sometimes singly.96,97 Both of these rial.40,106 mortality rates, which can be species also live in highly seasonal At Berenty there is considerable exacerbated by drought.15,58 The kill- habitats and exhibit seasonal repro- overlap of home ranges, and at Beza ing of infants, albeit rare, has been duction. Put in this context, female Mahafaly there is, in some cases, al- observed. However, the pattern varies dominance in ringtailed lemurs ceases most total home range overlap, so that between Berenty and Beza Mahafaly. to be a peculiarly lemur trait that many troops may time-share sites for At Berenty two cases of killing, one by requires some special explanation. It feeding, sleeping, or resting.39 Further- an immigrant male and one by a resi- becomes, rather, a behavioral response more, home ranges can change season- dent female, have been observed, in of group-living female primates of a ally.8,38,58,40 Nevertheless, there are core addition to seven cases of infant- nondimorphic species to mitigate feed- areas that are more intensely used by wounding by unknown causes.28,107 ing competition within a consistently L. catta groups at both Berenty and One eyewitness account of infant seasonally-stressed environment. The wounding by an immigrant male also role of female dominance as ‘‘behav- has been seen at this site.107 At Beza ioral compensation’’99 to minimize re- . . . based on earlier Mahafaly, no case has been observed productive costs remains a viable and reports from Berenty, L. in which a male killed or wounded an important approach. The robustness infant, despite three year-long inten- of reproductive and environmental fac- catta has been referred sive studies and another concentrated tors, both singly and in tandem, in to as the only primate study during the birth and lactation explaining the variety of lemur life- season.8,19,29 In fact, not a single epi- history patterns,62 as well as social species with multimale sode of male aggression toward any systems, is a promising arena of re- groups that is territorial. infant has been observed at this research that has been addressed in only serve.19,30,108–110 There has, however, 100–102 a few other lemur species. However, because been one eyewitness account of a fe- groups at Berenty have male wounding another female’s infant. In this case, the infant belonged CURRENT CONTROVERSIES highly overlapping to a female who was attempting to join In addition to what we now know of ranges, ringtailed lemurs the group. The infant was attacked ringtailed lemur socioecology, there have since been and bitten on the head by a resident continues to be vigorous debate con- female. The infant survived, but lost cerning other aspects of their behav- deemed a ‘‘dubious one eye. ior. Two especially lively controversies case’’ for territoriality, It has been recently suggested that revolve around territoriality and in- infanticide may be an adaptive aspect fant-killing in this species. There has one ‘‘best considered [to of the mating system of male ring- been some controversy about how to be] intermediates like tailed lemurs.61 In groups of ringtailed define the spatial relationships of ring- lemurs living in forest enclosures at tailed lemurs. For example, based on the Nairobi baboons.’’ the Duke University Primate Center, earlier reports from Berenty, L. catta immigrant males have never been ob- has been referred to as the only pri- served killing infants. However, they mate species with multimale groups have been seen attacking or preparing Beza Mahafaly. As noted, intergroup that is territorial.103 However, because to attack infants on four separate occa- encounters are common and may func- groups at Berenty have highly overlap- sions, and females have been reported ping ranges, ringtailed lemurs have tion, in part, to keep other groups out to attack and chase males repeatedly if since been deemed a ‘‘dubious case’’ of these core areas. Data from both they attempt to immigrate during the for territoriality, one ‘‘best considered sites indicate that such intergroup en- lactation period. It has been argued [to be] intermediates like the Nairobi counters of ringtailed lemurs might that such female aggression is a re- 40 baboons.’’6,7,104 Currently, however, best be seen as spatial defense, with sponse to preventing infanticide by ringtailed lemurs at Berenty are viewed population density and resource rich- males, which, in turn, is suggested to as being territorial or quasi-territorial; ness playing key roles in explaining be an established male strategy that that is, they become territorial at par- some of the variability seen.19,40 At has developed in tandem with pat- ticular population densities.38,40 Part Berenty, troops using more marginal terns of female mate choice in this of this confusion is related to the lack scrub areas have home range sizes, species. If a female loses her infant of a reliable operational definition of range use, and intertroop behavior one year, it is suggested that her next territoriality, which often makes the that are similar to those of troops infant has a better chance at survival. meaning of this concept quite differ- living in more marginal habitats at If infants die, for whatever reason, it is ent in different contexts. If territorial- Beza