Research

22 pages, 3052 KiB

Open AccessArticle

Exploratory Investigation of Infrared Thermography for Measuring Gorilla Emotional Responses to Interactions with Familiar Humans

by Matthew R. Heintz, Grace Fuller and Stephanie Allard

Animals 2019, 9(9), 604; https://doi.org/10.3390/ani9090604 - 25 Aug 2019

Cited by 14 | Viewed by 4196

Abstract

Interactions between zoo professionals and animals occur regularly and are believed to be enriching for animals. Little empirical information exists on how animals perceive these interactions, and particularly how the interactions affect the emotional states of animals. Infrared thermography (IRT) has shown some [...] Read more.

Interactions between zoo professionals and animals occur regularly and are believed to be enriching for animals. Little empirical information exists on how animals perceive these interactions, and particularly how the interactions affect the emotional states of animals. Infrared thermography (IRT) has shown some promise in the assessment of emotions in a variety of species, but further research is needed to determine if this method is useful in a zoo setting. We conducted a pilot study to determine if IRT is a valid measure of the emotional responses to routine interactions (positive reinforcement training and cognitive tasks, compared to a control condition) with familiar humans on three western lowland gorillas at the Detroit Zoo. We measured nasal temperatures associated with emotional change using IRT. To examine the validity of the IRT data, we collected saliva samples for hormone analysis before and after each condition, in addition to behavioral data during the interactions and control condition. Decreases in nasal temperatures for two gorillas and an increase in the third indicate that arousal changed consistently within individuals following the interactions but not the control condition. Pre-post cortisol levels and oxytocin concentrations decreased for all conditions, but the decreases seen did not differ among the conditions. The gorillas were highly engaged in the interactions, and two produced more grumble vocalizations during the human-animal interactions (HAIs) compared to the control condition. Additionally, the gorillas performed self-directed behaviors more often during the control condition, also suggesting HAIs were not a negative experience. In summary, we were able to measure changes in arousal using IRT, but we were unable to determine the emotional valence of these changes based on the additional indicators employed. Additionally, the inconsistency across these measures precluded firm conclusions about either the validity of IRT for measuring emotion in this context or how the interactions impacted these gorillas. These findings highlight the challenges of using IRT to measure emotional states in non-human animals, and we discuss further steps necessary to apply this method in future studies. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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25 pages, 4738 KiB

Open AccessArticle

Potential Impact of Construction Noise on Selected Zoo Animals

by Richard Jakob-Hoff, Michael Kingan, Chiaki Fenemore, Gian Schmid, John F. Cockrem, Amanda Crackle, Emily Van Bemmel, Rebecca Connor and Kris Descovich

Animals 2019, 9(8), 504; https://doi.org/10.3390/ani9080504 - 31 Jul 2019

Cited by 24 | Viewed by 9970

Abstract

In anticipation of a major construction project in an urban New Zealand zoo, a study was initiated to assess the response to construction noise of selected animal species (elephant, giraffe, emu and alligator) previously observed to be sensitive to this kind of noise. [...] Read more.

In anticipation of a major construction project in an urban New Zealand zoo, a study was initiated to assess the response to construction noise of selected animal species (elephant, giraffe, emu and alligator) previously observed to be sensitive to this kind of noise. The overall aim was to detect any signs of aversive responses to this noise to enable keepers to recognize these and take any necessary mitigating actions during the construction period. The experimental approach involved the creation of acoustic maps of each focal animal enclosure, a series of 90-min video recordings of the animals’ behavior in response to ambient noise (control) and amplified broadcast of pre-recorded continuous and intermittent construction noise. Concentration of fecal corticosterone metabolites was also measured for the emus. Key findings were that giraffes, elephants and emus appeared to show an increase in behaviors that could indicate stress or agitation including vigilance and locomotion and may prefer quieter regions of their enclosure during sound exposure. Giraffes also increased close contact with conspecifics when exposed to construction noise. While alligators did not show clear evidence of noise-related stress, our findings indicated that all focal species showed some behavioral responses to recorded construction noise. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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35 pages, 2363 KiB

Open AccessArticle

A Protocol for the Ethical Assessment of Wild Animal–Visitor Interactions (AVIP) Evaluating Animal Welfare, Education, and Conservation Outcomes

by Barbara de Mori, Linda Ferrante, Daniela Florio, Elisabetta Macchi, Ilaria Pollastri and Simona Normando

Animals 2019, 9(8), 487; https://doi.org/10.3390/ani9080487 - 25 Jul 2019

Cited by 24 | Viewed by 10471

Abstract

Due to the popularity of wild animal–visitor interactions (AVIs), there is a need for an ethical assessment of their impact on animal welfare, education, and conservation. The protocol presented in this study is designed to evaluate such interactions on an integrated level, using [...] Read more.

