Caterina Spiezio

Target animacy influences chimpanzee handedness

We employed a bottom-up, quantitative method to investigate great ape handedness. Our previous investigation of gorillas (Gorilla gorilla gorilla) demonstrated that contextual information influenced an individual’s handedness toward target objects. Specifically, we found a significant right-hand bias for unimanual actions directed toward inanimate target objects but not for actions directed to animate target objects (Forrester et al. in Anim Cogn 14(6):903–907, 2011). Using the identical methodological technique, we investigated the spontaneous hand actions of nine captive chimpanzees (Pan troglodytes) during naturalistic, spontaneous behavior. We assessed both the frequencies and proportions of lateralized hand actions directed toward animate and inanimate targets employing focal follow video sampling. Like the gorillas, the chimpanzees demonstrated a right-handed bias for actions directed toward inanimate targets, but not toward animate targets. This pattern was evident at the group level and for the majority of subjects at the individual level. We postulate that a right-hand bias for only inanimate targets reflects the left hemisphere’s dominant neural processing capabilities for objects that have functional properties (inanimate objects). We further speculate that a population-level right-hand bias is not a human-unique characteristic, but one that was inherited from a common human-ape ancestor.

Social Environment Elicits Lateralized Behaviors in Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

The influence of the social environment on lateralized behaviors has now been investigated across a wide variety of animal species. New evidence suggests that the social environment can modulate behavior. Currently, there is a paucity of data relating to how primates navigate their environmental space, and investigations that consider the naturalistic context of the individual are few and fragmented. Moreover, there are competing theories about whether only the right or rather both cerebral hemispheres are involved in the processing of social stimuli, especially in emotion processing. Here we provide the first report of lateralized social behaviors elicited by great apes. We employed a continuous focal animal sampling method to record the spontaneous interactions of a captive zoo-living colony of chimpanzees (Pan troglodytes) and a biological family group of peer-reared western lowland gorillas (Gorilla gorilla gorilla). We specifically focused on which side of the body (i.e., front, rear, left, right) the focal individual preferred to keep conspecifics. Utilizing a newly developed quantitative corpus-coding scheme, analysis revealed both chimpanzees and gorillas demonstrated a significant group-level preference for focal individuals to keep conspecifics positioned to the front of them compared with behind them. More interestingly, both groups also manifested a population-level bias to keep conspecifics on their left side compared with their right side. Our findings suggest a social processing dominance of the right hemisphere for context-specific social environments. Results are discussed in light of the evolutionary adaptive value of social stimulus as a triggering factor for the manifestation of group-level lateralized behaviors.

Leaf swallowing behavior in chimpanzees (Pan troglodytes): biased learning and the emergence of group level cultural differences

Demonstrating the ability to ‘copy’ the behavior of others is an important aspect in determining whether social learning occurs and whether group level differences in a given behavior represent cultural differences or not. Understanding the occurrence of this process in its natural context is essential, but can be a daunting task in the wild. In order to test the social learning hypothesis for the acquisition of leaf swallowing (LS), a self-medicative behavior associated with the expulsion of parasites, we conducted semi-naturalistic experiments on two captive groups of parasite-free, naïve chimpanzees (Pan troglodytes). Individuals in the group were systematically provided appropriate stimuli (rough hispid leaves) identical to those used by chimpanzees in the wild. Individuals initially responded in a variety of ways, ranging from total aversion to normal chewing and swallowing. Over time, however, the two groups adopted different variants for inserting and folding the leaves in the mouth prior to swallowing them (complete and partial LS), following the specific method spontaneously displayed by the first and primary LS models in their respective groups. These variants were similar to LS displayed by chimpanzees in the wild. Using the option-bias method, we found evidence for social learning leading to group-level biased transmission and group-level stabilization of these two variants. This is the first report on two distinct cultural variants innovated in response to the introduction of natural stimuli that emerged and spread spontaneously and concurrently within two adjacent groups of socially housed primates. These observations support the assertion that LS may reflect a generalized propensity for ingesting rough hispid leaves, which can be socially induced and transmitted within a group. Ingesting an adequate number of these leaves induces increased gut motility, which is responsible for the subsequent expulsion of particular parasite species in the wild. Cultural transmission and maintenance of LS within a group and associative learning by the individual of the positive consequences of this otherwise non-nutritive mode of ingestion is proposed to be the pivotal link between this feeding propensity and its maintenance as a self-medicative behavior by great apes in the wild.

