Declarative referential gesturing in a wild chimpanzee (Pan troglodytes).

Humans are argued to be unique in their ability and motivation to share attention with others about external entities-sharing attention for sharing's sake. Indeed, in humans, using referential gestures declaratively to direct the attention of others toward external objects and events emerges in the first year of life. In contrast, wild great apes seldom use referential gestures, and when they do, it seems to be exclusively for imperative purposes. This apparent species difference has fueled the argument that the motivation and ability to share attention with others is a human-specific trait with important downstream consequences for the evolution of our complex cognition [M. Tomasello, Becoming Human (2019)]. Here, we report evidence of a wild ape showing a conspecific an item of interest. We provide video evidence of an adult female chimpanzee, Fiona, showing a leaf to her mother, Sutherland, in the context of leaf grooming in Kibale Forest, Uganda. We use a dataset of 84 similar leaf-grooming events to explore alternative explanations for the behavior, including food sharing and initiating dyadic grooming or playing. Our observations suggest that in highly specific social conditions, wild chimpanzees, like humans, may use referential showing gestures to direct others' attention to objects simply for the sake of sharing. The difference between humans and our closest living relatives in this regard may be quantitative rather than qualitative, with ramifications for our understanding of the evolution of human social cognition.

Many morphs: Parsing gesture signals from the noise.

Parsing signals from noise is a general problem for signallers and recipients, and for researchers studying communicative systems. Substantial efforts have been invested in comparing how other species encode information and meaning, and how signalling is structured. However, research depends on identifying and discriminating signals that represent meaningful units of analysis. Early approaches to defining signal repertoires applied top-down approaches, classifying cases into predefined signal types. Recently, more labour-intensive methods have taken a bottom-up approach describing detailed features of each signal and clustering cases based on patterns of similarity in multi-dimensional feature-space that were previously undetectable. Nevertheless, it remains essential to assess whether the resulting repertoires are composed of relevant units from the perspective of the species using them, and redefining repertoires when additional data become available. In this paper we provide a framework that takes data from the largest set of wild chimpanzee (Pan troglodytes) gestures currently available, splitting gesture types at a fine scale based on modifying features of gesture expression using latent class analysis (a model-based cluster detection algorithm for categorical variables), and then determining whether this splitting process reduces uncertainty about the goal or community of the gesture. Our method allows different features of interest to be incorporated into the splitting process, providing substantial future flexibility across, for example, species, populations, and levels of signal granularity. Doing so, we provide a powerful tool allowing researchers interested in gestural communication to establish repertoires of relevant units for subsequent analyses within and between systems of communication.

[Retrospective Study of Long-term Patient Satisfaction after Bilateral Implantation of Multifocal Intraocular Lenses of Different Generations - a 10 Year Follow-up]. / Patientenzufriedenheit nach Implantation von Multifokallinsen verschiedener Generationen ­ ein 10-Jahres-Follow-up.

BACKGROUND: This retrospective study investigates the postoperative satisfaction of patients with a mixed generation background after bilateral implantation of non-toric multifocal intraocular lenses between the year 2006 and year 2017. PATIENTS/METHODS: 245 patients between 45 and 95 years old were included in the study. Patient satisfaction was examined with the Heidelberg DATE questionnaire (DATE: Daily Tasks Evaluation), with respect to everyday tasks and the perception of optical phenomena. All criteria of the questionnaire were assessed for significant differences with respect to the time of the operation, the age of the patient, gender as well as the model of the implanted intraocular lens. The data was analysed with the statistics software SPSS 23.0. RESULTS: At the time of the survey, 97.1% of patients reported they were completely or partially satisfied with the outcome of the operation. 95.9% of patients could accomplish all common tasks without any significant problems. 34.6% said they only needed glasses under very challenging visual circumstances. The older patients more often reported that they needed glasses (p < 0.01). Women wore glasses more frequently for driving during night than men. They also described dazzling as more disturbing (p < 0.03). Younger patients perceived halos more drastically than older patients (p < 0.01). Patients with bifocal lens implants used glasses for intermediary distances far more often than patients with trifocal implants (p < 0.01). CONCLUSION: Most patients were independent of additional optical correction. Optical phenomena are commonly reported, so extensive preoperative briefing is inevitable. The need for further information seems to be especially high among younger, female patients. The Heidelberg DATE questionnaire is well suited for surveying patient satisfaction after the implantation of multifocal intraocular lenses.

