Great apes track hidden objects after changes in the objects' position and in subject's orientation

Eight chimpanzees (Pan troglodytes), five bonobos (Pan paniscus), five gorillas (Gorilla gorilla), and seven orangutans (Pongo pygmaeus) were presented with two invisible object displacement tasks. In full view of the subject, a food item was hidden under one of three opaque cups resting on a platform and, after an experimental manipulation, the subject was allowed to select one of the cups. In the rotation task, the platform was rotated 180° while the subject remained stationary. In the translocation task, the platform remained stationary while the subject walked to the opposite side from where she saw the reward being hidden. The final position of the food relative to the subject was equivalent in both tasks. Single displacement trials consisted of only one manipulation, either a rotation or a translocation, whereas double displacement trials consisted of both a rotation and a translocation. We also included no displacement trials in which no displacements took place. No displacement trials were easier than single displacements which, in turn, were easier than double displacements. Unlike earlier studies with children, there was no difference in performance between rotation and translocation displacements. Overall, apes performed above chance in all conditions, but chimpanzees outperformed the other species. This study reinforces the notion that the great apes use an allocentric spatial coding. Am. J. Primatol. 72:349–359, 2010. © 2010 Wiley‐Liss, Inc.     

Molecular evolution of IgG subclass among nonhuman primates: implication of differences in antigenic determinants among Apes

The cross-reactivity of five different rabbit polyclonal antibodies to human IgG and IgG subclass (IgG1, IgG2, IgG3, and IgG4) was determined by competitive ELISA with nine nonhuman primate species including five apes, three Old World monkeys, and one New World monkey. As similar to those previously reported, the reactivity of anti-human IgG antibody with plasma from different primate species was closely related with phylogenic distance from human. Every anti-human IgG subclass antibody showed low cross-reactivity with plasma from Old World and New World monkeys. The plasma from all apes except for gibbons (Hylobates spp.) showed 60 to 100% of cross-reactivity with anti-human IgG2 and IgG3 antibodies. On the other hand, chimpanzee (Pan troglodytes andPan paniscus) and orangutan (Pongo pygmaeus) plasma showed 100% cross-reactivity with anti-human IgG1 antibody, but gorilla (Gorilla gorilla) and gibbon plasma showed no cross-reactivity. The chimpanzee and gorilla plasma cross-reacted with anti-human IgG4 antibody at different reactivity, 100% in chimpanzee and 50% in gorilla, but no cross-reactivity was observed in orangutan and gibbon plasma. These results suggest the possibilities that the divergence of “human-type” IgG subclasses might occur at the time of divergence ofHomo sapience fromHylobatidae, and that the molecular evolution of IgG1 as well as IgG4 is different from that of IgG2 and IgG3 in great apes, this is probably caused by different in development of immune function in apes during the course of evolution.     

Bonobos and chimpanzees exhibit human-like framing effects

Humans exhibit framing effects when making choices, appraising decisions involving losses differently from those involving gains. To directly test for the evolutionary origin of this bias, we examined decision-making in humans'' closest living relatives: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We presented the largest sample of non-humans to date (n = 40) with a simple task requiring minimal experience. Apes made choices between a ‘framed’ option that provided preferred food, and an alternative option that provided a constant amount of intermediately preferred food. In the gain condition, apes experienced a positive ‘gain’ event in which the framed option was initially presented as one piece of food but sometimes was augmented to two. In the loss condition, apes experienced a negative ‘loss'' event in which they initially saw two pieces but sometimes received only one. Both conditions provided equal pay-offs, but apes chose the framed option more often in the positive ‘gain’ frame. Moreover, male apes were more susceptible to framing than were females. These results suggest that some human economic biases are shared through common descent with other apes and highlight the importance of comparative work in understanding the origins of individual differences in human choice.     

Relative growth of the limbs and trunk in the African apes

Examination of relative growth and allometry is important for our understanding of the African apes, as they represent a closely related group of species of increasing body size. This study presents a comparison of ontogenetic relative growth patterns of some postcranial dimensions in Pan paniscus, Pantroglodytes, and Gorilla gorilla. Interspecific proportion differences among the three species are also analyzed. It is stressed that reliable ontogenetic information can only be obtained if subadults are examined-growth data cannot be inferred from static adult scaling. Results indicate that some postcranial relative growth patterns are very similar in the three species, suggesting differential extrapolation of a common growth pattern, whereas for other proportion comparisons the growth trends differ markedly among the species, producing distinct shape differences in the adults Interspecific shape changes among the three species are characterized by positive allometry of chest girth and negative allometry of body height and leg length. It is suggested that relative decrease of leg length with increasing body size among the African pongids might be expected on biomechanical grounds, in order to maintain similar locomotor abilities of climbing arborealism and quadrupedal terrestrialism. Relative to body weight or trunk length, the limbs of the bonobo (Pan paniscus) are longer than in the common chimpanzee or the gorilla, with a lower intermembral index. This may most closely resemble the primitive condition for the African apes.     

