Alban Lemasson

Campbell's monkeys concatenate vocalizations into context-specific call sequences

Primate vocal behavior is often considered irrelevant in modeling human language evolution, mainly because of the callers limited vocal control and apparent lack of intentional signaling. Here, we present the results of a long-term study on Campbells monkeys, which has revealed an unrivaled degree of vocal complexity. Adult males produced six different loud call types, which they combined into various sequences in highly context-specific ways. We found stereotyped sequences that were strongly associated with cohesion and travel, falling trees, neighboring groups, nonpredatory animals, unspecific predatory threat, and specific predator classes. Within the responses to predators, we found that crowned eagles triggered four and leopards three different sequences, depending on how the caller learned about their presence. Callers followed a number of principles when concatenating sequences, such as nonrandom transition probabilities of call types, addition of specific calls into an existing sequence to form a different one, or recombination of two sequences to form a third one. We conclude that these primates have overcome some of the constraints of limited vocal control by combinatorial organization. As the different sequences were so tightly linked to specific external events, the Campbells monkey call system may be the most complex example of ‘proto-syntax’ in animal communication known to date.

Patterns of vocal sharing and social dynamics in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli).

Although vocal sharing is widespread at several phylogenetic levels, few descriptions concerned primates. The present study involved the dynamics of vocal structures and social organization in a captive group of Campbells monkeys (Cercopithecus campbelli campbelli) at 3-year periods, using precise sound recording and comparison. The authors focused on combined harmonic 6 calls, often involved in vocal exchanges and associated with approaches. Each female produced 1 to 4 variants, shared, or not, between individuals. Changes appeared between years in the form of disappearance, appearance, or transformation of variants. There was a decrease in the global degree of sharing over the years. Greater changes were observed after social disturbance. Sharing would be more important in disturbed than stable groups to advertise bonds.

Sensory Perception in Cetaceans: Part I—Current Knowledge about Dolphin Senses As a Representative Species

A large part of the literature on sensory perception and behavior in dolphins is devoted to its well-developed vocal and echolocation abilities. In this review, we aim to augment current knowledge by examining the literature on dolphins’ entire “Merkwelt” (which refers to everything a subject perceives, creating a crucial part of the subject’s Umwelt). We will show that despite extensive knowledge on audition, aspects such as context relatedness, the social function of vocalizations or socio-sexual recognition, remain poorly understood. Therefore, we propose areas for further lines of investigation. Recent studies have shown that the sensory world of dolphins might well be much more diverse than initially thought. Indeed, although underwater and aerial visual systems differ in dolphins, they have both been shown to be important. Much debated electro- and magnetoreception appear to be functional senses according to recent studies. Finally, another neglected area is chemoreception. We will summarize neuroanatomical and physiological data on olfaction and taste, as well as corresponding behavioral evidence. Taken together, we will identify a number of technical and conceptual reasons for why chemosensory data appear contradictory, which is much debated in the literature. In summary, this article aims to provide both an overview of the current knowledge on dolphin perception, but also offer a basis for further discussion and potential new lines of research.

Sensory Perception in Cetaceans: Part II—Promising Experimental Approaches to Study Chemoreception in Dolphins

Chemosensory perception in cetaceans remains an intriguing issue as morphological, neuroanatomical and genetic studies draw unclear conclusions, while behavioral data suggest that dolphins may use it for food selection or socio-sexual interactions. Experimental approaches have been scarce due to the practical difficulties of testing chemoreception in wild dolphins. Go/no-go tasks are one elegant way to investigate discrimination abilities; however, they require to train the animals, thus preventing spontaneous responses and hence the expression of preferences. Here, we aimed at testing potential spontaneous responses to chemical stimuli and developed novel procedures. First, we conducted a study to test whether captive dolphins respond to a biologically relevant smell. Therefore, we placed dead fish within an opaque barrel at the border of the pool and counted the number of respirations at proximity as an indicator of investigation. The same dead fishes were presented several times during experiments lasting three consecutive days. From the second day on (i.e. when the odor composition changed), dolphins breathed more often close to the fish-smelling barrel than close to the visually identical but empty control barrel. Second, we conducted a study to test whether dolphins are able to discriminate food flavors. Captive dolphins are commonly provided with ice cubes as a source of enrichment. We took this opportunity to provide ice cubes with different flavors and to compare the reaction to these different flavors as a measure of discrimination. Hence, we used the latency of return to the ice cube begging spot as a measure of discrimination from the previous ice cube flavor. Thus, our method used a non-invasive and easily replicable technique based on the spontaneous begging responses of dolphins toward more or less attractive items bearing biological relevance. The procedures used enabled us to show that dolphins may discriminate odors and flavors respectively.