Due to the popularity of wild animal–visitor interactions (AVIs), there is a need for an ethical assessment of their impact on animal welfare, education, and conservation. The protocol presented in this study is designed to evaluate such interactions on an integrated level, using a transparent analysis of all the aspects involved, including all the stakeholders and the potential conflicts of values. The protocol consists of a six-step process encompassing dedicated data acquisition and a specific ethical assessment. When the protocol was applied to assess a “giraffe feeding” interaction, steps devoted to data acquisition found that animal welfare risks were low, and that visitors described giraffes with emotionally linked descriptors more often after the interaction. The net promoter score, which refers to how likely visitors would recommend to a friend to join the animal–visitor interaction, was 74%. The subsequent ethical assessment, which consisted of a comparison of the results of the previous steps with an ethical matrix highlighting the ideal situation for all stakeholders’ interests, allowed the overall identification of the ethical concerns entailed by the interaction. A final ethical checklist of the examined AVI had a “yes” in entries regarding animal welfare, emotional, and conservation mindedness outcomes and ethical assessment. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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14 pages, 895 KiB

Open AccessArticle

Using Qualitative Behaviour Assessment to Investigate Human-Animal Relationships in Zoo-Housed Giraffes (Giraffa camelopardalis)

by Freisha Patel, Françoise Wemelsfelder and Samantha J. Ward

Animals 2019, 9(6), 381; https://doi.org/10.3390/ani9060381 - 21 Jun 2019

Cited by 24 | Viewed by 9465

Abstract

Human-Animal Relationships (HAR) in zoos develop from repeated interactions between animals and their caretakers. HAR have been shown to affect health and welfare in farm animals, but limited zoo-based studies exist. This study investigates the association between the qualitative behaviour assessment (QBA) of [...] Read more.

Human-Animal Relationships (HAR) in zoos develop from repeated interactions between animals and their caretakers. HAR have been shown to affect health and welfare in farm animals, but limited zoo-based studies exist. This study investigates the association between the qualitative behaviour assessment (QBA) of emotional expression in giraffes and keeper action score in four types of keeper-animal interaction (KAI). Three giraffes generating 38 clips. QBA, using a free-choice profiling methodology, was applied instructing 18 observers to assess giraffe expressions shown in these clips. QBA scores were analysed using Generalized Procrustes Analysis. Keeper actions during each KAI event were rated by an independent marker, resulting in cumulative scores for keeper action quality. The association between QBA and the keeper action was analyzed using Spearman’s rank correlations. Two main QBA dimensions were identified explaining 59% of the variation between clips. There were significant effects of giraffe and KAI type on QBA dimension 2 (inquisitive/impatient—calm/distracted), and significant positive associations between keeper action quality rating and QBA dimensions 1 and 2, indicating that positive keeper actions resulted in calm and confident giraffes with a willingness to interact. This is the first successful application of QBA for empirically addressing HARs in zoos, however given the small sample size of giraffes in this study, it can be regarded as a pilot study only, and further research is needed to validate the use of QBA in this context. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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16 pages, 2757 KiB

Open AccessArticle

Looking for Visitor’s Effect in Sanctuaries: Implications of Guided Visitor Groups on the Behavior of the Chimpanzees at Fundació Mona

by Jana López-Álvarez, Yaiza Sanjorge, Sara Soloaga, Dietmar Crailsheim and Miquel Llorente

Animals 2019, 9(6), 347; https://doi.org/10.3390/ani9060347 - 13 Jun 2019

Cited by 5 | Viewed by 4213

Abstract

The question of ‘if and how captive primates are affected by visitors’ has gained increasing attention over the last decades. Although the majority reported undesirable effects on behavior and wellbeing, many studies reported contradicting results. Most of these studies were conducted at zoos, [...] Read more.

