Primates (2015) 56:119–125 DOI 10.1007/s10329-015-0461-7
NEWS AND PERSPECTIVES
Parturition and potential infanticide in free-ranging Alouatta guariba clamitans ´ scar M. Chaves • Valeska Martins • O Mariana Beal Neves • Ju´lio Ce´sar Bicca-Marques
Received: 17 December 2014 / Accepted: 18 February 2015 / Published online: 5 March 2015 Ó Japan Monkey Centre and Springer Japan 2015
Abstract Parturition is a key process of mammalian reproduction that is rarely documented in New World monkeys because it often occurs at night. However, diurnal births have been recorded in several species. In howler monkeys (Alouatta spp.) they have often been observed during prolonged resting periods. Similarly, infanticide is a behavior observed quite infrequently. Infanticide in howler monkeys is often inferred from infant deaths or disappearances after group takeovers by nonresident male(s). Here we report the first observation of parturition and birth-related behaviors in the brown howler monkey (Alouatta guariba clamitans) and the likely attack on the infant that caused its death. The mother was a multiparous female that lived in a ca. 3-ha Atlantic forest fragment in southern Brazil with nine group mates. The behavior (‘‘all occurrences’’) sampling method was used to record birth-related behaviors and social interactions. The parturition occurred during the day of 27 October 2013 during a feeding session. The female showed no sign of contraction or birth delivery posture. Parturition began apparently after matrix rupture and release of the amniotic fluid. Expulsion of the
Electronic supplementary material The online version of this article (doi:10.1007/s10329-015-0461-7) contains supplementary material, which is available to authorized users. ´ . M. Chaves M. B. Neves V. Martins O J. C. Bicca-Marques (&) Laborato´rio de Primatologia, Faculdade de Biocieˆncias, Pontifı´cia Universidade Cato´lica do Rio Grande do Sul, Avenida Ipiranga, 6681 Pre´dio 12A, Porto Alegre, RS 90619-900, Brazil e-mail: [email protected] V. Martins Centro de Cieˆncias da Sau´de, Universidade de Cruz Alta, Cruz Alta, RS, Brazil
newborn occurred between 1 and 3 min later (the exact moment of delivery was not observed). Then, the female held and licked the newborn and began to ingest the placenta and the umbilical cord. The other group members continued feeding and had no interaction with the parturient during the preparturition and parturition events. The infant died ca. 35 days later as a consequence of injuries to his forehead and face, potentially caused by a conspecific bite. Because the adult and subadult males chased the female in the day that the infant’s wounds were detected, we believe that one of them might have been the aggressor. We discuss this putative case of infanticide in light of the potential motivation of each male. Keywords Aggression Brown howler monkey Daytime birth Males Southern Brazil Wild birth
Introduction Mammalian reproduction involves the processes of finding a mate, courtship, mating, birth delivery, nursing, weaning, and infant care among others. Whereas behaviors associated with some of these processes are frequently observed in the wild as they are conspicuous, long-lasting, and occur during the species’ active period, others are rarely observed as they are more discrete, short-lasting, and/or occur at night or apart from the rest of the group. Parturition in primates fits best the latter category because it often occurs at night (Jolly 1972; Honnebier and Nathanielsz 1994; Bernis and Varea 2012) and/or takes place in locations where observers do not have an adequate view, such as in arboreal species (Dias 2005). However, diurnal births have been recorded among wild prosimians (Lemur catta:
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Takahata et al. 2001), Old World monkeys (Erythrocebus patas: Chism et al. 1983; Papio cynocephalus: Condit and Smith 1994; Rhinopithecus bieti: Ding et al. 2013), New World monkeys (Alouatta arctoidea: Sekulic 1982; A. caraya: Peker et al. 2009; Callicebus cupreus: Ruiz et al. 2004; Callicebus oenanthe: DeLuycker 2014; Saguinus imperator: Windfelder 2000; Saguinus labiatus: Bezerra and Porter 1999), and apes (Pan troglodytes schweinfurthii: Goodall and Athumani 1980; Pan paniscus: Douglas 2014). The pattern of nocturnal birth has been related to four potential advantages: reduction of the risk of (a) predation (Jolly 1972; Chism et al. 1983), (b) intragroup infanticide (Jolly 1972; Takahata et al. 2001), and (c) newborn fall during group locomotion soon after birth (Jolly 1972), and (d) enhancement of female recovery and infant care (Duboscq et al. 2008). Predation-related hypotheses have also been proposed to explain the occurrence of diurnal births. Dias (2005) and DeLuycker (2014) suggest that the absence of wild predators at their study sites may have released Alouatta palliata and Callicebus oenanthe, respectively, from the potential pressure to give birth at night. On the other hand, Turner et al. (2010) suggest that diurnal births in Macaca fuscata may have evolved as an antipredator strategy because more individuals are vigilant during the day, thereby increasing the likelihood of detecting and evading potential predators. Diurnal births in howler monkeys have often been observed during the prolonged resting periods (e.g., A. arctoidea: Sekulic 1982; A. palliata: Dias 2005; A. belzebul: Camargo and Ferrari 2007; A. caraya: Peker et al. 2009). Sekulic (1982) suggests that diurnal births during resting may allow female howlers to obtain similar advantages to parturition during the night because this may presumably favor both the recovery of the birthing female and the maternal care of the newborn. Overall, delivery time in howler monkeys may vary from \1 min (A. arctoidea: Sekulic 1982) up to 7 min (A. caraya: Peker et al. 2009) as a consequence of individual female differences or maternal experience (e.g., multiparous females tend to show shorter delivery times; Nisbett and Glander 1996; Camargo and Ferrari 2007; see also Yao et al. 2012). Like other mammals, including primates, female howler monkeys often ingest the placenta after the birth delivery (Peker et al. 2009; Douglas 2014). However, placentophagy is not universal among primates (e.g., Callicebus oenanthe: DeLuycker 2014). The adaptive significance of this behavior remains underexplored. It has been related to a reduction in the release of placenta odors that may attract predators or to a potential analgesic effect on the birthing female among other hypotheses (for a review, see Kristal et al. 2012). According to Kristal (1980;
