Interspecies semantic communication in two forest primates

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.     

Arctic roars – laryngeal anatomy and vocalization of the muskox (Ovibos moschatus Zimmermann, 1780, Bovidae)

The impressive roaring of adult male muskoxen most often occurs during rutting contests. Roaring in adult females is primarily relevant to mother–infant communication. Loud roars are produced by taking up a specific roaring posture. Acoustic recordings were made in a small herd of zoo muskoxen during three successive rutting seasons. Earlier recordings of a different herd were used for comparison. Head-and-neck specimens were subjected to vascular injection, macroscopic anatomical dissection, computer tomographic analysis and skeletonization. Isolated preserved larynges of young animals were dissected for ontogenetic comparison. Despite a pronounced sexual dimorphism of head mass, larynx size is almost identical in adult male and female muskoxen, as is the fundamental frequency of their roars. Remarkably, the larynges of both sexes of muskoxen are provided with an unpaired ventrorostral ventricle. Probably, this ventricle is inflated during the initial phase of a roar. The ventricle may have two functions: to increase the amplitude of roaring and to darken the timbre of the roars by acting as an additional resonance space. The vocal fold of adult female and young individuals has a sharp rostral edge and a vocal ligament is still present. During male ontogeny the vocal ligament becomes transformed into a large fat pad extending into the wall of the laryngeal vestibulum. Accordingly, the glottic region in the adult male lacks any sharp edges of the mucosa. In both sexes the thyroarytenoid muscle is divided into three portions. A single roar may comprise phases of different sound volume. The roars of both muskox sexes are characterized by a pulsed structure. We suggest that two oscillating systems are involved in the production of roars: one comprising only the medial portion of the vocal fold and one including its lateral portion.     

The consequences of crowned eagle central-place foraging on predation risk in monkeys

The African crowned eagle (Stepahnoaetus coronatus) is the primary predator for arboreal primates throughout sub-Saharan forests. Monkeys typically respond with alarm calls when they are aware of the presence of crowned eagles and such calls can be considered a corollary of predation risk within primate groups. Alarm calls from six species of monkeys were recorded across the home range of an eagle pair in Taï National Park, Côte d''Ivoire. Spatial and temporal variation in primate alarm calling was found to be related to eagle ranging behaviour according to the predictions of central-place foraging models. Radio-tracking data indicate that eagle activity is higher in the centre of their home range and monkey alarm-calling rates are correspondingly elevated near eagle nests as opposed to farther away. Alarm-calling rates are also temporally coupled with measures of eagle activity. There were considerable differences between the species in both rates and spatial patterns of alarm calling. The variation we measure in predation risk is expected to have consequences at the behavioural and population level.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

Hornbills can distinguish between primate alarm calls

Some mammals distinguish between and respond appropriately to the alarm calls of other mammal and bird species. However, the ability of birds to distinguish between mammal alarm calls has not been investigated. Diana monkeys (Cercopithecus diana) produce different alarm calls to two predators: crowned eagles (Stephanoaetus coronatus) and leopards (Panthera pardus). Yellow-casqued hornbills (Ceratogymna elata) are vulnerable to predation by crowned eagles but are not preyed on by leopards and might therefore be expected to respond to the Diana monkey eagle alarm call but not to the leopard alarm call. We compared responses of hornbills to playback of eagle shrieks, leopard growls, Diana monkey eagle alarm calls and Diana monkey leopard alarm calls and found that they distinguished appropriately between the two predator vocalizations as well as between the two Diana monkey alarm calls. We discuss possible mechanisms leading to these responses.     