The question of ‘if and how captive primates are affected by visitors’ has gained increasing attention over the last decades. Although the majority reported undesirable effects on behavior and wellbeing, many studies reported contradicting results. Most of these studies were conducted at zoos, typically with little or no control over visitors’ actions. Yet little is known about the impact under very controlled visitor conditions. In order to fill this gap, we conducted this study at a primate sanctuary which allows public access only via a guided visit under strict supervision. We observed 14 chimpanzees, recording their behavior during, after and in the absence of guided visits over a 10-month period. Furthermore, we categorized the visitors regarding group size and composition to see if certain group types would produce a stronger impact on the chimpanzees’ behavior. As expected, we found visitors at the sanctuary to produce only a neutral impact on the chimpanzees’ behavior, detecting a slight increase of locomotion and decrease of inactivity during visitor activities with chimpanzees demonstrating more interest towards larger sized groups. We argue that the impact has been greatly mitigated by the strict visitor restrictions and care strategies allowing chimpanzees a certain control regarding their visibility. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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14 pages, 1657 KiB

Open AccessArticle

Evaluating the Behavior and Temperament of African Penguins in a Non-Contact Animal Encounter Program

by Sana T. Saiyed, Lydia M. Hopper and Katherine A. Cronin

Animals 2019, 9(6), 326; https://doi.org/10.3390/ani9060326 - 06 Jun 2019

Cited by 26 | Viewed by 10121

Abstract

Animal ambassador programs are increasingly prevalent in zoos, yet few studies have investigated their impact on animal welfare. We assessed the effects of an ambassador program on the behavior of a colony (N = 15) of zoo-housed African penguins (Spheniscus demersus [...] Read more.

Animal ambassador programs are increasingly prevalent in zoos, yet few studies have investigated their impact on animal welfare. We assessed the effects of an ambassador program on the behavior of a colony (N = 15) of zoo-housed African penguins (Spheniscus demersus) and evaluated whether individual characteristics were predictive of participation. Behavioral data were collected for 16 weeks and included 43 “penguin encounters”, during which zoo visitors entered a designated portion of the penguins’ enclosure. When comparing colony behavior following encounters to behavior during a matched control period lacking an encounter, we found no significant difference between affiliative or aggressive behaviors, suggesting that the encounters did not disrupt interactions in the colony. The same was true when comparing behavior preceding the encounter to a matched control period, indicating that any anticipatory period was similarly non-disruptive. Space use during encounters suggested comfort near visitors. We also measured penguin temperament on the shy-bold continuum by recording the birds’ response to novel objects and found that penguins’ temperament, sex, and age were predictive of participation. We concluded that this program had a neutral or positive impact on penguin welfare and considered the findings in relation to aspects of the ambassador program that provided penguins with control over their involvement. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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11 pages, 1246 KiB

Open AccessArticle

The Social Rank of Zoo-Housed Japanese Macaques is a Predictor of Visitor-Directed Aggression

by Jocelyn M. Woods, Stephen R. Ross and Katherine A. Cronin

Animals 2019, 9(6), 316; https://doi.org/10.3390/ani9060316 - 02 Jun 2019

Cited by 12 | Viewed by 5679

Abstract

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social [...] Read more.

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social factors, such as social rank, can also have a large impact on behavior. Here, we considered the influence of both the role of visitors (crowd size and activity levels) and rank on the occurrence of visitor-directed aggression by zoo-housed Japanese macaques (Macaca fuscata, N = 12). We conducted 52 weeks of observation (443.8 h) of macaques living in a large outdoor habitat and recorded 1574 events of visitor-directed behavior, 94.2% of which was characterized as aggressive. We calculated rank using the Elo-rating method. GLMM comparisons indicate that rank was a significant predictor of visitor-directed aggression, with lower-ranked individuals displaying more frequent aggression towards visitors. Additionally, visitor-directed aggression differed by crowd activity levels, but not crowd size. These results support our prediction that rank is associated with differences in visitor-directed aggression, and we interpret this pattern as lower-ranking macaques redirecting aggression toward zoo visitors as safe targets. This work emphasizes how factors emanating from the zoo environment can combine with social dynamics to influence primate response to human presence in the zoo setting. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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17 pages, 3064 KiB

Open AccessArticle

Orangutans’ Comprehension of Zoo Keepers’ Communicative Signals

by Guillaume Dezecache, Aude Bourgeois, Christophe Bazin, Philippe Schlenker, Emmanuel Chemla and Audrey Maille

Animals 2019, 9(6), 300; https://doi.org/10.3390/ani9060300 - 31 May 2019

Cited by 4 | Viewed by 5360

Abstract

Zoological institutions often encourage cooperative interactions between keepers and animals so as to promote animals’ welfare. One useful technique has been conditioning training, whereby animals learn to respond to keepers’ requests, which facilitates a number of, otherwise sensitive, daily routines. As various media [...] Read more.

