Pair-Bonding, Female Aggression and theEvolution of Lemur SocietiesKeynote Address
Alison Jolly
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, N.J., USA
Key WordsLemur · Social structure · Pair-bonding · Female aggression · Social intelligence ·Female dominance
AbstractLemur societies have been described as convergent with those of anthropoids,
including Papio-like female-bonded multi-male groups. Recent research, however,shows at least 5 pair-bonded species among the Lemuridae and Indriidae. Three more,Eulemur mongoz, Eulemur fulvus and Varecia variegata, have societies combiningaspects of pairing with aspects of troop life. The best-known female-bonded societies,those of Lemur catta, Propithecus diadema edwardsi and Propithecus verreauxi, maybe assemblages of mother-daughter dyads, capable of high aggression towards otherfemales, but derived from more solitary female ancestors, perhaps also living as pairs.The internal structure of such lemur groups differs from the more extensive kin groupsof catarrhines. This in turn may relate to the lemurs’ level of social intelligence and tolemur female dominance over males.
Introduction
Early descriptions of lemur societies, especially my own [1, 2], pictured multi-male, multi-female lemur troops as strongly convergent with anthropoids of similartroop structure. Jones’ [3] and Sussman’s [4] later observations of male migration andfemale troop persistence in Lemur catta reinforced the view that at least L. catta haswhat Wrangham [5] defined as a typical female-bonded troop structure. Clearlyanthropoids differ enormously among themselves in the degree of female nepotismand in style of interaction [6, 7]. The original unspoken comparison was with savannababoons, as they were understood before Rowell [8] insisted on the differences be-tween baboon populations.
This equation of L. catta and an idealized papionine troop structure has two widerimplications. First, the argument that intelligence evolved in a social context derived
from the view that lemurs in a social group would need to keep track of, and relate to,kin and competitors in the group with the same complexity that monkeys do. Dunbar’s[9] correlation of neocortex size with group size in primates makes the same basicpoint: the more individuals, the greater the network of relationships to juggle andremember. The second implication is that lemur female dominance over males is a realproblem for evolutionary theory. If lemur multi-male, multi-female troops are just likethose of monkeys, how can the gender relations be reversed?
The body of this paper reviews the current knowledge of lemur social structure.Among diurnal lemurs, there is a surprisingly high incidence of pair-bonding. Female-female aggression in ‘female-bonded’ lemur groups may be intense, suggestingderivation from ancestors with a more limited social structure, where females expelothers as do pair-bonded animals. The possibility that pair-bonding illuminates thepresent diverse social structures, and may affect both intelligence and dominance,returns in the discussion.
Lemur Social Structures
CheirogaleidaeAlmost all cheirogaleids known to date forage alone, but with a multi-male multi-
female nexus of neighbors. In mouse lemurs (Microcebus murinus), animals of eithersex may share nest holes, and sometimes a male with a female. Males apparently havelarger home ranges than females, thus having more potential contacts with a variety ofmates. There is so far no indication of longer-term bonding between particular animals[10–12]. Information on the social system of the pygmy mouse lemur (Microcebusmyoxinus) [13] is not yet available.
Dwarf lemurs, Cheirogaleus, Allocebus and Mirza, are also little known, exceptthat they range mostly alone, but at least Allocebus shares tree holes with conspecifics[14]. Kappeler [15] has found that Mirza have the largest testes among solitaryprosimians. This implies scramble (sperm) competition polygyny. An earlier sugges-tion [16] that Mirza are pair bonded does not seem to hold.
Phaner furcifer was described as pair bonded by Charles-Dominique and Petter[17]. Their data are slight, being based on 4 visits of a month each, through the year,and on 5 adult males, ‘one bachelor, three monogamous, one bigamous’. However,the behavioral description does not resemble that of other cheirogaleids: ‘About8 months after the breeding season (June), these males continued to share manysocial relations with the females. The male and female are practically in continuousvocal contact throughout the night and in close proximity for at least half the night.Often, during movements, the male follows the female at a distance of 1–10 m. Whenthe female arrives at a gum-producing taly (Terminalia sp.) the male waits 2–5 mbehind, approaching to eat only when the female has left the tree. If the female con-tinues further on, the male may remain at a distance, but more often, 5–15 min laterthey renew vocal exchanges and the male rejoins the female. After being separated,the female was observed arriving in a taly still occupied by the male, who immedi-ately withdrew. The female seems to be “dominant” in this and most other situations.’(pp. 85–86).
