Mixed-species Associations Research Articles

First record of a mixed species association between Hatinh langur (Trachypithecus hatinhensis) and red-shanked douc (Pygathrix nemaeus).

In primates, mixed species associations are not common occurrences, and have been linked to both ecological and anthropogenic factors. We present camera-trapping records of a mixed association between two primates, the Hatinh langur (Trachypithecus hatinhensis) and red-shanked douc (Pygathrix nemaeus) and discuss possible hypotheses for this occurrence. To our knowledge, this is the first evidence of such an association in the wild of these two threatened primates, and thus contributes to our limited ecological knowledge of the species.

Two's company, three species is a crowd? A webcam-based study of the behavioural effects of mixed-species groupings in the wild and in the zoo.

Mixed species exhibits in zoos are used to create larger, more stimulating environments to support naturalistic interactions between species. In the wild, mixed species groups are observed as having lower rates of vigilance, presumably due to reduced predation risk through 'detection' and 'dilution' effects. This effect appears to be highly variable depending on factors such as food availability or degree of threat. This study aimed to collect data on mixed-species associations and consequent vigilance rates in the wild, collecting equivalent data from a large mixed-species zoo enclosure to compare the findings between free-ranging and captive populations. The study additionally investigated whether large mixed-species enclosures support natural associations and behaviours, by comparing the behaviour of captive animals with wild counterparts. The study used livestream video feeds from 10 national parks in South Africa and Kenya to observe free-ranging species, and a camera at the San Diego Zoo Safari Park's mixed species African exhibit. Scan and continuous sampling protocols were used simultaneously to record behavioural states as well as the rate of scanning (vigilance) events. GLMMs were run to test whether vigilance of a focal species varied according to the number of animals present, the density of animals in the group, and the diversity of species. In the wild, vigilance decreased with increasing number of animals in the surroundings but in captivity the group size had no impact. The results suggest that in the wild, these species benefit from increased perceived safety in larger groups, regardless of the species making up that group. No effect was noted in the zoo because of a reduced need for animals to show heightened vigilance to the same degree as in the wild. Similarities were observed in associations between species/mixed species group compositions, and in behaviour budgets. These findings provide a preliminary evaluation of how the impact of mixed species groupings may translate from the wild to the zoo, based on the associations and behaviour across a variety of African ungulates.

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.

Are dolphins modulating whistles in interspecific group contexts?

ABSTRACT Cetaceans depend highly on acoustic signals, such as whistles, for social communication. Mixed-species associations (MSAs), temporary or long-term encounters between different species, may play an important role on the acoustic dynamics of the species involved. Because of whistles’ communication function, we used these sounds to investigate the acoustic relationships of Tursiops truncatus when involved in different group contexts: in MSAs with two other delphinid species and in single species group. Acoustic recordings of T. truncatus single species groups and in associations with Globicephala melas and Grampus griseus were collected in the Western South Atlantic Ocean through a towed array of hydrophones. A total of 1267 whistles were analysed and acoustical parameters were extracted. To verify the differences among whistles produced in such contexts a support vector machine and random forest analysis were implemented. Both analyses revealed a clear separation of whistles from the single species versus the MSA as well as between both MSAs. The results indicate that interspecific associations may influence the whistle structure and suggests that T. truncatus whistles can be modified during interspecific interactions. These findings are useful to elucidate the possible factors underlying behavioural plasticity and interspecific associations and to understand dolphins’ acoustic communication.

Lesser spot-nosed monkeys coordinate alarm call production with associated Campbell\u2019s monkeys