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Kristal et al. 2012), placenta consumption is not related to nutrient replacement. Unlike some Old World monkeys (Ding et al. 2013; Pan et al. 2014) and apes (Douglas 2014), howler monkey group mates often show little or no interest in the delivery and the newborn (Moreno et al. 1991; Nisbett and Glander 1996; Camargo and Ferrari 2007). Exceptions to this pattern were reported by Sekulic (1982) and Dias (2005). Dias (2005) reported that two male, two female, and one juvenile mantled howler monkeys (A. palliata) approached the mother and inspected the newborn, whereas Sekulic (1982) reported only two adult male red howlers (A. arctoidea) showing interest in the new group member. In the latter case, the newborn was killed in the day following its birth. Infant killing, or infanticide, was observed 17 times in howler monkeys (for a review, see Van Belle and BiccaMarques 2015). These events were distributed in five species (A. palliata: Clarke 1983; A. caraya: Zunino et al. 1985; A. arctoidea: Agoramoorthy and Rudran 1995; A. pigra: Van Belle et al. 2010; A. seniculus: Beltra´n and Stevenson 2012). For A. guariba clamitans there is only a single inferred case (Galetti 1994). Three major hypotheses have been proposed to explain the killing of dependent infants: sexual selection (van Schaik 2000; Van Belle and Bicca-Marques 2015), resource competition (Agoramoorthy and Rudran 1995; Rimbach et al. 2012), and social pathology (Sussman et al. 1995; Aguiar et al. 2005). Here we report the first observation of parturition and birth-related behaviors in a wild group of brown howler monkeys (Alouatta guariba clamitans) and the potential infanticide of the infant male about 1 month after its birth. We describe the context in which the parturition took place, the behavior of the parturient female and her group mates before, during, and after the parturition, and the behavior of the infant, and discuss the potential causes and motivations leading to its death.
Methods The parturition was observed on 27 October 2013 by V.M. and M.B.N. during a 3-day monthly following of a brown howler monkey group. The group inhabits a 2.9-ha semideciduous seasonal forest fragment in Parque Sa˜o Paulo Village (30°120 2800 S, 51°050 5300 W, 35 m asl), a rural community in Porto Alegre, state of Rio Grande do Sul, Brazil. The fragment is surrounded by dwellings and is highly disturbed by human activities, including deforestation, selective logging, and dumping. The fragment is immersed in a matrix of agricultural lands, pastures, and human settlements, and is isolated from other forest remnants by C77 m. The study site is inhabited by a single group of
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Table 1 Birth phases and the time and duration of occurrence of key events Birth phase
Hour
Duration
Behavioral observations
Prepartum Labor
14:15
Unknown
No signs of contraction or birth delivery-related postures are observed
*14:33
1–3 min
The exact moment of delivery was not observed
Placenta expulsion
*14:33
Unknown
The exact moment of placenta expulsion was not observed
Placenta consumption
14:48
2 min
Female ingests placenta
15:03
2 min
Female resumes ingesting placenta
Parturition Postpartum
Consumption of umbilical cord
15:05
1 min
Female ingests umbilical cord
15:14
1 min
Female resumes ingesting umbilical cord
1st displacement
15:13
1 min
Female moves 7 m to a Ficus luschnathiana tree, carrying the newborn
1st feeding bout
16:30
3 min
Female eats young leaves of the vine Cuspidaria convoluta
howlers. Nearby fragments are also inhabited by howler groups. The study group was composed of nine individuals: one adult male, two adult females, one subadult male, one subadult female, three juvenile males, and one infant female. This group was followed bimonthly by O.M.C. from July 2011 to June 2014 and monthly by V.M. from January 2013 to January 2014. The adult female, whose parturition we report here, had given birth twice since July 2011. We used the behavior sampling method (‘‘all occurrences’’; Martin and Bateson 2007) to record the behaviors of the mother, infant, and the other group members during the delivery and the next 3.5 h until dusk, when the group stopped their activities at a sleeping site. The same method was used to record social interactions during the next month’s monitoring period following the birth delivery (V.M.: 29 November–1 December; O.M.C.: 4–10 December 2013). We also video-recorded most of the parturition with a digital camera (NikonÒ Coolpix P510).
Results
14:30–14:37
14:37–14:43
14:43–14:48
The delivery occurred on 27 October 2013 when the study group (including the pregnant female) was feeding on mature leaves of a Ceiba speciosa (Malvaceae) tree at the edge of the fragment. The events of the parturition are described in chronological order below and summarized in Table 1: 14:15
Pregnant female is feeding with her group mates at about 20 m height on the top of the C. speciosa tree and at 2 m from her nearest neighbor. No signs of contraction or birth delivery-related postures are observed (this lack of signs compromised the recording of the beginning of the predelivery phase and its total duration).
