Starting from scratch: A first look at a “displacement activity” in group-living rhesus monkeys

Data on scratching behavior were collected from a group of rhesus monkeys living in spacious surroundings. Juveniles scratched more often than adults. Adults scratched most often in social contexts and in close temporal association with a change of behavior. Subjects of intermediate dominance rank, in particular, scratched around the time of a behavioral change, and these subjects were the only ones to show increased scratching during tests involving restricted access to food (thwarting or frustration). The outer thighs, lower back, and sides were the sites scratched most frequently, not necessarily matching sites reported to be preferred for self-grooming. Scratching in monkeys has certain characteristics in common with some well-studied displacement activities in other species, and it possibly also serves as a signal that the individual is preparing to change behavior.     

Scratching as a Window into the Emotional Responses of Wild Tufted Capuchin Monkeys

Emotional responses to social interactions and the associated behavioural measures (e.g., self‐directed behaviours, SDBs) have been little studied in New World monkeys, especially in wild settings. In this study, we investigated the factors affecting anxiety in a wild group of tufted capuchin monkeys (Cebus apella nigritus) using self‐scratching (hereafter scratching) as its measure. Scratching was more strongly affected by the social context than by individual characteristics. Indeed, inter‐individual variability was not explained by the age, sex and dominance rank of the monkeys. The monkeys scratched themselves more often when being distant from other group members than when in close proximity with them, suggesting that even short‐distance separation from group members may be an important factor affecting capuchins emotional response. The risk of receiving aggression seemed also to elicit anxiety, as scratching was higher when in proximity to more dominant individuals and females, which were the categories of group members that were more aggressive. By contrast, scratching was lower when in proximity to more secure partners, like kin. Finally, scratching rates following the receipt of aggression were higher than at baseline, indicating a post‐conflict increase in anxiety. Overall, our results contribute to the understanding of the factors affecting emotional responses in capuchin monkeys, confirming and expanding previous findings in other animal species.     

Interspecific variation in extraction of buried seeds within an assemblage of sparrows

Most North American sparrows forage almost exclusively on herbaceous seeds during the winter months. Limited availability of surface seeds forces some birds to scratch for seeds buried beneath soil, snow, or litter. Artificial seed trays were used to test the ability of five different sparrow species to extract seeds buried at different depths in soil. The results suggest three functional groups based on relative scratching ability. Strong scratchers, which included eastern towhee and song and white-throated sparrows, met or exceeded their energetic requirements when foraging on seeds buried at all depths (down to a maximum depth of 1.50–2.25 cm). A weak scratching species, Savannah sparrow, scratched with the same frequency as the strong scratchers, but experienced negative energy budgets when forced to forage on sub-surface seeds. Finally, a non-scratching species, field sparrow, failed to extract any buried seeds. Level of scratching ability may influence foraging efficiency at low resource densities. As a result, interspecific differences in scratching ability may contribute to habitat selection. Strong scratchers may be adapted to foraging near woody vegetation where intense resource competition and abundant litter limit the availability of surface seeds. Weak scratchers, on the other hand, may be forced to feed away from areas where surface seeds are limited. Since woody vegetation serves as a primary source of protective cover in early successional habitats, a tradeoff between foraging efficiency and the risk of predation may promote the local coexistence of species that differ in relative scratching ability and adaptations to evading predators.     

Do rhesus monkeys recognize themselves in mirrors?

Self-recognition continues to attract attention because of the evidence of a striking difference between the great apes and humans, on the one hand, and all other primates; the former are capable of self recognition,whereas no compelling evidence exists for prosimians, monkeys, or lesser apes. This is inspite of numerous attempts to facilitate mirror self-recognition in other primates. Although all previous attempts to find self-recognition in rhesus macaques have failed, a recent article [Rajala et al., PLoS One9:e12865, 2010] claimed the opposite—that adult male rhesus monkeys did recognize their own image in a mirror. We critically examine this claim, and conclude that the article fails to provide acceptable evidence for self-recognition in rhesus monkeys.     

