Capuchin monkeys' use of human and conspecific cues to solve a hidden object-choice task.

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.

Effects of Intranasal and Oral Bordetella bronchiseptica Vaccination on the Behavioral and Olfactory Capabilities of Detection Dogs.

The bacterium Bordetella bronchiseptica is responsible for serious respiratory disease in dogs, most often associated with 'kennel cough' (canine infectious tracheobronchitis). It is recommended that dogs are vaccinated against the bacterium every 6-12 months, either by oral or intranasal administration. Any impairment of dogs' olfactory capabilities due to medical treatments may impact their efficiency and accuracy in their jobs. This study examined (1) the effect of intranasal and oral vaccines on the olfactory capabilities of detection dogs; as well as (1) effects of the vaccines on canine behavior. Dogs that were vaccinated initially with the oral and 28 days later with intranasal B. bronchiseptica were generally slower to find the target odor than the dogs that were assigned intranasal then oral vaccine. This result prompted a second between-subjects study to further investigate any impact of intranasal administration of the B. bronchiseptica vaccine on the olfactory capabilities of dogs. The intranasal vaccine was of particular interest due to its prevalent use and potential for nasal inflammation leading to decreased olfactory capabilities. Neither odor threshold nor time spent searching for odor were affected by the intranasal vaccine. Behavioral analyses showed that behaviors associated with the dogs' positive and negative motivation affected their time spent finding the target odor; this suggests that behavior should be considered in future studies of olfactory performance.

The first responder exposure to contaminating powder on dog fur during intranasal and intramuscular naloxone administration.

OBJECTIVE: To determine whether first responders delivering naloxone by either the IM or intranasal (IN) route were at risk of contamination with inert powder simulating canine opioid exposure. DESIGN: Prospective, crossover design. SETTING: Research study (university setting). ANIMALS: Ten clinically normal working dogs ranging from 9 to 44 months were enrolled based on training to detect odor and ability to be restrained with minimal stress. All enrolled dogs completed both arms of the study without adverse effects. INTERVENTIONS: Dogs were randomly assigned to fentanyl reversal with either IM or IN naloxone and then the alternate treatment after a 7-day washout period. Prior to reversal, dogs' heads were brushed with an inert glow-in-the-dark powder. First responders (the same 2 individuals for all dogs) performing the reversal were photographed under ultraviolet light prior to and 5 min after administering the medication. Digital photographs were scored by body region for presence of glowing powder by observers blinded to timing of photograph (pre- or postreversal) and route of reversal (IM vs IN). MEASUREMENTS AND MAIN RESULTS: Compared to pretreatment, the inert powder scores were higher after treatment regardless of route of naloxone administration (P < 0.001). IN administration led to higher contamination than IM naloxone, particularly in the chest area (P = 0.012). CONCLUSIONS: Both IN and IM naloxone administration to dogs with clinical signs of opioid exposure result in a risk of first responders becoming contaminated with powder, which could include opioids. Awareness, proper personal protective equipment, and appropriate posttreatment decontamination are important to reduce risk of inadvertent exposure of mucous membranes to these contaminating powders.

Genome scanning of behavioral selection in a canine olfactory detection breeding cohort.

Research on working dogs is growing rapidly due to increasing global demand. Here we report genome scanning of the risk of puppies being eliminated for behavioral reasons prior to entering the training phase of the US Transportation Security Administration's (TSA) canine olfactory detection breeding and training program through 2013. Elimination of dogs for behavioral rather than medical reasons was based on evaluations at three, six, nine and twelve months after birth. Throughout that period, the fostered dogs underwent standardized behavioral tests at TSA facilities, and, for a subset of tests, dogs were tested in four different environments. Using methods developed for family studies, we performed a case-control genome wide association study (GWAS) of elimination due to behavioral observation and testing results in a cohort of 528 Labrador Retrievers (2002-2013). We accounted for relatedness by including the pedigree as a covariate and maximized power by including individuals with phenotype, but not genotype, data (approximately half of this cohort). We determined genome wide significance based on Bonferroni adjustment of two quasi-likelihood score tests optimized for either small or nearly-fully penetrant effect sizes. Six loci were significant and five suggestive, with approximately equal numbers of loci for the two tests and frequencies of loci with single versus multiple mapped markers. Several loci implicate a single gene, including CHD2, NRG3 and PDE1A which have strong relevance to behavior in humans and other species. We briefly discuss how expanded studies of canine breeding programs could advance understanding of learning and performance in the mammalian life course. Although human interactions and other environmental conditions will remain critical, our findings suggest genomic breeding selection could help improve working dog populations.

