Attacks on a wild infant ring-tailed lemur (Lemur catta) by immigrant males at Berenty Madagascar interpreting infanticide by males.код для вставкиСкачать
American Journal of Primatology 67:267–272 (2005) BRIEF REPORT Attacks on a Wild Infant Ring-Tailed Lemur (Lemur catta) by Immigrant Males at Berenty, Madagascar: Interpreting Infanticide by Males SHINICHIRO ICHINOn Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, Japan An orphaned infant ring-tailed lemur (Lemur catta) was attacked persistently by immigrant males and disappeared with severe wounds at Berenty Reserve, Madagascar. Prior to the attacks, two troop members disappeared. On 20 November 1998, the only resident male in Troop C2B disappeared suddenly. After the disappearance, nine males from three neighboring troops approached, but only six males continued to shadow the troop. Of the females, the one lactating female attacked the males the most frequently. On 21 January 1999, the lactating female disappeared and her infant was orphaned. Subsequently, five attacks on the infant by immigrant males were observed for five consecutive days from January 23 to 27. The aggression was persistent and specifically targeted the infant, suggesting that the attacks were purposeful aggression, rather than redirected or accidental aggression. The primary attacker was the most dominant of the immigrant males, and mated with females in the next mating season. Am. J. Primatol. 67:267–272, 2005. r 2005 WileyLiss, Inc. Key words: infanticide; reproductive tactics; orphan; ring-tailed lemur; Madagascar INTRODUCTION Infanticide by males is a relatively common phenomenon in primates [van Schaik & Janson, 2000]. The adaptive significance of this phenomenon has been highly controversial [Hrdy, 1979; Haufater & Hrdy, 1984; Sussman et al., 1995; van Schaik & Janson, 2000]. The most commonly accepted theory in recent years considers infanticide by males to be a male reproductive strategy [van Schaik & Janson, 2000]. According to the classic sexual-selection hypothesis on which the male reproductive strategy theory is based, the female that loses an infant to Contract grant sponsor: Ministry of Education, Science and Culture of Japan. n Correspondence to: Shinichiro Ichino, Graduate School of Asian and African Area Studies, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan. E-mail: email@example.com Received 4 August 2003; revised 22 February 2005; revision accepted 3 March 2005 DOI 10.1002/ajp.20183 Published online in Wiley InterScience (www.interscience.wiley.com). r 2005 Wiley-Liss, Inc. 268 / Ichino infanticide returns rapidly to ovarian cycling, comes into estrus more quickly then she would have otherwise, and copulates with an infanticidal male [Haufater & Hrdy, 1984; Sugiyama, 1965]. Ring-tailed lemurs form multimale–multifemale, female resident troops [Jolly, 1966] and exhibit strict reproductive seasonality [Koyama et al., 2001; Sauther, 1991]. Attacks on infants by male ring-tailed lemurs may also be regarded as a male reproductive tactic [Hood, 1994; Pereira & Weiss, 1991]. At least nine cases of infant attacks were observed in a semifree-ranging population at the Duke University Primate Center [Jolly et al., 2000]. Pereira and Weiss  proposed a model of the ring-tailed lemur mating system that included the hypothetical co-evolution of female and male reproductive tactics. According to their model, immigrant males kill unrelated infants that are vulnerable. However, only two cases of infant attack by males have been reported in wild ring-tailed lemur populations [Hood, 1994; Jolly et al., 2000], both of which were observed at Berenty Reserve. In the first case, a nontroop male killed an abandoned infant that had fallen to the ground [Hood, 1994]. The killer male did not immigrate into the infant’s troop after the incident. Thus, Hood’s  observation was not a typical case as described in the model of Pereira and Weiss . In the second case, an immigrant male bit an infant while he was being chased by resident males during an attempt to join a troop [Jolly et al., 2000]. It is not possible to exclude the possibility that the attack was redirected or accidental aggression. Thus, more information is required to help test the model of Pereira and Weiss . In this paper, I present a case of attacks on a wild infant ring-tailed lemur by immigrant males. MATERIALS AND METHODS This study was conducted at Berenty Reserve, southern Madagascar. Jolly and her colleagues  have studied ring-tailed lemurs there since the 1960s. Koyama and his colleagues [2001, 2002] have conducted continuous long-term research since 1989 in a 14.2-ha area that partly overlaps Jolly’s study area. I observed attacks on an infant in Troop C2B, one of the troops in Koyama’s study area. Troop C2B consisted of six individuals, including three adult females and one adult