Phylogenetic Separation in Limb Use in Captive Gibbons (Hylobatidae): A Comparison Across the Primate Order

Although there have been few studies of self‐scratching in primates, some have reported distinct differences in whether hands or feet are used, and these variations seem to reflect the evolutionary history of the Order. Monkeys and prosimians use both hands and feet to self‐scratch while African great apes use hands almost exclusively. Gibbons represent an evolutionary divergence between monkeys and great apes and incidental observations at the Gibbon Conservation Center pointed to a difference in self‐scratching among the four extant gibbon genera (Hoolock, Nomascus, Symphalangus, and Hylobates). To validate and further explore these preliminary observations, we collected systematic data on self‐scratching from 32 gibbons, including nine species and all four genera. To supplement gibbon data, we also collected self‐scratching information from 18 great apes (four species), five prosimians (two species), 26 New World Monkeys (nine species) and 20 Old World Monkeys (seven species). All monkeys and some prosimians used both hands and feet to self‐scratch, whereas one prosimian species used only feet. All African great apes used hands exclusively (orangutans were an exception displaying occasional foot‐use). This appears to represent a fundamental difference between monkeys and great apes in limb use. Interestingly, there was a clear difference in self‐scratching between the four gibbon genera. Hylobates and Symphalangus self‐scratched only with hands (like all African great apes), while Hoolock and Nomascus self‐scratched with both hands and feet (like monkeys and prosimians). This difference in gibbon behavior may reflect the evolutionary history of gibbons as Hoolock and Nomascus are thought to have evolved before both Hylobates and Symphalangus. What evolutionary pressures led to this divergent pattern is currently opaque; however, this shift in limb preference may result from niche separation across the order facilitating differences in the behavioral repertoire associated with hind and forelimbs. Am. J. Primatol. 74:1035‐1043, 2012. © 2012 Wiley Periodicals, Inc.     

Mirror-image reactions in a tool-using,adult male Macaca tonkeana

This study examined reactions to mirror-image stimulation in a wild- reared adult male monkey (Macaca tonkeana) which had spontaneously developed a form of tool-use, namely the use of plant stems to reach mucus inside the nose. Initial intense social responsiveness to the mirror was followed by habituation, although some social responding persisted. Mirror- induced social facilitation of drinking was demonstrated, the first record of such an effect in a nonhuman primate. Rather than enhancing the subject's tool-using activity, the presence of the mirror disrupted tool-use. Finally, an objective test for the presence of self-recognition failed to obtain any evidence of self-recognition in the subject, lending support to the view that the capacity for self-recognition may be lacking in monkeys.     

Itch Relief by Mirror Scratching. A Psychophysical Study

Objective

The goal of this study was to test whether central mechanisms of scratching-induced itch attenuation can be activated by scratching the limb contralateral to the itching limb when the participant is made to visually perceive the non-itching limb as the itching limb by means of mirror images.

Methods

Healthy participants were asked to assess the intensity of an experimentally induced itch at their right forearm while they observed externally guided scratch movements either at their right (itching) or left (non-itching) forearm which were either mirrored or not mirrored. In the first experiment, a mirror placed between the participant’s forearms was used to create the visual illusion that the participant’s itching (right) forearm was being scratched while in fact the non-itching (left) forearm was scratched. To control visibility of the left (non-mirrored) forearm, a second experiment was performed in which unflipped and flipped real-time video displays of the participant’s forearms were used to create experimental conditions in which the participant visually perceived scratching either on one forearm only, on both forearms, or no scratching at all.

Results

In both experiments, scratching the non-itching limb attenuated perceived itch intensity significantly and selectively in the mirror condition, i.e., when the non-itching forearm was visually perceived as the itching limb.

Discussion

These data provide evidence that the visual illusion that an itching limb is being scratched while in fact the non-itching limb contralateral to the itching limb is scratched, can lead to significant itch relief. This effect might be due to a transient illusionary intersensory perceptual congruency of visual, tactile and pruriceptive signals. “Mirror scratching” might provide an alternative treatment to reduce itch perception in focal skin diseases with persistent pruritus without causing additional harm to the affected skin and might therefore have significant clinical impact.     