If Phaner is indeed a pair-living cheirogaleid, and/or the only one with continu-ous male-female associations, it merits much further study.
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LepilemuridaeLepilemur species, like most of the cheirogaleids, forage alone and have males
with larger home ranges that overlap several females’ ranges [18–21]. Lepilemur haveloud calls (like Phaner and Mirza) and defecation trees which may serve in some wayas territorial markers [C. Harcourt, pers commun.]. There is one suggestion that in thenorthern species, Lepilemur septentrionalis, a male and female are typically foundtogether [J. Ratsirarson, Sr., pers. commun.]. In general, Lepilemur, like cheirogaleids,seems to be loosely polygamous.
DaubentoniidaeSterling’s [22, 23] monumental study of Daubentonia madagascariensis on Nosy
Mangabe shows that aye-ayes mainly live and forage alone. They do, however, meetmore often than expected at feeding trees. During the 3 days, at any season of the year,when a female is in estrus, up to 6 males congregate from many hundreds of metersaway. The males chase and bite each other, as do males of many other lemurs. When amale succeeds in mating, copulation may last for an hour, perhaps as a form of mate-guarding. After mating, however, the two separate without further association. Feist-ner and Sterling [24] point out the paradox that there is no sexual dimorphism of bodysize in aye-ayes, in spite of apparent male competition – a paradox which reappears inthe troop-living L. catta.
This confirms Petter’s earlier description of the aye-aye as mainly solitary [25, 26].However, two short studies of aye-ayes in secondary forest and of a pair released on aforested island report that those females spent 20–25% of time with a male [27, 28].
IndriidaeAvahi are essentially always seen as pairs. Most studies have concentrated on
feeding and activity (or inactivity, in Harcourt’s phrase) rather than social behavior.Pairing is so obvious, consisting of feeding within a few meters during the night andsleeping wrapped up in a tight, two-part ball during the day, that it needs no insistence.[29–31]. Indri are also clearly paired, although the breeding adults may be accompa-nied by 3 or 4 young of different ages and sometimes adult size. Pollock’s [32, 33]classic study showed how full female dominance in Indri is expressed in the females’feeding priority for leafy branches in the crown of the tree, while the male waits histurn below.
Propithecus, in contrast, have been classed as forming multi-male, multi-femalegroups [1, 34]. It seems, however, that there is usually only 1 breeding female in agroup, and never more than 2. No more than 2 infants have been reported in a Pro-pithecus verreauxi group in 1 year, regardless of the number of females present [35].Sifaka groups may begin with the union of a single emigrant female and wanderingmales. ‘One explanation for (young females’) departure (from the natal group) mightbe that the onset of reproduction is delayed in young females in groups with severalreproductively active adult females, and dispersal may enable them to begin theirreproductive careers, … (and/or) adult females may precipitate dispersal by targetingyoung females for aggression and ultimate expulsion’ [36, p 16]. C. Saito [pers. com-mun.] has repeatedly observed this process at Berenty, in which maturing daughters areactively chased from the group by the breeding female. The population distribution atBerenty confirms this view: as the population has doubled, the number of troops alsodoubled, while the mean number of adult females per troop remained constant.
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In a group of Propithecus tattersalli, when two bred, the older one was chasedaway [37].
Finally, in three Propithecus diadema troops studied over a decade, the nucleus ofeach troop was a dyad of breeding females, either known to be, or plausibly, mother anddaughter. When a third matured in one group, the dominant female targeted her, andaggression escalated from July until the nulliparous female emigrated in September[P. Wright, pers. commun.; 38]. This sounds somewhat like callitrichid suppression ofsubordinate females, one way or another, by the breeding dominant. The difference isthat the two allied P. diadema females sleep and groom together, as do the two males,and in some years both allied females give birth. P. diadema society could turn out tobe a conversion of pair-bonding to an allied mother-daughter twosome: an intermedi-ate step between pairs and the larger troops of L. catta.
