Troop takeover is common in one-male primate groups, but there are few reports in multimale groups. Japanese macaques (
Male macaques migrate from their natal groups as they mature, often migrating among nonnatal groups several times during their lives. This behavior may increase the probability of attaining high rank and mating opportunities [
In Japanese macaques, intertroop movement is observed in the mating season. It is common for males to enter troops peacefully (i.e., without aggression), assuming low status in the existing dominance hierarchy [
In this study, our first objective is to describe the general feature of troop takeovers in this population. Previous studies on Japanese macaques showed that nontroop males (NTMs) usually enter troops after most of the troop females have already conceived, suggesting that males might fail to impregnate the females during the mating season [
We also examine predictor variables that may influence the probability of troop takeover (number of troop males, number of troop estrous females, and number of NTMs), using logistic regression analysis. Finally, we examine the reproductive success of takeover males using noninvasive collection of DNA samples, and we compare the reproductive success of takeover males to that of low- and high-ranking resident males.
The study site is located on the western coast of Yakushima Island (30°N, 130°E), Japan. The investigation was conducted on 4 troops, referred to as troops B, NA, E, and Momoe. Habituation and long-term research on these troops began on 1992, 1994, 2003, and 2000, respectively [
This study covers a 6-year period for troop B, 5 years for troop NA, and 1 year for each troops E and Momoe, with some observation gaps in each data set. The study troops were monitored with respect to their membership size at least twice a year, during the mating season (Sep–Jan) and the nonmating season (Feb–Aug). During the mating season, observations are focused on the mating behavior of the members and on monitoring the NTMs. Behavioral sampling procedures varied over the period and troops
Troop males are defined as males that have been observed in the troop from the previous nonmating season, and NTMs are defined as males that did not belong to the target troop in the previous nonmating season and first interacted with the troop after the onset of a mating season [
In this research, we defined troop takeover as those cases in which males (1) visited the troop over a minimum of 20 days continuously or intermittently, (2) showed aggressive behaviors, such as branch shaking with vocalizations, staring at or chasing group males, and mounting group members in the center of the group, and (3) received submissive behaviors from the majority of troop males, including the alpha male.
Paternity data on this population has been reported previously [
Genomic DNA was extracted using a QIAmp DNA stool kit and QIAmp DNA mini kit (Qiagen, Chatsworth, Calif) in accordance with the manufacturer’s instructions. DNA from single shed hairs was extracted using an ISOHAIR kit (Nippon gene). Semen and tissue samples were cut into small pieces and combined with 250
Eight microsatellite loci were used in the PCR (D5S1470, D1S533, D12S67, D6S493, D5S820, D6S501, D19S582, and D10S611). The calculated and observed heterozygosities of 8 microsatellite loci are shown in Table
Characterization of 8 microsatellite loci.
Locus | Allele | N | H (obs) | H (exp) | HW |
---|---|---|---|---|---|
D5S1470 | 8 | 94 | 0.787 | 0.717 | NS |
D1S533 | 6 | 105 | 0.733 | 0.73 | NS |
D12S67 | 8 | 109 | 0.734 | 0.755 | NS |
D6S493 | 7 | 108 | 0.731 | 0.687 | NS |
D5S820 | 6 | 104 | 0.76 | 0.752 | NS |
D6S501 | 6 | 101 | 0.743 | 0.752 | NS |
D19S582 | 4 | 106 | 0.726 | 0.738 | NS |
D10S611 | 7 | 103 | 0.738 | 0.698 | NS |
N indicates the number of individuals typed; H (obs) and H (exp) indicate the observed and expected heterozygosities. HW refers to deviation for Hardy-Weinberg equilibrium, and NS stands for nonsignificant.