Cross-Amplified Polymorphic Microsatellites for Campbell’s Monkey

Population genetic analyses are of considerable importance for conservation strategies to protect endangered primates. We tested microsatellites of human origin with an aim to understand the genetic diversity of a West African forest guenon, Campbell’s monkey, Cercopithecus campbelli. Twelve markers amplified successfully, were polymorphic and were inherited in a Mendelian fashion in a group of 4 individuals kept in captivity. These 12 markers were further amplified from 35 faecal samples collected in Taï National Park. These samples proved to originate from 18 free-ranging monkeys and showed that the 12 markers we developed for this species are polymorphic and suitable for future population genetic and parentage analyses.

Influence of prenatal experience with human voice on the neonatal behavioural reaction to human voices with different emotion

Chronic stress is a long-lasting negative emotional state which induces negative consequences on animals’ behavior. This study aimed at assessing whether unpredictable and repeated negative stimuli (URNS) influence feeding behavior in quail, and whether this can be modulated by their emotionality. Two lines of quail divergently selected on their inherent emotionality (low emotionality, STI; high emotionality, LTI) were either daily exposed to URNS or undisturbed from 17 to 40 days of age (n=32 for each line, in each group). During this time, quail were submitted twice to a sequential feeding procedure: they were offered a hypocaloric diet (7% less caloric than the normocaloric diet) on odd days and a hypercaloric diet (7% more caloric) on even days, for 8 days; then, they received a normocaloric diet (metabolizable energy=12.56 MJ) for 3 days. This sequential feeding procedure was used to assess anhedonia and diet preferences thanks to choice tests (hypo vs. hypercaloric diets) performed at the end of each period. Short-term (30 min) and daily intake were also measured each day. Behavioral tests were performed to assess quail’s emotional reactivity. Results showed that URNS enhanced quails’ emotional reactivity, e.g. in the reactivity to human test, disturbed quail came later (P=0.011) and spent less time (P 0.1), but URNS reduced their daily intake during the 2nd period (P<0.05). Motivation for each diet (assessed by their short-term intake) was differently affected by URNS during the 2nd period: STI quail decreased their motivation to eat the hypercaloric diet (P<0.01) whereas LTI increased their motivation to eat the hypocaloric diet (P<0.01). In conclusion, both lines of quail experienced a chronic stress as URNS induced an increase of their emotional reactivity. Interestingly, URNS induced opposite changes in quail’s feeding behavior: LTI disturbed quail seemed to express a short-term compensatory behavior because of their high motivation to eat, whereas STI disturbed quail seemed to be in a devaluation process as shown by their anhedonia and their decrease of daily intake.Farm animals have to adapt to human presence from birth and being handled may lead to fear and stress reactions. It is known that the mother can be used as a postnatal model in the development of young-human relationship. Through her, some information like auditory ones may even be learnt prenatally. We tested this idea in pigs because they communicate a lot by acoustic signals. The hypotheses were that prenatal experience with human voice could modify behavioural reactions to the experienced voice and to an unfamiliar voice expressing different emotions. We worked with 30 pregnant sows from the last month of gestation. Ten sows (treatment A) were submitted to recordings of human voices during handling: vA during positive interactions and vB during negative interactions, twice a day, 5 days a week, for 10 minutes. Ten other sows (treatment B) received the contrary, i.e. vB during positive interactions and vA during negative interactions. Ten last sows (treatment C) received no vocal stimulations during handling sessions. Two days old piglets (36 A, 39 B, 35 C) were submitted to a 5 min choice test between voices vA and vB in a testing pen (2×1 m). Each voice was played back through loudspeakers positioned at each end of the pen. At 15-18 days of age, 20 other piglets from each treatment were tested in the same conditions except that we played back the voice of an unknown person, reading the same text with a joyful or angry intention. In both tests we recorded vocalisations and locomotion. Data were analysed using non parametric statistics (Statview). In both tests, A and B piglets started to move sooner (P 0.05) to be and the time spent (178 s (46s)) close to the loudspeakers did not depend on the treatment (P>0.05). We also found no difference between the time spent close to one loudspeaker or the other, neither for vA versus vB, nor for joyful versus angry intention (P>0.05). The results show that the prenatal experience of human voice reduces postnatal behavioural reactions of stress (vocalisations, latency to move) during the playback human voices. However, it does not seem to induce specific attraction toward human voice, or human emotional intention. Therefore prenatal experience with human voice may be a good way of reducing fear reactions to human voice after birth.

