Toque macaque food calls: Semantic communication concerning food distribution in the environment

doi:10.1016/S0003-3472(84)80283-3

Animal Behaviour

Volume 32, Issue 2, May 1984, Pages 470, IN3, 471-477

https://doi.org/10.1016/S0003-3472(84)80283-3 Get rights and content

Abstract

Upon the rare occasions that wild toque macaques (Macaca sinica) discover a large quantity of food in their natural forest environment they give distinctive calls. The durations of feeding bouts and the rates of feeding are significantly greater at sites where food calls are given than at sites of the same food types where no foods call are given. The calls designate a new location of a large quantity of any one of several food types. Dispersed group members hearing the call immediately run to the site of the call and feed there. I conclude that food calls are semantic signals (or symbols) that evoke the same response (rapid direct approach) as seeing the external referent of the calls (a source of abundant food) itself would. Food calls convey information about the presence of an edible food source, its quantity and location in the environment. As a general type, food calls appear to be related to, but are distinct from, contact calls which function to mintain group cohesion.

References (19)

MarlerP.
Primate vocalizations: affective or symbolic?
PattersonF.G.
The gestures of a gorilla: language acquisition in another pongid
Brain Lang.
(1978)
SeyfarthR.M. et al.
Vervet monkey alarm calls: semantic communication in a free-ranging primate
Anim. Behav.
(1980)
AltmannJ.
Observational study of behavior: sampling methods
Behaviour
(1974)
AltmannS.A.
The structure of primate social communication
DittusW.P.J.
The ecology of a semi-evergreen forest community in Sri Lanka
Biotropica
(1977)
DittusW.P.J.
The social regulation of population density and age-sex distribution in the toque monkey
Behaviour
(1977)
EisenbergJ.F.
Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus, and related species
Smithson. Contrib. Zool.
(1976)
GardnerR.A. et al.
Teaching sign language to a chimpanzee
Science, N. Y.
(1969)

There are more references available in the full text version of this article.