LemuridaeTwo of the three Hapalemur species are pair-living animals: H. griseus and
H. aureus [39, 40]. Hapalemur simus lives in groups – the largest reported was 25animals – whose internal structure is not clear [39, 40; P. Wright, pers. commun.].
Varecia has caused much confusion. Some animals and populations seem to beclassically pair bonded, with high inter-female aggression, notably groups at DukeUniversity Primate Center, and at Vatoharanana, the high-altitude virgin forest site inRanomafana National Park [41–43]. However, some females tolerate others, even tothe point of cross-suckling young between mothers and an adult daughter at JerseyWildlife Preservation Trust. Morland [44] reported that Varecia variegata variegata(or subcincta) on Nosy Mangabe has a social structure that changes with the season:male-female pairs associate closely during the mating and nesting seasons, but lateron females associate with each other, rather than with males. Rigamonti [45] andVasey [46] confirm the same seasonal social change for Varecia variegata rubra.Females ranged in ‘core groups’ during mating and nesting seasons. In Vasey’s study,in 3 core groups, only 1 female apparently gave birth; in 2 core groups, 2 females didso, and each core group had 1 associated male. During the hot wet season of Decem-ber–February, as the young grew more independent, females of V.v. rubra associatedwith each other, abandoning the previous loosely bonded paired male-female socialstructure.
Eulemur comprises 5 species. One is paired, 1 sometimes paired, 1 has closemale-female associations within larger troops, and 2 are little published, though sub-ject to current study. Eulemur rubriventer lives in tight little pairs: male, female andyoung of the season [47, 48]. Eulemur mongoz can vary from paired to small polyga-mous groups both within and between populations [49–52]. As van Schaik and Kap-peler [53] point out, at places and times where E. mongoz is reported as nocturnal it ismonogamous, when diurnal, it lives in groups. Eulemur fulvus rufus forms year-roundmulti-male, multi-female troops of up to at least 16 animals [47, 48, 54]. However,within these troops, particular males and females have ‘special relationships’, inwhich the two groom, huddle and scent mark each other [55–57]. Male and femaleE. fulvus are equally likely to initiate or win conflicts, and many conflicts are not‘decided’, unlike the clear-cut female dominance of L. catta [55–60]. It is not clearwhat these co-dominant male-female associations mean in terms of mating, mate-guarding or parental care, but van Schaik and Kappeler [53] speculate that they func-tion as pair bonds in the prevention of infanticide (see Discussion).
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The remaining Eulemur species, E. macaco and E. coronatus, live in fairly largetroops of around a dozen animals. E. macaco and E. coronatus are both in some waysecologically convergent with the large troops of L. catta [61, 62]. Van Schaik andKappeler [53] found that within a small group of E. coronatus at Duke Primate Center,the two females and the two males preferentially associated as pairs, rather than asso-ciating within each sex. Fornasieri and Roeder [63] found 100% female dominancein E. macaco, like L. catta, and in contrast with their own results for E. fulvus [60].Petter’s original study of E. macaco on Nosy Komba [18] found small groups of2–5 females and 3–6 males, with more males than females in almost all groups, andseveral groups normally joining to sleep in the same tree. More recent studies have notyet published extensive censuses. It remains to be seen whether E. coronatus andE. macaco social structures are more reminiscent of the ‘pairs within troops’ of E. ful-vus or the very different groupings of L. catta, or something completely different.
It seems however that lemurid societies, like indriid societies, have pair-bondingas what Carpenter [64] called the ‘central tendency’ of the taxon, albeit with somespecies and most populations still undescribed.
Lemur catta: An Exception?The ring-tailed lemur now stands out as a glaring exception. Its females associate
preferentially with each other, not with males, and males are more likely to associatewith males than with females. Only in the lead-up to the mating season do males fre-quently sit grooming with females, and even then the female is likely to cuff the maleand move him away. Compared to E. fulvus, there is little preferential associationbetween particular males and females. There are low-key but temporary preferences,however [64]. The dominant male or males in a troop may be more tolerated and in atleast some breeding seasons have most access to first matings [65, 66]. Some malesattempt to mate-guard a female for as long as a day or 2 leading up to her few hours ofestrus [G. Wood, pers. commun.]. However, almost all females mate with many males,so even at that point there seems nothing one could call pair-bonding.