Forest monkeys often form semi-permanent mixed-species associations to increase group-size related anti-predator benefits without corresponding increases in resource competition. In this study, we analysed the alarm call system of lesser spot-nosed monkeys, a primate that spends most of its time in mixed-species groups while occupying the lowest and presumably most dangerous part of the forest canopy. In contrast to other primate species, we found no evidence for predator-specific alarm calls. Instead, males gave one general alarm call type (‘kroo’) to three main dangers (i.e., crowned eagles, leopards and falling trees) and a second call type (‘tcha-kow’) as a coordinated response to calls produced in non-predatory contexts (‘boom’) by associated male Campbell’s monkeys. Production of ‘kroo’ calls was also strongly affected by the alarm calling behaviour of male Campbell’s monkeys, suggesting that male lesser spot-nosed monkeys adjust their alarm call production to another species’ vocal behaviour. We discuss different hypotheses for this unusual phenomenon and propose that high predation pressure can lead to reliance on other species vocal behaviour to minimise predation.Significance statementPredation can lead to the evolution of acoustically distinct, predator-specific alarm calls. However, there are occasional reports of species lacking such abilities, despite diverse predation pressure, suggesting that evolutionary mechanisms are more complex. We conducted field experiments to systematically describe the alarm calling behaviour of lesser spot-nosed monkeys, an arboreal primate living in the lower forest strata where pressure from different predators is high. We found evidence for two acoustically distinct calls but, contrary to other primates in the same habitat, no evidence for predator-specific alarms. Instead, callers produced one alarm call type (‘kroo’) to all predator classes and another call type (‘tcha-kow’) to non-predatory dangers, but only as a response to a specific vocalisation of Campbell’s monkeys (‘boom’). The production of both calls was affected by the calling behaviour of Campbell’s monkeys, suggesting that lesser spot-nosed monkey vocal behaviour is dependent on the antipredator behaviour of other species. Our study advances the theory of interspecies interactions and evolution of alarm calls.

Delphinid Mixed-Species Associations in the Oceanic Waters of the Western South Atlantic

Delphinid Mixed-Species Associations in the Oceanic Waters of the Western South Atlantic

Mixed-species associations and attempted mating suggest hybridization between purple-faced and tufted gray langurs of Sri Lanka.

Hybridization is increasingly recognized as an important mechanism of evolutionary change in the order Primates. Here, we present the first observational data supporting natural hybridization between the critically endangered purple-faced langur (Semnopithecus vetulus philbricki) and the threatened tufted gray langur (Semnopithecus priam thersites) in Kaludiyapokuna Forest Reserve in Sri Lanka. In one case study, we observed a long-term (> 1 year) mixed-species group consisting of one adult tufted gray langur male coexisting with seven adult purple-faced females. Although copulations were not observed, two infants were conceived during the male’s tenure, and the coat color of one of these infants transitioned into that intermediate between those of the two langur species. The tufted gray langur male was also aggressive toward extra-group males of both species, as well as towards purple-faced juveniles within his group. However, we never witnessed the male exhibiting aggression towards the infants conceived during his tenure. In a second case study, a female purple-faced langur visited and sexually solicited a tufted gray langur male in a known study group of this species over the course of 2 days, in what resembled a sexual consortship. Taken together, the observed mixed-species association and attempted interspecific mating suggest that hybridization is very likely in these sympatric species. Genetic data are needed to confirm and determine the extent of hybridization in the dry zone of Sri Lanka where purple-faced langurs live in sympatry with tufted gray langurs.

Interspecies pectoral fin contact between bottlenose dolphins and Atlantic spotted dolphins off Bimini, The Bahamas

Affiliative interspecies interactions are important to community structure within an ecosystem yet understudied relative to antagonistic relationships. Mixed-species associations provide important benefits via foraging, predator avoidance and social interactions. Tactile behaviours help with social bond formation and group establishment among conspecifics during social interactions, but little is known about the role of contact between heterospecific animals in mixed-species groups. Our objective was to quantify characteristics of pectoral fin contact between individuals of two sympatric species of wild dolphins, spotted dolphins, Stenella frontalis, and bottlenose dolphins, Tursiops truncatus, off Bimini, The Bahamas, in order to assess possible benefits of heterospecific interactions. Using underwater video recordings from mixed-species dolphin encounters from 2011 to 2017, we observed 74 pectoral fin contacts, of which 27 were between heterospecific animals. Encounters were either affiliative (61.5%) or sociosexual (38.5%). Conspecific and heterospecific dolphins had similar rates of initiating and receiving contacts. This suggests that during mixed-species groups, the cost-benefit trade-off in choosing a social partner is similar for conspecific and heterospecific individuals. Heterospecific contacts initiated by S. frontalis were primarily affiliative whereas heterospecific contacts initiated by T. truncatus were sociosexual. Both sociosexual behaviour and pectoral fin contact in dolphins have been suggested as mechanisms of bond formation. We conclude that mixed-species interactions with pectoral fin contact may be a mechanism for social bond formation between heterospecifics and that these bonds may help to re-establish groups, as needed, for predator avoidance.