Egg masses as training aids for spotted lanternfly Lycorma delicatula detection dogs.

The spotted lanternfly (Lycorma delicatula) is an invasive species first detected in 2014. The insect feeds on plants causing severe damage in vineyards such as the occurrence of sooty mold fungus that impairs leaf photosynthesis. Currently, there is extensive research on how to track and ultimately prevent the spread of this species. It lays eggs that persist through the winter, while the adults die out, which presents a unique opportunity to enter infested or suspected infested areas to begin quarantine and management of the spread while the species is dormant. Detection dogs may be a tool that can be used to search out the spotted lanternfly egg masses during this overwintering period, however it is not known whether dogs can detect any specific odor from the spotted lanternfly eggs. Moreover, as the eggs are only available during certain times of the year, and hatch based on temperature, finding training aids for the dogs could prove difficult. In this study, we investigated whether three detection dogs could learn the odor from dead spotted lanternfly egg masses and if so, whether that would allow them to recognize live spotted lanternfly egg masses. We found that dogs could be trained to find dead spotted lanternfly egg masses, and could learn to ignore relevant controls, with high levels of sensitivity and specificity (up to 94.6% and 92.8%, respectively). Further, we found that after the training, dogs could find live spotted lanternfly egg masses without additional training and returned to previous levels of sensitivity and specificity within a few sessions. Coded videos of training and testing sessions showed that dogs spent more time at the egg masses than at controls, as expected from training. These results suggest that dead spotted lanternfly egg masses could be a useful training aid for spotted lanternfly detection dogs.

Studying animal innovation at the individual level: A ratings-based assessment in capuchin monkeys (Sapajus [Cebus] sp.).

Large-scale studies of individual differences in innovative behavior among nonhuman animals are rare because of logistical difficulties associated with obtaining observational data on a large number of innovative individuals across multiple locations. Here, we take a different approach, using observer ratings to study individual differences in innovative behavior in 127 brown capuchin monkeys (Sapajus [Cebus] sp.) from 15 social groups and 7 facilities. Capuchins were reliably rated by 1 to 7 raters (mean 3.2 ± 1.6 raters/monkey) on a 7-point Likert scale for levels of innovative behavior, task motivation, sociality, and dominance. In a subsample, we demonstrate these ratings are valid: Rated innovation predicted performance on a learning task, rated motivation predicted participation in the task, rated dominance predicted social rank based on win/loss aggressive outcomes, and rated sociality predicted the time that monkeys spent in proximity to others. Across all 127 capuchins, individuals that were rated as being more innovative were significantly younger, more social, and more motivated to engage in tasks. Age, sociality, and task motivation all had independent effects on innovativeness, whereas sex, dominance, and group size were nonsignificant. Our findings are consistent with long-term behavioral observations of innovation in wild white-faced capuchins. Observer ratings may, therefore, be a valid tool for studies of animal innovation. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Discrimination of SARS-CoV-2 infected patient samples by detection dogs: A proof of concept study.

While the world awaits a widely available COVID-19 vaccine, availability of testing is limited in many regions and can be further compounded by shortages of reagents, prolonged processing time and delayed results. One approach to rapid testing is to leverage the volatile organic compound (VOC) signature of SARS-CoV-2 infection. Detection dogs, a biological sensor of VOCs, were utilized to investigate whether SARS-CoV-2 positive urine and saliva patient samples had a unique odor signature. The virus was inactivated in all training samples with either detergent or heat treatment. Using detergent-inactivated urine samples, dogs were initially trained to find samples collected from hospitalized patients confirmed with SARS-CoV-2 infection, while ignoring samples collected from controls. Dogs were then tested on their ability to spontaneously recognize heat-treated urine samples as well as heat-treated saliva from hospitalized SARS-CoV-2 positive patients. Dogs successfully discriminated between infected and uninfected urine samples, regardless of the inactivation protocol, as well as heat-treated saliva samples. Generalization to novel samples was limited, particularly after intensive training with a restricted sample set. A unique odor associated with SARS-CoV-2 infection present in human urine as well as saliva, provides impetus for the development of odor-based screening, either by electronic, chemical, or biological sensing methods. The use of dogs for screening in an operational setting will require training with a large number of novel SARS-CoV-2 positive and confirmed negative samples.

Differences in the Search Behavior of Cancer Detection Dogs Trained to Have Either a Sit or Stand-Stare Final Response.