Does this mean that ringtail society does resemble polygamous kin groups of cer-copithecines, although without protective ‘friends’ as in baboons, and with inverteddominance relations? There are important differences.
The relations between female ringtails seem to be basically dyadic, rather thanradiating among a large kin group as described for baboons or macaques. Kappeler[67, 68] showed that relationships between any two lemurs are remarkably black orwhite: either almost wholly affiliative or almost wholly antagonistic. Furthermore,lemurs have relatively few ‘close friends’. The commonest physical grouping is adyad – 2 females sitting in contact or sunning together, perhaps with their infants ofthe year or flanked by a year-old juvenile. At Duke Primate Center, these dyads proveto be generally a mother and adult daughter. This does not mean that ringtails cannotform a close group of 3, such as a mother and 2 daughters, or grandmother, daughterand granddaughter. Rarely, close affiliation may extend to a foursome. Observationsdo need to be calibrated for temperature and season. In winter in either hemispheremost females are pregnant, aggression is at its lowest, and contact groups are thermalballs of available warm fur. The distinction between affiliates and nonaffiliates sharp-ens in the spring birth season, when female nutritional need is also high [69–72].
Aggression also differs. Female lemurs take the most active role in between-troopconflict [69–74]. Within troops, female ringtails have more aggressive encounters
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than males [70]. Matrilines can effectively eliminate other matrilines, through a longsequence of aggressive episodes [75–77]. However, few of the aggressive acts arepolyadic [59]. Taylor [77] observed 253 coalitions out of 7,096 aggressive interac-tions, all involving cooperation between mother/daughter or adult sisters and only 6%of the coalitions in support of the victim. When females intervene in the conflicts ofjuvenile or subadult lemurs, only 50–70% are actually on the side of reinforcing kindominance [78]. Immatures do not respond to maternal support by joining in to attackthe aggressor [78, 79]. Female hierarchies are often circular and can be upset fromyear to year as females attack each other [79]. Although a female and her daughtersmay have similar dominance ranks at any one time, dominance is not nepotisticallyinherited over the long term as it is in macaques and baboons [78–80].
Targeting aggression [81] seems to be unique to the lemurs. Lemurs may repeat-edly attack a member of their own sex. The outcome is sometimes wounding, expul-sion from the troop and, in extreme cases, death. Both E. fulvus and L. catta target, andboth males and females may be targeted. However, in the Duke situation similar num-bers of male and female E. fulvus were targeted (n = 30) while 79% of L. catta targetswere females (n = 24). Similar targeting has repeatedly been seen between females inthe wild [M. Pereira, pers. commun., pers. observation]. Although catarrhines havestrong female dominance relations within troops, it does not seem that they expel indi-vidual members of their own troop.
Troop fission occurs in L. catta as it does in cercopithecines. One clique (proba-bly a group of close female kin) separates from another. When this has been seen atBerenty, it leads to physical fighting between females as the new troop establishes itsown home range at the expense of neighbors or of the parent troop [74, 82]. The degreeof violence may well be related to the population density at Berenty, in that there is nounoccupied range. However, qualitative aspects of intertroop encounters are the sameboth in the sparse and the densely populated areas of Berenty. Although intertroopencounters are less frequent in drier areas, about 80% involve aggressive threat in anyhabitat during the birth season [pers. observation]. Again, although fission, and subse-quent threat between troops, happens in monkeys, the high degree of physical conflictbetween former within-group female kin seems to be characteristic of lemurs.
Finally, lemur females seem to arrange the demise of each others’ infants. Manyinfants die in the first month of life [83]. A common trigger for dropping an earlyinfant is the chases that occur during intertroop conflict or targeting aggression, whenmothers move fast and jerkily. The lemurs move too quickly to be sure whetheraggressors’ cuffs are or are not directed at the infants themselves. More conservatively,this may simply be the situation when infants which are weak for other reasons aremost likely to fall.
Infant lemurs which lose contact give a piercing repeated call, which persists indying infants almost beyond any other capacity except breathing [84, 85]. As Gould[86, 87] first reported, when an infant is dropped, all females crowd around the peep-ing infant. If the mother reaches the infant, it almost always clings at once to her fur.If, however, the mother is subordinate, she may be repeatedly chased away by thedominants within her troop [86; J. Andrews, pers. commun.; M. Pereira, pers. com-mun., pers. observation]. If the mother belongs to an opposing troop, she and herwhole troop may be chased. The infant is then left to its fate or may even cling toan animal of the wrong troop, which carries it out of the mothers’ home range [74;M. Pereira, pers. commun.].
