From the first intention movement to the last joiner: macaques combine mimetic rules to optimize their collective decisions

Mechanisms related to collective decision making have recently been found in almost all animal reigns from amoebae to worms, insects and vertebrates, including human beings. Decision-making mechanisms related to collective movements-including pre-departure and joining-have already been studied at different steps of the movement process, but these studies were always carried out separately. We therefore have no understanding of how these different processes are related when they underlie the same collective decision-making event. Here, we consider the whole departure process of two groups of Tonkean macaques (Macaca tonkeana), using a stochastic model. When several exclusive choices are proposed, macaques vote and choose the majority. Individuals then join the movement according to a mimetism based on affiliative relationships. The pre-departure quorum and the joining mimetic mechanism are probably linked, but we have not yet identified which transition mechanism is used. This study shows that decision-making related to macaque group movements is governed by a quorum rule combined with a selective mimetism at departure. This is the first time that transition mechanisms have been described in mammals, which consequently helps understand how a voting process leads to social amplification. Our study also provides the first complete proof that there is continuity in the decision-making processes underlying collective movements in mammals from the first intention movement right through to the last joiner.     

The Organization of Collective Group Movements in Wild Barbary Macaques (Macaca sylvanus): Social Structure Drives Processes of Group Coordination in Macaques

Social animals have to coordinate activities and collective movements to benefit from the advantages of group living. Animals in large groups maintain cohesion by self-organization processes whereas in smaller groups consensus decisions can be reached. Where consensus decisions are relevant leadership may emerge. Variation in the organization of collective movements has been linked to variation in female social tolerance among macaque species ranging from despotic to egalitarian. Here we investigated the processes underlying group movements in a wild macaque species characterized by a degree of social tolerance intermediate to previously studied congeneric species. We focused on processes before, during and after the departure of the first individual. To this end, we observed one group of wild Barbary macaques (Macaca sylvanus) in the Middle Atlas, Morocco using all-occurrence behaviour sampling of 199 collective movements. We found that initiators of a collective movement usually chose the direction in which more individuals displayed pre-departure behavior. Dominant individuals contributed to group movements more than subordinates, especially juveniles, measured as frequencies of successful initiations and pre-departure behaviour. Joining was determined by affiliative relationships and the number of individuals that already joined the movement (mimetism). Thus, in our study group partially shared consensus decisions mediated by selective mimetism seemed to be prevalent, overall supporting the suggestion that a species’ social style affects the organization of group movements. As only the most tolerant species show equally shared consensus decisions whereas in others the decision is partially shared with a bias to dominant individuals the type of consensus decisions seems to follow a stepwise relation. Joining order may also follow a stepwise, however opposite, relationship, because dominance only determined joining in highly despotic, but not in intermediate and tolerant species.     

Social Network Influences Decision Making During Collective Movements in Brown Lemurs (<Emphasis Type="Italic">Eulemur fulvus fulvus</Emphasis>)

Many animal species live as a group and must therefore move as such. Several authors have suggested that the mechanisms underlying collective movements in primate species appear to rely on complex cognitive skills, given their high level of cognitive abilities. However, recent studies have highlighted the fact that complex patterns do not necessarily imply complex mechanisms. We used a modeling approach to investigate the patterns of collective movement in a semi-free-ranging group of brown lemurs. We recorded via digital video cameras the order and joining latencies of the 11 individuals of the group during the departure time of spontaneous group movements. We then assessed whether mimetic mechanisms or the existence of a leader were underlying conditions for the joining process by testing 5 computer models relying respectively on 5 hypotheses: the independence of individuals, an anonymous mimetism, a mimetism according to kinship, a mimetism according to affiliation, and eventually the existence of a leader. We found that departure latencies, associations, and the order of individuals at departure time could all be explained by the mimetism according to affiliation model. Thus, an individual’s decision to join the collective movement or not depended on the decision taken by its preferred social partners. These results show the importance of social parameters in primate decision making and that the high cohesion displayed by the group members might not be constrained merely by ecological factors such as predation or foraging consideration.     