Recent literature has demonstrated that dogs have the potential to detect, and communicate the presence of, various human diseases. However, there is a lack of investigation into whether commonplace training differences within the field could influence a dog's behavior during a biomedical detection task. Here we report on the behavior of four dogs trained to alert to blood plasma samples taken from individuals with ovarian cancer. One hundred trials per dog were selected from routine video recordings collected over a period of 13 months. Videos were coded frame by frame to quantify sample checking, alerting behavior, and durations of alert. Dogs had previously been trained to elicit a final response behavior once they had located the target odor. Two dogs had a "sit" response while the other two had a "stand-stare" response. Alert behavior was categorized as true positive (a correct alert to a cancer sample) or false positive (an incorrect alert to biological and non-biological controls and distractors). Hesitations were also recorded, where the dog either checks the sample twice or, spends a longer duration of time sniffing the sample than a true pass without carrying out their final response. Results show individual variation in the total frequency of false alerts elicited. However, the rate of hesitations appears to be influenced by alert style, with stand-stare dogs carrying out 40 and 32, respectively (total = 72) and sit dogs carrying out 7 and 8, respectively (total = 15). The stand-stare dogs had a non-significant difference in the duration of their true and false positive alerts. In contrast, the sit dogs showed a significant difference (p < 0.001), maintaining their false alerts for, on average, two times the duration of their true alerts. Stand-stare dogs increased the duration of time spent in contact with the port when plasma samples were present, whereas sit dogs spent on average 0.3 s in contact with the port regardless of what sample type it contained. These findings suggest that the type of operant response a biomedical detection dog has been trained may influence their sample checking and response behavior.

A Randomized Cross-Over Trial Comparing the Effect of Intramuscular Versus Intranasal Naloxone Reversal of Intravenous Fentanyl on Odor Detection in Working Dogs.

Fentanyl is a potent opioid used clinically as a pain medication and anesthetic but has recently seen a sharp rise as an illicit street drug. The potency of fentanyl means mucous membrane exposure to a small amount of the drug can expose first responders, including working canines, to accidental overdose. Naloxone, a fast-acting opioid antagonist administered intranasally (IN) or intramuscularly (IM) is currently carried by emergency personnel in the case of accidental exposure in both humans and canines. Despite the fact that law enforcement relies heavily on the olfactory abilities of canine officers, the effects of fentanyl exposure and subsequent reversal by naloxone on the olfactory performance of canines are unknown. In a block-randomized, crossover trial, we tested the effects of IN and IM naloxone on the abilities of working dogs to recognize the odor of Universal Detection Calibrant (UDC) prior to, and two, 24, and 48 h after intravenous fentanyl sedation and naloxone reversal. No detectable influence of fentanyl sedation and naloxone reversal on the dogs' olfactory abilities was detected. We also found no difference in olfactory abilities when dogs received IN or IM naloxone. Together, results suggest no evidence that exposure to intravenous fentanyl followed by naloxone reversal impairs canine olfactory ability under these conditions.

In wolves, play behaviour reflects the partners' affiliative and dominance relationship.

Puppy packs (consisting of only puppies) and mixed-age packs (composed of puppies and adults) were observed to test whether social play can be used for assessing and establishing social relations in wolves, Canis lupus. Differently from previous studies, we looked at play behaviours in detail, allowing us to categorize play interactions as either competitive or relaxed, and predicted that different types of play would be associated with different relationships between individuals. We found that the more time dyads spent in relaxed play, the more affiliative interactions they exchanged outside of play. In the mixed-age packs, dyads that spent more time in both relaxed and competitive play showed fewer exchanges of aggressive behaviours. Conversely, in puppy packs, the more time dyads spent in competitive play, the more aggressive interactions were exchanged outside of play. Since clear dominance relationships emerged in the mixed-age packs, but not in puppy packs, we suggest that play can help to reduce the frequency of aggressive interactions only when a clear hierarchy exists between pack members. Furthermore, we found that in both puppy and mixed-age packs, dominance relationships were reflected and rarely reversed during play. Finally, dyads with a less clear dominance relationship spent more time playing in a competitive way. Overall, our results support the social assessment hypothesis suggesting that social relationships outside of play are reflected during playful interactions. Moreover, we revealed how different types of play, that is, playing in a competitive or relaxed way, may be related to different social relationships. This distinction between play types has not been acknowledged before but could help researchers better understand the functions of play in different species.

The influence of reward quality and quantity and spatial proximity on the responses to inequity and contrast in capuchin monkeys (Cebus [Sapajus] apella).