Social, contextual, and individual factors affecting the occurrence and acoustic structure of drumming bouts in wild chimpanzees (Pan troglodytes).

The production of structured and repetitive sounds by striking objects is a behavior found not only in humans, but also in a variety of animal species, including chimpanzees (Pan troglodytes). In this study we examined individual and social factors that may influence the frequency with which individuals engage in drumming behavior when producing long distance pant hoot vocalizations, and analyzed the temporal structure of those drumming bouts. Male chimpanzees from Budongo Forest, Uganda, drummed significantly more frequently during travel than feeding or resting and older individuals were significantly more likely to produce drumming bouts than younger ones. In contrast, we found no evidence that the presence of estrus females, high ranking males and preferred social partners in the caller's vicinty had an effect on the frequency with which an individual accompanied their pant hoot vocalization with drumming. Through acoustic analyses, we demonstrated that drumming sequences produced with pant hoots may have contained information on individual identity and that qualitatively, there was individual variation in the complexity of the temporal patterns produced. We conclude that drumming patterns may act as individually distinctive long-distance signals that, together with pant hoot vocalizations, function to coordinate the movement and spacing of dispersed individuals within a community, rather than as signals to group members in the immediate audience.

Chimpanzee gestural exchanges share temporal structure with human language.

Humans regularly engage in efficient communicative conversations, which serve to socially align individuals1. In conversations, we take fast-paced turns using a human-universal structure of deploying and receiving signals which shows consistent timing across cultures2. We report here that chimpanzees also engage in rapid signal-to-signal turn-taking during face-to-face gestural exchanges with a similar average latency between turns to that of human conversation. This correspondence between human and chimpanzee face-to-face communication points to shared underlying rules in communication. These structures could be derived from shared ancestral mechanisms or convergent strategies that enhance coordinated interactions or manage competition for communicative 'space'.

Network analysis of social changes in a captive chimpanzee community following the successful integration of two adult groups.

Chimpanzees are highly territorial and have the potential to be extremely aggressive toward unfamiliar individuals. In the wild, transfer between groups is almost exclusively completed by nulliparous females, yet in captivity there is often a need to introduce and integrate a range of individuals, including adult males. We describe the process of successfully integrating two groups of chimpanzees, each containing 11 individuals, in the Budongo Trail facility at the Royal Zoological Society of Scotland's Edinburgh Zoo. We use social network analysis to document changes in group dynamics within this population over the 16 months following integration. Aggression rates were low overall and members of the two original groups engaged in significantly fewer aggressive interactions over time. Association and grooming data indicate that relationships between members of the original groups became stronger and more affiliative with time. Despite these positive indicators the association data revealed the continued existence of two distinct subgroups, a year after integration. Our data show that when given complex space and freedom to exhibit natural fission-fusion groupings, in which the chimpanzees choose whom they wish to associate and interact with, the building of strong affiliative relationships with unfamiliar individuals is a very gradual process.

Call combinations and compositional processing in wild chimpanzees.