14:48–15:05
The parturition begins apparently after matrix rupture and release of the amniotic fluid. The newborn male is expulsed between 1 and 3 min later (the exact moment of delivery was not observed). The adult female holds and licks the infant immediately after birth in a hunched posture. The placenta and umbilical cord remain attached to a 3-cm-thick branch, probably limiting the infant’s capacity to move (Online Resource 1). No individual shows any interest in or approaches the birthing female and her newborn. While the other group members move to nearby trees during the postdelivery phase, the parturient female remains at the same location trying to move (14 times) with her infant held on her belly. She cannot move because she is united to the infant by the umbilical cord that is still tied to the branch (Online Resource 1). The infant releases himself from his mother, grabs a branch with his tail, and vocalizes. Then, because he is still tied to the branch by the umbilical cord, the mother tries unsuccessfully to liberate him during 5 min. First, she tries to release him by pulling his arms. Then, she inspects the branch, looks under the newborn, and pulls him several times while turning him to the sides. The female eats part of the placenta during 2 min before licking the infant’s body. She then embraces him from 14:54 to 15:03. She resumes eating the placenta until full ingestion from 15:03 to 15:05 (Fig. 1a, Online Resource 1).
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15:05–15:13
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She pulls the newborn with both hands, but cannot release him because the umbilical cord is still tied to the branch. Then, she eats a portion of the umbilical cord during 1 min before holding the infant near her belly until he frees himself from the branch at 15:13. The female moves about 7 m with the infant grabbing her belly with his hands only, free feet, and with his back in contact with her belly (an unconventional posture). She moves until reaching a fig tree (Ficus luschnathiana, Moraceae), where she continues eating the remaining ca. 10 cm of the umbilical cord (Fig. 1b, Online Resource 1). After ingesting the umbilical cord, she rests during 17 min in a hunched posture with the infant attached to her ventral area. During this time it was not possible to determine whether she was breastfeeding him or not because of poor visibility. The female travels about 140 m with the infant grabbing her ventral area until arriving to the crown of another fig tree (Ficus cestrifolia). She joins the other group members. She eats young leaves of the vine Cuspidaria convoluta (Bignoniaceae) during 3 min and rests again for 42 min. The female travels away from the rest of the group for about 108 m until reaching a sleeping site at a plantation of the alien Pinus taeda (Pinaceae). She rests and remains isolated with her newborn until dawn, when the observers leave the site.
Fig. 1 Post-birth delivery behaviors of the female brown howler monkey. a Ingestion of the placenta. b Ingestion of the umbilical cord (photos by V.M.) (color figure online)
Throughout the events described above, no group member interacted with the female or manifested interest in the newborn. The infant male was gray and appeared to be in good health with enough vigor to cling to his mother. On the first day of the next monthly monitoring period by V.M., 29 November, all group members were behaving as usual and no agonistic interaction was observed. The now hairier infant remained apparently healthy (Fig. 2a). He was frequently seen exploring the environment around his mother. However, at 06:45 on 30 November the adult and subadult males suddenly attacked the female during a feeding session on mature fruit of Campomanesia xanthocarpa (Myrtaceae). They chased her while howling, and she fled carrying the infant on her back. About 2 h later, at 08:48, a severe injury was seen in the infant’s forehead, including a
large hole (ca. 2 cm in diameter) in the skull exposing part of the brain (Fig. 2b, c). It is likely that this wound was made on the previous day because the infant’s face was considerably swollen. The size, shape, and distance of the holes appear to be compatible with marks made by howler monkey canines. At 10:58, the female was attacked again by the adult male. She emitted a stress scream and ran, leaving the infant with the other adult female. As soon as she escaped, she retrieved the infant. The female remained away from other group members with the infant on her belly from 11:00 to 17:45, when the researchers left the site. The mother remained isolated from most group members from 06:00 to 18:45 on 1 December. During this time she only allowed the two other females to get closer to her
15:13–15:15
15:15–15:35
15:35–15:44
16:02–16:30 16:30–17:15
17:15
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Aggressions to the female stopped after the death of the infant and did not resume until the end of the study. Discussion
Fig. 2 Infant brown howler monkey a at the age of 27 days, b with severe injury in the forehead with the brain exposed at the age of 34 days, and c with the brain exposed and the face swollen at the age of 35 days (photos by V.M.) (color figure online)
and her infant. The infant was alive, but he could not open his eyes because his face was extremely swollen (Fig. 2c). O.M.C. did not see the infant from 07:00 to 18:45 on 4 December. The infant’s highly decomposed carcass was found by V.M. on 14 December lying on the forest floor near the sleeping tree used by the group on 1 December.