Recent evidence within the field of comparative psychology has demonstrated that small differences in procedure may lead to significant differences in outcome. Therefore, failing to fully explore the impact of different contexts on a behavior limits our ability to fully understand that behavior. A behavior that has exhibited substantial variation, both within and across studies, is animals' responses to violations of their expectations, either when expectations were based on another's outcome (inequity) or one's previous outcome (contrast). We explored this further in capuchin monkeys, focusing on the following 2 factors that often vary in such tests but have not yet been rigorously explored: the relative values of the food rewards and the degree of separation of the subjects. Concerning the first, we examined responses to violation of expectations when the difference between what was expected (or what the partner got) and what was received differed in either quality or quantity. Concerning the second, we compared responses when the 2 individuals were separated by a clear partition (barrier condition) versus sharing the same enclosure without the partition (no-barrier condition). Our results suggest that responses to inequity are most likely to emerge when the food received is low-value food, regardless of the difference between the actual and the expected outcome. However, capuchins did not respond differently to different quantities of rewards, nor did the degree of separation between subjects significantly affect results. We consider the implications of this work for both studies of violation of expectation and other cognitive and behavioral tasks. (PsycINFO Database Record

Domestication Does Not Explain the Presence of Inequity Aversion in Dogs.

Sensitivity to inequity is thought to be an important mechanism for recognizing undesirable cooperative partners and thus crucial for the evolution of human cooperation [1]. This link may not be unique to humans, as cooperative non-human primates also react to unequal outcomes [2], whereas non-cooperative species do not [3]. Although this hypothesis has not been tested in non-primate species, studies revealed that pet dogs show a limited form of inequity aversion, responding to reward, but not quality inequity [4-6]. It has been proposed that this primitive form of inequity aversion was selected for during domestication and thus absent in their ancestors, wolves. Alternatively, wolves, which hunt, raise pups, and defend their territory cooperatively, are similarly inequity averse as non-human primates, or at least to the same degree as pet dogs. Testing similarly raised and kept pack-living dogs and wolves, we found both to be inequity averse when their partner was being rewarded but they were not for performing the same action. Additionally, both wolves and dogs reacted to receiving a lower-quality reward than their partner. These results suggest that the inequity response found in pack-living dogs and wolves is comparable to that observed in non-human primates; results from studies on pet dogs may be confounded by the dogs' relationship with humans. Consequently, our results suggest that inequity aversion was present already in the common-probably cooperative-ancestor of wolves and dogs and thus support the hypothesis of a close link of cooperation and inequity aversion.

What Are the Ingredients for an Inequity Paradigm? Manipulating the Experimenter's Involvement in an Inequity Task with Dogs.

Cooperation is only beneficial if the outcome is equally shared between individuals involved in the cooperative interaction. A mechanism to limit the development of unequal cooperation is inequity aversion, the negative reaction to unequal treatment. While inequity aversion has been studied extensively across many animal species, it remains unclear whether inequity aversion elicited in experimental settings is directed to the cooperative partner animal or rather to the experimenter distributing the rewards unequally. In the current study we aimed to further investigate whether the presence of an experimenter distributing rewards is essential in order to elicit inequity aversion in dogs. We tested 22 dog dyads in an inequity task, requiring dyads to alternately press a buzzer in order to receive rewards of equal or unequal value. We manipulated the extent of the experimenter's involvement in the task: in the experimenter-present version an experimenter gave a command to the dogs to press the buzzer and delivered the rewards by pushing the bowls into the dogs' enclosure. In contrast, in the experimenter-absent version, no experimenter was visible and the buzzer and bowls were moved from behind a curtain. We found that dogs did not respond to the unequal treatment regardless of the experimenter's involvement in the task. Nonetheless, we found that dogs based their behavior on frustration and social facilitation in the experimenter-absent version of the task, suggesting that a social interaction with an experimenter may be one aspect necessary to elicit inequity aversion. One potential explanation for the absence of inequity aversion in the experimenter-present version of the task might be the reward delivery method. Using separate sets of reward bowls for each dog instead of a shared bowl could have removed a potentially important competitive aspect (i.e., shared resource) from the inequity paradigm. In addition, delivering the rewards via bowls, rather than directly handing the rewards to the dogs, might have caused dogs to perceive the task as less cooperative. These results suggest that both the presence of an experimenter causing inequity and the inclusion of a competitive or cooperative element in the task may be basic requirements for eliciting inequity aversion.

Inequity Aversion Negatively Affects Tolerance and Contact-Seeking Behaviours towards Partner and Experimenter.