Roaring Behavior of Two Syntopic Howler Species (Alouatta caraya and A. guariba clamitans): Evidence Supports the Mate Defense Hypothesis

Long-distance calls are loud vocalizations involved in within and between group communication in animals. These calls may maintain cohesion with group members or communicate the ownership of valuable resources such as territory, food, or mates to individuals from other groups. In howlers (Alouatta spp.), three nonmutually exclusive hypotheses suggest that the ultimate function of roaring (howling) behavior is to protect resources from neighboring groups. The space/food defense hypothesis maintains that roars are used to gain exclusive access to food; the mate defense hypothesis holds that roars ensure exclusive access to mates; and the infanticide avoidance hypothesis states that the roaring behavior serves to avoid male takeovers and infanticide. To test these three hypotheses, we conducted a study on black-and-gold howlers (Alouatta caraya) and brown howlers (A. guariba clamitans) living in syntopy at El Pi?alito provincial park in northeast Argentina. We recorded 12 mo of data on the roaring behavior of two groups of each species, along with data on food availability and diet. Although all four groups overlapped extensively in their use of food resources during the study period, roars occurred much more frequently during interactions between groups of the same species than between groups of different species. Roaring frequency was not higher during the lean season, when high-quality food was less abundant. Howlers did not roar more frequently at home range boundaries, nor were roaring bouts spatially associated with valuable feeding resources. Males participated in all of the roaring bouts, whereas females participated in only 29% of them. Adults did not roar more frequently when there were unweaned infants in the group, as expected if roaring behavior decreases infanticide risk. These results provide no support for the food defense or infanticide avoidance hypotheses, but support predictions derived from the mate defense hypothesis.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

In order to increase understanding of African elephant vocal communication and to standardise the terminology used to describe vocalisations, this study examined acoustic and temporal characteristics of 983 vocalisations from 2 male and 6 female captive African elephants. Recording collars were used to monitor vocalisations and videotape to simultaneously record behaviour, allowing for unambiguous attribution of sounds to individuals, even in close proximity. Eight acoustically distinct categories of calls were defined in terms of structural characteristics; two of these categories are described for the first time. Low-frequency vocalisations containing infrasonic components were predominant in this localised communication context and showed a gradation of variation in acoustic structure and duration. Most calls were part of temporally closed exchanges between individuals and coincided with short-distance interactions. In addition, male-female choruses and non-musth rumbles from males were documented, suggesting that the African elephant vocal repertoire may be more complex than previously reported.     

Activity patterns at the Arctic Circle: nocturnal eagle owls and interspecific interactions during continuous midsummer daylight

Circadian rhythms result from adaptations to biotic and abiotic environmental conditions that cycle through the day, such as light, temperature, or temporal overlap between interacting species. At high latitudes, close to or beyond the polar circles, uninterrupted midsummer daylight may pose a challenge to the circadian rhythms of otherwise nocturnal species, such as eagle owls Bubo bubo. By non‐invasive field methods, we studied eagle owl activity in light of their interactions with their main prey the water vole Arvicola amphibius, and their competitor the white‐tailed eagle Haliaeetus albicilla during continuous midsummer daylight on open, treeless islands in coastal northern Norway. We evaluated circadian rhythms, temporal overlap, exposure, and spatial distribution. The owls maintained a nocturnal activity pattern, possibly because slightly dimmer light around midnight offered favourable hunting conditions. The eagles were active throughout the 24‐h period as opposed to the strictly diurnal rhythm reported elsewhere, thus increasing temporal overlap and the potential for interference competition between the two avian predators. This may indicate an asymmetry, with the owls facing the highest cost of interference competition. The presence of eagles combined with constant daylight in this open landscape may make the owls vulnerable to interspecific aggression, and contrary to the available literature, eagle owls rarely exposed themselves visually during territorial calls, possibly to avoid detection by eagles. We found indications of spatial segregation between owls and eagles reflecting differences in main prey, possibly in combination with habitat‐mediated avoidance. Eagle owl vocal activity peaked in the evening before a nocturnal peak in visual observations, when owls were active hunting, consistent with the hypothesis of a dusk chorus in nocturnal bird species. The owls may have had to trade‐off between calling and foraging during the few hours around midnight when slightly dimmer light reduced the detection risk while also providing better hunting conditions     

Vocal behaviour and neighbour spatial arrangement during vocal displays in eagle owls (Bubo bubo)

We quantified temporal and spatial patterns of adult eagle owl Bubo bubo vocal behaviour throughout an entire year. The duration of adult eagle owl vocal displays showed significant differences during different periods of the year: there was one major peak in the pre-laying period, when duets of mates were also more frequent. The daily distribution of adult vocalizations showed a similar pattern among the different periods, with vocal activity being most intense at sunset and sunrise. Analyses of the characteristics of call posts showed that the choice of such focal points was guided by the trade-off between the need to defend the territory and within-pair communication inside the core areas, as well as efficient communication with neighbours.     