When close neighbours become good friends: plasticity of behavioural traits in sympatric fishes that form mono- and mixed-species groups

ABSTRACTLike mono-species fish groups, formation of mixed-species assemblages is likely driven by trophic influences and interspecific behavioural traits. Our aim was to identify how sympatric estuarine species of differing phenotypes form mixed-species group associations, and to identify changes to group structure of fish that migrate between mono- and mixed-species groups. We used sympatric yellow-eyed mullet (Aldrichetta forsteri), kahawai (Arripis trutta), and Australian snapper (Chrysophrys auratus), representing different phenotypes for the mixed-species group, and yellow-eyed mullet for the mono- and mixed-species comparison. Group formation and structure was quantified in predator and foraging treatment groups. We used previous research in mono-species yellow-eyed mullet to compare behavioural plasticity with the current study. Our novel results suggest similar behavioural traits in mono- and mixed-species fish groups have beneficially co-evolved and importantly, behavioural plasticity is necessary for migration between groups. Overall, our observations highlight key behavioural responses associated with mixed-species fish formations in estuarine ecosystems.

Flexible use of simple and combined calls in female Campbell's monkeys

Call combinations allow animals to expand the communicative power of small repertoires with acoustically inflexible elements. In Campbell's monkeys, Cercopithecus campbelli, males possess a small repertoire of calls that can be merged to an acoustically invariable suffix and which are concatenated into various sequences, mainly in response to external disturbances. The vocal repertoire of adult females has been less well studied although it is much richer, containing both alarm and various social calls. In particular, females possess a low-pitched contact call, produced either alone or merged with a high-pitched, arched unit. Combined contact calls are identity-richer and easier to detect than simple calls. Here, we investigated the socioecological factors that determined the production of single and combined utterances and found that combined utterances were more common when identity was relevant such as in mixed-species associations and during socially important vocal exchanges. In contrast, single calls were used mainly when predation risk was high, as part of this species' generally cryptic antipredator strategy. We discuss these finding in the light of current theories regarding the evolution of combinatorial signalling.

Chronic Plasmodium brasilianum infections in wild Peruvian tamarins.

There is an increased interest in potential zoonotic malarias. To date, Plasmodium malariae that infects humans remains indistinguishable from Plasmodium brasilianum, which is widespread among New World primates. Distributed throughout tropical Central and South America, the Callitrichidae are small arboreal primates in which detection of natural Plasmodium infection has been extremely rare. Most prior screening efforts have been limited to small samples, the use of low-probability detection methods, or both. Rarely have screening efforts implemented a longitudinal sampling design. Through an annual mark-recapture program of two sympatric callitrichids, the emperor (Saguinus imperator) and saddleback (Saguinus fuscicollis) tamarins, whole blood samples were screened for Plasmodium by microscopy and nested PCR of the cytochrome b gene across four consecutive years (2012–2015). Following the first field season, approximately 50% of the samples collected each subsequent year were from recaptured individuals. In particular, out of 245 samples from 129 individuals, 11 samples from 6 individuals were positive for Plasmodium, and all but one of these infections was found in S. imperator. Importantly, the cytochrome b sequences were 100% identical to former isolates of P. malariae from humans and P. brasilianum from Saimiri sp. Chronic infections were detected as evidenced by repeated infections (7) from two individuals across the 4-year study period. Furthermore, 4 of the 5 infected emperor tamarins were part of a single group spanning the entire study period. Overall, the low prevalence reported here is consistent with previous findings. This study identifies two new natural hosts for P. brasilianum and provides evidence in support of chronic infections in wildlife populations. Given that callitrichids are often found in mixed-species associations with other primates and can be resilient to human-disturbed environments, they could contribute to the maintenance of P. malariae populations if future work provides entomological and epidemiological evidence indicating human zoonotic infections.