Social responding to mirrors in rhesus macaques (Macaca mulatta): Effects of changing mirror location

Two rhesus macaques (Macaca mulatta) with a lifetime of continuous exposure to mirrors showed a dramatic and reliable reinstatement of social behavior directed toward the mirror when it was simply moved to a new location. These data are discussed in the context of repeated failures to find self-recognition in monkeys and several recent claims that a cessation of social behavior directed toward mirrors can be used as evidence for the beginning of self-recognition in nonhuman primates.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

A developmental approach to the origins of self-recognition in great apes

In this paper I present an hypothesis to explain the presence of mirror self-recognition (MSR) in great apes and human infants, and the absence of MSR in monkeys. This hypothesis is based on the following elements: 1) review of Gallupian studies of MSR in monkeys and apes; 2) review of Lewis & Brooks-Gunn's study for self-recognition in human infants; 3) application of the human model to comparative data on MSR in nonhuman primates; 4) discussion of cognitive correlates of MSR in human infants; 5) analysis of the cognitive correlates of MSR absence in monkeys, and MSR presence in apes; 6) comparative analysis of the modalities of occurrence of imitation and understanding of causality in monkeys and apes; and 7) a cladistic reconstruction of the evolution of MSR.     

Putative mechanism of the itch-scratch circle: repeated scratching decreases the cutaneous level of prostaglandin D2, a mediator that inhibits itching

In atopic dermatitis, scratching of the skin as a reaction to itching causes injury to the skin, which, in turn, further increases the itching resulting in the establishment of the so-called itch-scratch circle. We have shown that prostaglandin (PG) D2 plays an inhibitory role against pruritus in mice with atopic-like dermatitis; therefore, we examined the relationship between scratching and the cutaneous PGD2 level using an artificial scratching model with a wire brush. Mechanical scratching induced a temporary increase of the skin PGs levels (PGE2, PGD2, 6-ketoPGF1alpha, PGF2alpha). The skin PGD2 level and the ability of PGD2 production decreased at 48 h after repeated scratch, compared to that of normal skin, not so after single scratch. Immunohistochemical analysis and Western blotting revealed a decrease in the levels of cyclooxygenase-1 (COX-1) and hematopoietic PGD synthase in mechanically scratched skin. The reduced ability of the skin for PGD2 production following mechanical scratching could be caused by this decrease in the expression levels of COX-1 and PGD2 synthase. The results suggest that repeated scratching in mice decreases the ability of the skin to produce PGD2, which is an endogenous mediator that inhibits pruritus, resulting in the establishment of the itch-scratch circle.     

Postexposure immunoprophylaxis against B virus (Herpesvirus simiae) infection.

Local infiltration of antiserum into sites inoculated with B virus protected rabbits from an otherwise fatal encephalomyelitis. Treatment was effective when delayed for six hours but not after 24 hours. Homologous rabbit antisera were more effective than heterologous monkey antisera, and protection was unrelated to neutralisation titres. Protection apparently depended not on neutralisation of inoculated virus but on destruction of infected cells before they produced progeny virus. Normal human immunoglobulin able to neutralise B virus did not protect. Intravenously administered antibody was effective only if large doses were given. The findings suggest that persons bitten or scratched by monkeys latently infected with B virus may be treated successfully by immunoprophylaxis with specific antibody. Stocks of human or of more readily available simian antisera should be held in laboratories where such animals are used.     