Self-Organization in Primates: Understanding the Rules Underlying Collective Movements

Patterns of collective movements, such as the distribution of leadership and the organization of individuals, may be either homogeneously (no leader, no specific order), or heterogeneously (1 or several leaders, and a highly stable order) distributed. Members of a group need to synchronize their activities and coordinate their movements, despite the fact that they differ in physiological or morphological traits. The degree of difference in these traits may affect their decision-making strategy. We demonstrate how a theoretical model based on a variation of a simple mimetic rule, i.e., an amplification process, can result in each of the various collective movement patterns and decision-making strategies observed in primates and other species. We consider cases in which 1) the needs of different individuals are identical and social relationships are equivalent between group members, 2) the needs of individuals are different and social relationships are equivalent, and 3) the needs of individuals are different and social relationships are different. Finally, 4) we assess how the synergy between 2 mimetism rules, specifically the probability of joining a movement and that of canceling an initiation, allows group members to stay synchronized and cohesive. Our models suggest that similar self-organized processes have been selected as reliable and well-adapted means for optimal collective decisions across species, despite differences in their biological and social characteristics.     

Collective decision-making in white-faced capuchin monkeys

In group-living animals, collective movements are a widespread phenomenon and occur through consensus decision. When one animal proposes a direction for group movement, the others decide to follow or not and hence take part in the decision-making process. This paper examines the temporal spread of individual responses after the departure of a first individual (the initiator) in a semi-free ranging group of white-faced capuchins (Cebus capucinus). We analysed 294 start attempts, 111 succeeding and 183 failing. Using a modelling approach, we have demonstrated that consensus decision-making for group movements is based on two complementary phenomena in this species: firstly, the joining together of group members thanks to a mimetic process; and secondly, a modulation of this phenomenon through the propensity of the initiator to give up (i.e. cancellation rate). This cancellation rate seems to be directly dependent upon the number of followers: the greater this number is, the lower the cancellation rate is seen to be. The coupling between joining and cancellation rates leads to a quorum: when three individuals join the initiator, the group collectively moves. If the initiator abandons the movement, this influences the joining behaviour of the other group members, which in return influences the initiator''s behaviour. This study demonstrates the synergy between the initiator''s behaviour and the self-organized mechanisms underlying group movements.     

Reproductive behavior of the Japanese treefrog,Rhacophorus arboreus (Anura: Rhacophoridae)

Reproductive behavior of the foam-nesting treefrog,Rhacophorus arboreus, is described. Oviposition was made either by an amplectant pair (a female, and an amplectant male) alone or by an amplectant pair and other males (joiners). The snout-vent length of males and females was negatively correlated with the date of the first appearance in the pond. The period of staying in the pond in males was longer than that in females. Physical body contacts of other males, and encounter calls by ampletant males were frequently observed before oviposition with joiners. Snout-vent length of the female and an amplectant male were positively correlated. Encounter calls by amplectant males were likely to precede movement of females. There was no difference of snout-vent length between amplectant males and joiners. Females moved the hindlimbs more frequently than males during oviposition. Amplectant males made encounter cells more frequently in oviposition with joiners, than oviposition without joiners. The patterns of transitions between acts of females and amplectant males were similar between oviposition with and without joiners. Females more frequently responded to amplectant males than joiners. Both the duration of a bout of the movements of hindlimbs of females and the interval between the bouts were longer in oviposition without joiners than that with joiners. The number of the movements per bout in oviposition without joiners was smaller than that with joiners. Encounter calls by amplectant males during oviposition tended to precede the hindlimb movements of females.     

Directed assembly of a bacterial quorum

Many reports have elucidated the mechanisms and consequences of bacterial quorum sensing (QS), a molecular communication system by which bacterial cells enumerate their cell density and organize collective behavior. In few cases, however, the numbers of bacteria exhibiting this collective behavior have been reported, either as a number concentration or a fraction of the whole. Not all cells in the population, for example, take on the collective phenotype. Thus, the specific attribution of the postulated benefit can remain obscure. This is partly due to our inability to independently assemble a defined quorum, for natural and most artificial systems the quorum itself is a consequence of the biological context (niche and signaling mechanisms). Here, we describe the intentional assembly of quantized quorums. These are made possible by independently engineering the autoinducer signal transduction cascade of Escherichia coli (E. coli) and the sensitivity of detector cells so that upon encountering a particular autoinducer level, a discretized sub-population of cells emerges with the desired phenotype. In our case, the emergent cells all express an equivalent amount of marker protein, DsRed, as an indicator of a specific QS-mediated activity. The process is robust, as detector cells are engineered to target both large and small quorums. The process takes about 6 h, irrespective of quorum level. We demonstrate sensitive detection of autoinducer-2 (AI-2) as an application stemming from quantized quorums. We then demonstrate sub-population partitioning in that AI-2-secreting cells can ‘call'' groups neighboring cells that ‘travel'' and establish a QS-mediated phenotype upon reaching the new locale.     