Interactions of Lion-Tailed Macaque (<i>Macaca silenus</i>) with Non-Primates in the Western Ghats, India

Primates and non-primates inhabiting tropical forests may interact with each other since they coexist in the same communities. Primates usually interact with their prey, predators, competitors and neutral species. Using 'all occurrence' sampling, we have studied inter-specific interactions of lion-tailed macaques with non-primate species found in their habitat. We observed that the percentage of total time spent on interactions with non-primates was less than 1. Also, the percentage of total time spent in interacting with competitors, predators and neutral species was less than 0.5. The lack of predation pressure and lack of opportunities for mixed-species associations for increasing foraging efficiency appear to be the major reasons for the absence of interactions with nonprimates. By comparing with studies from other primate habitat regions, we observed that primates in South Asia interact much lesser with non-primates than those in South America and Africa. A previous study showed that the interactions of lion-tailed macaques even with other primate species in the Western Ghats are less than expected by chance.

Mixed-Species Associations of Marine Mammals in the Southern California Bight, with Emphasis on Risso’s Dolphins (Grampus griseus)

Mixed-Species Associations of Marine Mammals in the Southern California Bight, with Emphasis on Risso’s Dolphins (Grampus griseus)

Cetacean sightings, mixed-species assemblages and the easternmost record of Indopacetus pacificus from the northern Indian ocean

A visual survey of cetaceans was carried out during a voyage from Singapore to Sri Lanka, through the Straits of Malacca, Andaman Sea and across the Bay of Bengal in the northern Indian Ocean in November/December 2012. Forty sightings of 11 cetacean species were recorded in 19 days of observation. Two mixed-species associations of interest were recorded. One of these contained four species of odontocetes in association with each other. The second group was of Indopacetus pacificus in association with Globicephala macrorhynchus and this while being the easternmost live sighting of I. pacificus in the northern Indian Ocean is also the first such mixed group in the Bay of Bengal.

North Atlantic humpback whale (Megaptera novaeangliae) hotspots defined by bathymetric features off western Puerto Rico

North Atlantic humpback whales (Megaptera novaeangliae (Borowski, 1781)) are increasing in number, necessitating current data from winter areas for assessing potential interactions with humans. Occurrence patterns of humpback whales wintering off Puerto Rico were investigated to predict where whales aggregate in nearshore areas. Here we describe the relationship between group associations of humpback whales and bathymetric features off western Puerto Rico. Data were collected from 2011 to 2014. Effort consisted of 240.9 vessel h, 13.0 aerial h, and 303.6 h of land observations conducted over 165 days. A total of 197 humpback whale groups were observed with n = 331 individuals: 91 (46.2%) singletons, 67 (34%) dyads, 17 (8.6%) mother–calf pairs, 8 (4.1%) competitive groups, 8 (4.1%) mother–calf–escort groups, and 6 (3.1%) mixed-species associations. A linear regression model supported that group composition correlated with hotspots associated with four bathymetric features. Dyads and competitive groups were dispersed among features in deeper water. Singletons were observed farther from a shelf edge, whereas singing males were closely associated with a shelf edge. Mother–calf pairs occurred nearshore in shallow water; however, when mother–calf pairs were sighted with an escort, they were offshore. This study is especially important ahead of possible removal from the Endangered Species list.

Mixed-species associations in cuxiús (genus Chiropotes).

