Figures
Abstract
Behavioral studies in non-human primates have become ideal models for further investigations into advanced cognitive function in humans. To date, there is no systematic ethogram of the cynomolgus monkey (Macaca fascicularis) in a free enclosure. In a field observation of 6012 subjects, 107 distinct behaviors of M. fascicularis were preliminarily described. 83 of these behaviors were then independently validated through a randomized cohort and classified into 12 behavioral categories. 53 of these behaviors were then selected to accurately reflect the daily mundane activity of the species in a free enclosure. These findings systematically document the behavior of M. fascicularis in a free enclosure for use in further investigations.
Citation: Xu F, Xie L, Li X, Li Q, Wang T, Ji Y, et al. (2012) Construction and Validation of a Systematic Ethogram of Macaca fascicularis in a Free Enclosure. PLoS ONE 7(5): e37486. https://doi.org/10.1371/journal.pone.0037486
Editor: Gonzalo G. de Polavieja, Cajal Institute, Consejo Superior de Investigaciones Científicas, Spain
Received: December 13, 2011; Accepted: April 20, 2012; Published: May 25, 2012
Copyright: © 2012 Xu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the National Basic Research Program of China (the 973 Program; Grant No. 2009CB918300), the National Natural Science Foundation of China (Grant No. 30900456) and the Natural Science Foundation Project of Chongqing (CSTC, 2010BB5185 and 2011BA5012). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have read the journal's policy and have the following conflicts: The observations for this study were carried out at the Macaca fascicularis Feeding Base of Zhongke Experimental Animal Co., Ltd. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials.
Introduction
Behavioral science has garnered considerable attention in contemporary neurological and psychological scientific circles as a platform for studying advanced cognitive function in humans. The United States declared 2000–2010 as the “Decade of Behavior” [1], in line with the increasing volume of research into psychopathology and human behavior. This phenomenon has been accompanied by a rising number of behavioral studies on human subjects [2].
However, due to ethical considerations, certain advanced functional and structural investigations cannot be conducted in humans [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13], [14], [15]. Non-human primate models offer a viable alternative, as humans share neuroanatomical and psychological homology with these species. But, behavioral descriptions and classifications on non-human primates are often incomplete and scattered across disparate studies. Therefore, to support future behavioral investigations and concomitant quantitative studies, it is imperative to establish systematic ethogram of non-human primates on a species-specific basis [16], [17].
Several macaque species have demonstrated promise as non-human primate models for behavioral studies. In the 1930's, Skinner et al. [18] constructed a systematic ethogram of a captive lion-tailed macaque (Macaca silenu) through behavioral descriptions, definitions and classifications, as well as comparisons with other monkey species. Adams et al. [19] studied the sexual behavior of the adult cynomolgus monkey (Macaca fascicularis), uncovering the value of this macaque species as an animal model for human behavioral studies. Jolly et al. [20] reported this species is capable of acquiring feeding and social behaviors by example, indicating its behavioral homology to humans. William et al. [21] cataloged the behavior of 8 male rhesus monkeys (Macaca mulatta) for approximately 3 years under conditions of separation and confinement. Furthermore, Zhang, J. [22] investigated the post conflict settlement of group-living primate, among adult females Sichuan snub-nosed monkeys Rhinopithecus roxellana, which is crucial understanding for primate's competition and cooperation, and indicated that the pattern of post conflict affiliation demonstrates that the R. roxellana belongs to a tolerant species. In addition, Mear and Harlow [23] investigated the development of play behaviors in 8 rhesus infants over a 12-week period. Ultimately, Yamada, Kazunori [24] reviewed the studies concerning the social behavior of Old World monkeys and concluded that the social environments plays an important role in their daily routine on how to manage themselves.
However, to date, no systematic ethogram of the cynomolgus monkey (M. fascicularis) has been established. In this study, a comprehensive systematic ethogram (including behavioral descriptions, definitions and classifications) for M. fascicularis in a free enclosure was constructed and validated which satisfies the technical requirements for future hypothesis-testing and quantitative studies on the species.