Scalable rules for coherent group motion in a gregarious vertebrate

Individuals of gregarious species that initiate collective movement require mechanisms of cohesion in order to maintain advantages of group living. One fundamental question in the study of collective movement is what individual rules are employed when making movement decisions. Previous studies have revealed that group movements often depend on social interactions among individual members and specifically that collective decisions to move often follow a quorum-like response. However, these studies either did not quantify the response function at the individual scale (but rather tested hypotheses based on group-level behaviours), or they used a single group size and did not demonstrate which social stimuli influence the individual decision-making process. One challenge in the study of collective movement has been to discriminate between a common response to an external stimulus and the synchronization of behaviours resulting from social interactions. Here we discriminate between these two mechanisms by triggering the departure of one trained Merino sheep (Ovis aries) from groups containing one, three, five and seven naïve individuals. Each individual was thus exposed to various combinations of already-departed and non-departed individuals, depending on its rank of departure. To investigate which individual mechanisms are involved in maintaining group cohesion under conditions of leadership, we quantified the temporal dynamic of response at the individual scale. We found that individuals'' decisions to move do not follow a quorum response but rather follow a rule based on a double mimetic effect: attraction to already-departed individuals and attraction to non-departed individuals. This rule is shown to be in agreement with an adaptive strategy that is inherently scalable as a function of group size.     

Recognition of social relationships in bridging behavior among Tibetan macaques (Macaca thibetana)

Bridging behavior among male Tibetan macaques (Macaca thibetana) was studied in a free-ranging group at Mt. Huangshan, China. This behavior was defined as a type of affiliative behavior in which two individuals simultaneously lifted up one infant. Bridging behavior occurred after an adult male carried an infant to another male or approached another male who was holding an infant. Each male frequently held and groomed a particular infant in the group, which was named an “affiliated” infant of the male. Males were more frequently provided with their affiliated infant by other males than with other non-affiliated infants. This finding suggests that male Tibetan macaques recognized the affiliative relationship between a male and his affiliated infant, and chose that infant for bridging behavior on the basis of this knowledge. Such choice might be important for effective bridging behavior or other affiliative interactions between males. © 1995 Wiley-Liss, Inc.     

Development of eighteen tetranucleotide microsatellite markers in Tibetan Macaque (Macaca thibetana) and genetic diversity analysis of captive population

In this study, eighteen tetranucleotide microsatellite loci were isolated from AAAG-enriched and GATA-enriched libraries of the Tibetan macaque, Macaca thibetana. These loci were tested on 53 individuals of M. thibetana, and most loci were proved to be highly polymorphic. A total of 109 alleles were detected with an average of 6.06 alleles per locus. The PIC values of these loci ranged from 0.192 to 0.879, with an average of 0.624. The observed and expected heterozygosities ranged from 0.170 to 0.800 and from 0.217 to 0.898, with an average of 0.583 and 0.675, respectively. 5 loci significantly deviated from Hardy–Weinberg equilibrium (HWE). Significant linkage disequilibrium (LD) was found between 9 pairs of loci. The newly identified polymorphic markers would facilitate the study of M. thibetana on the population structure and genetic diversity.     

The stumptail macaques of China

The stumptail macaque species Macaca thibetana and Macaca arctoides replace one another from north to south in subtropical and tropical China. These species differ in external and cranial characters. Neonatal pelage color is pale grayish-brown in M. thibetana and whitish in M. arctoides. In adults, ventral pelage is whitish in M. thibetana and brown in M. arctoides. The forehead and cheeks are thickly furred in adult M. thibetana and bald in M. arctoides. Facial skin color typically is sexually dimorphic in M. thibetana—buffy in males and reddish in females—and monomorphic in M. arctoides—reddish in both sexes. Head and body length, weight, relative tail length, and relative ear length all tend to average greater in M. thibetana than in M. arctoides. Skull length, rostral-postrostral ratio, and relative canine length in males average greater in M. thibetana. than in M. arctoides; relative zygomatic breadth and relative bimalar breadth average greater in M. arctoides than in M. thibetana. Reproductive anatomy in both sexes is strikingly divergent in these two species. Although these species are adapted to different climatic zones, many aspects of their natural history are generally similar, as far as is now known. One apparent behavioral difference is that M. thibetana usually sleeps in caves or rocky crevices, while M. arctoides usually sleeps in trees.     

