Mixed-species Troops Research Articles

Mixed-species association and a record of a hybrid offspring between Trachypithecus pileatus and Trachypithecus phayrei in Bangladesh

The term mixed-species association has a broad range of definitions, from temporary foraging association to permanent group living. A mixed-species association mostly involves species from closely related taxa and is found in birds, mammals and fish. It ranges from passive association with little interaction to coordinated behavioural interactions between the group members of a mixed-species group. Mixed-species association can result in the production of hybrid offspring in the wild. In this study, we present, to the best of our knowledge, the first observational evidence of mixed-species association between the two threatened primate species Phayre’s langur (Trachypithecus pileatus) and capped langur (Trachypithecus phayrei), in fragmented forest patches of northeast Bangladesh. We also report a presumed hybrid offspring between these species. We conducted a short-term study from December 2021 to April 2022 in three forest patches based on information from eco-tourism guides. We confirmed the presence of three mixed-species troops; in two of the groups an adult male T. phayrei had permanently immigrated into a group of T. pileatus, and in the other one an adult male T. pileatus had permanently immigrated into a group of T. phayrei. A long-term detailed study is needed to elucidate the reasons for these mixed-species associations, their behavioural patterns, the fate of the presumed hybrid offspring, and to understand the genetic relatedness between the individuals.

Primate seed dispersal leaves spatial genetic imprint throughout subsequent life stages of the Neotropical tree Parkia panurensis

Key message The Neotropical tree Parkia panurensis shows a spatial genetic structure from the seed to the adult stage that is most likely the outcome of the seed dispersal provided by primates. Seed dispersal and pollination determine the gene flow within plant populations. In addition, seed dispersal creates the template for subsequent stages of plant recruitment. Therefore, the question arises whether and how seed dispersal affects the spatial genetic structure (SGS) of plant populations. In this study, we used microsatellites to analyse the SGS of the Neotropical tree Parkia panurensis (Fabaceae). This plant species is a major food resource for primates and its seeds are mainly dispersed by primates. Seeds were collected during behavioural observations of a tamarin mixed-species troop in north-eastern Peru. Additionally, leaf samples of juveniles and of adults trees of this species were collected throughout the home range of the tamarin troop. A significant SGS for embryos (located within the dispersed seeds) and for non-reproductive plants are found up to a distance of 300 m. This matches the distance within which most seeds are dispersed. In the adult stage, the scale of a significant SGS is reduced to 100 m. While we cannot explain this scale reduction, our study provides the first evidence that primate seed dispersal does influence the SGS of a tropical tree species.

Reporting social behaviours of mixed-species troops formed by Callithrix jacchus and Callithrix penicillata (Primate, Callitrichidae).

In New World primates, mixed-species troops have been reported. Here, we analysed the performance of affiliative and agonistic behaviours of Callithrix jacchus and Callithrix penicillata living in mixed groups. For this purpose, we recorded the interaction of the individuals from two groups located in Bauru city, in the state of São Paulo (Brazil). Our data show that in both groups, affiliative behaviours appeared more frequently than agonistic ones. We concluded that there is cohesion inside the mixed-species troops observed. We suggest that a deeper knowledge about the social behaviour of mixed-species troop species certainly may be useful in projects linked with the management of the impact caused by them.

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (Saguinus fuscicollis)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.Electronic supplementary materialThe online version of this article (doi:10.1007/s10764-011-9516-9) contains supplementary material, which is available to authorized users.