Polyspecific or mixed-species associations, where two or more species come together to forage and travel as a unit, have been reported in many primate species. These associations appear to offer a number of benefits to the species involved including increased foraging efficiency and decreased risk of predation. While several researchers have suggested that cuxiús (genus Chiropotes) form mixed-species associations, previous studies have not identified the circumstances under which cuxiús form associations or whether they form associations more often than would be expected by chance. Here we present data on the formation of mixed-species associations by four species of cuxiús at eight different sites in Brazil, Suriname, and Guyana. We analyzed data from two of the study sites, (Biological Dynamics of Forest Fragments Project (BDFFP), Brazil and the Upper Essequibo Conservation Concession (UECC), Guyana, to assess whether associations occurred more than would be expected by chance encounters and identify the factors influencing their formation. Cuxiús showed a high degree of inter-site variation in the frequency of time spent in association (ranging from 2 to 26% of observation time) and duration of associations (mean duration from 22 min to 2.5 hr). Sapajus apella was the most common association partner at most sites. At BDFFP, cuxiús formed associations more frequently but not for longer duration than expected by chance. For much of the year at UECC, associations were not more frequent or longer than chance. However, during the dry season, cuxiús formed associations with S. apella significantly more often and for longer duration than predicted by chance. Cuxiús at UECC formed associations significantly more often when in smaller subgroups and when foraging for insects, and alarm called significantly less frequently during associations. We suggest cuxiús form mixed-species associations at some sites as an adaptive strategy to decrease predation risk and/or increase foraging efficiency.

When biogeographical provinces collide: hybridization of reef fishes at the crossroads of marine biogeographical provinces in the Arabian Sea

AbstractAimSuture zones are areas where closely related species from different biogeographical regions come into contact and interbreed. This concept originated from the study of terrestrial ecosystems but it remains unclear whether a similar phenomenon occurs in the marine environment. Here we investigate a potential suture zone from a previously unknown hybrid hotspot at the Socotra Archipelago (Yemen), located in the Arabian Sea, where fauna from the Red Sea, Gulf of Aden, Arabian Sea, western Indian Ocean and greater Indo‐Polynesian Province intersect.LocationRed Sea, Gulf of Aden, Arabian Sea and Indian Ocean.MethodsPutative hybrid reef fish were identified based on intermediate coloration and morphology. Underwater observations and collections were conducted to determine: (1) whether parent species form heterospecific social groups or breeding pairs; (2) the sex and reproductive status of morphologically intermediate individuals; and (3) whether parent species were forming mixed species associations owing to a dearth of conspecific partners. To support hybrid status, morphologically intermediate and parental individuals were genotyped using mitochondrial DNA cytochrome c oxidase subunit I (COI), nuclear recombination‐activating gene 2 (RAG2) and the nuclear TMO‐4C4 (TMO) gene.ResultsWe observed putative hybrids involving 14 species from four reef fish families at Socotra. Most cases involved a parental species with a restricted distribution (e.g. Red Sea or Arabian Sea) and a broadly distributed Indo‐Pacific species. In most cases, at least one of the parent species was rare at Socotra. Hybrid gene flow was largely unidirectional, and although introgression was rare, we found evidence that some butterflyfish and surgeonfish hybrids were fertile and formed breeding groups with parental species.Main conclusionsThe rate of hybrid discovery at Socotra is much greater than that recorded elsewhere in the marine environment and involved both allopatric and sympatric species. This study highlights the importance of biogeographical location, reef habitat, environmental conditions and abundance disparities at Socotra in potentially facilitating hybridization among reef fishes at the edge of their distribution.

Solitary Ethiopian wolves increase predation success on rodents when among grazing gelada monkey herds

Mixed-species associations generally form to increase foraging success or to aid in the detection and deterrence of predators. While mixed-species associations are common among mammals, those involving carnivorous predators and potential prey species are seldom reported. On the Guassa Plateau, in the Ethiopian highlands, we observed solitary Ethiopian wolves (Canis simensis) foraging for rodents among grazing gelada monkey (Theropithecus gelada) herds. The tolerant and sometimes prolonged (> 1h) associations contrasted with the defensive behaviors exhibited by geladas toward other potential predators. Ethiopian wolves spent a higher proportion of time foraging and preyed more successfully on rodents when among geladas than when alone, providing evidence that gelada herds increase the vulnerability of subterranean rodents to predation. Ethiopian wolves appear to habituate gelada herds to their presence through nonthreatening behavior, thereby foregoing opportunistic foraging opportunities upon vulnerable juvenile geladas in order to feed more effectively on rodents. For Ethiopian wolves, establishing proximity to geladas as foraging commensals could be an adaptive strategy to elevate foraging success. The novel dynamics documented here shed light on the ecological circumstances that contribute to the stability of mixed groups of predators and potential prey.