We report a daytime parturition in Alouatta guariba clamitans that took place during a feeding session. No sign of contraction was detected in the multiparous birthing female, and expulsion of the newborn male lasted between 1 and 3 min. Soon after the delivery the mother ate the placenta and umbilical cord. The female remained alone during the entire process, as no group member showed interest in the parturition or newborn. Finally, 1 month after the parturition, we detected a serious injury in the infant’s forehead after the nursing female being chased more than once by the group’s adult and subadult males. This injury caused his death soon after. Unlike previous observations on daytime parturition in Alouatta spp. (Sekulic 1982; Dias 2005; Peker et al. 2009), the birth reported here did not occur during a period of inactivity. It is possible that this was enabled by the multiparous condition of the mother. For instance, Yao et al. (2012) reported that experienced white-headed langur (Trachypithecus leucocephalus) females can minimize the energetic costs of birth with a rapid and efficient delivery process. On the other hand, the observations of placentophagy and quick return to feeding activities after the parturition are in accordance with reports by Peker et al. (2009) and Dias (2005). However, energy recovery, as proposed by Peker et al. (2009) for A. caraya, is an unlikely explanation for the first feeding bout after the parturition because the female ate young leaves, a resource that is often energy poor (Garber 1987). Although the female did not eat any energy-rich plant food until dawn, we cannot discard the possibility that she ingested other foods after the researchers left the site. Although the proximate motivation for eating the umbilical cord must be rupturing the tie between mother and infant, our data do not allow assessing the potential roles of placentophagy reviewed by Kristal et al. (2012). While the known indifferent behavior of group mates towards birth delivery (Dias 2005; Camargo and Ferrari 2007; Peker et al. 2009) may increase the survival of howler infants by reducing the risk of intragroup conflict and aggression, it is unlikely that it benefits birthing females and newborns with increased vigilance against predators as proposed for the highly terrestrial Japanese macaque (Macaca fuscata; Turner et al. 2010). However, it is not possible to rule out the hypothesis that the diurnal birth reported here represents an antipredator strategy, as proposed by these authors. Although the study site is a small and disturbed fragment, O.M.C. recorded individual
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Leopardus sp. (a potential predator; Miranda et al. 2005; Bianchi and Mendes 2007) resting in trees near the core area of the study group on three occasions in 2012 and 2013. Additionally, according to Cristo´bal-Azkarate et al. (2015), most predators of howler monkeys are nocturnal. On the other hand, the height and location of the female at the periphery of the canopy during the delivery could have exposed her and her newborn to birds of prey. Finally, the serious injury found in the infant’s forehead and face 1 month after his birth is compatible with marks made by howler monkey canines. This resemblance suggests that this was a case of attempted infanticide instead of a case of fall or unsuccessful predation. If this is true, the lack of information on the relatedness among group members and the identity of the aggressor compromise our ability to evaluate the hypotheses proposed to explain this behavior. Although we did not know when and how the infant was injured, the observation of agonistic behaviors from the resident adult and subadult males towards the infant’s mother on the day when the wound was detected suggests that one of them may have been the aggressor. The occurrence of allomaternal care by the other adult female is compatible with observations on Alouatta caraya particularly at the end and after the first month of an infant’s life (Calegaro-Marques and Bicca-Marques 1993). The hypothesis of within-group male aggression towards the infant remains valid in light of the lack of adult male turnovers and the absence of extragroup solitary males at the study site during the entire period of monitoring of this group (July 2011–June 2014). Considering the absence of adult mating competitors to the single resident adult male, it is unlikely that the tenured male would injure his own offspring (see van Schaik 2000; Aguiar et al. 2005), unless the attack on the infant was a by-product of a raised level of aggressiveness triggered by local circumstances, such as human intervention (Sussman et al. 1995; Aguiar et al. 2005). Although the full habituation of the study group to researchers weakens this hypothesis, we cannot reject the possibility that human activities developed near or within the fragment cause increases in the stress level of howler monkeys, thereby keeping the hypothesis viable. This explanation applies to both the adult and the subadult male. The latter might also attack the infant as a consequence of two nonmutually exclusive motivations, namely gaining sexual access to the female and eliminating a potential resource competitor (Agoramoorthy and Rudran 1995; van Schaik 2000; Van Belle and Bicca-Marques 2015). The lack of any sign of aggression towards the older, more independent, but still lactating four-month infant female, would not weaken these hypotheses if the subadult male is her brother. Acknowledgments We thank E.G. Fernandes, E.F. Vianna, D. Camaratta, and E. Chassot for their hospitality, collaboration, and
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Primates (2015) 56:119–125 logistical support during fieldwork. We also thank F. Sehn, H.M. Prates, S.F. Castro, M. Fiedler, P.D.S. Santos, and P.B.E. Silva for field assistance. We thank the Brazilian Higher Education Authority (CAPES) for supporting V.M. (PhD fellowship, #11189/13-4) and O.M.C. (PNPD postdoctoral fellowship, #2755/2010), the Irma˜o Jose´ Ota˜o Foundation/PUCRS for supporting M.B.N. (undergraduate fellowship), and the Brazilian National Research Council (CNPq) for supporting J.C.B.-M. (research fellowships, #303154/2009-8 and 303306/2013-0).