Through syntax, i.e., the combination of words into larger phrases, language can express a limitless number of messages. Data in great apes, our closest-living relatives, are central to the reconstruction of syntax's phylogenetic origins, yet are currently lacking. Here, we provide evidence for syntactic-like structuring in chimpanzee communication. Chimpanzees produce "alarm-huus" when surprised and "waa-barks" when potentially recruiting conspecifics during aggression or hunting. Anecdotal data suggested chimpanzees combine these calls specifically when encountering snakes. Using snake presentations, we confirm call combinations are produced when individuals encounter snakes and find that more individuals join the caller after hearing the combination. To test the meaning-bearing nature of the call combination, we use playbacks of artificially-constructed call combinations and both independent calls. Chimpanzees react most strongly to call combinations, showing longer looking responses, compared with both independent calls. We propose the "alarm-huu + waa-bark" represents a compositional syntactic-like structure, where the meaning of the call combination is derived from the meaning of its parts. Our work suggests that compositional structures may not have evolved de novo in the human lineage, but that the cognitive building-blocks facilitating syntax may have been present in our last common ancestor with chimpanzees.

Maternal attitudes and behaviours differentially shape infant early life experience: A cross cultural study.

Early life environments afford infants a variety of learning opportunities, and caregivers play a fundamental role in shaping infant early life experience. Variation in maternal attitudes and parenting practices is likely to be greater between than within cultures. However, there is limited cross-cultural work characterising how early life environment differs across populations. We examined the early life environment of infants from two cultural contexts where attitudes towards parenting and infant development were expected to differ: in a group of 53 mother-infant dyads in the UK and 44 mother-infant dyads in Uganda. Participants were studied longitudinally from when infants were 3- to 15-months-old. Questionnaire data revealed the Ugandan mothers had more relational attitudes towards parenting than the mothers from the UK, who had more autonomous parenting attitudes. Using questionnaires and observational methods, we examined whether infant development and experience aligned with maternal attitudes. We found the Ugandan infants experienced a more relational upbringing than the UK infants, with Ugandan infants receiving more distributed caregiving, more body contact with their mothers, and more proximity to mothers at night. Ugandan infants also showed earlier physical development compared to UK infants. Contrary to our expectations, however, Ugandan infants were not in closer proximity to their mothers during the day, did not have more people in proximity or more partners for social interaction compared to UK infants. In addition, when we examined attitudes towards specific behaviours, mothers' attitudes rarely predicted infant experience in related contexts. Taken together our findings highlight the importance of measuring behaviour, rather than extrapolating expected behaviour based on attitudes alone. We found infants' early life environment varies cross-culturally in many important ways and future research should investigate the consequences of these differences for later development.

Detecting joint attention events in mother-infant dyads: Sharing looks cannot be reliably identified by naïve third-party observers.

Joint attention, or sharing attention with another individual about an object or event, is a critical behaviour that emerges in pre-linguistic infants and predicts later language abilities. Given its importance, it is perhaps surprising that there is no consensus on how to measure joint attention in prelinguistic infants. A rigorous definition proposed by Siposova & Carpenter (2019) requires the infant and partner to gaze alternate between an object and each other (coordination of attention) and exchange communicative signals (explicit acknowledgement of jointly sharing attention). However, Hobson and Hobson (2007) proposed that the quality of gaze between individuals is, in itself, a sufficient communicative signal that demonstrates sharing of attention. They proposed that observers can reliably distinguish "sharing", "checking", and "orienting" looks, but the empirical basis for this claim is limited as their study focussed on two raters examining looks from 11-year-old children. Here, we analysed categorisations made by 32 naïve raters of 60 infant looks to their mothers, to examine whether they could be reliably distinguished according to Hobson and Hobson's definitions. Raters had overall low agreement and only in 3 out of 26 cases did a significant majority of the raters agree with the judgement of the mother who had received the look. For the looks that raters did agree on at above chance levels, look duration and the overall communication rate of the mother were identified as cues that raters may have relied upon. In our experiment, naïve third party observers could not reliably determine the type of look infants gave to their mothers, which indicates that subjective judgements of types of look should not be used to identify mutual awareness of sharing attention in infants. Instead, we advocate the use of objective behaviour measurement to infer that interactants know they are 'jointly' attending to an object or event, and believe this will be a crucial step in understanding the ontogenetic and evolutionary origins of joint attention.