Ontogeny and the evolution of adult body size dimorphism in apes

This analysis investigates the ontogeny of body size dimorphism in apes. The processes that lead to adult body size dimorphism are illustrated and described. Potential covariation between ontogenetic processes and socioecological variables is evaluated. Mixed-longitudinal growth data from 395 captive individuals (representing Hylobates lar [gibbon], Hylobates syndactylus [siamang], Pongo pygmaeus [orangutan], Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) form the basis of this study. Results illustrate heterogeneity in the growth processes that produce ape dimorphism. Hylobatids show no sexual differentiation in body weight growth. Adult body size dimorphism in Pongo can be largely attributed to indeterminate male growth. Dimorphism in African apes is produced by two different ontogenetic processes. Both pygmy chimpanzees (Pan paniscus) and gorillas (Gorilla gorilla) become dimorphic primarily through bimaturism (sex differences in duration of growth). In contrast, sex differences in rate of growth account for the majority of dimorphism in common chimpanzees (Pan troglodytes). Diversity in the ontogenetic pathways that produce adult body size dimorphism may be related to multiple evolutionary causes of dimorphism. The lack of sex differences in hylobatid growth is consistent with a monogamous social organization. Adult dimorphism in Pongo can be attributed to sexual selection for indeterminate male growth. Interpretation of dimorphism in African apes is complicated because factors that influence female ontogeny have a substantial effect on the resultant adult dimorphism. Sexual selection for prolonged male growth in gorillas may also increase bimaturism relative to common chimpanzees. Variation in female growth is hypothesized to covary with foraging adaptations and with differences in female competition that result from these foraging adaptations. Variation in male growth probably corresponds to variation in level of sexual selection. © 1995 Wiley-Liss, Inc.     

Transgenerational soil‐mediated differences between plants experienced or naïve to a grass invasion

Invasive species may undergo rapid change as they invade. Native species persisting in invaded areas may also experience rapid change over this short timescale relative to native populations in uninvaded areas. We investigated the response of the native Achillea millefolium to soil from Holcus lanatus‐invaded and uninvaded areas, and we sought to determine whether differential responses between A. millefolium from invaded (invader experienced) and uninvaded (invader naïve) areas were mediated by soil community changes. Plants grown from seed from experienced and naïve areas responded differently to invaded and uninvaded soil with respect to germination time, biomass, and height. Overall, experienced plants grew faster and taller than their naïve counterparts. Naïve native plants showed negative feedbacks with their home soil and positive feedbacks with invaded soil; experienced plants were less responsive to soil differences. Our results suggest that native plants naïve to invasion may be more sensitive to soil communities than experienced plants, consistent with recent studies. While differences between naïve and experienced plants are transgenerational, our design cannot differentiate between differences that are genetically based, plastic, or both. Regardless, our results highlight the importance of seed source and population history in restoration, emphasizing the restoration potential of experienced seed sources.     

Controlled cortical impact injury affects dopaminergic transmission in the rat striatum

The therapeutic benefits of dopamine (DA) agonists after traumatic brain injury (TBI) imply a role for DA systems in mediating functional deficits post‐TBI. We investigated how experimental TBI affects striatal dopamine systems using fast scan cyclic voltammetry (FSCV), western blot, and d‐amphetamine‐induced rotational behavior. Adult male Sprague–Dawley rats were injured by a controlled cortical impact (CCI) delivered unilaterally to the parietal cortex, or were naïve controls. Amphetamine‐induced rotational behavior was assessed 10 days post‐CCI. Fourteen days post‐CCI, animals were anesthetized and underwent FSCV with bilateral striatal carbon fiber microelectrode placement and stimulating electrode placement in the medial forebrain bundle (MFB). Evoked DA overflow was assessed in the striatum as the MFB was electrically stimulated at 60 Hz for 10 s. In 23% of injured animals, but no naïve animals, rotation was observed with amphetamine administration. Compared with naïves, striatal evoked DA overflow was lower for injured animals in the striatum ipsilateral to injury (p < 0.05). Injured animals exhibited a decrease in V_max (52% of naïve, p < 0.05) for DA clearance in the hemisphere ipsilateral to injury compared with naïves. Dopamine transporter (DAT) expression was proportionally decreased in the striatum ipsilateral to injury compared with naïve animals (60% of naïve, p < 0.05), despite no injury‐related changes in vesicular monoamine transporter or D₂ receptor expression (DRD₂) in this region. Collectively, these data appear to confirm that the clinical efficacy of dopamine agonists in the treatment of TBI may be related to disruptions in the activity of subcortical dopamine systems.     