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125 spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. Am J Primatol 74:990–997 Ruiz WIT, Diaz DMV, Amasifuen CF, Heymann EW (2004) Diurnal birth of a wild red titi monkey, Callicebus cupreus, at the Estacio´n Biolo´gica Quebrada Blanco. Neotrop Primates 12:15–16 Sekulic R (1982) Birth in free-ranging howler monkeys Alouatta seniculus. Primates 23:580–582 Sussman RW, Cheverud JM, Bartlett TQ (1995) Infant killing as an evolutionary strategy: reality or myth? Evol Anthropol 3:311–314 Takahata Y, Koyama N, Miyamoto N, Okamoto M (2001) Daytime deliveries observed for the ring-tailed lemurs of the Berenty Reserve, Madagascar. Primates 42:267–271 Turner SE, Fedigan LM, Nakamichi M, Matthews HD, McKenna K, Nobuhara H, Nobuhara T, Shimizu K (2010) Birth in freeranging Macaca fuscata. Int J Primatol 31:15–37 Van Belle S, Bicca-Marques JC (2015) Insights into reproductive strategies and sexual selection in howler monkeys. In: Kowalewski MM, Garber PA, Corte´s-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology, and conservation. Springer, New York, pp 57–84 Van Belle S, Kulp AE, Thiessen-Bock R, Garcia M, Estrada A (2010) Observed infanticide following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Primates 51:279–284 van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60 Windfelder TL (2000) Observations on the birth and subsequent care of twin offspring by a lone pair of wild emperor tamarins (Saguinus imperator). Am J Primatol 52:107–113 Yao M, Yin L, Zhang L, Liu L, Qin D, Pan W (2012) Parturitions in wild white-headed langurs (Trachypithecus leucocephalus) in the Nongguan Hills, China. Int J Primatol 33:888–904 Zunino GE, Chalukian SC, Rumiz DI (1985) Infanticidio y desaparicio´n de infantes asociados al reemplazo de macho en grupos de Alouatta caraya. In: Mello MT (ed) A primatologia no Brasil, vol 2. Sociedade Brasileira de Primatologia, Brası´lia, pp 185–190
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NEWS AND PERSPECTIVES
Parturition and potential infanticide in free-ranging Alouatta guariba clamitans ´ scar M. Chaves • Valeska Martins • O Mariana Beal Neves • Ju´lio Ce´sar Bicca-Marques
Received: 17 December 2014 / Accepted: 18 February 2015 / Published online: 5 March 2015 Ó Japan Monkey Centre and Springer Japan 2015
Abstract Parturition is a key process of mammalian reproduction that is rarely documented in New World monkeys because it often occurs at night. However, diurnal births have been recorded in several species. In howler monkeys (Alouatta spp.) they have often been observed during prolonged resting periods. Similarly, infanticide is a behavior observed quite infrequently. Infanticide in howler monkeys is often inferred from infant deaths or disappearances after group takeovers by nonresident male(s). Here we report the first observation of parturition and birth-related behaviors in the brown howler monkey (Alouatta guariba clamitans) and the likely attack on the infant that caused its death. The mother was a multiparous female that lived in a ca. 3-ha Atlantic forest fragment in southern Brazil with nine group mates. The behavior (‘‘all occurrences’’) sampling method was used to record birth-related behaviors and social interactions. The parturition occurred during the day of 27 October 2013 during a feeding session. The female showed no sign of contraction or birth delivery posture. Parturition began apparently after matrix rupture and release of the amniotic fluid. Expulsion of the
Electronic supplementary material The online version of this article (doi:10.1007/s10329-015-0461-7) contains supplementary material, which is available to authorized users. ´ . M. Chaves M. B. Neves V. Martins O J. C. Bicca-Marques (&) Laborato´rio de Primatologia, Faculdade de Biocieˆncias, Pontifı´cia Universidade Cato´lica do Rio Grande do Sul, Avenida Ipiranga, 6681 Pre´dio 12A, Porto Alegre, RS 90619-900, Brazil e-mail: [email protected] V. Martins Centro de Cieˆncias da Sau´de, Universidade de Cruz Alta, Cruz Alta, RS, Brazil
newborn occurred between 1 and 3 min later (the exact moment of delivery was not observed). Then, the female held and licked the newborn and began to ingest the placenta and the umbilical cord. The other group members continued feeding and had no interaction with the parturient during the preparturition and parturition events. The infant died ca. 35 days later as a consequence of injuries to his forehead and face, potentially caused by a conspecific bite. Because the adult and subadult males chased the female in the day that the infant’s wounds were detected, we believe that one of them might have been the aggressor. We discuss this putative case of infanticide in light of the potential motivation of each male. Keywords Aggression Brown howler monkey Daytime birth Males Southern Brazil Wild birth
Introduction Mammalian reproduction involves the processes of finding a mate, courtship, mating, birth delivery, nursing, weaning, and infant care among others. Whereas behaviors associated with some of these processes are frequently observed in the wild as they are conspicuous, long-lasting, and occur during the species’ active period, others are rarely observed as they are more discrete, short-lasting, and/or occur at night or apart from the rest of the group. Parturition in primates fits best the latter category because it often occurs at night (Jolly 1972; Honnebier and Nathanielsz 1994; Bernis and Varea 2012) and/or takes place in locations where observers do not have an adequate view, such as in arboreal species (Dias 2005). However, diurnal births have been recorded among wild prosimians (Lemur catta:
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Takahata et al. 2001), Old World monkeys (Erythrocebus patas: Chism et al. 1983; Papio cynocephalus: Condit and Smith 1994; Rhinopithecus bieti: Ding et al. 2013), New World monkeys (Alouatta arctoidea: Sekulic 1982; A. caraya: Peker et al. 2009; Callicebus cupreus: Ruiz et al. 2004; Callicebus oenanthe: DeLuycker 2014; Saguinus imperator: Windfelder 2000; Saguinus labiatus: Bezerra and Porter 1999), and apes (Pan troglodytes schweinfurthii: Goodall and Athumani 1980; Pan paniscus: Douglas 2014). The pattern of nocturnal birth has been related to four potential advantages: reduction of the risk of (a) predation (Jolly 1972; Chism et al. 1983), (b) intragroup infanticide (Jolly 1972; Takahata et al. 2001), and (c) newborn fall during group locomotion soon after birth (Jolly 1972), and (d) enhancement of female recovery and infant care (Duboscq et al. 2008). Predation-related hypotheses have also been proposed to explain the occurrence of diurnal births. Dias (2005) and DeLuycker (2014) suggest that the absence of wild predators at their study sites may have released Alouatta palliata and Callicebus oenanthe, respectively, from the potential pressure to give birth at night. On the other hand, Turner et al. (2010) suggest that diurnal births in Macaca fuscata may have evolved as an antipredator strategy because more individuals are vigilant during the day, thereby increasing the likelihood of detecting and evading potential predators. Diurnal births in howler monkeys have often been observed during the prolonged resting periods (e.g., A. arctoidea: Sekulic 1982; A. palliata: Dias 2005; A. belzebul: Camargo and Ferrari 2007; A. caraya: Peker et al. 2009). Sekulic (1982) suggests that diurnal births during resting may allow female howlers to obtain similar advantages to parturition during the night because this may presumably favor both the recovery of the birthing female and the maternal care of the newborn. Overall, delivery time in howler monkeys may vary from \1 min (A. arctoidea: Sekulic 1982) up to 7 min (A. caraya: Peker et al. 2009) as a consequence of individual female differences or maternal experience (e.g., multiparous females tend to show shorter delivery times; Nisbett and Glander 1996; Camargo and Ferrari 2007; see also Yao et al. 2012). Like other mammals, including primates, female howler monkeys often ingest the placenta after the birth delivery (Peker et al. 2009; Douglas 2014). However, placentophagy is not universal among primates (e.g., Callicebus oenanthe: DeLuycker 2014). The adaptive significance of this behavior remains underexplored. It has been related to a reduction in the release of placenta odors that may attract predators or to a potential analgesic effect on the birthing female among other hypotheses (for a review, see Kristal et al. 2012). According to Kristal (1980;
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Kristal et al. 2012), placenta consumption is not related to nutrient replacement. Unlike some Old World monkeys (Ding et al. 2013; Pan et al. 2014) and apes (Douglas 2014), howler monkey group mates often show little or no interest in the delivery and the newborn (Moreno et al. 1991; Nisbett and Glander 1996; Camargo and Ferrari 2007). Exceptions to this pattern were reported by Sekulic (1982) and Dias (2005). Dias (2005) reported that two male, two female, and one juvenile mantled howler monkeys (A. palliata) approached the mother and inspected the newborn, whereas Sekulic (1982) reported only two adult male red howlers (A. arctoidea) showing interest in the new group member. In the latter case, the newborn was killed in the day following its birth. Infant killing, or infanticide, was observed 17 times in howler monkeys (for a review, see Van Belle and BiccaMarques 2015). These events were distributed in five species (A. palliata: Clarke 1983; A. caraya: Zunino et al. 1985; A. arctoidea: Agoramoorthy and Rudran 1995; A. pigra: Van Belle et al. 2010; A. seniculus: Beltra´n and Stevenson 2012). For A. guariba clamitans there is only a single inferred case (Galetti 1994). Three major hypotheses have been proposed to explain the killing of dependent infants: sexual selection (van Schaik 2000; Van Belle and Bicca-Marques 2015), resource competition (Agoramoorthy and Rudran 1995; Rimbach et al. 2012), and social pathology (Sussman et al. 1995; Aguiar et al. 2005). Here we report the first observation of parturition and birth-related behaviors in a wild group of brown howler monkeys (Alouatta guariba clamitans) and the potential infanticide of the infant male about 1 month after its birth. We describe the context in which the parturition took place, the behavior of the parturient female and her group mates before, during, and after the parturition, and the behavior of the infant, and discuss the potential causes and motivations leading to its death.
Methods The parturition was observed on 27 October 2013 by V.M. and M.B.N. during a 3-day monthly following of a brown howler monkey group. The group inhabits a 2.9-ha semideciduous seasonal forest fragment in Parque Sa˜o Paulo Village (30°120 2800 S, 51°050 5300 W, 35 m asl), a rural community in Porto Alegre, state of Rio Grande do Sul, Brazil. The fragment is surrounded by dwellings and is highly disturbed by human activities, including deforestation, selective logging, and dumping. The fragment is immersed in a matrix of agricultural lands, pastures, and human settlements, and is isolated from other forest remnants by C77 m. The study site is inhabited by a single group of
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Table 1 Birth phases and the time and duration of occurrence of key events Birth phase
Hour
Duration
Behavioral observations
Prepartum Labor
14:15
Unknown
No signs of contraction or birth delivery-related postures are observed
*14:33
1–3 min
The exact moment of delivery was not observed
Placenta expulsion
*14:33
Unknown
The exact moment of placenta expulsion was not observed
Placenta consumption
14:48
2 min
Female ingests placenta
15:03
2 min
Female resumes ingesting placenta
Parturition Postpartum
Consumption of umbilical cord
15:05
1 min
Female ingests umbilical cord
15:14
1 min
Female resumes ingesting umbilical cord
1st displacement
15:13
1 min
Female moves 7 m to a Ficus luschnathiana tree, carrying the newborn
1st feeding bout
16:30
3 min
Female eats young leaves of the vine Cuspidaria convoluta
howlers. Nearby fragments are also inhabited by howler groups. The study group was composed of nine individuals: one adult male, two adult females, one subadult male, one subadult female, three juvenile males, and one infant female. This group was followed bimonthly by O.M.C. from July 2011 to June 2014 and monthly by V.M. from January 2013 to January 2014. The adult female, whose parturition we report here, had given birth twice since July 2011. We used the behavior sampling method (‘‘all occurrences’’; Martin and Bateson 2007) to record the behaviors of the mother, infant, and the other group members during the delivery and the next 3.5 h until dusk, when the group stopped their activities at a sleeping site. The same method was used to record social interactions during the next month’s monitoring period following the birth delivery (V.M.: 29 November–1 December; O.M.C.: 4–10 December 2013). We also video-recorded most of the parturition with a digital camera (NikonÒ Coolpix P510).