Comparison of the infant and maternal genotypes allowed for the deduction of the paternal allele(s). Males whose alleles did not match the deduced paternal allele(s) were excluded as paternity candidates. When all candidate fathers except one were excluded, the remaining male was assumed to be the likely father. In cases in which all the candidate males were excluded, it was assumed that the father was probably an NTM whose DNA sample we failed to collect. Furthermore, the parentage likelihood was calculated using the program CERVUS 2.0 (Trisran Marshall, Edinburgh, UK; [
We used binary logistic regression to test troop composition, and the number of NTMs affect the occurrence of troop takeover. The occurrence of takeover (yes/no) was the dependent variable, and the number of NTMs, troop males, and estrous females were independent variables. To detect multicollinearity between the independent variables, diagnostic statistics were examined via linear regression analysis. The variance inflation factors (VIF) determined were 1.818 (NTMs), 5.373 (troop males), and 4.638 (females). Values exceeding 10 are often considered to indicate multicollinearity. Based on our results, we concluded that there was no multicollinearity between the independent variables.
We also used binary logistic regression to test between the category of candidate fathers and the success of infant siring (yes/no). The infant siring (yes/no) was the dependent variable, and the category of candidate fathers (higher-ranking troop males, lower-ranking troop males and takeover males) and the number of infants born were independent variables.
All observed troop takeovers on Yakushima Island (
The composition of the target troops.
B troop
Year | Troop takeover | Num of troop males | Num of troop females | Num of NTMs |
---|---|---|---|---|
1996 | Yes | 6 | 7 (4) | 13 |
1997 | No | 7 | 6 (5) | 5 |
1998 | No | 5 | 5 (3) | 0 |
1999 | Yes | 0 | 2 (2) | 4 |
2000 | Yes | 2 | 4 (3) | 4 |
2003 | No | 2 (4)* | 3 (3) | 10 |
*Two males who moved with females in the previous nonmating season were never found in B troop during the mating season; however, they were again found in the troop after the mating season was over.
NA troop
Year | Troop takeover | Number of troop males | Number of troop females | Number of NTMs |
---|---|---|---|---|
1997 | No | 15 | 15 (11) | 0 |
1998 | No | 12 | 13 (6 ) | 0 |
1999 | Yes | 7 | 6 (6) | 11 |
2000 | No | 7 | 7 (4) | 2 |
2003 | Yes | 1 | 5 (4) | 13 |
Momoe troop
Year | Troop takeover | Number of troop males | Number of troop females | Number of NTMs |
---|---|---|---|---|
2003 | Yes | 4 | 6 (6) | 10 |
E troop
Year | Troop takeover | Number of troop males | Number of troop females | Number of NTMs |
---|---|---|---|---|
2003 | Yes | 7 | 8 (8) | 17 |
When NTMs successfully took over a troop and assumed the alpha position, the 7 former alpha males never left the troop during the concurrent mating season. Although 2 of these previous alpha males suffered severe wounds during the mating season (usually the aggressor was unknown), they remained in the troop in the beta or gamma dominance position. During takeover mating seasons, there were few or no unweaned infants, and there was no directly observed infanticide. Circumstantial evidence for infanticide by NTMs was also lacking, as there were no infant disappearances during takeover mating seasons.
Univariate binary logistic regression analyses revealed that the number of NTMs significantly predicted the occurrence of troop takeover but that the number of troop males and the number of estrous females did not (Table
Contribution of the variables (B), standard error (SE), and significance (P) of binary logistic regression model concerning the occurrence of troop takeover.
Independent variable | B | SE | P | |
---|---|---|---|---|
Univariate analyses | ||||
Number of NTMs | 0.356 | 0.178 | 0.045* | |
Number of troop males | −0.335 | 0.217 | 0.124 | |
Number of estrus females | −0.113 | 0.242 | 0.640 | |
Bivariate analyses | ||||
NTM | Controlling for: | |||
Troop males | 0.345 | 0.201 | 0.087 | |
Estrous females | 0.386 | 0.206 | 0.061 | |
Troop males | NTMs | −0.372 | 0.321 | 0.248 |
Estrous females | −0.969 | 0.502 | 0.054 | |
Estrous females | NTMs | −0.330 | 0.553 | 0.537 |
Troop males | 1.227 | 0.780 | 0.116 |
*
All males that took over troops appeared when most of the troop females had not yet conceived (Table
Factors associated with troop takeover.