Southward extension of the range ofmacaca thibetana

Based on results of recent fieldwork, the known geographic range of Macaca thibetanais extended approximately 55 km southward, to 23°48’N, in Jinxiu County, Guangxi Province, China.     

Co-evolutionary Dynamics of Collective Action with Signaling for a Quorum

Collective signaling for a quorum is found in a wide range of organisms that face collective action problems whose successful solution requires the participation of some quorum of the individuals present. These range from humans, to social insects, to bacteria. The mechanisms involved, the quorum required, and the size of the group may vary. Here we address the general question of the evolution of collective signaling at a high level of abstraction. We investigate the evolutionary dynamics of a population engaging in a signaling N-person game theoretic model. Parameter settings allow for loners and cheaters, and for costly or costless signals. We find a rich dynamics, showing how natural selection, operating on a population of individuals endowed with the simplest strategies, is able to evolve a costly signaling system that allows individuals to respond appropriately to different states of Nature. Signaling robustly promotes cooperative collective action, in particular when coordinated action is most needed and difficult to achieve. Two different signaling systems may emerge depending on Nature’s most prevalent states.     

Behavioral mechanisms of collective nest-site choice by the ant Temnothorax curvispinosus

This paper examines the individual behavior underlying collective choice among nest sites by the ant Temnothorax (formerly Leptothorax) curvispinosus. Colonies can actively compare options, rejecting a mediocre site when it is paired with a good one, but accepting the same mediocre design if it is instead paired with a worse site. This ability emerges from the behavior of an active minority of workers who organize emigrations. When one of these finds a promising site, she recruits nest mates to it, but only after a delay that varies inversely with site quality. Ants first recruit fellow active ants via slow tandem runs, but eventually switch to speedier transports of the colony’s passive majority. Later transports grow faster still, as ants improve their speed with experience. An ant’s choice of recruitment type is governed by a quorum rule, such that her likelihood of starting to transport increases with the population of the new site. The size of the quorum depends on experience, with ants demanding a larger population to launch immediately into transport than they do to switch to transport after first leading a few tandem runs. Perception of quorum attainment requires direct contact between ants. The ants’ behavior qualitatively matches that of T. albipennis, where models have shown that decentralized choice of the best site depends on quality-dependent recruitment delays, amplified by a quorum rule for initiating transport. Parameter estimates for an agent-based model show significant quantitative differences between the species, and suggest that T. albipennis may place relatively greater emphasis on emigration speed. Received 11 February 2005; revised 10 May 2005; accepted 20 May 2005.     

Reappraisal of <Emphasis Type="Italic">Macaca speciosa subfossilis</Emphasis> from the Late Pleistocene of Northern Vietnam Based on the Analysis of Cranial Anatomy

Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) described Macaca speciosa subfossilis on the basis of her study of the external anatomy of a nearly complete cranium (PV F1; Muséum national d’Histoire naturelle, Paris) found in the Late Pleistocene cave deposits, Thung-Lang, northern Vietnam. Whereas Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) considered it to belong to an ancestor of Macaca arctoides or M. thibetana, Fooden (Journal of Human Evolution 19:607–686, 1990) reexamined the facial anatomy and assigned it to the extant species M. arctoides. We used computed tomography images to reevaluate the phylogenetic position of Macaca speciosa subfossilis by comparing the external and internal features of PV F1 with those of the crania of the extant macaque species. PV F1 shows a lower degree of preorbital concavity than Macaca arctoides, M. assamensis, and M. thibetana, but shares an anteriorly directed malar as seen in the crania of the two former species. The size of the molars of PV F1 falls within a range such that the cranium may be assigned to any of the five species of Macaca arctoides, M. assamensis, M. thibetana, M. mulatta, and M. nemestrina. An analysis of the internal structure of the cranium reveals that only PV F1 and the cranium of Macaca arctoides have a pear-shaped nasal cavity expanding laterally at both the anterior and posterior regions. Such a feature is probably a derived condition in the macaque lineage, suggesting a close relationship between Macaca speciosa subfossilis and M. arctoides. This finding supports the paleobiological scenario that the members of the lineage of Macaca arctoides diverged from the other members of Asian macaques and became distributed in northern Vietnam as early as the Late Pleistocene.     

