Acoustic convergence and divergence in two sympatric burrowing nocturnal seabirds

Shearwaters are nocturnal burrowing seabirds. They return to their colony at dusk and exhibit high vocal activity, underlining the usefulness of acoustic cues to nocturnal communication. The present study aimed to test whether acoustic communication systems of two sympatric shearwater species, the Yelkouan shearwater Puffinus yelkouan and the Mediterranean Cory's shearwater Calonectris diomedea diomedea , converge to similar strategies. Inter-annual mate fidelity and incubation relays led us to focus on sex and individual acoustic signatures. We first characterized those two signatures by analysing the major call emitted by incubating birds. Second, we performed playback experiments to assess ability of birds to vocally discriminate between sexes and mate versus non-mate. The results obtained show that both species use a reliable sex vocal signature supported by frequency and energy features, enabling sex identification of the emitter. By responding only to conspecific same-sex calls, birds may ensure burrow and mate guarding. Conversely, individual vocal signature was mainly supported by temporal parameters, and was more reliable in the Cory's shearwater. Moreover, this species uses vocal exchanges to identify the mate during incubation relays, whereas Yelkouan shearwaters probably need additional cues. In conclusion, we observe an evolutionary convergence in intra-sex communication process but a divergence in mate greeting strategy.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 115–134.     

Sex-specific responses to vocal convergence and divergence of contact calls in orange-fronted conures (Aratinga canicularis)

We investigated the signal function of vocal imitation of contact calls in orange-fronted conures (OFCs; Aratinga canicularis) in Costa Rica. OFCs live in dynamic social systems with frequent flock fusions and fissions. Exchanges of contact calls precede these flock changes. During call exchanges, the similarity between the contact calls of different individuals may either increase (converge) or decrease (diverge). We conducted a playback experiment on wild-caught captive birds in which we simulated convergent, divergent and no-change interaction series with male and female contact calls. OFCs responded differently to convergent and divergent series of contact calls, but only when we considered the sex of the test birds. Males called most in response to convergent series, whereas females demonstrated high calling rates in response to both convergent and divergent interactions. Both sexes responded most to contact calls from the opposite sex, but overall females produced more calls and had shorter latencies to calling than males. These results demonstrate that OFCs can discriminate between male and female contact calls and that subtle changes in contact call structure during interactions have signal function. The stronger overall response to convergent series suggests that convergence of contact calls is an affiliative signal.     

Selection for acoustic individuality within the vocal repertoire of wild chimpanzees

Individual primates typically produce acoustically distinct calls. To investigate the factors that facilitate the evolution of individual vocal signatures, we examined two components of the call repertoire of chimpanzees: the pant hoot and pant grunt. Pant hoots are long-distance signals whose recipients can be several hundred meters away, while pant grunts are short-range calls given to conspecifics within close visual range. Given their markedly different contexts of emission, we predicted that natural selection would favor the elaboration of individually distinctive acoustic features in pant hoots compared with pant grunts. Analyses of nine acoustic features revealed that pant hoots are more stereotyped within-individuals and variable between-individuals than pant grunts. These data are consistent with the hypothesis that selection may act to encode varying degrees of individuality in different components of the vocal repertoire of a single species.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Assessment of early placental development in the cynomolgus monkey (Macaca fascicularis) using colour and pulsed wave Doppler sonography

Abstract: Colour flow mapping and pulsed wave Doppler were used to assess the process of placental growth and development in the cynomolgus monkey from 32 to 71 days gestational age. Fetal and maternal vessels were reliably visualised and insonated. Accurate longitudinal non-invasive assessment of placentation is possible using this technique.     

Variation in primate decision-making under uncertainty and the roots of human economic behaviour

Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generate this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here, we examine decision-making under risk across non-human primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess the current evidence for variation in animal preferences between species and populations, between individuals based on personality, sex and age, and finally, between different contexts and individual states. We then use these primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Preliminary observations on squirrel monkey (Saimiri oerstedi) vocalizations in Costa Rica

This study was an initial attempt to analyze quantitatively vocalizations from the Central American squirrel monkey, Saimiri oerstedi. Vocalizations were recorded in the wild at P. N. Corcovado (S. o. oerstedi). and at P. N. Manuel Antonio (S. o. citrinellus). Additional recordings were made from captive individuals of both subspecies. The acoustic structure of analyzed vocalizations resembled most closely the vocal repertoire of South American Saimiri with the “gothic arch” phenotype, in agreement with the prominent gothic arch facial pattern of S. oerstedi. New structural subtypes of the twitter (“dog-tooth twitter”) and the chuck (“bent-mast chuck”) not previously found in an extensive library of South American Saimiri sound spectrograms were documented. Calls used by older infants when socially separated and when approaching an adult male were essentially identical (sharing typical “isolation peep” structural features) but had significantly different duration and peak frequency. Analysis of recordings from an escaped captive female calling outside her compound over a 3-day period indicated the presence of numerous structural intermediates between typical chuck, twitter, and peep calls.     