Ontogeny of body size variation in African apes

Size variation in African apes (Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) is substantial, both within and between species. We investigate the possible evolutionary significance of this variation through an analysis of the ontogeny of size variation in this group. In addition, we highlight possible areas of future endocrinological research, and evaluate recently proposed alternative models that attempt to account for ontogenetic variation in apes. The present study shows that intergeneric variation in size is largely a consequence of differences among species in the rate of body weight growth. Interspecific size variation in Pan is a product of both rate and duration differences in growth. The ontogenetic bases of sexual dimorphism vary in this group. Dimorphism is largely a result of sex differences in the duration of body weight growth in gorillas and pygmy chimpanzees, but results from differences in the rate of growth in common chimpanzees. Ontogenetic analyses largely confirm earlier interpretations, but with better data and methods. The great degree of ontogenetic variation within and among these species, especially in the timing and magnitude of “pubertal” growth spurts, implies that studies of endocrine growth control in African apes could be a productive line of future research. We also suggest that ontogenetic variation can be understood with respect to ecological risks. Growth rates seem to be negatively correlated with ecological risk in African apes, suggesting links between ontogenetic patterns and social and ecological variables. High growth rates in gorillas compared to Pan are most consistent with this model. Variation between chimpanzees and pygmy chimpanzees (especially females) also seem to fit predictions of this model. © 1996 Wiley-Liss, Inc.     

Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination

The lady beetle Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) is an important predator of aphids in agroecosystems. The inundative release of coccinellid beetles can be an effective biological control strategy. An understanding of how biological control agents perceive and use stimuli from host plants is the key to successfully implement commercially produced predators. Here, we studied the relative role of visual and volatile cues. Dual‐choice assays using foraging‐naïve and foraging‐experienced P. japonica adults were conducted using cotton plants [Gossypium hirsutum L. (Malvaceae)] with or without infestation by the cotton aphid, Aphis gossypii (Glover) (Hemiptera: Aphididae). Overall, experienced beetles were more attracted than naïve beetles toward cues associated with aphid‐infested plants. Experienced beetles were also more responsive to olfactory cues compared with naïve beetles. Both foraging‐naïve and ‐experienced lady beetles integrate olfactory and visual cues from plants infested with aphids, with an apparently greater reliance on olfactory cues. The results suggest that foraging experience may increase prey location in P. japonica.     

Mass spectral analyses of the two major apolipoproteins of great ape high density lipoproteins

The two major apolipoproteins associated with human and chimpanzee (Pan troglodytes) high density lipoproteins (HDL) are apoA-I and dimeric apoA-II. Although humans are closely related to great apes, apolipoprotein data do not exist for bonobos (Pan paniscus), western lowland gorillas (Gorilla gorilla gorilla) and the Sumatran orangutans (Pongo abelii). In the absence of any data, other great apes simply have been assumed to have dimeric apoA-II while other primates and most other mammals have been shown to have monomeric apoA-II. Using mass spectrometry, we have measured the molecular masses of apoA-I and apoA-II associated with the HDL of these great apes. Each was observed to have dimeric apoA-II. Being phylogenetically related, one would anticipate these apolipoproteins having a high percentage of invariant sequences when compared with human apolipoproteins. However, the orangutan, which diverged from the human lineage between 16 and 21 million years ago, had an apoA-II with the lowest monomeric mass, 8031.3 Da and the highest apoA-I value, 28,311.7 Da, currently reported for various mammals. Interestingly, the gorilla that diverged from the lineage leading to the human–chimpanzee branch after the orangutan had almost identical mass values to those reported for human apoA-I and apoA-II. But chimpanzee and the bonobo that diverged more recently had identical apoA-II mass values that were slightly larger than reported for the human apolipoprotein. The chimpanzee A-I mass values were very close to those of humans; however, the bonobo had values intermediate to the molecular masses of orangutan and the other great apes. With the already existing genomic data for chimpanzee and the recent entries for the orangutan and gorilla, we were able to demonstrate a close agreement between our mass spectral data and the calculated molecular weights determined from the predicted primary sequences of the respective apolipoproteins. Post-translational modification of these apolipoproteins, involving truncation and oxidation of methionine, are also reported.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