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.     

Male blue monkeys alarm call in response to danger experienced by others

Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.     

Cross-Taxa Similarities in Affect-Induced Changes of Vocal Behavior and Voice in Arboreal Monkeys

Measuring the affective state of an individual across species with comparable non-invasive methods is a current challenge in animal communication research. This study aims to explore to which extent affect intensity is conveyed in the vocal behaviours of three nonhuman primate species (Campbell''s monkeys, De Brazza''s monkeys, red-capped mangabeys), which vary in body size, ecological niche and social system. Similarly in the three species, we experimentally induced a change in captive social groups'' affect by locking all group members together in their outside enclosure. The two experimental conditions which varied in affect intensity consisted in imposing a pre-reunion 90 mn-separation by splitting up the respective group into two subgroups (High affect condition) or not (Low affect condition). We measured call rates as well as voice features at the time of reunion in both conditions. The three studied species reacted in a very similar way. Across species, call rates changed significantly between the behaviourally defined states. Furthermore, contact call duration and, to some extent, voice pitch increased. Our results suggest, for the first time in arboreal Old World monkeys, that affect intensity is conveyed reliably in vocal behaviour and specific acoustic characteristics of voice, irrespective of body size and ecological niche differences between species. Cross-taxa similarities in acoustic cues of affect intensity point to phylogenetic constraints and inheritance from a common ancestor, whereas variations in vocal behaviour and affect intensity-related acoustic cues between species may be an adaptation to specific social requirements and depend on social systems. Our findings as well as a comparison with published works on acoustic communication in other vertebrate groups support the hypothesis that affect intensity in human voice originates from precursors already found deep inside the vertebrate phylogeny.     

BREEDING SUCCESS IN SOME AFRICAN EAGLES RELATED TO THEORIES ABOUT SIBLING AGGRESSION AND ITS EFFECTS

Brown, L. H., Gargett, V. & Steyn, P. 1977. Breeding success in some African Eagles related to theories about sibling aggression and its effects. Ostrich 48:65-71. Previous explanations for fatal inter-sibling strife in eagles (lack of food, extra aggressiveness which enhances survival, and an expression of the innate aggressiveness or territoriality of raptors) can not be supported by recent evidence. The latest theory, that the second egg acts as a “reserve”, is examined. If so, eagles normally laying two eggs should have better reproductive success than eagles laying a single egg. However there was no significant difference between the mean reproductive success of five African eagle species that lay two eggs and that of five African eagle species laying one egg. Even excluding inequalities due to sample size, and other factors, the overall finding is the same. In Verreaux's Eagle Aquila verreauxi for which the largest number of records is available there was a significantly higher total loss in clutches recorded as c/l than in c/2 clutches, but the reasons for the laying of a one-egg clutch, and its success or failure, have not been investigated. In three out of 120 c/2 the second-laid egg acted as a “reserve”, but in 110 cases the second-laid egg was “wasted”. Direct evidence and a comparison of reproductive success between two-egg and one-egg African eagles does not support the latest theory, therefore inter-sibling strife which effectively reduces the clutch of two to one, is still inexplicable.     