Mahafaly. The differing behavior argued that their mothers will not ARTICLES Evolutionary Anthropology 129 choose to mate again with the same males, who then abandoned it. The males of different groups peak during males, but rather will choose the immi- male of that subgroup then bit and the birth season when access to re- grant males. This is called the ‘‘incom- killed the infant. In this case, the death sources is especially critical.13,19,42 In- petent father’’ hypothesis.61 resulted from separation during inter- fants can be wounded or killed during This hypothesis is problematic on group fighting.28 The second case in- aggressive encounters between fe- several levels. First, despite thousands volved a dominant female attacking a males of different groups.19 The con- of hours of observation on identified, subordinate female and her infant. troversy is thus not whether killing habituated individuals, the phenom- The infant died from its wounds.107 and wounding of infants occurs in this ena of increased agonism by females Attacks by higher ranking females species, but whether such acts are a toward males during the lactation pe- against lower ranking mothers have by-product of social aggression, inter- riod has not been observed in other also been observed at Beza Mahafaly group encounters, resource competi- studies of free-ranging or semi-free- and in semi-free-ranging contexts.18,27,42 tion, or a form of reproductive compe- ranging populations.18,30,53,106,108 Sec- What is not clear in these cases is tition for males or females or, perhaps, ond, as noted earlier, most females whether the infant or the mother is the both. On a wider scope, the high in- give birth annually, and between 30 to target. Nevertheless, increases in such fant mortality rate has yet to be ex- 51% of these infants perish each year.8 targeting aggression have been linked plained, although determining the in- If male infanticide is a viable male to birth seasons in semi-free-ranging terplay among stochastic events such strategy, presumably a high propor- groups and thus may be a form of as predation, parasites, illness, and tion of these deaths should be the reproductive competition.27 falls, socially induced fatalities, fe- result of male infanticide. Yet only one Reproductive competition also could male reproductive stress, and preco- case of male infanticide by L. catta has cial infant development would clearly been seen at Berenty, and, as previ- be critical. ously noted, neither male aggression toward infants nor infanticide has been Clearly, one can no observed at Beza Mahafaly. Males in longer make the case WHERE NEXT? three focal groups at Beza Mahafaly that female dominance Clearly, one can no longer make the have been observed engaged in allopa- case that female dominance is system- rental care of infants and, in some is systematic for the atic for the Lemuridae.87 Further- cases, the male alloparent did not mate Lemuridae. more, female dominance and even fe- with the mother of the infant.108 Third, male feeding priority have different current data indicate that losing an Furthermore, female implications depending on social orga- infant one year does not enhance the dominance and even nization (for example, group-living, chances of survival of the next year’s pair bonds, or solitary but social). infant.15 Finally, because females regu- female feeding priority Direct feeding competition, and hence larly mate with males both from within have different implications advantages of female feeding priority, and outside of the group, it is difficult depending on social will presumably be more intense in to conceive of either the female or the larger groups. Thus, it makes little male recognizing the father of any organization . . . sense to treat female dominance particular infant, a prerequisite for the among lemurs as either a ubiquitous incompetant father hypothesis.61 The or unitary trait. In addition, even if advantages of infanticide as a male there is some identifiable stressor com- reproductive strategy in L. catta thus occur through less direct ways. For mon to all lemurs, (such as more remain problematic. example, one study reported that six seasonal rainfall or extreme tempera- What is clear from the data is that of the seven deaths in four study ture), there is no inherent reason to socially28 and perhaps even ecologi- groups at Berenty were not associated expect all lemurs to respond in the cally mediated wounding and killing with either killing or wounding, but same manner. Studies of ringtailed of infants does occur among ringtailed these infants were the offspring of lemurs indicate that female domi- lemurs. During intergroup fights, in- middle- or low-ranking mothers.51 This nance may indeed be one way to mini- fants fall off, are abandoned, and even pattern also is seen at Beza Maha- mize the effects of resource seasonal- attacked by individuals of their own faly.47 Rank affects access to resources ity on successful reproduction, but and other groups.28,42,107 The two as well as levels of feeding competi- there are additional and even alterna- clearly documented observations of tion. At Beza Mahafaly, low-ranking tive strategies for other lemur species infant-killing are cases in point. The females face such competition from that