Results
14:30–14:37
14:37–14:43
14:43–14:48
The delivery occurred on 27 October 2013 when the study group (including the pregnant female) was feeding on mature leaves of a Ceiba speciosa (Malvaceae) tree at the edge of the fragment. The events of the parturition are described in chronological order below and summarized in Table 1: 14:15
Pregnant female is feeding with her group mates at about 20 m height on the top of the C. speciosa tree and at 2 m from her nearest neighbor. No signs of contraction or birth delivery-related postures are observed (this lack of signs compromised the recording of the beginning of the predelivery phase and its total duration).
14:48–15:05
The parturition begins apparently after matrix rupture and release of the amniotic fluid. The newborn male is expulsed between 1 and 3 min later (the exact moment of delivery was not observed). The adult female holds and licks the infant immediately after birth in a hunched posture. The placenta and umbilical cord remain attached to a 3-cm-thick branch, probably limiting the infant’s capacity to move (Online Resource 1). No individual shows any interest in or approaches the birthing female and her newborn. While the other group members move to nearby trees during the postdelivery phase, the parturient female remains at the same location trying to move (14 times) with her infant held on her belly. She cannot move because she is united to the infant by the umbilical cord that is still tied to the branch (Online Resource 1). The infant releases himself from his mother, grabs a branch with his tail, and vocalizes. Then, because he is still tied to the branch by the umbilical cord, the mother tries unsuccessfully to liberate him during 5 min. First, she tries to release him by pulling his arms. Then, she inspects the branch, looks under the newborn, and pulls him several times while turning him to the sides. The female eats part of the placenta during 2 min before licking the infant’s body. She then embraces him from 14:54 to 15:03. She resumes eating the placenta until full ingestion from 15:03 to 15:05 (Fig. 1a, Online Resource 1).
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15:05–15:13
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She pulls the newborn with both hands, but cannot release him because the umbilical cord is still tied to the branch. Then, she eats a portion of the umbilical cord during 1 min before holding the infant near her belly until he frees himself from the branch at 15:13. The female moves about 7 m with the infant grabbing her belly with his hands only, free feet, and with his back in contact with her belly (an unconventional posture). She moves until reaching a fig tree (Ficus luschnathiana, Moraceae), where she continues eating the remaining ca. 10 cm of the umbilical cord (Fig. 1b, Online Resource 1). After ingesting the umbilical cord, she rests during 17 min in a hunched posture with the infant attached to her ventral area. During this time it was not possible to determine whether she was breastfeeding him or not because of poor visibility. The female travels about 140 m with the infant grabbing her ventral area until arriving to the crown of another fig tree (Ficus cestrifolia). She joins the other group members. She eats young leaves of the vine Cuspidaria convoluta (Bignoniaceae) during 3 min and rests again for 42 min. The female travels away from the rest of the group for about 108 m until reaching a sleeping site at a plantation of the alien Pinus taeda (Pinaceae). She rests and remains isolated with her newborn until dawn, when the observers leave the site.
Fig. 1 Post-birth delivery behaviors of the female brown howler monkey. a Ingestion of the placenta. b Ingestion of the umbilical cord (photos by V.M.) (color figure online)
Throughout the events described above, no group member interacted with the female or manifested interest in the newborn. The infant male was gray and appeared to be in good health with enough vigor to cling to his mother. On the first day of the next monthly monitoring period by V.M., 29 November, all group members were behaving as usual and no agonistic interaction was observed. The now hairier infant remained apparently healthy (Fig. 2a). He was frequently seen exploring the environment around his mother. However, at 06:45 on 30 November the adult and subadult males suddenly attacked the female during a feeding session on mature fruit of Campomanesia xanthocarpa (Myrtaceae). They chased her while howling, and she fled carrying the infant on her back. About 2 h later, at 08:48, a severe injury was seen in the infant’s forehead, including a
large hole (ca. 2 cm in diameter) in the skull exposing part of the brain (Fig. 2b, c). It is likely that this wound was made on the previous day because the infant’s face was considerably swollen. The size, shape, and distance of the holes appear to be compatible with marks made by howler monkey canines. At 10:58, the female was attacked again by the adult male. She emitted a stress scream and ran, leaving the infant with the other adult female. As soon as she escaped, she retrieved the infant. The female remained away from other group members with the infant on her belly from 11:00 to 17:45, when the researchers left the site. The mother remained isolated from most group members from 06:00 to 18:45 on 1 December. During this time she only allowed the two other females to get closer to her
15:13–15:15
15:15–15:35
15:35–15:44
16:02–16:30 16:30–17:15
17:15
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Aggressions to the female stopped after the death of the infant and did not resume until the end of the study. Discussion
Fig. 2 Infant brown howler monkey a at the age of 27 days, b with severe injury in the forehead with the brain exposed at the age of 34 days, and c with the brain exposed and the face swollen at the age of 35 days (photos by V.M.) (color figure online)
and her infant. The infant was alive, but he could not open his eyes because his face was extremely swollen (Fig. 2c). O.M.C. did not see the infant from 07:00 to 18:45 on 4 December. The infant’s highly decomposed carcass was found by V.M. on 14 December lying on the forest floor near the sleeping tree used by the group on 1 December.