male, in November 1998. The attacks were observed during my 14-month study that lasted from August 1998 to September 1999. In this paper I use the notes that I recorded as ad libitum sampling [Altmann, 1974] from 20 November 1998 to 28 January 1999. The emission of a ‘‘spat call,’’ the typical submissive call [Jolly, 1966; Pereira & Kappeler, 1997], was used as an operational indicator of dominance. RESULTS Immigration of New Males On 20 November 1998, the lone adult male (NT) in Troop C2B disappeared suddenly. It is possible that he died. Subsequently, nine males from three different troops approached Troop C2B. Six males continued to shadow the troop until January 1999. By 20 January, I had observed a total of 45 attacks on the immigrating males by troop females. The only lactating female (MI-91~) attacked the males the most frequently (80.0%, 36 cases). Attacks on Infants by Immigrant Males / 269 Attacks on an Infant by Immigrant Males On 21 January 1999 the lactating female (MI-91~) disappeared from Troop C2B and probably died. Her 4-month-old daughter (MI-9198~) was orphaned. After the female disappeared, a total of five attacks on the infant by immigrant males were observed over the next 7 days (Table I). The two attackers were the most dominant male (TJ) and the second-most dominant male (SH-93#) of the immigrant males (Table I). The first attack (case 1) was observed at 0706 hr on 23 January. When the troop females moved away from the infant, an immigrant male (TJ) approached and attacked the infant. A female (RH) came back immediately and chased away the male. At 1558 hr on 24 January, another male (SH-93#) also attempted to attack the infant. However, the infant’s grandmother (MI) chased him. The second attack (case 2) was observed at 1524 hr on 25 January. TJ, the dominant immigrant male, responded to the infant’s distress call by turning back and searching for the infant, which he then attacked. Two adult females (RH and MI) chased the male immediately. Around 0600 hr on January 26, the infant was found near the tourist cafeteria with deep (5 cm) slashes on each hind leg (Fig. 1). At 0748 hr, the third attack (case 3) was observed. When the infant exchanged calls with a juvenile female, TJ noticed the call, approached, and attacked the infant. No females supported the infant at that time. After the attack, the infant remained sitting alone in a bush until the evening. The fourth attack (case 4) was also observed on 26 January. At 1757 hr, when the troop females came back near the infant, the infant began to follow the traveling troop. At 1801 hr, TJ passed under the tree where the infant was feeding with troop females. He seemed to notice the infant, but remained sitting under the tree for around 30 min, looking up into the tree. At 1834 hr, TJ suddenly climbed the tree and attacked her. The infant dropped to the ground, and the other male (SH-93#) on the ground attacked her. The infant’s grandmother (MI) chased SH-93# immediately. At 1851 hr, TJ attempted to approach the infant again. However, her grandmother (MI) chased him away again. The fifth attack (case 5) was observed at 1746 hr on 27 January. The infant was resting with troop females at 1736 hr. At 1742 hr, when the females moved away from the infant, TJ attacked the infant. The infant’s grandmother (MI) came back and chased TJ immediately. On 29 January, the infant disappeared from the study area and probably died. At 0900 hr she was sitting in a bush and seemed to be unhealthy. That was the last time I observed her, and her carcass was never found. TABLE I. Observed Cases of Attacks on Infant (MI-9198~) Case 1 2 3 4 5 Date Jan. Jan. Jan. Jan. Jan. 23 25 26 26 27 Time Attackers 7:06 15:24 7:48 18:34 17:46 TJ TJ TJ TJ, SH-93# TJ 270 / Ichino Fig. 1. Wounds on the hind legs of an infant (MI-9198~). After the Attacks on the Infant After the infant disappeared, only three males, including the most dominant male (TJ), successfully completed immigration into Troop C2B. They mated with troop females in the next mating season (Ichino, unpublished data). The other three males disappeared from Troop C2B by April 1999. DISCUSSION An orphaned infant ring-tailed lemur was attacked and presumably killed by immigrant males. The attacks were persistent and specifically targeted the infant. An immigrant male (TJ) responded to the distress calls from the infant and attacked her (cases 2 and 3). Multiple sneak approaches by males toward infants have been observed at the Duke University Primate Center (DUPC) [Pereira & Weiss, 1991] (Pereira, personal communication). These observations suggest that attacks on infants by males are purposeful aggressions, rather than accidental or redirected aggressions. After the lone troop male disappeared, the newly immigrant males attacked the infant. This case is similar to what has been reported for