Approach Direction Prior to Landing Explains Patterns of Colour Learning in Bees.

Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect's movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.

Scratching beneath the surface: intentionality in great ape signal production.

Despite important similarities having been found between human and animal communication systems, surprisingly little research effort has focussed on whether the cognitive mechanisms underpinning these behaviours are also similar. In particular, it is highly debated whether signal production is the result of reflexive processes, or can be characterized as intentional. Here, we critically evaluate the criteria that are used to identify signals produced with different degrees of intentionality, and discuss recent attempts to apply these criteria to the vocal, gestural and multimodal communicative signals of great apes and more distantly related species. Finally, we outline the necessary research tools, such as physiologically validated measures of arousal, and empirical evidence that we believe would propel this debate forward and help unravel the evolutionary origins of human intentional communication. This article is part of the theme issue 'What can animal communication teach us about human language?'

Speciation of the trivalent f-elements Eu(III) and Cm(III) in digestive media.

In case radioactive materials are released into the environment, their incorporation into our digestive system would be a significant concern. Trivalent f-elements, i.e., trivalent actinides and lanthanides, could potentially represent a serious health risk due to their chemo- and radiotoxicity, nevertheless the biochemical behavior of these elements are mostly unknown even to date. This study, therefore, focuses on the chemical speciation of trivalent f-elements in the human gastrointestinal tract. To simulate the digestive system artificial digestive juices (saliva, gastric juice, pancreatic juice and bile fluid) were prepared. The chemical speciation of lanthanides (as Eu(III)) and actinides (as Cm(III)) was determined experimentally by time-resolved laser-induced fluorescence spectroscopy (TRLFS) and the results were compared with thermodynamic modeling. The results indicate a dominant inorganic species with phosphate/carbonate in the mouth, while the aquo ion is predominantly formed with a minor contribution of the enzyme pepsin in the stomach. In the intestinal tract the most significant species are with the protein mucin. We demonstrated the first experimental results on the chemical speciation of trivalent f-elements in the digestive media by TRLFS. The results highlight a significant gap in chemical speciation between experiments and thermodynamic modeling due to the limited availability of thermodynamic stability constants particularly for organic species. Chemical speciation strongly influences the in vivo behavior of metal ions. Therefore, the results of this speciation study will help to enhance the assessment of health risks and to improve decorporation strategies after ingestion of these (radio-)toxic heavy metal ions.

Skin temperature and reproductive condition in wild female chimpanzees.

Infrared thermal imaging has emerged as a valuable tool in veterinary medicine, in particular for evaluating reproductive processes. Here, we explored differences in skin temperature of twenty female chimpanzees in Budongo Forest, Uganda, four of which were pregnant during data collection. Based on previous literature in other mammals, we predicted increased skin temperature of maximally swollen reproductive organs of non-pregnant females when approaching peak fertility. For pregnant females, we made the same prediction because it has been argued that female chimpanzees have evolved mechanisms to conceal pregnancy, including swellings of the reproductive organs, conspicuous copulation calling, and solicitation of male mating behaviour, to decrease the infanticidal tendencies of resident males by confusing paternity. For non-pregnant females, we found slight temperature increases towards the end of the swelling cycles but no significant change between the fertile and non-fertile phases. Despite their different reproductive state, pregnant females had very similar skin temperature patterns compared to non-pregnant females, suggesting little potential for males to use skin temperature to recognise pregnancies, especially during maximal swelling, when ovulation is most likely to occur in non-pregnant females. We discuss this pattern in light of the concealment hypothesis, i.e., that female chimpanzees have evolved physiological means to conceal their reproductive state during pregnancy.

Trivalent f-elements in human saliva: a comprehensive speciation study by time-resolved laser-induced fluorescence spectroscopy and thermodynamic calculations.