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Note that this ‘behaviorally imposed mortality’ [88] is not the same as activefemale-caused infanticide, which Andrews [89] has seen in E. macaco. Neither is itmale-caused infanticide, though it might sometimes open the way to that [90, 91].This is the occasionally lethal result of two apparently simple rules of thumb: ‘go topeeping infant’ and ‘treat the mother as usual’.
In sum, the internal structure of ‘female-bonded’ L. catta troops is actually dif-ferent from that of cercopithecines. The female-female bonds are much less diffuseand less ambivalent, being mainly closely linked mother-daughter dyads. Female-female aggression in turn is much higher, including rank reversals, targeted expulsionof troop members, physical fighting with females of other troops (particularly newlyseparated kin) and behaviorally induced mortality of other females’ infants.
Although there is no trace of male-female pairing within a L. catta troop, we mayrecognize a potential for female-female antagonism resembling that of other species’females who live alone, as male-female pairs or in mother-daughter dyads with fewmales.
Discussion
Pair-bonding, then, is widespread among diurnal lemurs (table 1). Even thosewhich live in larger social groups have some behaviors which suggest that femalescould be more solitary: either pairing within the group or aggressive expulsion offemales beyond some limit. It may be that pairing is an ancestral trait for diurnallemurs.
Origins of Pairing: Child Care or Defense?How did pair-bonding itself originate? All arguments start from the premise that
females are ecologically constrained to feed in small groups. P. Wright [pers. com-mun.] points out that the formula ‘feeding alone’ is not accurate. If a monogamousgroup is actually 5 animals including dependent offspring, adding 1 more female and
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Cheirogaleus major Lepilemur ruficaudatus Eulemur rubriventer1
Allocebus trichotis Lepilemur septentrionalis Hapalemur griseus1
Phaner furcifer1 Hapalemur aureus1
Hapalemur simusVarecia variegata2
1 Pair-bonded social structure.2 Variant of pair-bonding (see text).
her offspring raises the group size to 9. Wright adds that low and erratic fruit avail-ability in Madagascar’s rain forests may be a general constraint on lemur and indriidgroup size.
Small group size is clearly not an explanation for the pairs within troops of E. ful-vus. Van Schaik and Kappeler [53] and van Schaik [92] speculate that pairing is linkedto cathemerality, infanticide and predation. The core of the argument is that pairingderived from the female’s need for protection against infanticidal males of her ownspecies. In nocturnal animals, a male could keep track of and defend only one femaleat a time, even in species where it is ecologically possible for several females to feedtogether. This would explain why there are more females per group and less obviouspairing in the wholly diurnal L. catta and Propithecus spp., although the diurnal Indriis also paired. One problem with this scenario is that in two well-observed infanticidesby immigrant P. diadema males, the resident male did not defend the infant and indeedgroomed the newcomer [38].
Lemur and Propithecus, like other lemurs, retain the reflecting tapetum character-istic of nocturnal eyes. It might even be that lemurs as a whole are still shifting to diur-nal life, following the extinction of the large subfossil hawks and eagle, within the lastfew centuries [92–94]. Males might have played a role in predator protection againsteither the extinct or modern menaces [93–97], although it seems that modern preda-tors simply eat lemurs without much chance for defense apart from vigilance [98].Males in L. catta are not more vigilant than females, so in this case they do not seemto defend against predators more than extra females would [L. Gould, pers. commun.].
Dunbar [99] argues that callitrichid paternal care and increased female reproduc-tion (postpartum estrus and twinning) must have followed rather than preceded theevolution of pair bonds. If females became dependent on male care of infants beforepair bonds developed, they would too often risk losing their own parental investment.Thus a male originally benefited by staying with a single solitarily feeding female andher young for defense against something – either predators or conspecifics. In pair-bonded lemurs, male care is limited to territorial defense and vocal advertisementagainst conspecifics, with almost no carrying of young, so Dunbar’s argument shouldapply even more strongly. Pending more information on actual infanticide [38, 90, 91,100, 101], and with no published information on male roles, if any, in predatordefense, the origins of pair-bonding must remain speculations to pursue. However,van Schaik and Kappeler [53] were the first to point out the extent of pair-bonding inmodern lemurs. The present paper is mainly concerned to underline the widespreadexistence of pair bonds and of a high level of female-female aggression among thelemurs.