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Effect of urbanization on zoonotic gastrointestinal parasite prevalence in endemic toque macaque (Macaca sinica) from different climatic zones in Sri Lanka
2022, International Journal for Parasitology: Parasites and Wildlife
Citation Excerpt :
In addition, macaques are also listed in Appendix II of CITES (Convention on International Trade in Endangered Species) that includes species not necessarily threatened with extinction (CITES, 2005). Even though there are reports on the health, behaviour, and ecology of toque macaques (Dittus, 1984, 1986; Dittus and Ratnayeke, 1989; Keane et al., 1997; Weerasekara et al., 2021), parasite diversity of these animals is not well studied. A single study was reported on the macaque populations across the country, representing the three subspecies (Huffman et al., 2013) while others were mainly focused on macaques inhabiting specific regions, i.e Polonnaruwa (M. s. sinica), Peradeniya (M. s. aurifrons) (Dewit et al., 1991; Ekanayake et al., 2004, 2006; Thilakarathne et al., 2021), and in captivity (Gunasekera et al., 2012; Aviruppola et al., 2016).
Understanding variations in host-parasite relationships with urbanization is vital for both, public health management and conservation of endemic animals with high anthropogenic interactions. Toque macaques (Macaca sinica) are such endemic old-world monkeys in Sri Lanka. Three macaque sub species inhabit the main climatic zones of the island; M. s. sinica, M. s. aurifrons and M. s. opisthomelas inhabit the dry zone, wet zone, and montane regions of the island, respectively. This study aimed to examine parasite prevalence in this host in association with urbanization. A total of 180 fecal samples were collected from the three sub species of toque macaques inhabiting the main climatic zones (dry, wet, and montane) in Sri Lanka; 20 samples each were collected from urban, suburban, and wild populations representing each climatic zone. Twenty gastrointestinal (GI) parasite genera types i.e. five types of protozoan cysts, two types of trematode ova, four types of cestode ova, eight types of nematode ova, and a single type of acanthocephalan ova were identified. The overall prevalence of parasites was 62% (112/180) with the highest prevalence of Strongyloides infection. In all three sub species, toque macaque populations with proximity to human settlements, including urban and suburban populations, manifested a greater GI parasitic prevalence, mean ova/cyst counts and species richness, compared to their wild counterparts. Importantly, records of five parasite types in toques in Sri Lanka are reported for the first time, while Moniliformis type was reported as a first record in free ranging macaques, globally. This study clearly demonstrated that human contact and habitat modification may influence patterns of parasitic infections in macaques. As most of the parasite types identified manifest zoonotic potential, with public health implications, close associations of macaques may cause a threat to human well-being.
Eavesdropping magpies respond to the number of heterospecifics giving alarm calls but not the number of species calling
2019, Animal Behaviour
Social information varies in its reliability and relevance, requiring individuals to use rules to avoid inappropriate responses to false information. A simple rule is to respond only when a certain number of individuals provide similar information. Although individuals within social groups can use such numerical rules to assess conspecific information and make consensus decisions, it is unknown whether individuals apply similar rules when assessing the value of heterospecific information. We consider the case of individuals eavesdropping on heterospecific alarm calls. Eavesdroppers may be particularly vulnerable to false alarms because of the large pool of potential callers and variability in the specific threats to which they call. Individuals might therefore value alarm calls more if they come from multiple callers or multiple species than from a single caller or a single species. We tested these predictions using field playback experiments on wild Australian magpies, Gymnorhina tibicen. Magpies responded more strongly to alarm calls coming from two callers versus one caller of the same heterospecific species. However, in contrast to our prediction, magpies responded similarly to alarm calls from two individuals of different species as they did to alarm calls from two individuals of the same species. We conclude that the number of calling individuals does affect response, probably because information from multiple callers is more reliable, but that the value or reliability of information from multiple species may depend on the types of alarm calls and combination of species involved.
Fruits of the forest: Human stable isotope ecology and rainforest adaptations in Late Pleistocene and Holocene (∼36 to 3 ka) Sri Lanka
2017, Journal of Human Evolution
Citation Excerpt :
This, and the above interpretation of δ13C, highlights the main problem – equifinality –with detailed primate niche reconstructions on the basis of stable isotope analysis, in the absence of modern observation data (Roberts et al., 2017 - accepted in press). Elevated δ18O could simultaneously result from M. sinica drinking from open, evaporative water sources on the ground (Fooden, 1979; Dittus, 1984) and T. vetulus being a non-obligate drinker obtaining the majority of its water from foliage (Cerling et al., 2004; Krigbaum et al., 2013). In the case of the Sri Lankan Microlithic tradition, the basic zooarchaeological identification of these monkey species, with known ecological distinctions in the present, provides a better indication of human hunting strategies.
Sri Lanka has yielded some of the earliest dated fossil evidence for Homo sapiens (∼38-35,000 cal. years BP [calibrated years before present]) in South Asia, within a region that is today covered by tropical rainforest. Archaeozoological and archaeobotanical evidence indicates that these hunter-gatherers exploited tropical forest resources, yet the contribution of these resources to their overall subsistence strategies has, as in other Late Pleistocene rainforest settings, remained relatively unexplored. We build on previous work in this tropical region by applying both bulk and sequential stable carbon and oxygen isotope analysis to human and faunal tooth enamel from the sites of Batadomba-lena, Fa Hien-lena, and Balangoda Kuragala. Tooth enamel preservation was assessed by means of Fourier Transform Infrared Spectroscopy. We use these data to produce a detailed stable isotope ecology for Late Pleistocene–Holocene foragers in Sri Lanka from ∼36-29,000 to 3000 cal. years BP, allowing us to test the degree of human tropical forest resource reliance over a considerable time period. Given that non-human primates dominate the mammalian assemblages at these sites, we also focus on the stable isotope composition of three monkey species in order to study their ecological preferences and, indirectly, human hunting strategies. The results confirm a strong human reliance on tropical forest resources from ∼36-29,000 cal. years BP until the Iron Age ∼3 cal. years BP, while sequential tooth data show that forest resources were exploited year-round. This strategy was maintained through periods of evident environmental change at the Last Glacial Maximum and upon the arrival of agriculture. Long-term tropical forest reliance was supported by the specialised capture of non-human primates, although the isotopic data revealed no evidence for niche distinction between the hunted species. We conclude that humans rapidly developed a specialisation in the exploitation of South Asia's tropical forests following their arrival in this region.