Results
From April to December 2010, 107 behavioral items were created based on the Posture-Action-Environment principle [25], and the scanning method was employed to verify these behaviors among 6012 M. fascicularis subjects in a free enclosure. 83 of these behaviors were then validated on 40 randomly selected female subjects and classified into 12 behavioral categories .From this set of 83 behaviors, 53 behaviors were then selected from these 12 behavioral categories: i) ingestion, ii) thermo-regulatory, iii) rutting and estrous, iv) mating, v) resting, vi) parental, vii) amicable, iix) conflict, ix) vigilance, x) communication, xi) locomotive and xii) miscellaneous behaviors, more detail data, please see File S3. Across all 12 behavioral categories per day and 12 behavior categories within all observational phases per day, resting and vigilance behaviors occurred at a significantly greater average daily duration per subject than other behaviors (11.56× and 10.39× the median value, respectively; Fig. 1, Table 1 and table 2). Across all 53 behaviors and all observational phases, watching company (a vigilance behavior), quadrupedal walking on floor (a locomotive behavior), and sitting on floor (a resting behavior) were the most frequent behaviors observed (77.10×, 47.88×, and 46.27× the median value, respectively; Table 3). The average durations per subject for all 12 behavioral categories on both a daily and observational phase basis are listed in Tables 1 and 2, respectively. The average counts per subject for all 53 behaviors on both a daily and observational phase basis are detailed in Tables 3 and 4, respectively.
The average daily duration per subject (total duration of each behavior/40 subjects/4 days) are aggregated by category and displayed by phase. Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Ingestion behaviors occurred at a moderately higher average daily duration per subject with respect to other behavioral categories (1.36× the median value; Table 1). Chewing (5.57× the median value), picking remaining food (3.94× the median value), and feeding while sitting (3.73× the median value) were the most frequent ingestion behaviors observed across all phases with the notable exception of phase P2 (Fig. 2, Table 3) ingestion. In this phase, drinking (1.32× the median value) was the most frequently observed ingestion behavior. In addition, the average daily count per subject for ingestion behaviors was significantly higher in phase P5.
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each ingestion behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase (total no. of actions/40 subjects/4 days).Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Thermo-regulatory behavior occurred at a higher average daily duration per subject as compared to other behavioral categories (2.65× the median value; Table 1). Rutting, estrous and mating behaviors occurred at a significantly lower average daily duration per subject relative to other behavioral categories (0.03× and 0.01× the median value, respectively; Table 1). Average daily counts per subject and relative frequencies for thermo-regulatory, rutting and estrous, and mating behaviors are shown in Figure 3. Embracing, a thermo-regulatory behavior, accounted for the highest proportion of these behaviors across all phases (5.84× the median value). Presenting buttocks was the most frequent rutting and estrous behavior (0.61× the median value), and copulating (0.46× the median value) was the most frequent mating behavior across all phases. (Fig. 3, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each thermo-regulatory, rutting, estrous, and mating behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase (total no. of actions/40 subjects/4 days). Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Resting behavior, the behavioral category of longest duration, occurred at a significantly higher average daily duration per subject as compared to other categories (11.56× the median value; Table 1). Across all phases, sitting on the floor (46.27× the median value) was the most frequent resting behavior, distantly followed by perching on shelf (6.97× the median value)shelf, and hanging on window or door (6.84× the median value; Fig. 4, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each resting behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase (total no. of actions/40 subjects/4 days). Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Parental and amicable behaviors occurred at a moderately higher average daily duration per subject as compared to other categories (1.56× and 1.18× the median value, respectively; Table 1). Among parental and amicable behaviors, four (4) primary constituent behaviors occurred in every phase. Across all phases, the frequencies of grooming and being groomed were approximately equivalent (3.63× and 4.48× the median value, respectively), and holding infant occurred approximately four (4) times more frequently than nursing infant (7.91× and 1.81× the median value, respectively; Fig. 5, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each parental and amicable behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase (total no. of actions/40 subjects/4 days). Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Conflict behaviors occurred at a significantly lower average daily duration per subject as compared to other categories; vigilance behaviors, in contrast, occurred at a significantly higher average daily duration per subject as compared to other categories (0.01× and 10.39× the median value, respectively; Table 1). Among conflict and vigilance behaviors across all phases, watching company was the most frequent behavior (77.10× the median value), distantly seconded by shifting position (10.61× the median value; Fig. 6, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each conflict and vigilance behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase(total no. of actions/40 subjects/4 days). Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Locomotive behaviors occurred at a moderately lower average daily duration per subject as compared to other categories (0.82× the median value; Table 1). Among locomotive behaviors across all phases, quadrupedal walking on floor (47.88× the median value), climbing (13.44× the median value), walking on shelf (5.10× the median value) , and standing (4.30× the median value) were the most frequent behaviors (Fig. 7, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each locomotive behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase (total no. of actions/40 subjects/4 days). Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Communication behaviors occurred at a significantly lower average daily duration per subject as compared to other categories; miscellaneous behaviors occurred at a moderately lower average daily duration per subject (0.02× and 0.66× the median value, respectively; Table 1). Among communication and miscellaneous behaviors, scratching body by foreleg (21.90× the median value) was the most frequent behavior, distantly followed by scratching by hind leg (3.36× the median value), shaking body (2.79× the median value), and yawning (2.78× the median value; Fig. 8, Table 3).
The average daily count per subject (total no. of actions/40 subjects/4 days) and relative frequencies of each communication and miscellaneous behavior are displayed by phase. Each figure in related color bar represents the average daily frequencies of respective action per subject in each phase(total no. of actions/40 subjects/4 days).Phase timing: A2 = 10:00–10:30, A3 = 10:30–11:00, A4 = 11:00–11:30, P2 = 14:30–15:00, P3 = 15:00–15:30, P4 = 15:30–16:00, P5 = 16:00–16:30.
Discussion
The systematic ethogram of M. fascicularis in a free enclosure precisely describes, defines and classifies the behaviors observed in the daily mundane routine of this species. The most important characteristic of this ethogram is the coding and transfer of raw video-based observations into digital data for further statistical analysis. By employing this methodology, the ethogram satisfies the technical requirements for future hypothesis-testing and quantitative studies [16], [17] by enabling NOLDUS software [26] to perform advanced statistical analysis on behavioral data. Another technical merit of this ethogram is that it can be updated in real-time through direct field observation and data importation into the software for later analysis.
In addition to these technical advantages, underlying psychological elements can be assessed through an analysis of the quantitative data on observable behaviors. For example, appetite can be measured by the frequency and duration of ingestion behavior; the social relationships between subjects can be analyzed by the frequency and duration of amicable, conflict and vigilance behaviors; sexual drive can be measured by the frequency and duration of rutting, estrous and mating behaviors; activity levels can be ascertained by the frequency and duration of rest and locomotive behaviors; and social interaction and affect can be studied through the frequency and duration of communication and miscellaneous behaviors.