Stingrays as possible facilitators for foraging trevallies in a nearshore sandflat

Mixed-species associations are temporary aggregations of individuals of different species that are driven by improved foraging, anti-predator benefits, and host/ cleaner relationships (Morse 1977). Host/cleaner relationships are common among fishes, including between elasmobranchs and teleosts (Papastamatiou et al. 2007). However, the function of associations between teleosts and elasmobranchs for other purposes is poorly described (Heithaus et al. 2010). On 27 April 2013, in the waters of Petite-Terre, along the north shore of Terre de Bas (Guadeloupe archipelago, 16°10’23.10”N, 61°06’32.41”W), a ∼90 cm (disk width) southern stingray (Dasyatis americana) was observed (∼15 min) and filmed (102 s) in association with a ∼40 cm bar jack (Caranx ruber). The observation occurred at 340 pm in shallow waters (<1.5 m) over a sandflat that is adjacent to a coral reef ecosystem. Video footage shows the jack swimming above the ray and actively maintaining the association during periods when the ray stopped to forage or changed headings (Fig. 1a, see supplementary material). During extractive foraging by the ray, the jack was observed inspecting the sand plume expelled by the ray and striking at prey that were dislodged (Fig. 1b). It therefore appears that the jack was associated to the stingray to forage and may have been able to access otherwise unavailable resources. Similar commensal associations were observed in the Pacific Ocean by two of the authors (JJK and JPQ), where trevallies were associated with stingrays for foraging purposes : a t Cocos Is land (5°31 ’08 ’N, 87°04’18”W), involving the bluefin trevally (Caranx melampygus) and the black-spotted stingray (Taeniurops meyeni), and in the lagoon of Tetiaroa, French Polynesia (17°0’S, 149°33”W), where several associations between pink whiprays (Himantura fai) and both bluefin and giant trevallies (Caranx ignobilis) were observed. Stingrays were always alone, but up to three trevallies could be observed with a single ray. In several of these cases, trevallies were seen lunging in plumes created by rays. Although other benefits to trevallies (e.g. reduced predation risk) cannot be discounted, we hypothesize that rays constitute facilitators for foraging trevallies. As documented for other batoids such as bat rays (Myliobatus californica) and round stingrays (Urobatis halleri) (VanBaricom 1982; Heithaus et al. 2010), stingrays in coral reef ecosystems may facilitate other predators that take advantage of prey that are disturbed or excavated during ray foraging. Electronic supplementary material The online version of this article (doi:10.1007/s12526-014-0304-6) contains supplementary material, which is available to authorized users.

Sociality across species: spatial proximity of newborn bats promotes heterospecific social bonding

Mixed-species groups occur in a variety of animals and have been widely investigated in many different orders of mammals. The advantages of mixed-species groups include improved information transfer, dilution of predation risk, and thermoregulation. We hypothesized that interspecific associations may be facilitated by the development of heterospecific social preferences. We manipulated the early environment of captive Kuhl’s pipistrelles (Pipistrellus kuhlii) and Savi’s bats (Hypsugo savii), raising newborns in artificial mixed-species groups to simulate conditions in natural mixed-species nurseries. We then measured association patterns among all bats and analyzed the occurrence of interactions by behavioral observation protocols and network analyses. Bats preferentially interacted and affiliated with former group members regardless of species, showing that bonding may occur between different species and that it develops after close contact with newborn heterospecifics, possibly through imprinting-like mechanisms. To our best knowledge, this is the first time such a phenomenon is documented for mammals. Although thermal preferences are often advocated to explain mixed-species associations among bats, individual experience may facilitate heterospecific groups in bats and other taxa.