VOCAL ABILITIES IN A GROUP OF NONHUMAN PRIMATES

Human language is too complex to have emerged in the absence of any evolutionary precursors, which suggests that primitive forms of pre-linguistic communication can be found in animals. Whether this was based on acoustic or gestural communication is an ongoing debate. An argument against a vocal origin is the absence of vocal flexibility and complexity in non-human primates. However, human language is primarily a vocal behaviour, and vocal flexibility – as assessed by vocal plasticity, semanticity, compositionality, and intentional signalling - is not a uniquely human trait. Our research focuses on the precursors of the various types of vocal flexibility in forest guenons (Cercopithecus spp). The vocal tract of nonhuman primates is in principle capable of producing speech-like sounds (Riede et al 2005) and one puzzle is why nonhuman primates do not make greater use of this feature. Instead, primates produce a finite range of calls that develop under strong genetic control. Within some call types, however, some flexibility can be seen at the level of call morphology, as for example demonstrated by socially-determined vocal plasticity and vocal sharing in Campbells monkey contact calls used in conversation-like socially controlled vocal exchanges (Lemasson & Hausberger 2004; Lemasson et al 2010). Second, many primates produce acoustically distinct calls to specific external events, including Diana and Campbells monkeys. In both species, the adult males and females produce acoustically different alarm calls to the same predator (Ouattara et al 2009a), but calls are meaningful to others, both within and between species. Alarm calls are not only predator-specific but also vary depending on the modality by which the predator is discovered, i.e. the visual or acoustic domain. In Campbells monkeys females produced a complex alarm call repertoire, although differences were found between captive and wild individuals. Captive ones did not produce predator-specific calls but had a unique call to humans (Ouattara et al 2009a). For males, we found a repertoire of six call types, which could be classified into different morphs, according to the frequency contour and whether calls were trailed by an acoustically invariable suffix. Suffixed calls carried a broader meaning than unsuffixed ones (Ouattara et al 2009b). The six calls were concatenated into context-specific call sequences, following basic combinatorial principles (Ouattara et al 2009c). In sum, the vocal abilities in guenons go significantly beyond the currently assumed default case for nonhuman primates. Flexibility can be seen at all relevant levels, including limited control over call morphology, conversational rules, ability to produce context-specific calls, and some basic combinatorial properties. The data are at odds with a gestural origins of language theory. Gestural signals do not appear to play a key role in these species, while vocal flexibility is seen in all key components despite the fact that they have split from the human line about 30 million years ago. Field playback experiments will be needed to confirm whether receivers utilise these rich patterns to guide their behavioural decisions. But even in the absence of such evidence data suggest that a strong dichotomy between human language and nonhuman primate communication may no longer be tenable in the vocal domain. The visually dense forest habitat may have played a key role in the evolution of advanced vocalisation skills.