Troop | Year | Male | Date he was first consorting with a troop female | Date the alpha male first showed submissive behavior | Fate of the alpha male | Number of estrous females | Infants born | Infants conceived after his appearance | Number of unweaned infants |
---|---|---|---|---|---|---|---|---|---|
B | 1996 | PE | 17th October | 24th October | Stayed | 4 | 1 | 1 | 2 |
NA | 1999 | BT | No data | No data | Stayed | 6 | 3 | 1 | 0 |
B | 1999 | MS | No data | No data | 2 | 1 | 1 | 0 | |
B | 2000 | AO | No data | No data | Stayed | 3 | 1 | 1 | 0 |
NA | 2003 | MD | 26th October | 4th November | Stayed | 5 | 3 | 2 | 1 |
Momoe | 2003 | TR | 25th October | 5th November | Stayed | 5 | 2 | 1 | 0 |
E | 2003 | MN | 14th October | 15th October | Stayed | 8 | 6 | 5 | 0 |
*All resident males had left the troop before MS appeared in the troop.
Table
Tenure of takeover males in the alpha position.
Troop | Male | Time of appearance | Time of his leaving | Reason he lost his tenure | Tenure as top-dominant male | Number of siring infant |
---|---|---|---|---|---|---|
B | PE | 1996 October | 1996 November | Another takeover | Part of one season | 0 |
B | MR | 1996 October | 1998 August | Presumably died | 2 years | 0 |
NA | BT | 1999 October | 1999 November | He left voluntarily | Part of one season | 0 |
B | MS | 1999 October | 2001 | Another takeover | 1 year* | 0 |
B | AO | 2000 October | 2002 | Another takeover | Part of one season* | 0 |
B | MA | 2000 October | 2002 | Another takeover | 2 years | 1 |
NA | MD | 2003 November | 2004 | ? | 1 year | 1 |
Momoe | TR | 2003 November | 2004 or 2005 | ? | 1 year or 2 years | 0 |
E | MN | 2003 October | Still in the troop in 2009 | Another takeover | 4 years | 2 |
We compared the number of offspring sired by takeover males to that sired by high-ranking and low-ranking troop males (Table
Reproductive success of takeover males.
Year | Troop | Troop takeover | Average number of estrous females per day | Infants born (paternity decided) | Number of male siring offspring | |||
---|---|---|---|---|---|---|---|---|
High-ranking troop malec | Low-ranking troop malec | NTM | Takeover | |||||
1996a | B | Yes | 1.53 | 1 (1) | 0 (2) | 0 (4) | 1 | 0 (2) |
1997a | B | No | 1.73 | 3 (2) | 1 (2) | 0 (5) | 1 | — |
1998a | B | No | No data | 0 | 0 (1) | 0 (4) | 0 | — |
1999a | B | Yes | No data | 1 (1) | — | — | 1 | 0 (1) |
2000a | B | Yes | No data | 1 (1) | 0 (1) | 0 (1) | 0 | 1 (2) |
2003 | B | No | 0.52 | 0 | 0 (1) | 0 (1) | 0 | — |
1997b | NA | No | 2.42 | 11 (9) | 2d (2) | 3 (13) | 3 | — |
1998b | NA | No | 0 | 0 (2) | 0 (10) | 0 | — | |
1999a | NA | Yes | 1.77 | 3 (2) | 0 (2) | 1 (5) | 1 | 0 (1) |
2000a | NA | No | 1.28 | 1 (1) | 0 (2) | 1 (5) | 0 | — |
2003 | NA | Yes | 1.63 | 3 (2) | 1 (1) | 0 (0) | 0 | 1 (1) |
2003 | E | Yes | 2.13 | 6 (5) | 0 (2) | 1 (5) | 2 | 1e (1) |
2003 | Momoe | Yes | 1.39 | 2 (2) | 0 (1) | 2 (3) | 0 | 0 (1) |
Total | 32 (26) | 4 (19) | 9 (56) | 9 | 3 (9) |
aData are from Hayakawa 2008. bData are from Soltis et al., 2000, 2001. cThe number in parenthesis shows the number of candidate fathers. For example, in 1996, the number of high-ranking troop males was two, but the number of high-ranking males successfully siring offspring was zero. dOne of the high ranking male succeeded in siring two offspring. eTake over male succeeded in siring two offspring.