In the current study, resting and vigilance behaviors were the most prominently occurring behavioral categories, with sitting on the floor and watching company dominating their respective categories; this finding did not vary significantly by observational phase. It can be reasonably surmised that this species dedicates substantial time to conserving energy through rest and promoting social ties/avoiding conflict through vigilance. As to ingestion behaviors, it should be noted that there were three (3) daily feedings at 7:30, 10:30 (phase A3) and 16:00 (phase P5). The more frequent drinking behavior, absence of chewing behavior, and significantly lower average daily count per subject value in phase P2 is likely attributable to this fixed feeding schedule. Moreover, during the 10:30 feeding, primarily fresh fruit was supplied; this dietary difference may explain the fact that the average daily count per subject value in phase A3 was less than half the corresponding value in phase P5. As to rutting, estrous, and mating behaviors, it appears that these behaviors peak in frequency in phases A3–A4 and P5; whether this phenomenon is correlated or just coincident with the feeding schedule remains an open question. As to parental and amicable behaviors, the average daily count per subject value peaks and grooming behaviors are more frequent in phase A3–A4; as a speculation, the late morning may mark a time period for social bonding in this species. As to conflict, vigilance and locomotive behaviors, the average daily count per subject value peaks in phases A3–A4 and P5. This finding may be correlated with the feeding schedule, as conflict, vigilance and locomotive behaviors may be heightened in order to protect feeding position and/or food from other monkeys. As to communication and miscellaneous behaviors, the average daily count per subject value peaks in phases P2–P3; this category is primarily concerned with self-directed behaviors such as self-scratching and shaking. The early afternoon hours may mark a time period for solitary self-caring activities in this species. There are several limitations to this study. First, while observation of M. fascicularis in the wild would have been preferable, issues of subject identification and repeat observation required the use of a free enclosure environment. Second, it should be noted that observations spanned daytime hours only (9:30–11:30 and 14:30–16:30); thus, nocturnal behaviors were not investigated nor recorded in this study. Third, parturition behavior was not observed nor recorded. Fourth, behaviors were classified according to specific ecological functions. As a result, the edges of some behavioral sets may overlap, which may lead to inaccuracies in behavioral classifications. Fifth, some less commonly occurring behaviors may have been overlooked through human error. Further behavioral studies on the species can address these limitations.
In conclusion, this systematic ethogram of the cynomolgus monkey (M. fascicularis) in a free enclosure provides a platform for future behavioral investigations and concomitant quantitative studies on this species. These studies, combined with others on non-human primates, should provide further insight into advanced cognitive function in humans.
Methods
Location
The M. fascicularis Feeding Base of Zhongke Experimental Animal Co., Ltd. (hereinafter “the company”) is located in Suzhou, P.R.C. at E 31°07′03″ to 31°07′06″, N 120°19′08″to 120°19′15″. The company imported the M. fascicularis subjects from Guangdong and Vietnam in 1990 and established a domestication and breeding base for these monkeys.
Observation
First, the initial observations of 6012 M. fascicularis subjects followed by a detailed verification were performed by the scanning method to construct the preliminary ethogram. Then, an independent validation by focal observation was performed on a randomized cohort of 40 young adult female M. fascicularis subjects (each weighing 3–6 kg and aged 8–16 years)who were selected by means of simple random sample, seed 20101207, from the original population (n = 6012). The subjects were housed in 25 free enclosures measuring 8 m×3 m×3 m (L×W×H), given water and libitum, and fed daily with fresh fruit, vegetables and compound high-nutrition monkey food. Two (2) male and 20 female subjects were placed into each free enclosure to match the wild male: female ratio range of 1∶7–11. There was no statistically significant difference in male: female ratios across all free enclosures (chi square test, person = 1.0). All free enclosures were consistently maintained on a 12 h light/dark cycle.
In recording observations, three (3) high-pixel videos of the subjects were recorded using a SONY 1100 megapixel camcorder. Then, a Lenovo PC was used to transfer and convert the videos into a viewable format for analysis through NOLDUS Observer XT software (version 10.0, Noldus Information Technology, Leesburg, PA) [26]. The list of behaviors was encoded to satisfy the operational requirements of the software [27]. Three (3) qualified observers blindly watched the videos and used the software to record data on the frequency and duration of each behavior. Inter-observer reliability between the three (3) observers was determined to be greater than 85% for each behavior.
A six (6)-month preliminary observation was performed from April-December 2010. More than 1000 hours of video footage was collected to obtain a comprehensive view of the subjects' behavior. A systematic ethogram was then constructed using behavioral observations collected from qualitative sampling ad libitum, focal animal sampling and instantaneous scans. Sampling was limited to daytime hours after feeders completed their daily cleaning procedure (9:30–11:30 and 14:30–16:30 daily).