gorillas [Watts, 1989]. However, ring-tailed lemur troops usually contain several males. Troop males may play a role in defending infants against lethal aggression by immigrant males. Troop males have attacked and tried to drive nontroop males off [Nakamichi & Koyama, 1997; Pereira & Weiss, 1991], and have often responded to infant distress calls by running toward the infant (Pereira, unpublished data; Ichino, unpublished data). Attacks on Infants by Immigrant Males / 271 The primary attacker (TJ) was the most dominant of the immigrant males (Table I), and mated with the troop females in the next mating season. These results are consistent with the prediction from the model of Pereira and Weiss , which is based on the sexual-selection hypothesis. However, it remains obscure how males gain a reproductive benefit from infanticide in these strictly seasonal breeders [Sussman et al., 1995]. Jolly et al.  argued that reproductive effort during lactation may affect the mother’s physical condition, which is related to the birth rate and infant survival rate in the following year, and this hypothesis is partly supported by observations at the DUPC (Pereira, unpublished data). Of the troop females, the lactating female attacked the immigrant males the most frequently. Aggression by the lactating female has been observed at the DUPC and is considered a female counterstrategy for infanticide [Pereira & Weiss, 1991]. Ring-tailed lemur females can attack and disperse males effectively because they are dominant over males [Jolly, 1966; Kappeler, 1990]. In contrast, nonlactating females (including the infant’s grandmother) rarely attacked the males even after the infant was orphaned, although they supported the infant when she was attacked by the males. This observation suggests that ring-tailed lemur females rarely defend infants cooperatively against lethal attack by immigrant males. ACKNOWLEDGMENTS I thank Jean de Heaulme and his family for their kind hospitality and permission to carry out this study at Berenty Reserve; A. Randrianjafy, director of the Botanical and Zoological Park of Tsimbazaza, and the Government of the Malagasy Republic for their kind permission to perform this research in Madagascar; G. Yamakoshi for his useful comments; N. Koyama for his invaluable advice; and M.E. Pereira for his useful comments and kind permission to refer to his unpublished data. This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan to N. Koyama (no. 06610072). REFERENCES Altmann J. 1974. Observational study of behaviour: sampling methods. Behaviour 49: 227–267. Haufater G, Hrdy SB. 1984. Infanticide. Comparative and evolutionary perspectives. New York: Aldine. 598p. Hood LC. 1994. Infanticide among ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Am J Primatol 33: 65–69. Hrdy SB. 1979. Infanticide among animals. A review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1: 13–40. Jolly A. 1966. Lemur behavior. Chicago: University of Chicago Press. 187p. Jolly A, Caless S, Cavigelli S, Gould L, Pereira ME, Pitts A, Pride RE, Rabenandrasana HD, Walker JD, Zafison T. 2000. Infant killing, wounding and predation in Eulemur and Lemur. Int J Primatol 21: 21–40. Jolly A, Dobson A, Rasamimanana HM, Walker J, O’Connor S, Solberg M, Perel V. 2002. Demography of Lemur catta at Berenty Reserve, Madagascar: effects of troop size, habitat and rainfall. Int J Primatol 23:327–353. Kappeler PM. 1990. Female dominance in Lemur catta: more than just female feeding priority? Folia Primatol 55:92–95. Koyama N, Nakamichi M, Oda R, Miyamoto N, Ichino S, Takahata Y. 2001. A ten-year summary of reproductive parameters for ring-tailed lemurs at Berenty, Madagascar. Primates 42:1–14. Koyama N, Nakamichi M, Ichino S, Takahata Y. 2002. Population and social dynamics changes in ring-tailed lemur troop at Berenty, Madagascar between 1989–1999. Primates 43:291–314. 272 / Ichino Nakamichi M, Koyama N. 1997. Social relationships among ring-tailed lemurs (Lemur catta) in two free-ranging troops at Berenty Reserve, Madagascar. Int J Primatol 18:73–93. Pereira ME, Weiss ML. 1991. Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behav Ecol Sociobiol 28:141–152. Pereira ME, Kappeler PM. 1997. Divergent systems of agonistic behaviour in Lemurid primates. Behaviour 134:225–274. Sauther ML. 1991. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am J Phys Anthropol 84:463–477. Sugiyama Y. 1965. On the social change of Hanuman langurs (Presbytis entellus) in their natural condition. Primates 6: 381–418. Sussman RW, Cheverud JM, Bartlett TQ. 1995. Infant killing as an evolutionary strategy: reality or myth? Evol Anthropol 3:149–151. van Schaik CP, Janson CH. 2000. Infanticide by males and its implications. Cambridge: Cambridge University Press. 569p. Watts DP. 1989. Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology 81:1–18.