The result is that 3 of the 9 (33.3%) takeover males succeeded in siring infants, while 4 of the 19 (21.1%) high-ranking troop males and 8 of 56 (16.0%) low-ranking troop males did so. Step-wise logistic regression analyses revealed that the factor “Category of candidate fathers” and the factor “Number of infants” are the significant factors predicted sirehood (Table
Contribution of the variables (B), standard error (SE), and significance (P) of binary logistic regression model concerning the success of infant siring.
Independent variables | B | SE | P |
---|---|---|---|
Category of candidate father | .061 | ||
Category of candidate father | |||
(1) | 1.834 | .906 | .043* |
(2) | 0.882 | .760 | .246 |
Number of infants born | .223 | .078 | .004* |
Troop takeover only occurred in the mating season, consistent with the idea that such actions are part of a reproductive strategy. Once appearing in the troop, NTMs rapidly established high rank (Table
A newly dominant male could benefit from committing infanticide when he has not possibly sired the infant and very likely to sire the next. However, the only observed infanticide in this population involved a troop male who recently rose in rank, not a male who took over the troop [
The number of NTMs associating with a troop was the main predictor of troop takeover. This was the case despite the fact that NTMs did not cooperate with each other during takeovers. The number of NTMs may positively influence the probability of takeover because (1) the higher the number of males in the NTM group, the greater the probability that one of them will outrank the alpha male, (2) NTMs may be drawn to groups with relatively weak alpha males, or (3) large groups of NTMs who independently attack the troop may wear down resident males from their repeated efforts, even though only one of them takes over the troop at a time.
Another possibility is that the occurrence of troop takeover itself leads to the increased number of NTMs, because the number of NTMs includes those who visited after the occurrence of troop takeover. When the troop is taken over, it become less cohesive because (1) the takeover male often copulates on the periphery of the troop, perhaps to prevent cooperative aggression by troop males [
Our analysis failed to show that the number of troop males affects the occurrence of troop takeover. However, previous studies indicate that the number of troop males negatively correlates with the number of NTMs on a daily basis [
The result showed that 3 of the 9 (33.3%) takeover males succeeded in siring infants. The logistic regression analyses revealed that takeover males can expect higher reproductive success than males of other categories. But the success rate is smaller compared to that of other species [
Second, takeover males often mate with estrous females in the periphery of the troop [
If a male retains his dominant status for a long period, he could increase the possibility of enjoying high reproductive success, but this was not the case. The main reason that a usurping male loses the top dominance so quickly is another troop takeover (Table
Troop takeover has been observed in several multimale primate groups [
Another remarkable feature of Japanese macaque takeovers is that NTMs do not cooperate. In white-faced capuchins, on the other hand, 4 of 7 (57%) takeovers involved multimale, cooperative invasions. In most of these cases, invaders matched or outnumbered resident males. Larger numbers of cooperating intruders should increase the likelihood of troop takeover, but it also increases within group competition after takeover. Further investigation will be needed to account for the variability in takeover strategies within and across primate species.
The author thanks Drs. Yukimaru Sugiyama, Jyuichi Yamagiwa, Shigeo Uehara, Osamu Takenaka, Michael A. Huffman, and colleagues at the Ecology and Behavior Department for their continuous support of his work and critical comments. Also, he thanks Dr. Shin Nakamura for special technical Support for DNA analysis. Also, he thanks all members of the Yakushima Research Group for their discussions on Yakushima Island and thanks Dr. Elizabeth Nakajima and Dr. Fred B. Bercovitch for correcting his paper. This research was supported by the Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists (No. 9611) and a Grant for Global COE (A6) to Kyoto University from the Ministry of Education, Culture, Sports, Science and Technology of Japan. This study complied with the protocols approved by the Animal Care and Use Guideline of Primate Research Institute, Kyoto University.