Physiological Function of Gastrin-Releasing Peptide and Neuromedin B Receptors in Regulating Itch Scratching Behavior in the Spinal Cord of Mice

Pruritus (itch) is a severe side effect associated with the use of drugs as well as hepatic and hematological disorders. Previous studies in rodents suggest that bombesin receptor subtypes i.e. receptors for gastrin-releasing peptide (GRPr) and neuromedin B (NMBr) differentially regulate itch scratching. However, to what degree spinal GRPr and NMBr regulate scratching evoked by intrathecally administered bombesin-related peptides is not known. The first aim of this study was to pharmacologically compare the dose-response curves for scratching induced by intrathecally administered bombesin-related peptides versus morphine, which is known to elicit itch in humans. The second aim was to determine if spinal GRPr and NMBr selectively or generally mediate scratching behavior. Mice received intrathecal injection of bombesin (0.01–0.3 nmol), GRP (0.01–0.3nmol), NMB (0.1–1nmol) or morphine (0.3–3 nmol) and were observed for one hour for scratching activity. Bombesin elicited most profound scratching over one hour followed by GRP and NMB, whereas morphine failed to evoke scratching response indicating the insensitivity of mouse models to intrathecal opioid-induced itch. Intrathecal pretreatment with GRPr antagonist RC-3095 (0.03–0.1 nmol) produced a parallel rightward shift in the dose response curve of GRP-induced scratching but not NMB-induced scratching. Similarly, PD168368 (1–3 nmol) only attenuated NMB but not GRP-induced scratching. Individual or co-administration of RC-3095 and PD168368 failed to alter bombesin-evoked scratching. A higher dose of RC-3095 (0.3 nmol) generally suppressed scratching induced by all three peptides but also compromised motor function in the rotarod test. Together, these data indicate that spinal GRPr and NMBr independently drive itch neurotransmission in mice and may not mediate bombesin-induced scratching. GRPr antagonists at functionally receptor-selective doses only block spinal GRP-elicited scratching but the suppression of scratching at higher doses is confounded by motor impairment.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

Self-agency in rhesus monkeys

Rhesus monkeys (Macaca mulatta) have shown the ability to monitor their own mental states, but fail the mirror self-recognition test. In humans, the sense of self-agency is closely related to self-awareness, and results from monitoring the relationship between intentional, sensorimotor and perceptual information. Humans and rhesus monkeys were trained to move a computer icon with a joystick while a distractor icon partially matched their movements. Both humans and monkeys were able to monitor and identify the icon they were controlling, suggesting they have some understanding of self-agency.     

A novel acoustic evaluation system of scratching in mouse dermatitis: rapid and specific detection of invisibly rapid scratch in an atopic dermatitis model mouse

Scratching is an essential and a skin specific behavior induced by itching, which is a common symptom of atopic dermatitis (AD) and other types of dermatitis. Itching sensation and scratching are closely associated and thus scratching times are currently used for evaluating itching in animal models. However, objective measuring systems of scratching to assess the grade of dermatitis and the effectiveness of anti-pruritic drugs in animal dermatitis models are lacking. To investigate a quantitative evaluation system for itching, we have developed a novel acoustic scratching counting system and compared its accuracy with time-consuming slow-motion video recording system. We have also objectively evaluated the efficacy of an antihistamine using this novel system. Scratching behavior of an AD model mouse (K14 driven IL-18 transgenic mouse) was recorded visually and acoustically. Specific scratching sound produced by mice was recorded and counted using a software we have developed, and the results obtained using our acoustic system were not statistically different from data obtained using slow motion video system. Surprisingly, mice scratched more than 10 times/second, which was invisibly rapid motion and revealed inaccuracy of conventional hand counting system. Results were identical to that of measured by 10 times time costing slow-motion video analysis. The antihistamine is clearly effective for suppression of scratching as demonstrated using this objective and accurate method. This novel motion analysis system will open a window for physiological and pathological analysis for animal models and development of anti-pruritic drugs.     