First Documentation of Cultural Transmission of Predator Recognition by Larval Amphibians

Predation is a pervasive selective agent shaping a prey's behaviour, morphology and life history. To survive, prey animals have to respond adaptively to predation threats and this can be achieved through learned predator recognition. Cultural transmission of predator recognition is likely a widespread means of learning in social animals, including mammals, birds and fishes. However, no studies have investigated the cultural transmission of predator recognition in amphibians. In our study, we examined whether naïve woodfrog (Rana sylvatica) tadpoles can acquire the recognition of the odour of a predatory tiger salamander (Ambystoma tigrinum) from experienced conspecifics. After conditioning some tutors to recognize salamander odour, we paired naïve observer tadpoles with either a salamander‐naïve or salamander‐experienced tutor and exposed the pairs to either salamander odour or a water control. Observers were subsequently tested alone for a response to salamander odour. We found that when given salamander odour, observer tadpoles that were paired with a salamander‐experienced tutor successfully learned to recognize the salamander odour as a threat, whereas the observers paired with salamander‐naïve tutors did not. Likewise, tadpoles exposed to the water control did not learn to recognize the salamander regardless of whether they were paired with a naïve or experienced tutor. This is the first study demonstrating cultural transmission of predator recognition in an amphibian species.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

Hand preferences in chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and orangutans (Pongo pygmaeus) in food-reaching and other daily activities

We observed 36 captive great apes [31 chimpanzees (Pan troglodytes),2 bonobos (Pan paniscus), and3 orangutans (Pongo pygmaeus)]reaching for items of food and engaging in other spontaneous behaviors. We consider circumstantial factors that could influence the preferred choice of one hand or the other. Most of the subjects (81%) showed a significant hand preference in food reaching that is consistent in directionality with the hand preferences that they showed during other spontaneous behaviors. The results show that the postural adjustment required when carrying out an action seems to influence directly the expression of manual laterality in individuals. Moreover, the results indicate the possible existence of a relationship between maturational factors and persistence in directionality of hand preferences.     

African grey parrots (Psittacus erithacus) use inference by exclusion to find hidden food

Exclusion allows the detection of hidden food when confronted with the choice between an empty and a potentially baited food location. However, exclusion may be based on avoidance of the empty location without drawing inferences about the presence of the food in the baited location. So far, such inferences have been demonstrated in the great apes only: after seeing an experimenter eating one of two food types, which both had been hidden previously in two boxes, the apes were able to choose the box that still contained the other food type. African grey parrots are capable of exclusion, and we here assessed if they are capable of inference by exclusion. In our task, two different but equally preferred food items were hidden in full view of the birds under two opaque cups. Then, an experimenter secretly removed one food type and showed it to the bird. Similarly to the apes, one out of seven parrots significantly preferred the baited cup; control conditions rule out that its choice was based on associative learning or the use of olfactory cues. Thus, we conclude that-like the apes-some grey parrots are able to infer the location of a hidden food reward.     

Does Sympathy Motivate Prosocial Behaviour in Great Apes?

Prosocial behaviours such as helping, comforting, or sharing are central to human social life. Because they emerge early in ontogeny, it has been proposed that humans are prosocial by nature and that from early on empathy and sympathy motivate such behaviours. The emerging question is whether humans share these abilities to feel with and for someone with our closest relatives, the great apes. Although several studies demonstrated that great apes help others, little is known about their underlying motivations. This study addresses this issue and investigates whether four species of great apes (Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, Pan paniscus) help a conspecific more after observing the conspecific being harmed (a human experimenter steals the conspecific’s food) compared to a condition where no harming occurred. Results showed that in regard to the occurrence of prosocial behaviours, only orangutans, but not the African great apes, help others when help is needed, contrasting prior findings on chimpanzees. However, with the exception of one population of orangutans that helped significantly more after a conspecific was harmed than when no harm occurred, prosocial behaviour in great apes was not motivated by concern for others.     