are just beginning to be docu- male infanticide at Berenty was ob- both males and high-ranking females.31 mented.102,112 served during a time of great social It remains to be demonstrated that Based on earlier reports by Shaw,2 upheaval, a group fission.111 In this this directly and adversely affects the Elliot113 stated that ringtailed lemurs case, an infant of one subgroup was ability of low-ranking females to nurse ‘‘dwell among the rocks . . . and are not dropped during a confrontation with and care for their infants. Ecologically arboreal’’ (p. 60). Rand3 reported that the other subgroup. After the infant’s mediated infanticide and infant ‘‘the animals spend as much time on subgroup retreated, the infant was in- wounding may also occur. Intergroup the ground as in the trees. In the trees vestigated by the other subgroup’s fe- encounters and agonism between fe- . . . they are not as agile or as active as 130 Evolutionary Anthropology ARTICLES others of this group. On the ground life-history characteristics of lemurs believe that a detailed survey of the they are quite at home....’’(p. 96). at these three sites could give fresh distribution and abundance of L. catta Napier and Walker114 concluded that insight to the nature of this primate’s may reveal that this intriguing lemur L. catta is intermediate, both evolution- physiological and behavioral flexibil- and its habitat are in far greater dan- arily and behaviorally, between a verti- ity. ger than is generally believed. cal clinger and leaper and an arboreal Yet even with such flexibility, there quadruped. Others have said that the is increasing demographic evidence ringtailed lemur is mainly arboreal that this species is highly sensitive to ACKNOWLEDGMENTS 6 and restricted to forests. This may habitat quality and change. For ex- Our work in Madagascar would not seem to be an old and not very interest- ample, denser populations and smaller have been possible without the gener- ing question because it is now obvious home ranges are characteristic of ous aid of the Ministries of Higher from quantitative studies that the ring- groups inhabiting gallery forest as op- Education and Scientific Research, the 8,119 tailed lemur spends a great deal of posed to transitional dry forest. School of Agronomy of the University time both on the ground and in Due to the extreme seasonality of their of Antananarivo, and the Museúm 6,10,19 trees. However, these observa- habitat, ringtailed lemurs appear to be d’Art et d’Archeologie. We especially tions exemplify an important charac- highly dependent on specific keystone thank B. Rakotosamimanana, B. An- teristic of L. catta—their behavioral resources. Key species provide impor- driamihaja, B. and V. Randrianasolo, flexibility. This is an edge species and, tant food items during critical periods J. Andriamampianina, P. Rakoto- 58 like many other edge or weed species, of the reproductive cycle. During manga, J.-A. Rakotoarisoa, and A. Ra- it has an amazing ability to rebound drought years, mortality for mothers kotozafy. The hospitality and assis- from environmental perturbations.15 and infants increases dramatically, tance of the people of Analafaly and Furthermore, as an edge species, the the Beza Mahafaly reserve guards is ringtailed lemur is adapted to many also gratefully acknowledged. Re- habitats that do not provide continu- ...inthehighly seasonal search at Beza Mahfaly was funded in ous arboreal pathways. Thus it is found part by the World Wildlife Fund, Ful- in dense brush, on the edges of savan- habitats characteristic bright Senior Research Grants, the nah, in the low limestone forests of the for this species, the loss National Science Foundation, the Na- southwest, on the edges of the desert- tional Geographic Society, the L.S.B. like didierea forest,115 and even on of key resources can be Leakey Fund BRSG SO7 RR077055 rocks. Recently, a potential new sub- expected to have an awarded by the Biomedical Research species was located living in the rocks enormous impact on Support Grant Program, Division of and low bush on the Andringitra Mas- Research Resources, National Insti- sif above the tree line at an elevation of ringtailed lemur tutes of Health, and Washington Uni- more than 2,510 meters.116 The ring- demography and versity. We also thank John Fleagle for tailed lemur is the only extant lemur inviting us to submit this contribution that can take advantage of these transi- survival. and three not-so-anonymous review- tional and even marginal regions, ers for their valuable suggestions. partly because of its behavioral flexibility and in part because it does so much of its traveling on the ground. providing indirect evidence that this REFERENCES In this edge adaptation, the ring- species is highly dependent on the phenological reliability of food re- 1 Linnaeus C. 1758. Systema Naturae, 10th ed. tailed lemur is in many ways an eco- Stockholm: Laurentii Sylvii. 58 logical equivalent of vervet monkeys sources. Thus, in the highly seasonal 2 Shaw FA. 1879. A few notes upon four species and many macaque species. The behav- habitats characteristic for this species, of lemurs, specimens of which were brought alive the loss of key resources can be ex- to England in 1878. 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