Tourist impact on Tibetan macaques

Abstract

Ecotourism is a growing sector of the tourism industry, but few studies to date have quantified its impacts on local people, tourists and wildlife. We present a preliminary study on threat and affiliative behaviors of two groups of free-ranging Tibetan macaques (Macaca thibetana) as a function of habituation and tourist presence. Data indicate that the less habituated group spent less time within sight of tourists compared with the more habituated group. The more habituated group engaged in frequent affiliative behaviors while within sight of humans, whereas affiliative behavior was not observed in the less habituated group. The general pattern of threats consisted of adults primarily threatening juveniles and juveniles primarily threatening humans, possibly due to redirection. No clear pattern of threats as a function of tourist density emerged. Tourist feeding, although discouraged, potentially provided a catalyst for some aggression. Future research will focus on clarifying which human behaviors evoke specific threat responses from monkeys. These data will be used to refine the existing management plan for this monkey population.     

Identification and molecular evolutionary analysis of TLR5 gene from the Tibetan macaque (Macaca thibetana)

In order to identify the Toll-like receptor 5 (TLR5) as a putative candidate disease-resistance gene in Tibetan macaque (Macaca thibetana), two pairs of primers were designed based on the TLR5 gene sequence of rhesus macaque (Macaca mulatta, NM_001130429). The primers were used to amplify the TLR5 gene from Tibetan macaque, by the polymerase chain reaction (PCR). The compiled sequences were analyzed by bioinformatics. The DNA sequencing and additional combined results showed that the Tibetan macaque TLR5 gene is about 2825 bp and contains an open reading frame of 2577 bp encoding for 858 amino acids. Homology analysis of TLR5 in both species showed that the amino acid and nucleotide identity is about 99.7% and 99.8% and their transmembrane and intracellular domains appeared more conservative than the extracellular domains of proteins. However, re-examining the entire Tibetan macaque TLR5 coding sequence we found that a purifying selection was also acting on the TLR5 gene region encoding for its intracellular domain of the protein. Even though the selection tests indicated that the TLR5 gene experienced a strong purifying selection in the process of evolution, most likely because its potential role in the primate adaptive immune defense, the Tibetan macaque still has the highest relationship with the rhesus macaque.     

Colony size affects collective decision-making in the ant Temnothorax albipennis

Social insects are well-known for their ability to achieve robust collective behaviours even when individuals have limited information. It is often assumed that such behaviours rely on very large group sizes, but many insect colonies start out with only a few workers. Here we investigate the influence of colony size on collective decision-making in the house-hunting of the ant Temnothorax albipennis. In experiments where colony size was manipulated by splitting colonies, we show that worker number has an influence on the speed with which colonies discover new nest sites, but not on the time needed to make a decision (achieve a quorum threshold) or total emigration time. This occurred because split colonies adopted a lower quorum threshold, in fact they adopted the same threshold in proportion to their size as full-size colonies. This indicates that ants may be measuring relative quorum, i.e. population in the new nest relative to that of the old nest, rather than the absolute number. Experimentally reduced colonies also seemed to gain more from experience through repeated emigrations, as they could then reduce nest discovery times to those of larger colonies. In colonies of different sizes collected from the field, total emigration time was also not correlated with colony size. However, quorum threshold was not correlated with colony size, meaning that individuals in larger colonies adopted relatively lower quorum thresholds. Since this is a different result to that from size-manipulated colonies, it strongly suggests that the differences between natural small and large colonies were not caused by worker number alone. Individual ants may have adjusted their behaviour to their colony’s size, or other factors may correlate with colony size in the field. Our study thus shows the importance of experimentally manipulating colony size if the effect of worker number on the emergence of collective behaviour is to be studied. Received 13 December 2005; revised 9 May 2006; accepted 15 May 2006.