Individuals' behaviors following dye-marking in wild black-and-white colobus (Colobus vellerosus)

The ability to recognize individuals is a prerequisite for analyzing social relationships. We marked five adult and subadult Colobus vellerosus (three in 2002, and two in 2003) at the Boabeng Fiema Monkey Sanctuary, Ghana, to assess the feasibility of dye-marking black-and-white colobus, describe their reactions, and compare some of their behaviors with those of unmarked individuals. We used Nyanzol-D, a nontoxic black dye sprayed on the white tail (or white thigh) of the animal with a spray gun or a tree sprayer. Reactions to the marking procedure ranged from moving away and staring at the observer, without interruption in feeding (in one subject), to fleeing about 5 m away (in four subjects). In 234 hr of ad libitum observations (in 2002 and 2003), marks were scratched or otherwise were the object of attention from the bearer or other individuals on only one occasion. In 2002 we collected 22 hr of observations on the three marked monkeys and some unmarked monkeys in 10-min focal samples. Neither the marked nor the unmarked animals attended to the marks during focal samples. Marked and unmarked individuals displayed similar rates of displacement activities (autogrooming, scratching, and yawning). The proportion of scans with at least one near neighbor varied between marked and unmarked subjects, but the direction of the difference was not the same between males and females. The only aggression observed was displacements, and only in one comparison (out of four) did a difference emerge: the marked subadult male received more displacements than the unmarked males. Overall, marked and unmarked individuals did not differ consistently in our measures. Examination of the potential effects of marking should continue, since changes in pelage coloration may have longer-term social effects in species that rely largely on vision.     

Differential effects of ambient temperature and humidity on allogrooming, self-grooming, and scratching in wild Japanese macaques

This study presents data on the effects of variations in ambient temperature and humidity on behaviors related to the care of the pelage (allogrooming, self-grooming, and scratching) in wild Japanese macaques (Macaca fuscata yakui). The amount of time monkeys spent allogrooming was essentially unaffected by variations in ambient temperature and relative humidity. Frequency of scratching and, to a lesser extent, time spent self-grooming significantly increased when ambient temperature and/or relative humidity increased. These results are interpreted in relation to the differences in ultimate function that exist between allogrooming (with both hygienic and social functions) and self-grooming and scratching (with a solely hygienic function).     

Role of COX-1 and COX-2 on skin PGs biosynthesis by mechanical scratching in mice

We examined the involvement of cyclooxygenase (COX)-1 and COX-2 on mechanical scratching-induced prostaglandins (PGs) production in the skin of mice. The dorsal regions of mice were scratched using a stainless brush. COXs expressions in the skin were analyzed using real-time PCR and Western blotting. The effect of acetylsalicylic acid (ASA) on the ability of PGs production were determined based on skin PGs level induced by arachidonic acid (AA) application. Mechanical scratching increased PGD2, PGE2, PGI2 and PGF(2 alpha). COX-1 was constitutively expressed and COX-2 expression was enhanced by scratching. Intravenous administration of ASA inhibited PGs biosynthesis in the normal skin. PGs levels of the skin 6h after ASA administration (ASA 6 h) were almost equal to those of the skin 10 min after ASA administration (ASA 10 min). In the scratched skin, AA-induced PGE2 and PGI2 of ASA 6 h were significantly higher than those of ASA 10 min. The skin PGD2 and PGF(2 alpha) of ASA 10 min were almost same to those of ASA 6 h. In the normal skin of COX-1-deficient mice, skin PGD2 level was lower than that of wild-type mice, although PGE2, PGI2 and PGF(2 alpha) levels were almost equal to those of wild type. In the scratched skin of COX-1-deficient mice, PGD2, PGE2, PGI2 and PGF(2 alpha) levels were lower than those of wild-type mice. These results suggested that cutaneous PGD2 could be mainly produced by COX-1, and PGE2 and PGI2 could be produced by COX-1 and COX-2, respectively, in mice.     

Sperm production and fertility of bonnet monkeys (Macaca radiata) following immunization with ovine follicle stimulating hormone.

Adult male bonnet monkeys were rendered oligospermic but not azoospermic following active immunization with ovine follicle stimulating hormone. The percentage of sperms in the semen having good motility was reduced with a concomitant increase in the sperm ATPase activity. Eight out of 10 immunized monkeys failed to impregnate females of proven fertility after mating for consecutive three cycles while the remaining two impregnated the cohabitated females during the third cycle at a time when the antibody titer was reduced. Active immunization with ovine follicle stimulating hormone may not produce complete azoospermia but renders adult male monkeys infertile provided sufficient antibody titer is maintained.