Pair-Bonding and Female DominanceWright [102, 103] has explored the variety of correlations, or lack of them,
between monogamy, codominance, body size, ecology and paternal care in primates.The strongest correlation is between monogamy and codominance between sexes, orsometimes female dominance. Female dominance in a truly monogamous pair can beinterpreted as paternal investment in the males’ own current offspring, or through hismate’s health, in his future offspring [33]. If the ancestors of present social lemurswent through an earlier stage of monogamy, this would help explain the origins offemale dominance or codominance, and at least offer a ‘level playing field’ for laterevolution.
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It is tempting to relate the lack of sexual dimorphism in lemurs, including thelarge extinct lemurs, to a legacy of monogamy. The problem is that polygamouslemurs also have no or reduced dimorphism, including those with visible, physicalfighting between males over estrous females, such as the solitary aye-aye and thetroop-living L. catta [57, 104, 105].
Some modern lemurs have 100% female dominance, others 50%. Furthermoresome species which are paired or pairs within troops seem to be codominant or havetotally unpredictable relations between sexes, which can hardly be called dominance(e.g. E. fulvus). The ones with total adult female dominance over adult males includeIndri [33] but also those with larger groups, where one might expect every opportunityfor male polygyny and ‘normal’ male sexual selection for the ability to controlfemales (e.g. L. catta) [106, 107].
It may be that some combination of female need [69, 71, 80, 108–111] – but seeKappeler [57, 59] – and more importantly of female choice to mate with compliantmales [90], all starting from a phyletic legacy of pairing, may afford a complete expla-nation. Even so, I suspect we are still missing a piece of the puzzle.
Social IntelligenceFinally, the apparent convergence of L. catta social structure with that of the Old
World monkeys led me to write in 1966 [2, p 506]: ‘In general, the organization ofL. catta troops seems as complex as the troops of many monkeys. There are longchains of interactions: approaches, spats, stink-fights, redirected aggression… (How-ever) most single interactions could be considered as involving only two animals at atime. I did not see “protected threat” [112]. After further study, it may be possible tosay that such subtle behavior does exist or that it never exists among lemurs… Wehave no scale by which to compare their relative sophistication.’
Following the work of Byrne and Whiten [113–115] we now have such a scale.Kummer’s’ ‘tripartite behavior’ is indeed remarkably rare among lemurs. Deceptionat any level has never been reported among prosimians. Reconciliation after conflictapparently does not occur in L. catta [67], which is in keeping with their fairly whole-hearted classification of others as affiliates or enemies. Enlistment of others in attackis rare, if it happens at all. Enlistment is more questionable, since joint attack on othersis quite common. However, the glancing back and forth which a monkey may use torecruit an hesitating ally is at least unusual in lemurs. Pereira [pers. commun.] borrowsMark Twain’s summary of when an auctioneer lies: ‘I never saw a lemur attackanother unless it was strictly convenient.’
This emerging picture of the lack of social subtlety among L. catta accords withthe picture drawn here of their females as partway between female dyads and female-bonded kin groups. Numerically they range as kin groups, but in social relations theymay still react as aggressively solitary animals, cosily grooming daughters and sistersbut with little commitment to a wider troop nexus.
The original argument of the 1966 paper stands that intelligence was formidablyselected for in a social context – but now we can finally correlate degrees of intelli-gence with just what sort of social context.
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Note Added in Proof
Brockman [116] extends Richard’s [34] view of P. verreauxi’s mating. Although P. verreauxilives year-round in small groups with a clearly dominant female and male, both sexes mate polyga-mously, like Daubentonia or L. catta. It is thus debatable whether P. verreauxi shows even a variantof pairing.
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![The red ruffed lemur[1]](https://static.documents.pub/doc/80x56/5451a068af7959b9648b5e19/the-red-ruffed-lemur1.jpg)