Mercury and persistent organic pollutant concentrations in African fish eagles, marabou storks, and Nile tilapia in Uganda

The purpose of this research was to evaluate persistent organic pollutant (POP) and mercury concentrations in tissues of African fish eagles (Haliaeetus vocifer) and Nile tilapia (Oreochromis niloticus) from Lake Victoria near Entebbe and Lake Mburo, Uganda. Marabou stork (Leptoptilos crumeniferus) nestlings from urban Kampala (40 km from Entebbe) also were sampled for POPs and mercury. Total mercury was measured in the breast feathers of eight nestling and 10 adult African fish eagles from Lake Mburo, 10 nestling and five adult African fish eagles from Lake Victoria near Entebbe, and 20 nestling marabou storks from Kampala from June 2002 through January 2003. Mercury concentrations in all samples were below levels associated with adverse effects in similar species. Mercury concentrations were significantly higher in eagle adults and nestlings from Entebbe than in adults and nestlings from Lake Mburo (P< or =0.05). No significant differences (P> or =0.05) were found in mercury concentrations between sexes or between the entire fish eagle population sampled at Entebbe and marabou stork nestlings sampled at nearby Kampala. Plasma samples from the same birds were analyzed for 1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane, aldrin, hexachlorocyclohexane (alpha-HCH), dieldrin, endrin, heptachlor and their metabolites, as well as total polychlorinated biphenyls (PCBs). Nile tilapia whole-body cross sections collected from Lake Mburo (n=3) and Lake Victoria near Entebbe (n=8) also were analyzed for these POPs and mercury. No samples contained POPs or PCBs at the limits of detection except for 4,4'-1,1-dichloro-2,2-bis(4-chlorophenyl)ethylene in five adult eagle plasma samples (0.0026+/-0.0015 ppm wet weight) and five Nile tilapia samples (0.002+/-0.001 ppm wet weight) from Entebbe.     

Leadership in elephants: the adaptive value of age

The value of age is well recognized in human societies, where older individuals often emerge as leaders in tasks requiring specialized knowledge, but what part do such individuals play in other social species? Despite growing interest in how effective leadership might be achieved in animal social systems, the specific role that older leaders may play in decision-making has rarely been experimentally investigated. Here, we use a novel playback paradigm to demonstrate that in African elephants (Loxodonta africana), age affects the ability of matriarchs to make ecologically relevant decisions in a domain critical to survival—the assessment of predatory threat. While groups consistently adjust their defensive behaviour to the greater threat of three roaring lions versus one, families with younger matriarchs typically under-react to roars from male lions despite the severe danger they represent. Sensitivity to this key threat increases with matriarch age and is greatest for the oldest matriarchs, who are likely to have accumulated the most experience. Our study provides the first empirical evidence that individuals within a social group may derive significant benefits from the influence of an older leader because of their enhanced ability to make crucial decisions about predatory threat, generating important insights into selection for longevity in cognitively advanced social mammals.     

Tetranucleotide microsatellites for aquila and haliaeetus eagles

A unique community of four syntopic eagle species exists in north‐central Kazakhstan. Questions about behaviour and genetics in these four species would benefit from the development of microsatellite markers. We isolated eight polymorphic microsatellite repeats (AAAG)_n from the eastern imperial eagle (Aquila heliaca) genome using a hybridization enrichment technique. These loci revealed moderate diversity in a local population of eastern imperial eagles (observed heterozygosity 0.26–0.78), and were also polymorphic in steppe eagles (A. nipalensis) and white‐tailed sea eagles (Haliaeetus albicilla). These primers may be polymorphic in other species of Aquila and Haliaeetus eagles.     

A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition

Although predation avoidance is the most commonly invoked explanation for vertebrate social evolution, there is little evidence that individuals in larger groups experience lower predation rates than those in small groups. We compare the morphological and behavioural traits of mammal prey species in the Taï forest, Ivory Coast, with the diet preferences of three of their non-human predators: leopards, chimpanzees and African crowned eagles. Individual predators show marked differences in their predation rates on prey species of different body sizes, but clear patterns with prey behaviour were apparent only when differences in prey habitat use were incorporated into the analyses. Leopard predation rates are highest for terrestrial species living in smaller groups, whereas eagle predation rates are negatively correlated with group size only among arboreal prey. When prey predation rates are summed over all three predators, terrestrial species incur higher predation rates than arboreal species and, within both categories, predation rates decline with increasing prey group size and decreasing density of groups in the habitat. These results reveal that it is necessary to consider anti-predator strategies in the context of a dynamic behavioural interaction between predators and prey.