Bifidobacterium aerophilum sp. nov., Bifidobacterium avesanii sp. nov. and Bifidobacterium ramosum sp. nov.: Three novel taxa from the faeces of cotton-top tamarin (Saguinus oedipus L.) ☆

Forty-five microorganisms were isolated on bifidobacteria selective medium from one faecal sample of an adult subject of the cotton-top tamarin (Saguinus oedipus L.). All isolates were Gram-positive, catalase-negative, anaerobic, fructose-6-phosphate phosphoketolase positive, and asporogenous rod-shaped bacteria. In this study, only eight out of the forty-five strains were characterized more deeply, whereas the others are still currently under investigation. They were grouped by BOX-PCR into three clusters: Cluster I (TRE 17(T), TRE 7, TRE 26, TRE 32, TRE 33, TRE I), Cluster II (TRE C(T)), and Cluster III (TRE M(T)). Comparative analysis of 16S rRNA gene sequences confirmed the results from the cluster analysis and revealed relatively low level similarities to each other (mean value 95%) and to members of the genus Bifidobacterium. All eight isolates showed the highest level of 16S rRNA gene sequence similarities with Bifidobacterium scardovii DSM 13734(T) (mean value 96.6%). Multilocus sequence analysis (MLSA) of five housekeeping genes (hsp60, rpoB, clpC, dnaJ and dnaG) supported their independent phylogenetic position to each other and to related species of Bifidobacterium. The G+C contents were 63.2%, 65.9% and 63.0% for Cluster I, Cluster II and Cluster III, respectively. Peptidoglycan types were A3α l-Lys-l-Thr-l-Ala, A4β l-Orn (Lys)-d-Ser-d-Glu and A3β l-Orn-l-Ser-l-Ala in Clusters I, II and III, respectively. Based on the data provided, each cluster represented a novel taxon for which the names Bifidobacterium aerophilum sp. nov. (TRE 17(T)=DSM 100689=JCM 30941; TRE 26=DSM 100690=JCM 30942), Bifidobacterium avesanii sp. nov. (TRE C(T)=DSM 100685=JCM 30943) and Bifidobacterium ramosum sp. nov. (TRE M=DSM 100688=JCM 30944) are proposed.

Testing for Localized Stimulus Enhancement and Object Movement Reenactment in Pig-Tailed Macaques (Macaca nemestrina) and Young Children (Homo sapiens)

Four puzzle boxes were used to investigate localized stimulus enhancement and object movement reenactment (OMR) in 13 pig-tailed macaques (Macaca nemestrina) and 30 human infants (Homo sapiens). Participants received contrasting demonstrations on each box. A circular lid was gripped by its rim or handle and swiveled to the left or right. A flap door was pushed or flipped. A sliding lid was pushed to the left or right. A pin bolt was demonstrated being pushed down, or the participants were left to solve the puzzle for themselves. Despite the fact that the monkeys watched the demonstrations about 60% of the time, only a weak OMR effect was found on the sliding lid. In contrast, the children watched significantly more, and there was clear evidence of socially mediated learning on all of the boxes.

Bifidobacterium. eulemuris sp. nov. isolated from the faeces of the black lemur (Eulemur macaco).

Forty-three strains of bifidobacteria were isolated from the faeces of two adult black lemurs, Eulemur macaco. Thirty-four were identified as Bifidobacterium lemurum, recently described in Lemur catta. The nine remaining isolates were Gram-positive-staining, non-spore-forming, fructose-6-phosphate phosphoketolase-positive, microaerophilic, irregular rod-shaped bacteria that often presented Y- or V-shaped cells. Typing techniques revealed that these isolates were nearly identical, and strain LMM_E3T was chosen as a representative and characterized further. Phylogenetic analysis based on 16S rRNA gene sequences clustered this isolate inside the genus Bifidobacterium and showed the highest levels of sequence similarity with B. lemurum DSM 28807T (99.3 %), with Bifidobacterium pullorum LMG 21816T and Bifidobacterium longum subsp. infantis ATCC 15697T (96.4 and 96.3 %, respectively) as the next most similar strains. The hsp60 gene sequence of strain LMM_E3T showed the highest similarity to that of Bifidobacterium stellenboschense DSM 23968T (93.3 %), and 91.0 % similarity to that of the type strain of B. lemurum. DNA-DNA reassociation with the closest neighbour B. lemurum DSM 28807T was found to be 65.4 %. The DNA G+C content was 62.3 mol%. Strain LMM_E3T showed a peptidoglycan structure that has not been detected in bifidobacteria so far: A3α l-Lys-l-Ser-l-Thr-l-Ala. Based on the phylogenetic, genotypic and phenotypic data, strain LMM_E3T represents a novel species within the genus Bifidobacterium, for which the name Bifidobacterium eulemuris sp. nov. is proposed; the type strain is LMM_E3T ( = DSM 100216T = JCM 30801T).