Of Least Concern? Range Extension by Rhesus Macaques (Macaca mulatta) Threatens Long-Term Survival of Bonnet Macaques (M. radiata) in Peninsular India

Rhesus and bonnet macaques are the 2 most common and widely distributed of the 8 macaque species of India. Rhesus macaques are widely distributed across southern and southeastern Asia, whereas bonnet macaques are restricted to peninsular India. We studied the current distributional limits of the 2 species, examined patterns of their coexistence in the interspecific border zones, and evaluated losses in the distributional range of bonnet macaques over the last 3 decades. Our results indicate that whereas rhesus macaques have extended their geographical range into the southern peninsula, bonnet macaques have been displaced from many areas within their former distributional range. The southern and the northern distributional limits for rhesus and bonnet macaques, respectively, currently run parallel to each other in the western part of the country, are separated by a large gap in central India, and converge on the eastern coast of the peninsula to form a distribution overlap zone. This overlap region is characterized by the presence of mixed-species troops, with pure troops of both species sometimes occurring even in close proximity to one another. The range extension of rhesus macaque—a natural process in some areas and a direct consequence of introduction by humans in other regions—poses grave implications for the endemic and declining populations of bonnet macaques in southern India.

Long‐term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): Effects of foraging, thermoregulation, predation, and resource defense constraints

Sleeping sites are an important aspect of an animal's ecology given the length of time that they spend in them. The sleep ecology of wild saddleback and mustached tamarins is examined using a long-term data set covering three mixed-species troops and 1,300+ tamarin nights. Seasonal changes in photoperiod accounted for a significant amount of variation in sleeping site entry and exit times. Time of exit was more closely correlated with sunrise than time of entry was with sunset. Both species entered their sleeping sites when light levels were significantly higher than when they left them in the morning. Troops of both species used >80 individual sites, the majority being used once. Mustached tamarins never used the same site for more than two consecutive nights, but saddlebacks reused the same site for up to four consecutive nights. Mustached tamarins slept at significantly greater heights than saddleback tamarins. There were consistent interspecific differences in the types of sites used. Neither the presence of infants, season, nor rainfall affected the types or heights of sites chosen. Sleeping sites were located in the central area of exclusive use more often than expected, and their position with respect to fruiting trees indicated a strategy closer to that of a multiple central place forager than a central place forager. These findings are discussed in light of species ecology, with particular reference to predation risk, which is indicated as the major factor influencing the pattern of sleeping site use in these species.

Niche expansion of a cryptic primate,Callimico goeldii, while in mixed species troops

We examined the effects of polyspecific associations on the behavior of one group of Callimico goeldii in northwestern Bolivia. Data were collected for 1 year using focal animal sampling at 5-min intervals, for a total of 1,375 observation hours. In total, C. goeldii formed mixed species troops with five groups of Saguinus fuscicollis and six groups of S. labiatus, and these were maintained during 81% of observations. C. goeldii rested more and traveled less while alone than while associated, but neither vigilance behavior in the understory nor habitat use were affected by association status. The composition of the group's diet was different while alone (higher in structural carbohydrates [fungi] and lower in simple sugars [ripe fruits] and protein [insects]) than while associated (fungi 65 vs. 37%; fruits 13 vs. 32%; insects 5 vs. 15%). We propose therefore, that C. goeldii has a lower quality and more narrowly based diet while alone as compared to while associated. The factors that allow for this dietary expansion while in mixed species troops require further investigation.

Factors Affecting Group Spread within Wild Mixed-Species Troops of Saddleback and Mustached Tamarins

We examined group spread and interindividual spacing within wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Mustached tamarin groups were spread over larger areas than those of saddleback tamarins. Group size and behavior affected group spread and interspecific proximity: larger groups of both species were dispersed over greater areas, and the larger troop had the lowest degree of interspecific proximity. Behavior also affected group spread and interspecific proximity: when traveling individuals were spread over a larger area, and the distance between heterospecifics was greater than when stationary. We examined spatial proximity using data on the distance from nearest neighbor. Overall, distance to nearest neighbor was not affected by group size. Based on specific behaviors, foraging saddleback tamarins were significantly nearer conspecifics than to mustached tamarins. Tamarins have polymorphic color vision, and trichromats—having 3 types of visual pigment—versus dichromatic individuals—with two types of pigment—may be better at perceiving yellow or russet colored predators and conspecifics than their dichromatic counterparts are. Color vision status affected spatial positioning, with vigilant trichromats being further from their neighbors than their dichromatic conspecifics were. We discuss the findings with respect to the ecology of the species. Specifically, interspecific differences in group spread and spatial proximity are related to differences in the supports used, and the effect of troop size on interspecific proximity is related to increased resource competition. The finding that trichromats are further from their neighbors represents the first example of a behavioral correlate of color vision ability in a wild species with polymorphic color vision, and is explained through the perception of predation risk.