Inequity aversion has been proposed to act as a limiting factor for cooperation, thus preventing subjects from disadvantageous cooperative interactions. While a recent study revealed that also dogs show some sensitivity to inequity, the underlying mechanisms of this behaviour are still unclear. The aim of the current study was threefold: 1) to replicate the study by Range et al. (2009, PNAS, 106, 340-345); 2) to investigate the emotional mechanisms involved in the inequity response by measuring the heart rate and 3) to explore the link between inequity aversion and cooperation in terms of behaviours shown towards the partner dog and towards the experimenter who caused the inequity. Dog tested in dyads were alternately asked to give their paw and were either equally or unequally rewarded by the experimenter. After each social test condition, we conducted food tolerance tests and free interaction tests in which the subjects' social behaviour towards the partner and the experimenter were observed. As in the previous study, subjects refused to continue giving their paw when only the partner was rewarded, but not when both dogs were rewarded with rewards of different quality. Although subjects did not react to this quality inequity during the test, we did find reduced durations of food sharing in the subsequent tolerance test, indicating that dogs perceived the inequity but were not able to react to it in the test context. Moreover, subjects avoided their partner and the experimenter more during the free interaction time following unequal compared to equal treatment. Despite the clear behavioural reactions to inequity, we could not detect any changes in heart rate. Results suggest that inequity aversion might in fact be mediated by simple emotional mechanisms: sharing a negative experience, like inequity, might reduce future cooperation by decreasing the likelihood of proximity being maintained between partners.

Play Behavior in Wolves: Using the '50:50' Rule to Test for Egalitarian Play Styles.

Social play is known as a cooperative interaction between individuals involving multiple mechanisms. However, the extent to which the equality of individuals' play styles affects the interaction has not been studied in many species. Dyadic play between wolf puppies, as well as between puppies and adults, was studied to investigate both self-handicapping and offensive behaviors to determine the extent to which wolves engage in play styles where one individual does not dominate the play. Our results did not support the hypothesized '50:50' rule, which suggests that more advantaged individuals should show higher rates of self-handicapping behaviors in order to facilitate play with others. Adult wolves performed significantly less self-handicapping behaviors than their puppy partners, and they performed significantly more offensive behaviors than their puppy partners. While the '50:50' rule was not supported at any time during our study period, dyads consisting of two puppies had significantly more equal play than dyads consisting of one puppy and one adult. These results suggest that wolf puppies are more likely to play on equal terms with similarly-aged play partners, while the dominance status of the partners dictates offensive and self-handicapping behaviors between animals of different ages.

Divergent personality structures of brown (Sapajus apella) and white-faced capuchins (Cebus capucinus).

One way to gain insights into personality evolution is by comparing the personality structures of related species. We compared the personality structure of 240 wild white-faced capuchin monkeys to the personality structure of 100 captive brown capuchin monkeys. An ancillary goal was to test the degree to which different personality questionnaires yielded similar personality dimensions. Both species were rated on a common set of 26 antonym pairs. The brown capuchin monkeys were also rated on the 54-item Hominoid Personality Questionnaire. Our cross-species comparisons revealed 3 personality dimensions-Assertiveness, Openness, and Neuroticism-shared by brown and white-faced capuchins, suggesting that these dimensions were present in the common ancestor of these species. Our comparison of the dimensions derived from the antonym pairs and the Hominoid Personality Questionnaire revealed that three common dimensions were identified by both questionnaires. In addition, the dimension Attentiveness was only identified using the Hominoid Personality Questionnaire. These results indicate that major features of capuchin personality are conserved and that the structure of some traits, such as those related to focus, persistence, and attention, diverged. Further work is needed to identify the evolutionary bases that led to the conservation of some dimensions but not others. (PsycINFO Database Record

Personality structure in brown capuchin monkeys (Sapajus apella): comparisons with chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta).

Species comparisons of personality structure (i.e., how many personality dimensions and the characteristics of those dimensions) can facilitate questions about the adaptive function of personality in nonhuman primates. Here we investigate personality structure in the brown capuchin monkey (Sapajus apella), a New World primate species, and compare this structure to those of chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta). Brown capuchins evolved behavioral and cognitive traits that are qualitatively similar to those of great apes, and individual differences in behavior and cognition often reflect differences in personality. Thus, we hypothesized that brown capuchin personality structure would overlap more with great apes than with rhesus macaques. We obtained personality ratings from seven sites, including 127 brown capuchin monkeys. Principal-components analysis identified five personality dimensions (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness), which were reliable across raters and, in a subset of subjects, significantly correlated with relevant behaviors up to a year later. Comparisons between species revealed that brown capuchins and great apes overlapped in personality structure, particularly chimpanzees in the case of Neuroticism. However, in some respects (i.e., capuchin Sociability and Openness) the similarities between capuchins and great apes were not significantly greater than those between capuchins and rhesus macaques. We discuss the relevance of our results to brown capuchin behavior and the evolution of personality structure in primates.