Versatility in a loud call: Dual affiliative and agonistic functions in the blue monkey boom

To investigate the selective agents that shape signals, we examined function (adaptive benefit to signaler) in the boom loud call by male blue monkeys. Using natural observation and playbacks in a wild population in Kenya, we characterized boom function from conspecifics' behavioral responses and also variation in call usage relating to context and reproductive season. Booms occurred in several contexts and after varied stimuli, including falling branches, yet were strongly associated with intragroup activity and, in particular, affiliative interactions between callers and females. Males produced more booms during the mating season and, congruently, when more females in their groups were sexually active. After hearing booms, compared to no call, females spent more time near groupmates and the caller and were more likely to approach and have mating interactions with him. Males tended to move away after hearing a boom. In the aggregate, results indicate that booms achieve multiple functions relating to facilitating group cohesion, affiliative interactions, and mating opportunities, while also repelling rival males. An observed association with falling branches is puzzlingly distinct from these social functions. We explore the hypothesis that booms enable affiliative encounters by acting as signals of benign intent, and discuss the functional versatility of signals perceived by multiple receivers that vary in age, sex, and relationship to signalers.     

Multimodal communication and language origins: integrating gestures and vocalizations

The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non‐human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn‐taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close‐range communication, whereas the opposite holds for face‐to‐face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.     

Clinical outcome of a protocol to produce immunosuppression in rhesus monkeys (Macaca mulatta): application to infectious disease and gene therapy studies

Induced immunosuppression is required for a number of studies using rhesus monkeys (Macaca mulatta). This report describes the clinical outcome and safety of a dose-finding experiment that determined doses of cyclophosphamide and prednisone that could be used to induce a state of immunosuppression in rhesus monkeys. After determining the optimum dose of immunosuppressive agents, the protocol was then used on animals participating in infectious disease and gene therapy studies. Splenectomy was performed in some animals to increase the severity of immunosuppression. The onset, duration, and severity of lymphopenia and leukopenia were consistent in all animals. In most animals, physical examination findings and clinical serum chemistry profiles demonstrated only transient abnormalities. With proper clinical monitoring, combination treatment with cyclophosphamide and prednisone is an effective and safe method for inducing immunosuppression in rhesus monkeys.     

Abdominal pregnancy in a baboon: a first case report

The abdominal pregnancy is a rare, but life threatening complication of ectopic embryo implantation. Only three cases of abdominal pregnancy have been previously described in primates: in a squirrel monkey, owl monkey and in a rhesus macaque. A 14-year-old wild-caught olive baboon (Papio cynocephalus anubis) was diagnosed at the ultrasound examination with advanced gestational age extrauterine pregnancy. At the initial laparotomy and necropsy the diagnosis of abdominal pregnancy was made on Studdiford's criteria. This case indicates the possibility of developing a model for further study of different types of ectopic pregnancy and indicates a cesarean section as a risk factor for abdominal pregnancy.     

A novel Brucella isolate in association with two cases of stillbirth in non-human primates – first report

Background  Brucellosis is veterinary and human health problem.
Methods  A 13-year-old wild caught multiparous and an 8-year-old colony-born nulliparous baboon had stillbirths in the second trimester of pregnancy. Culture isolates from both postpartum uteruses were characterized using traditional biochemical analysis, PCR, and multilocus sequencing.
Results  The isolates morphologically resembled Brucella although their phenotypic characteristics were not consistent with any currently described species. The isolates represent a novel lineage within the genus with unique alleles, not previously seen in surveys of greater than 300 isolates representing the known diversity of the genus, present at 5/9 loci examined.
Conclusions  The described cases are to the best of our knowledge the first presentation of a naturally acquired Brucella infection in non-human primates associated with stillbirths from the same colony where Brucella seropositivity in the baboons was described 45 years ago. The organism appears to represent a previously undescribed Brucella species.     

A case study of male tawny owl (Strix aluco) vocalizations in South Korea: call feature,individuality, and the potential use for census

Vocal individuality has been used as a monitoring tool, and two criteria are a prerequisite: high variation among individuals and low variation within individuals, and vocal consistency within and across seasons. We examined individual variation in the territorial hoot calls of the tawny owl (Strix aluco) to discriminate between males and to assess a possible conservation technique that would allow for monitoring individuals within a study area. The territorial calls were recorded from five males in the Naejang Mountain National Park in South Korea during the breeding season in 2015 and 2016 and analyzed both quantitatively and qualitatively to determine the amount of variation within and between individuals. Our results showed that the territorial calls were specific to individuals within a population and that the acoustic distances between males living in the same territory during the two years were the smallest for the four nesting sites. Our results suggest that territorial calls of the tawny owls are individually identifiable over two years and that this acoustic technique can be useful for monitoring individual site fidelity.     