In the case of oral ingestion of radioactive contaminants, the first contact medium is saliva in the mouth. To gain a first insight into the interaction of radioactive contaminants in human saliva, the speciation of curium (Cm(iii)) and europium (Eu(iii)), i.e., trivalent f-elements, was investigated in different salivary media with time-resolved laser-induced fluorescence spectroscopy (TRLFS). The results indicate that these metal cations are primarily complexed with carbonates and phosphates, forming ternary complexes with a possible stoichiometry of 1 : 1 : 2 (M(iii) : carbonate : phosphate). For charge compensation, calcium is also involved in these ternary complexes. In addition to these inorganic components, organic substances, namely α-amylase, show a significant contribution to the speciation of the trivalent f-elements in saliva. This protein is the major enzyme in saliva and catalyzes the hydrolysis of polysaccharides. In this context, the effect of Eu(iii) on the activity of α-amylase was investigated to reveal the potential implication of these metal cations for the in vivo functions of saliva. The results indicate that the enzyme activity is strongly inhibited by the presence of Eu(iii), which is suppressed by an excess of calcium.

Distribution of a Chimpanzee Social Custom Is Explained by Matrilineal Relationship Rather Than Conformity.

High-arm grooming is a form of chimpanzee grooming in which two individuals mutually groom while each raising one arm. Palm-to-palm clasping (PPC) is a distinct style of high-arm grooming in which the grooming partners clasp each other's raised palms. In wild communities, samples of at least 100 observed dyads grooming with raised hands showed PPC frequencies varying from <5% (M group, Mahale) to >30% dyads grooming (Kanyawara, Kibale), and in a large free-ranging sanctuary group, the frequency reached >80% dyads (group 1, Chimfunshi) [1, 2]. Because between-community differences in frequency of PPC apparently result from social learning, are stable across generations, and last for at least 9 years, they are thought to be cultural, but the mechanism of transmission is unknown [2]. Here, we examine factors responsible for individual variation in PPC frequency within a single wild community. We found that in the Kanyawara community (Kibale, Uganda), adults of both sexes varied widely in their PPC frequency (from <10% to >50%) and did not converge on a central group tendency. However, frequencies of PPC were highly consistent within matrilines, indicating that individuals maintained lifelong fidelity to the grooming style of their mothers. Matrilineal inheritance of socially learned behaviors has previously been reported for tool use in chimpanzees [3] and in the vocal and feeding behavior of cetaceans [4, 5]. Our evidence indicates that matrilineal inheritance can be sufficiently strong in nonhuman primates to account for long-term differences in community traditions.

Reply to Fischer et al.

We welcome the correspondence from Fischer and colleagues regarding our recent paper on vocal learning in chimpanzee food grunts [1]. Fischer et al. make two challenges to our paper's conclusions, which we address here.

Vocal learning in the functionally referential food grunts of chimpanzees.

One standout feature of human language is our ability to reference external objects and events with socially learned symbols, or words. Exploring the phylogenetic origins of this capacity is therefore key to a comprehensive understanding of the evolution of language. While non-human primates can produce vocalizations that refer to external objects in the environment, it is generally accepted that their acoustic structure is fixed and a product of arousal states. Indeed, it has been argued that the apparent lack of flexible control over the structure of referential vocalizations represents a key discontinuity with language. Here, we demonstrate vocal learning in the acoustic structure of referential food grunts in captive chimpanzees. We found that, following the integration of two groups of adult chimpanzees, the acoustic structure of referential food grunts produced for a specific food converged over 3 years. Acoustic convergence arose independently of preference for the food, and social network analyses indicated this only occurred after strong affiliative relationships were established between the original subgroups. We argue that these data represent the first evidence of non-human animals actively modifying and socially learning the structure of a meaningful referential vocalization from conspecifics. Our findings indicate that primate referential call structure is not simply determined by arousal and that the socially learned nature of referential words in humans likely has ancient evolutionary origins.