Zoological institutions often encourage cooperative interactions between keepers and animals so as to promote animals’ welfare. One useful technique has been conditioning training, whereby animals learn to respond to keepers’ requests, which facilitates a number of, otherwise sensitive, daily routines. As various media have been used to convey keepers’ instructions, the question remains of which modality is best to promote mutual understanding. Here, we explored this question with two captive female orangutans. In the first experiment, we compared orangutans’ understanding of previously acquired instructions when those were performed with verbal signals only, gazes only, gestures only, and when all those modalities were combined. Our results showed that gestures were sufficient for successful comprehension by these two apes. In the second experiment, we asked whether this preference could be driven by the non-arbitrary relationship that gestures bear to what they refer to, through iconicity or pointing. Our results revealed that neither iconicity nor pointing helped the subjects comprehend the keepers’ instructions. Our results indicate a preference for instructions given through gestural signals in two captive female orangutans, although its cause remains elusive. Future practice may encourage the use of gestures in communication between keepers and orangutans in general or potentially other animals. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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19 pages, 1848 KiB

Open AccessArticle

Effects of Regulating Visitor Viewing Proximity and the Intensity of Visitor Behaviour on Little Penguin (Eudyptula minor) Behaviour and Welfare

by Samantha J. Chiew, Kym L. Butler, Sally L. Sherwen, Grahame J. Coleman, Kerry V. Fanson and Paul H. Hemsworth

Animals 2019, 9(6), 285; https://doi.org/10.3390/ani9060285 - 28 May 2019

Cited by 40 | Viewed by 7171

Abstract

We examined the effects of regulating the viewing proximity of visitors and the intensity of visitor behaviour on behaviours indicative of fear and stress physiology of 15 zoo-housed little penguins (Eudyptula minor). A 2 × 2 factorial fully randomised design was [...] Read more.

We examined the effects of regulating the viewing proximity of visitors and the intensity of visitor behaviour on behaviours indicative of fear and stress physiology of 15 zoo-housed little penguins (Eudyptula minor). A 2 × 2 factorial fully randomised design was used to examine the effects of regulating: (1) the viewing proximity of visitors to enclosure, ‘normal viewing distance’ and ’increased viewing distance’ (using a physical barrier set up 2 m away from the enclosure), and (2) the intensity of visitor behaviour, ‘unregulated visitor behaviour’ and ‘regulated visitor behaviour’ (using signage and uniformed personnel). In addition, a treatment consisting of closing the enclosure to visitors was included. Penguin behaviour, visitor numbers and visitor behaviour were recorded by CCTV video recordings and direct observations, respectively. Penguin faecal glucocorticoid metabolites were also analysed as a measure of stress physiology. We found that increased viewing distance reduced (p < 0.05) all visitor behaviours except for loud vocalisations and tactile contact with penguins. However, there were no direct effects of signage and uniformed personnel on visitor behaviour (p > 0.05). As the regulation of viewing proximity increased from a closed exhibit to an open exhibit with increased viewing distance, and then to an open exhibit with normal viewing distance, this increased the proportion of penguins huddling (p = 0.0011), vigilant (p = 0.0060) and retreating (p = 0.00013), and decreased the proportion of penguins within 1 m of the visitor viewing area (p = 0.00066), surface swimming (p = 0.00091) and preening in the water (p = 0.042). There were also limited effects of regulating visitor behaviour on penguin behaviour. No treatment effects were found on faecal glucocorticoid metabolites (p > 0.05). These results indicate that regulating visitor viewing proximity affects penguin behaviours indicative of fear and visitor behaviour. This suggests that close visitor contact can be fear-provoking for little penguins but increasing the distance between visitors and penguins can reduce fear responses of penguins by regulating both viewing proximity and visitor behaviour. However, it is unclear whether these changes in penguin behaviour are due to the increased separation between visitors and penguins and/or specific visitor behaviours associated with close viewing proximity to the enclosure, such as leaning over the enclosure or tactile contact with the pool, which are impeded when visitors are further away. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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Review

Jump to: Research, Other

27 pages, 331 KiB

Open AccessFeature PaperReview

The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare

by Sally L. Sherwen and Paul H. Hemsworth

Animals 2019, 9(6), 366; https://doi.org/10.3390/ani9060366 - 17 Jun 2019

Cited by 143 | Viewed by 52420

Abstract

Achieving and maintaining high standards of animal welfare is critical to the success of a modern zoo. Research has shown that an animal’s welfare is highly dependent on how various individual animal factors (e.g., species traits, genetics, temperament and previous experience) interact with [...] Read more.