Factors affecting vigilance within wild mixed-species troops of saddleback ( Saguinus fuscicollis ) and moustached tamarins ( S. mystax )

We examine vigilance within a mixed-species troop of saddleback (Saguinus fuscicollis) and moustached (S. mystax) tamarins over a complete year. Saddleback tamarins were consistently more vigilant than moustached tamarins. This may be linked to their preference for lower strata. In accordance with previous studies of other primates, vigilant tamarins of both species were significantly further away from their nearest neighbours, and were also at lower heights in the forest than non-vigilant individuals. There was no observed sex difference in the amount of time spent vigilant. In terms of modes of scanning, the saddleback tamarins looked up significantly more frequently than the moustached tamarins, whereas there was no difference between the species in the frequency of side sweeps. There were no differences between the sexes in the frequencies of either type of vigilant behaviour. The proportion of time spent vigilant was higher than average immediately prior to entering a sleeping site for saddleback tamarins, but not for moustached tamarins. Both species were more vigilant immediately after exiting a sleeping site than at other times of the day. There was significant variation in the amount of time devoted to vigilance over the course of the year. These findings are discussed with respect to the social structure, ecology and main predator threats facing these species.

Experimental field study of the relative costs and benefits to wild tamarins (Saguinus imperator and S. fuscicollis) of exploiting contestable food patches as single- and mixed-species troops.

Several species of tamarins form stable mixed-species troops in which groups of each species feed, forage, rest, and travel together during much of the year. Although the precise set of factors that facilitate this ecological relationship remains unclear, predator detection and foraging benefits are presumed to play a critical role in maintaining troop stability. In this work we present data from an experimental field study designed to examine how factors such as social dominance and within-patch foraging decisions affect the costs and benefits to tamarins of visiting feeding sites as single- and mixed-species troops. Our data indicate that when they exploited contestable food patches (sets of eight feeding platforms, two of which contained a 100-g banana), each tamarin species experienced foraging costs when they arrived as part of a mixed-species troop. These costs were found to be less severe for emperor tamarins because they were socially dominant to saddle-back tamarins and could displace them at feeding sites. We conclude that the foraging benefits to tamarins residing in mixed-species troops are asymmetrical, and that at feeding sites in which the amount of food in a patch is insufficient to satiate all troop members, even minor differences in the timing of return to food patches and changes in troop cohesion have a measurable effect on the costs and benefits to participating tamarin species.

Patterns of positional behavior in mixed‐species troops ofCallimico goeldii,Saguinus labiatus, andSaguinus fuscicollisin northwestern Brazil

We present the results of a 4-month field investigation of positional behavior, vertical ranging, and species differences in limb proportions and body mass in a mixed-species troop of Saguinus fuscicollis, Saguinus labiatus, and Callimico goeldii in northwestern Brazil. Despite certain similarities in overall positional repertoire, patterns of positional behavior varied significantly between species. Travel in Callimico occurred principally in the lowest levels of the canopy, and was characterized by an exaggerated form of hindlimb-dominated bounding (bounding-hop), and leaping to and from vertical trunks (55.1% of leaps). In contrast, saddle-back tamarins traveled in the lower and middle levels of the canopy, and engaged in a range of leaping behaviors, including stationary leaps (37.3%), acrobatic leaps (31.3%), and trunk-to-trunk leaps (20%). Red-bellied tamarins exploited the highest levels of the arboreal canopy. Travel in this species was dominated by quadrupedal bounding and acrobatic leaps (67% of leaps) that began and ended on thin, flexible supports. Species differences in positional behavior correlated with species differences in limb proportions and locomotor anatomy, and provide a framework for understanding niche partitioning in mixed-species troops of Saguinus and Callimico.