Development of an enzyme-immunoassay (EIA) for the measurement of follicle-stimulating-hormone (FSH) in callitrichid primates using a monoclonal antibody against the human-FSH-β-subunit

Despite the importance of Callitrichid primates in both biomedical and conservation research, practical and reliable immunoassays for the measurement of follicle-stimulating hormone (FSH) have not yet been described. A panel of monoclonal antibodies against specific peptide fragments within either the alpha or beta subunit of human FSH was evaluated for their ability to recognize FSH from Callitrichid and other New World primates. One of these, monoclonal antibody 46.3h6.b7 raised against human FSH, was selected due to its ability to recognize marmoset monkey FSH and its low crossreactivity with other gonadotrophins. The antibody formed the basis of an enzymeimmunoassay using a highly purified human urinary FSH (Metrodin®, Serono) preparation coupled to biotin as label and unmodified as standard. After 24 h incubation, antibody bound label was visualized by addition of streptavidin-peroxidase followed by the appropriate substrate. Parallelism was obtained between the standard and dilutions of pituitary extracts, urine and plasma from the common marmoset (Callithrix jacchus) as well as from two tamarin species (Saguinus fuscicollis and S. oedipus) and one squirrel monkey (Saimiri sciureus). Profiles of plasma and urinary FSH during the follicular phase are shown for two individual marmosets. The ability to measure FSH in Callitrichidae provides new opportunities for studies of the reproductive biology of these New World primate species. Am. J. Primatol. 41:179–193, 1997. © 1997 Wiley-Liss, Inc.     

Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human-transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae

Background  During an outbreak of respiratory disease in captive chimpanzees ( Pan troglodytes ), gorillas ( Gorilla gorilla ), Bornean orangutans ( Pongo pygmaeus ), and red-capped mangabeys ( Cercocebus torquatus ) also staff members showed non-specific upper respiratory signs. One infant female chimpanzee with severe respiratory symptoms died despite immediate medical treatment and was submitted for necropsy.
Methods  Routine post mortem, histological and bacteriological examinations were conducted. Additionally lung tissue samples form the chimpanzee and swab samples from the staff members and the other primates were examined by PCR.
Results  A severe catarrhal to purulent bronchopneumonia and an interstitial pneumonia were found and human respiratory syncytial virus (HRSV) as well as Streptococcus pneumoniae was detected in lung samples by PCR. Swab samples from one animal keeper revealed the same HRSV sequence as of the chimpanzee.
Conclusions  Therefore, it is suggested that the outbreak of respiratory disease within a zoological institution was due to transmission of HRSV between both human and primates.     

Comparison of rectal and infrared thermometry for obtaining body temperature in cynomolgus macaques (Macaca fascicularis)

BACKGROUND: It would be clinically advantageous to develop a method of body temperature evaluation in cynomolgus macaques (Macaca fascicularis) that did not require sedation, restraint, surgical manipulation, or expensive equipment. METHODS: Body temperatures of 51 cynomolgus macaques were taken with rectal thermometry and non-contact infrared thermometry (NIFT) on the shoulder, face, abdomen, and axillary region. RESULTS AND CONCLUSIONS: Body temperature measurements from NIFT were statistically different (P < 0.0001) from rectal thermometry. In addition, there was greater between- and within-subject variability in values using NIFT. There was no correlation between any sites of the NIFT and rectal thermometry. It was concluded that NIFT was not a valid alternative to rectal thermometry in cynomolgus macaques.     

Hematology and serum chemistry parameters in juvenile cynomolgus monkeys (Macaca fascicularis) of Mauritius origin: comparison between purpose-bred and captured animals

Background  The vast majority of non-human primates used for experimental activities are purpose-bred. However, in case of particular procedures or specific projects, it may still be necessary to use animals captured in the wild.
Methods  Sixty cynomolgus monkeys were randomly selected on the basis of breeding origin, and assigned to two groups, each of fifteen males and fifteen females. Analyses included the most frequently investigated parameters for hematology, coagulation, and biochemistry.
Results  Differences were observed in some parameters, particularly in eosinophils, basophils and monocytes, and in fibrinogen, total protein, globulins, alanine amino-transferase, creatinine, aspartate amino-transferase, alkaline phosphatase, γ-glutamyl transferase, lactate dehydrogenase, α-hydroxybutyrate dehydrogenase, iron, potassium, and phosphorus.
Conclusions  Some values in the cynomolgus monkey may show significant differences according to the breeding background of the animals. Only data obtained from animals of similar origin have to be compared, to avoid misinterpretation during the evaluation of the experimental results.     

Immunogenicity of a DNA prime and recombinant adenovirus boost regime significantly varies between rhesus macaques of Chinese and Indian origins

BACKGROUND: Due to an ever increasing shortage of rhesus macaques of Indian origin (InR) that have been generally used for preclinical AIDS vaccine trials in non-human primates, demand is rising for Chinese rhesus macaques (ChR). However, the immunogenicity of an AIDS vaccine candidate has not been compared in parallel in both rhesus macaque subspecies. METHODS: ChR and InR were immunized with SIV/HIV DNA and adenovirus vaccine and their immune responses to SIV and HIV evaluated. RESULTS: SIV Gag- and Env-specific T-cell responses and SIV-specific lymphoproliferative responses measured in ChR were significantly weaker than those in InR (P < 0.05). By contrast, antibody responses to SIV Env, Tat, and Nef in ChR were stronger than those in InR (P < 0.05). CONCLUSIONS: Immunogenicity of an AIDS vaccine can vary significantly depending on the geographic origin implying genetic differences of macaques. This must be considered when describing and interpreting results of such vaccine studies.