Leaf Surface Roughness Elicits Leaf Swallowing Behavior in Captive Chimpanzees (Pan troglodytes) and Bonobos (P. paniscus), but not in Gorillas (Gorilla gorilla) or Orangutans (Pongo abelii)

Researchers have described apparently self-medicative behaviors for a variety of nonhuman species including birds and primates. Wild chimpanzees, bonobos, and gorillas have been observed to swallow rough leaves without chewing, a behavior proposed to be self-medicative and to aid control of intestinal parasites. Researchers have hypothesized that the presence of hairs on the leaf surface elicits the behavior. We investigated the acquisition and the underlying mechanisms of leaf swallowing. We provided 42 captive great apes (24 chimpanzees, six bonobos, six gorillas, and six orangutans) with both rough-surfaced and hairless plants. None of the subjects had previously been observed to engage in leaf swallowing behavior and were therefore assumed naïve. Two chimpanzees and one bonobo swallowed rough-surfaced leaves spontaneously without chewing them. In a social setup six more chimpanzees acquired the behavior. None of the gorillas or orangutans showed leaf swallowing. Because this behavior occurred in naïve individuals, we conclude that it is part of the behavioral repertoire of chimpanzees and bonobos. Social learning is thus not strictly required for the acquisition of leaf swallowing, but it may still facilitate its expression. The fact that apes always chewed leaves of hairless control plants before swallowing, i.e., normal feeding behavior, indicates that the surface structure of leaves is indeed a determinant for initiating leaf swallowing in apes where it occurs.     

Differential effects of age,cytomegalovirus-seropositivity and end-stage renal disease (ESRD) on circulating T lymphocyte subsets

The age- and cytomegalovirus (CMV)-seropositivity-related changes in subsets and differentiation of circulating T cells were investigated in end-stage renal disease (ESRD) patients (n = 139) and age-matched healthy individuals. The results show that CMV-seropositivity is associated with expansion of both CD4⁺ and CD8⁺ memory T cells which is already observed in young healthy individuals. In addition, CMV-seropositive healthy individuals have a more differentiated memory T cell profile. Only CMV-seropositive healthy individuals showed an age-dependent decrease in CD4⁺ naïve T cells. The age-related decrease in the number of CD8⁺ naïve T cells was CMV-independent. In contrast, all ESRD patients showed a profound naïve T-cell lymphopenia at every decade. CMV-seropositivity aggravated the contraction of CD4⁺ naïve T cells and increased the number of differentiated CD4⁺ and CD8⁺ memory T cells. In conclusion, CMV-seropositivity markedly alters the homeostasis of circulating T cells in healthy individuals and aggravates the T cell dysregulation observed in ESRD patients.     

IL-10 producing CD8+ T cells in human infection with Leishmania guyanensis

Cytokines are increasingly recognized as important components of the cellular immune responses to intracellular pathogens. In this study, we analyzed the production of TGF-β, IL-10 and IFN-γ by PBMC of unexposed naïve subjects and LCL patients after stimulation with live Leishmania guyanensis (L.g.). We demonstrated that IFN-γ is produced in controls and LCL patients, IL-10 only in LCL patients and TGF-β only in naïve subjects. Furthermore, in naive subjects, neutralization of TGF-β induced IL-10 production. IL-10 produced in naïve subjects when TGF-β is neutralized or in LCL patients did not modify the IFN-γ production but inhibit reactive nitrogen species production. Analysis of the phenotype of IL-10 producing cells in naive subjects when TGF-β is neutralized clearly showed that they are memory CD45RA⁻ CD8⁺ T cells. In LCL patients, IL-10 producing cells are both CD45RA⁻ CD4 and CD8⁺ T cells. The role of these IL-10 producing CD8⁺ T cells in the development of the diseases should be carefully evaluated.     

Male Success in Intrasexual Contests Extends to the Level of Sperm Competition in a Species of Dung Roller Beetle

Contests between males fighting over limited resources often determine the reproductive success of the contestants. It is possible that the outcomes of such contests are affected by traits that also contribute to the likelihood of males achieving paternity when sperm from multiple males compete to fertilize the ova of a single female; however, this relationship has been poorly characterized. In dung and carrion roller beetles, contests among males for the possession of a food ball – a vital resource for nesting – are frequent in nature. However, females that roll and nest with a male often store the sperm of previous mates, forcing males to engage in sperm competition. We analyzed the relationship between wins and losses in contests between food ball owner males and subsequent paternity success in the carrion roller beetle Canthon cyanellus using both naïve (virgin) and experienced (previously mated) males. Owner males that initiated contests were more likely to win, and contest durations were longer between experienced owner males than between naïve owners. The paternity of the winner owner males nesting with a female that had previously mated with another male was higher than for loser owner males, and the paternity of experienced owners also tended to be higher than for virgin owners. Our results indicate that winning and being an experienced male are associated with greater success at fighting and sperm competition than losing and being a naïve male.