Manual lateralization in macaques: handedness, target laterality and task complexity

ABSTRACT Non-human primates represent models to understand the evolution of handedness in humans. Despite several researches have been investigating non-human primates handedness, few studies examined the relationship between target position, hand preference and task complexity. This study aimed at investigating macaque handedness in relation to target laterality and tastiness, as well as task complexity. Seven pig-tailed macaques (Macaca nemestrina) were involved in three different “two alternative choice” tests: one low-level task and two high-level tasks (HLTs). During the first and the third tests macaques could select a preferred food and a non-preferred food, whereas by modifying the design of the second test, macaques were presented with no-difference alternative per trial. Furthermore, a simple-reaching test was administered to assess hand preference in a social context. Macaques showed hand preference at individual level both in simple and complex tasks, but not in the simple-reaching test. Moreover, target position seemed to affect hand preference in retrieving an object in the low-level task, but not in the HLT. Additionally, individual hand preference seemed to be affected from the tastiness of the item to be retrieved. The results suggest that both target laterality and individual motivation might influence hand preference of macaques, especially in simple tasks.

Red-green color vision in three catarrhine primates.

The evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, specifically the detection of either ripe fruits or young leaves amid mature foliage, and to the intraspecific socio-sexual communication, namely the signal of the male rank, the mate choice and the reproductive strategies in females. New data should be added to the debate regarding the evolution of trichromatic color vision. Three catarrhine primates were observed to achieve this goal. The research was performed on captive groups of vervet monkeys (Chlorocebus aethiops), pig-tailed macaques (Macaca nemestrina) and chimpanzees (Pan troglodytes) housed at Parco Natura Viva - Garda Zoological Park (Italy). Using pairs of red-green bags containing the same hidden reward in comparable outdoor enclosures, we recorded the choices by observed individuals (n = 25) to investigate the role of color cues in choosing an object. The results indicate that chimpanzees used red color as cue to choose an object that contains food by showing a preference toward red objects; in contrast, vervet monkeys and pig-tailed macaques do not demonstrate a clear choice based on the color of the object. Our findings highlight the importance of the foraging hypothesis but not rule out the potential role of the intraspecific socio-sexual communication and may serve to add useful information to the debate regarding the adaptive value of the evolution of color vision in order to fill a phylogenetic gap from Old World monkeys to humans. Future studies should address the role of socio-sexual communication, such as the selection of the reproductive partner of both high genetic quality and with compatible genes, to determine how this influenced the evolution of color vision in non-human primates.

Three actions, two groups: Looking for the origin of primate manual lateralization.

Handedness is the most evident behavioral asymmetry in humans: to study nonhuman primate hand preference could be optimal to investigate the evolutionary origin of handedness in our species, even though behavioral asymmetries are widespread among vertebrates. This study investigated hand preferences in 32 Old World monkeys and 26 great apes during 3 spontaneous actions, assessing the effect of taxonomic group, sex and age on primate handedness. Data about foraging, locomotion, and manipulation were collected and 50 bouts per behavioral category per subject were recorded. A bias toward right-hand use for starting locomotion was reported in both Old World monkeys and great apes. Furthermore, in the great apes, a group-level right-hand preference for manipulation was found. Results suggest an important role of factors such as posture and task complexity in the evolution of primate manual lateralization. The effect of taxonomic group, sex, and age on the hand preference are also discussed. (PsycINFO Database Record

Hand preference on unimanual and bimanual tasks in strepsirrhines: The case of the ring-tailed lemur (Lemur catta)

Assessing manual lateralization in non‐human primates could be an optimal way to understand the adaptive value of this asymmetry in humans. Though many studies have investigated hand preferences in Old and New World monkeys and apes, fewer studies have considered manual lateralization in strepsirrhines, especially in experimental tasks. This study investigated hand preferences for a unimanual and a bimanual task of 17 captive ring‐tailed lemurs (Lemur catta), housed at Parco Natura Viva (VR), Italy. The effect of age on handedness has been also investigated. The lemurs were tested on a unimanual task, in which subjects were restricted to using one hand to retrieve the food inside an apparatus, and on a bimanual task, in which lemurs had to use one hand to keep the apparatus door open while reaching with the other hand to retrieve the food inside it. At the population‐level, our results revealed an asymmetrical hand use distribution, in particular a bias toward a right hand preference for food reaching in both the unimanual and the bimanual tasks. Furthermore, at the individual‐level, the bimanual task seems to elicit a greater hand preference than the unimanual task. Results of this study underline the importance of experimental tasks in determining hand preference in strepsirrhines. Furthermore, as bimanual tasks elicited a stronger degree of lateralization, they appear to be more suited to investigate manual laterality. Finally, findings from this study highlight the presence of a right hand preference in ring‐tailed lemurs, shedding new light on the evolution of human right handedness. Am. J. Primatol. 78:851–860, 2016.