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1 December 2011 Extragroup Copulations in Alouatta Guariba Clamitans
Karine Galisteo Diemer Lopes, Júlio César Bicca-Marques
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Howler monkeys often live in unimale-multifemale or multimale-multifemale cohesive groups in which the alpha male may monopolize estrus females, although females may mate promiscuously with subordinate and extragroup males (Kowalewski and Garber, 2010; Di Fiore et al., 2011). Extragroup copulations (EGCs) have been reported for A. arctoidea (Agoramoorthy and Hsu, 2000), A. caraya (Kowalewski and Garber, 2010), A. guariba clamitans (Fialho and Setz, 2007), A. palliata (Glander, 1992), and A. pigra (Van Belle et al., 2008). EGCs in Alouatta spp. have been related to a female strategy to increase paternity confusion (both inside and outside the group) and decrease the risk of infanticide following alpha male takeover (Kowalewski and Garber, 2010) and to female choice of higher quality or unfamiliar males (Fialho and Setz, 2007). Considering that fertility and compatibility may vary among males, EGCs may also maximize the reproductive success of promiscuous females (Reeder, 2003). These hypotheses are not mutually exclusive.

Here we report seven EGCs between an adult male brown howler monkey (Alouatta guariba clamitans) from a group monitored from dawn to dusk during 26 days from January to July 2011 in a ca. 1-ha forest fragment (30°19′57″S, 51°00′47″W; ca. 45 m a.n.s.l.) in Itapuã District, Viamão, state of Rio Grande do Sul, Brazil, with an adult female from a neighboring group. In January, our study group was composed of six individuals: an adult male (Jorge), two adult females, one juvenile, and two infants. An adult female died electrocuted in a power line in March. In May, a birth increased group size to six individuals again. Also, the juvenile was classified as subadult and the infants as juveniles beginning this month. The neighboring group was composed of, at least, four individuals, including two adult males, an adult female (Jane), and a subadult male. We have no information about the degree of relatedness between individuals both within and between groups. The forest fragments that they inhabited are separated by a 20 m-wide dirty road.

Intergroup interactions were witnessed between April and July. These are described in chronological order below.

When Jorge reached the canopy, the neighboring adult males chased him back to the post. Jorge rubbed his chin at the post and was supplanted by a male. Then, the male also rubbed his chin in the same place, while Jorge observed him from the electric wire. When the adult male left the pole and returned to a place behind Jane in the canopy, Jorge attempted to approach her again and was once more chased by her male mates. Finally, Jorge went back to the other side of the road and his group left the border of the fragment.

June 22nd: At noon, all members of the study group ran to a strip of forest near the road. At 12:15, Jorge and the three males were howling at their home range borders. Jorge moved to the electric post at the other side using the cables and came back without trying to get closer to Jane. At 13:00, Jane crossed the road using the cable. Jorge unsuccessfully attempted to mate with her on the cable and they almost fell to the ground. After that, the couple moved to an electric post and mated. Jorge's group was resting in a nearby tree. There was no attempt of copulation interruption by his group's adult female or her adult male group mates, who remained at the other side of the road. At 13:15, the couple mated again and Jane returned to her group. Jorge vocalized while she crossed the road via the cable.

July 19th: Jorge, the adult female, and the subadult vocalized at 16:15 when Jane arrived at the border of her home range. She crossed the road as usual at 16:30, reaching a tree within the home range of Jorge's group. The couple mated four times near his group while her male group members howled at the other side of the road. At 16:45, Jorge began to slowly moving away from the border of the road, only stopping to rub his chin on tree trunks. He was followed by Jane. An adult male from Jane's group (apparently slightly larger than Jorge) also crossed the road using the electric cable, reaching the trees. The last EGC was recorded at 17:15. After that, Jane returned to her home range, whereas Jorge remained with his group. We don't know whether the adult male from Jane's group left the area prior or together with her.

In sum, both Jorge and Jane sought EGCs, but only her attempts were successful. When Jorge moved to her home range, he was chased away by her adult male group mates. On the other hand, his adult female group mate appeared to ignore his sexual interactions with Jane. We have no data on the occurrence and frequency of EGCs during the days we were not monitoring our study group and whether Jane mated within her group during our study. We also do not know whether Jane got pregnant as a result of these EGCs because our study ended only five weeks after the record of the first event. Therefore, our data do not allow excluding any of the aforementioned hypotheses for explaining the EGCs between Jorge and Jane. This was the second report on EGC in Alouatta guariba clamitans.


We thank Silvia Beatriz Saint-Martin Ribeiro, Vera Lúcia dos Santos, Celso dos Santos, and Mr. Ari for logistical support, and Jonas da Rosa Gonçalves for helping in the field at the beginning of the study. This study was approved by the Scientific Committee of the Faculdade de Biociências/Pontifícia Universidade Católica do Rio Grande do Sul (project #3477). KGDL was supported by a FAPERGS PROBIC grant and JCBM by a CNPq PQ-1D grant (# 303154/2009–8).



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Karine Galisteo Diemer Lopes and Júlio César Bicca-Marques "Extragroup Copulations in Alouatta Guariba Clamitans," Neotropical Primates 18(2), 52-53, (1 December 2011).
Published: 1 December 2011
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