Contextually variable signals can be functionally referential
2015, Animal Behaviour
Citation Excerpt :
For example, fork-tailed drongos, Dicrurus adsimilis, utter drongo-specific false alarm calls but also mimic false alarm calls of other target species (e.g. meerkats, Suricata suricatta, and pied babblers, Turdoides bicolor) to scare members of such species away from their food source, which they then steal (Flower, 2011; Flower, Gribble, & Ridley, 2014). Food-associated calls typically show even less stimulus specificity than alarm signals and are often produced in a variety of nonfeeding contexts (e.g. toque macaque, Macaca sinica: Dittus, 1984; Geoffroy's spider monkey, Ateles geoffroyi: Chapman & Lefebvre, 1990; rhesus macaques, Macaca mulatta: Hauser & Marler, 1993; golden lion tamarins, Leontopithecus roaslia: Halloy & Kleiman, 1994; cottontop tamarins, Saguinus oedipus: Roush & Snowdon, 2000; bonobos, Pan paniscus: Clay, Smith, & Blumstein, 2012; Clay & Zuberbühler, 2009). For example, golden lion tamarins and spider monkeys produce food calls during intergroup encounters and predator mobbing (Chapman & Lefebvre, 1990; Halloy & Kleiman, 1994).
With whom to dine? Ravens' responses to food-associated calls depend on individual characteristics of the caller
2015, Animal Behaviour
Upon discovering food, common ravens, Corvus corax, produce far-reaching ‘haa’ calls or yells, which are individually distinct and signal food availability to conspecifics. Here, we investigated whether ravens respond differently to ‘haa’ calls of known and unknown individuals. In a paired playback design, we tested responses to ‘haa’ call sequences in a group containing individually marked free-ranging ravens. We simultaneously played call sequences of a male and a female raven in two different locations and varied familiarity (known or unknown to the local group). Ravens responded strongest to dyads containing familiar females, performing more scan flights above and by perching in trees near the respective speaker. Acoustic analysis of the calls used as stimuli showed no sex-, age- or familiarity-specific acoustic cues, but highly significant classification results at the individual level. Taken together, our findings indicate that ravens respond to individual characteristics in ‘haa’ calls, and choose whom to approach for feeding, i.e. join social allies and avoid dominant conspecifics. This is the first study to investigate responses to ‘haa’ calls under natural conditions in a wild population containing individually marked ravens.
Food-associated vocalizations in mammals and birds: What do these calls really mean?
2012, Animal Behaviour
Citation Excerpt :
Golden-lion tamarins produce the ‘chuck’ call during feeding but also during intergroup encounters and predator mobbing (Halloy & Kleiman 1994). Toque macaques produce a specific call in response to food; however, they also sometimes produce this call during nonfood contexts associated with elation, such as at the onset of rain following dry periods, or on hot sunny days towards the end of the rainy season (Dittus 1984). Thus, although such calls may be associated with feeding, their production within nonfood contexts indicates that these calls may function more generally in social recruitment and may more accurately reflect the caller’s motivational response to an event rather than the caller’s discovery of food specifically.
Alarm calls and food-associated calls from a diverse range of species are said to be functionally referential, in that receivers can use these sounds to predict environmental events in the absence of other contextual cues. The evolutionary driver for referential alarm calls has been hypothesized to be the mutually incompatible escape behaviours required to avoid different predators. However, some species produce acoustically distinctive and referential alarm calls but do not show highly referential abilities in other domains. We examined whether food-associated calls in many species are likely to be functionally referential and whether they specifically communicate about characteristic features of food. Food-associated calls are given in both feeding and nonfeeding contexts, and the types of information contained vary greatly. Most species do not produce unique calls for different foods; more common is variation in the call rate, which suggests that call structure reflects the callers’ internal state rather than the food type. We also examined the ultimate function of food-associated calls to evaluate whether there is a unifying explanation for the evolution of functionally referential food calls. Based on the literature, there does not appear to be a unifying function. In conclusion, while functionally referential food-associated calls have been convincingly demonstrated in a few species, it is more common for these vocalizations to reflect arousal rather than additionally providing specific referential information about the feeding event. At this point, there is no compelling hypothesis to explain the evolution of functionally referential food-associated calls. Given the multiple functions of food-associated signals, we should not expect a unitary explanation.

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Animal Behaviour

Abstract

References (19)

Primate vocalizations: affective or symbolic?

The gestures of a gorilla: language acquisition in another pongid

Brain Lang.

Vervet monkey alarm calls: semantic communication in a free-ranging primate

Anim. Behav.

Observational study of behavior: sampling methods

Behaviour

The structure of primate social communication

The ecology of a semi-evergreen forest community in Sri Lanka

Biotropica

The social regulation of population density and age-sex distribution in the toque monkey

Behaviour

Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus, and related species

Smithson. Contrib. Zool.

Teaching sign language to a chimpanzee

Science, N. Y.

Cited by (125)

Effect of urbanization on zoonotic gastrointestinal parasite prevalence in endemic toque macaque (Macaca sinica) from different climatic zones in Sri Lanka

Eavesdropping magpies respond to the number of heterospecifics giving alarm calls but not the number of species calling

Fruits of the forest: Human stable isotope ecology and rainforest adaptations in Late Pleistocene and Holocene (∼36 to 3 ka) Sri Lanka

Contextually variable signals can be functionally referential

With whom to dine? Ravens' responses to food-associated calls depend on individual characteristics of the caller

Food-associated vocalizations in mammals and birds: What do these calls really mean?