The behavioural ecology of mixed-species troops of callitrichine primates.

This review summarizes information on the behavioural ecology of mixed-species troops (interspecific associations) formed by different species of callitrichines, small New World monkeys, in western and central Amazonia. The formation of mixed-species troops is an integral part of the biology of several species of this subfamily. Niche separation between associated species is obtained through vertical segregation which results in differences in the prey spectrum. The degree of niche separation is a predictor for the stability of mixed-species troops. Individuals may benefit from the formation of mixed-species troops through increased safety from predators, increased foraging efficiency, and/or increased resource defence. Costs of mixed-species troop formation are probably very low and mainly relate to patterns of interspecific behavioural interactions. We point to gaps in our knowledge and suggest pathways for future research into mixed-species troops.

The behavioural ecology of mixed‐species troops of callitrichine primates

ABSTRACTThis review summarizes information on the behavioural ecology of mixed‐species troops (interspecific associations) formed by different species of callitrichines, small New World monkeys, in western and central Amazonia. The formation of mixed‐species troops is an integral part of the biology of several species of this subfamily. Niche separation between associated species is obtained through vertical segregation which results in differences in the prey spectrum. The degree of niche separation is a predictor for the stability of mixedspecies troops. Individuals may benefit from the formation of mixed‐species troops through increased safety from predators, increased foraging effciency, and or increased resource defence. Costs of mixed‐species troop formation are probably very low and mainly relate to patterns of interspecific behavioural interactions. We point to gaps in our knowledge and suggest pathways for future research into mixed‐species troops.

Hand specialization, sympatry, and mixed-species associations in callitrichines

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands ofLeontopithecusdiffer in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands ofSaguinus fuscicollisadapted to manipulative foraging, and are they functionally similar toLeontopithecus’ hands? 3. Is hand morphology inS. fuscicollismore similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollisandS. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, andS. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, andCallimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands ofLeontopithecusare adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands ofS. fuscicollis, S. tripartitusandS. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.

Intra-and Inter-Specific Social Learning of a Novel Food Task in Two Species of Tamarin

Intra- and inter-specific social learning was investigated in two species ofNew World monkey, the saddle-backed tamarin {Saguinus fuscicoUis) and the redbelliedtamarin {S. labiatus), which form stable and permanent mixed-species troops inthe wild. We explored whether improved food acquisition, through social learning, is apotential advantage of mixed-species troop formation by allowing a pair of naiveobservers to watch a pair of trained demonstrators complete a novel foraging task. Theaims of the study were (a) to determine if individuals succeeded at the task morequickly after having observed demonstrators, (b) to investigate whether speed ofacquisition differed after observation of conspecific demonstrators as opposed tocongeneric demonstrators, and (c) to compare performance between species. Thenumber of trials taken by observers to succeed on the task was compared with that takenby naive demonstrators to succeed on the task initially. Individuals succeeded on thetask more quickly if they had had the opportunity to watch demonstrators perform thetask, regardless of whether the demonstrator was a conspecific or congeneric. There wasno difference in performance between species. It is concluded that, for both species, thelearning of a new foraging technique is facilitated by the presence of both conspecificsand congenerics and that the likely mechanism for this facilitation is a combination ofstimulus enhancement and response facilitation. Social learning of this kind is discussedwith respect its adaptive value in wild mixed-species tamarin troops.

The Relationship between Body Size and Mixed-Species Troops of Tamarins (Saguinusspp.)