Achieving and maintaining high standards of animal welfare is critical to the success of a modern zoo. Research has shown that an animal’s welfare is highly dependent on how various individual animal factors (e.g., species traits, genetics, temperament and previous experience) interact with environmental features (e.g., social grouping, enclosure design and sensory environment). One prominent feature of the zoo environment is the presence of visitors. Visitor contact can be unpredictable and intense, particularly in terms of auditory and visual interaction. Depending on an animal’s perception of this interaction, visitors can have either negative, neutral or positive impacts on zoo animal behaviour and welfare. This paper reviews the literature on the implications and potential opportunities of human-zoo animal interactions on animal behaviour and welfare, with the aim of stimulating interest, understanding and exploration of this important subject. The literature to date presents a mixed range of findings on the topic. It is possible this variation in the responses of zoo animals to visitors may be due to species-specific differences, the nature and intensity of the visitor interactions, enclosure design, and individual animal characteristics. Analysing these studies and better understanding animal preferences and motivations can provide insight into what animals find negatively and positively reinforcing in terms of visitor contact in a specific zoo setting. This understanding can then be applied to either safeguard welfare in cases where visitors can have a negative impact, or, conversely, it can be applied to highlight opportunities to encourage animal-visitor interaction in situations where animals experience positive emotions associated with visitor interaction. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

Other

Jump to: Research, Review

15 pages, 1234 KiB

Open AccessCommentary

Assessing and Enhancing the Welfare of Animals with Equivocal and Reliable Cues

by Jason V. Watters and Bethany L. Krebs

Animals 2019, 9(9), 680; https://doi.org/10.3390/ani9090680 - 13 Sep 2019

Cited by 10 | Viewed by 3494

Abstract

The actions of human caretakers strongly influence animals living under human care. Here, we consider how intentional and unintentional signals provided by caretakers can inform our assessment of animals’ well-being as well as help to support it. Our aim is to assist in [...] Read more.

The actions of human caretakers strongly influence animals living under human care. Here, we consider how intentional and unintentional signals provided by caretakers can inform our assessment of animals’ well-being as well as help to support it. Our aim is to assist in further developing techniques to learn animals’ affective state from their behavior and to provide simple suggestions for how animal caretakers’ behavior can support animal welfare. We suggest that anticipatory behavior towards expected rewards is related to decision-making behavior as viewed through the cognitive bias lens. By considering the predictions of the theories associated with anticipatory behavior and cognitive bias, we propose to use specific cues to probe the cumulative affective state of animals. Additionally, our commentary draws on the logic of reward sensitivity and judgement bias theories to develop a framework that suggests how reliable and equivocal signals may influence animals’ affective states. Application of this framework may be useful in supporting the welfare of animals in human care. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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13 pages, 306 KiB

Open AccessCommentary

Dilemmas for Natural Living Concepts of Zoo Animal Welfare

by Mark James Learmonth

Animals 2019, 9(6), 318; https://doi.org/10.3390/ani9060318 - 05 Jun 2019

Cited by 20 | Viewed by 19807

Abstract

This ethical discourse specifically deals with dilemmas encountered within zoological institutions, namely for the concept of natural living, and a new term—wilding. It is agreed by some that zoos are not ethically wrong in principle, but there are currently [...] Read more.

This ethical discourse specifically deals with dilemmas encountered within zoological institutions, namely for the concept of natural living, and a new term—wilding. It is agreed by some that zoos are not ethically wrong in principle, but there are currently some contradictions and ethical concerns for zoos in practice. Natural living is a complicated concept, facing multiple criticisms. Not all natural behaviours, nor natural environments, are to the benefit of animals in a captive setting, and practical application of the natural living concept has flaws. Expression of natural behaviours does not necessarily indicate positive well-being of an animal. Herein it is suggested that highly-motivated behaviours may be a better term to properly explain behaviours of more significance to captive animals. Wilding refers to extrapolation of the natural living concept to treating an animal as wild, residing in a wild habitat. This definition is intrinsically problematic, as quite literally by definition, captivity is not a wild nor natural environment. Treating a captive animal exactly the same as a wild counterpart is practically impossible for many species in a few ways. This article discusses complexities of natural living versus natural aesthetics as judged by humans, as well as the possibility of innate preference for naturalness within animals. Zoos nobly strive to keep wild animals as natural and undomesticated as possible. Here it is argued that unintended and unavoidable genetic and epigenetic drift favouring adaptations for life in a captive environment may still occur, despite our best efforts to prevent this from occurring. This article further discusses the blurred lines between natural and unnatural behaviours, and the overlaps with more important highly-motivated behaviours, which may be better predictors of positive affective states in captive animals, and thus, better predictors of positive well-being and welfare. Finally, as we are now in the Anthropocene era, it is suggested that human-animal interactions could actually be considered natural in a way, and notwithstanding, be very important to animals that initiate these interactions, especially for “a life worth living”. Full article

(This article belongs to the Special Issue Human Influences on the Behaviour and Welfare of Zoo Animals)

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