We report a daytime parturition in Alouatta guariba clamitans that took place during a feeding session. No sign of contraction was detected in the multiparous birthing female, and expulsion of the newborn male lasted between 1 and 3 min. Soon after the delivery the mother ate the placenta and umbilical cord. The female remained alone during the entire process, as no group member showed interest in the parturition or newborn. Finally, 1 month after the parturition, we detected a serious injury in the infant’s forehead after the nursing female being chased more than once by the group’s adult and subadult males. This injury caused his death soon after. Unlike previous observations on daytime parturition in Alouatta spp. (Sekulic 1982; Dias 2005; Peker et al. 2009), the birth reported here did not occur during a period of inactivity. It is possible that this was enabled by the multiparous condition of the mother. For instance, Yao et al. (2012) reported that experienced white-headed langur (Trachypithecus leucocephalus) females can minimize the energetic costs of birth with a rapid and efficient delivery process. On the other hand, the observations of placentophagy and quick return to feeding activities after the parturition are in accordance with reports by Peker et al. (2009) and Dias (2005). However, energy recovery, as proposed by Peker et al. (2009) for A. caraya, is an unlikely explanation for the first feeding bout after the parturition because the female ate young leaves, a resource that is often energy poor (Garber 1987). Although the female did not eat any energy-rich plant food until dawn, we cannot discard the possibility that she ingested other foods after the researchers left the site. Although the proximate motivation for eating the umbilical cord must be rupturing the tie between mother and infant, our data do not allow assessing the potential roles of placentophagy reviewed by Kristal et al. (2012). While the known indifferent behavior of group mates towards birth delivery (Dias 2005; Camargo and Ferrari 2007; Peker et al. 2009) may increase the survival of howler infants by reducing the risk of intragroup conflict and aggression, it is unlikely that it benefits birthing females and newborns with increased vigilance against predators as proposed for the highly terrestrial Japanese macaque (Macaca fuscata; Turner et al. 2010). However, it is not possible to rule out the hypothesis that the diurnal birth reported here represents an antipredator strategy, as proposed by these authors. Although the study site is a small and disturbed fragment, O.M.C. recorded individual
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Leopardus sp. (a potential predator; Miranda et al. 2005; Bianchi and Mendes 2007) resting in trees near the core area of the study group on three occasions in 2012 and 2013. Additionally, according to Cristo´bal-Azkarate et al. (2015), most predators of howler monkeys are nocturnal. On the other hand, the height and location of the female at the periphery of the canopy during the delivery could have exposed her and her newborn to birds of prey. Finally, the serious injury found in the infant’s forehead and face 1 month after his birth is compatible with marks made by howler monkey canines. This resemblance suggests that this was a case of attempted infanticide instead of a case of fall or unsuccessful predation. If this is true, the lack of information on the relatedness among group members and the identity of the aggressor compromise our ability to evaluate the hypotheses proposed to explain this behavior. Although we did not know when and how the infant was injured, the observation of agonistic behaviors from the resident adult and subadult males towards the infant’s mother on the day when the wound was detected suggests that one of them may have been the aggressor. The occurrence of allomaternal care by the other adult female is compatible with observations on Alouatta caraya particularly at the end and after the first month of an infant’s life (Calegaro-Marques and Bicca-Marques 1993). The hypothesis of within-group male aggression towards the infant remains valid in light of the lack of adult male turnovers and the absence of extragroup solitary males at the study site during the entire period of monitoring of this group (July 2011–June 2014). Considering the absence of adult mating competitors to the single resident adult male, it is unlikely that the tenured male would injure his own offspring (see van Schaik 2000; Aguiar et al. 2005), unless the attack on the infant was a by-product of a raised level of aggressiveness triggered by local circumstances, such as human intervention (Sussman et al. 1995; Aguiar et al. 2005). Although the full habituation of the study group to researchers weakens this hypothesis, we cannot reject the possibility that human activities developed near or within the fragment cause increases in the stress level of howler monkeys, thereby keeping the hypothesis viable. This explanation applies to both the adult and the subadult male. The latter might also attack the infant as a consequence of two nonmutually exclusive motivations, namely gaining sexual access to the female and eliminating a potential resource competitor (Agoramoorthy and Rudran 1995; van Schaik 2000; Van Belle and Bicca-Marques 2015). The lack of any sign of aggression towards the older, more independent, but still lactating four-month infant female, would not weaken these hypotheses if the subadult male is her brother. Acknowledgments We thank E.G. Fernandes, E.F. Vianna, D. Camaratta, and E. Chassot for their hospitality, collaboration, and
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