While Saguinus fuscicollis forms mixed-species troops with sympatric tamarin species in parts of its geographic range, in other parts it does not. The question is addressed whether body size divergence is a critical factor for this difference. Analysis of body size (head-body length) data shows that body size divergence ranges between 8 and 17% for associated species and between 1 and 4% for non-associated species. In associated species, the degree of body size divergence seems to correlate with the stability of mixed-species troops (i.e., time spent in interspecific association). It is concluded that body size plays an important role for niche differentiation, sympatric coexistence and the formation of mixed-species troops in tamarins.

Do black colobus in mixed-species groups benefit from increased foraging efficiency?

Seed-eating in the African colobines varies according to species and site. Because seeds are more palatable than leaves, seed-eating is considered to result from a positive choice by colobines. A year-long study of the diet of Colobus satanas in Central Gabon confirmed that this species eats a significant amount of seeds. Furthermore, despite large variations in fruit availability, this amount consistently increases when colobines feed in mixed-species troops including frugivorous cercopithecines and mangabeys. Our results show that colobines benefit when feeding in mixed troops and suggest that polyspecific associations are an adaptive strategy that could have positive effects on colobine populations, especially during the period of fruit shortage.

Reactions of wild tamarins,Saguinus mystax andSaguinus fuscicollis to avian predators

During a field study in northeastern Peru, the reactions of a group ofSaguinus mystax on Padre Isla and of a mixed-species troop ofS. mystax andSaguinus fuscicollis at the Rio Blanco to raptorial and other birds were observed. Alarms that are specific to flying stimuli were elicited by birds of prey, but other birds that do not represent a threat to the tamarins also caused alarm calls. Alarm events (i.e., instances when one or more alarm calls were given) were observed at rates of 0.3/hr (Padre Isla) and 0.5/hr (Rio Blanco). Rates of alarm events significantly increased after the birth of an infant in the Padre Isla group and after the attack of an ornate hawk-eagle (Spizaetus ornatus) on the Rio Blanco group. Reactions to alarming stimuli/alarm calls ranged from looking up to falling down from trees. The modification of the tamarins' behavior by the potential presence of aerial predators indicates that raptors represent an important predatory threat to tamarins.

Mechanisms promoting stability in mixed Saguinus mystax and S. fuscicollis troops.

Mixed-species troops composed of two species of tamarin monkeys, and rarely other ceboids, occur throughout much of western Amazonia and are notable for their long-term stability. This study identified several variables that appeared to promote mixed-species troop cohesion and yet maintained spatial segregation between species. Three variables enhanced in terspecific spatial segregation: differences in support use, vertical stratification, and interindividual spacing. In contrast, early morning vocalizations and well-coordinated movement patterns contribute to cohesion within a mixed-species troop. The combination of these variables may help explain how two congeneric species accommodate one another with little apparent interspecific aggression. The exact nature of benefits and costs to each individual in a mixed troop is still elusive; however, a comparison of population densities of sympatric and allopatric tamarins suggests that population growth of one partner (Saguinus fuscicollis) is enhanced in the presence of a congeneric species.

Interspecific relations in a mixed-species troop of moustached tamarins, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis (Platyrrhini:Callitrichidae), at the Río Blanco, Peruvian Amazonia.

This study examined the social interactions between moustached tamarins, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis, living in a mixed-species troop at the Río Blanco, Peruvian Amazonia, between July 1985 and July 1986. Mixed-species troops were common among the S. mystax and S. fuscicollis populations in the Río Blanco study area; 72% of all sightings of S. mystax and 82% of all sightings of S. fuscicollis were in mixed-speices troops (study group excluded from analysis). In the study group, the two species spent on average 82% of time in association. Interactions were observed at a rate of one per 5 h of observation. Most interactions (96%) were agonistic. About 70% of agonistic interactions occurred at small food resources (crown diameter < 5 m and/or limited number of ripe fruits). Moustached tamarins were always dominant over saddle-back tamarins. Friendly interactions were extremely rare and were restricted to play invitations. Mutual calling was observed in the morning before the two species joined each other and during the day when they became separated. It is concluded that interspecific interactions and mutual calling incur some costs to the associated species but that these costs may be low.