Ethics Statement
All procedures described were observational under normal rearing circumstance and did not involve physical manipulation of the subjects or changes to their environment or diet. Animal care and housing procedures were in compliance with Chinese regulatory requirements (see addendum entitled “Ethics Statement on Non-human Primate Research”) and AAALAC statements.
In brief, complete animal husbandry and veterinary care was provided daily. Animals were fed a nutritious standardized diet, supplemented daily with fresh fruits and vegetables. Animals had unrestricted access to potable water. Animal enclosures were cleaned daily. Animals were observed daily by trained care-takers. Any observed abnormality, disease or injury was reported to the veterinary staff for diagnosis and treatment; this veterinary support was documented in both hardcopy and electronic formats.
In addition, this study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the Institute of Neuroscience of Chongqing Medical University (Approval No: 20100031). The protocol was approved prior to implementation by the Committee on the Ethics of Animal Experiments at the Chongqing Medical University and is in accordance with state regulations.
Definitions
Behavior is generally defined as a “combination of posture and action, with obvious environmental adaptation functions.” Each discreet behavior occurs at a location within the environment. Therefore, the behavior of M. fascicularis in a free enclosure environment can be segregated into three discreet elements: posture, action and location. [25] These elements are defined as follows:
- Posture: a particular bearing of the subject's body.
- Action: a coordinated series of contractions, extensions, rotations and/or translations of the subject's body part(s) occurring in a relatively short period of time.
- Location: a specific position within the free enclosure environment.
Ethogram Construction
Posture Coding.
Through observation, nine (9) postures were identified and encoded. These postures can be separated into two (2) groups: static postures (standing, sitting, lying, mounting, hanging) and dynamic postures (walking, galloping, jumping, climbing).These postures are defined are defined as follows:
- Standing: supporting the body erect on hind legs or all four limbs for at least 5 seconds
- Sitting: resting on the buttocks.
- Lying: resting recumbent on the floor or shelf.
- Mounting: rising upon the rear of another subject for copulation.
- Hanging: suspending on four limbs from the skylight.
- Walking: translating by steps on the floor.
- Galloping: translating swiftly such that all limbs leave the floor for an instant.
- Jumping: springing up from the floor by the muscular contraction of the limbs.
- Climbing: ascending by all limbs along the window or the door.
Action coding.
All actions are encoded and defined in the attached addendum entitled “File S1 and File S2”.
Location coding.
Seven (7) locations were identified and encoded: floor, skylight, iron chain, shelf, window, door, and ventilator.
Posture-Action-Location System.
From April to December 2010, 107 behavioral items were created based on the Posture-Action-Environment principle, and the scanning method was employed to verify these behaviors among 6012 M. fascicularis subjects in a free enclosure. 83 of these behaviors were then independently validated and classified into 12 behavioral categories through focal observation of a randomized cohort of 40 young-adult female M. fascicularis subjects (each weighing 3–6 kg and aged 8–16 years) selected from the original population (n = 6012). 53 of these behaviors were then selected belonging to 12 categories based on ecological function: ingestion, thermo-regulatory, rutting and estrous, mating, resting, parental, amicable, conflict, vigilance, locomotive, communication and miscellaneous behaviors. These behavioral categories are defined below:
- Ingestion behavior: taking food material into the subject's digestive system.
- Thermo-regulatory behavior: regulating body heat through movement.
- Rutting and estrous behavior: arousing sexual interest in another subject.
- Mating behavior: sexual intercourse between opposite-sex subjects.
- Resting behavior: refraining from activity.
- Parental behavior: providing supervision and care to the subject's offspring.
- Amicable behavior: providing friendly actions towards another subject, such as grooming.
- Conflict behavior: struggling between subjects resulting from incompatible or opposing demands.
- Vigilance behavior: responding to threatening external stimuli.
- Locomotive behavior: engaging in activity (as opposed to resting behavior).
- Communication behavior: transmitting information to other subjects via gestures, emitting sounds, etc.
- Miscellaneous behavior: a set of defined miscellaneous actions.
Supporting Information
File S2.
Behavioral Definitions and Ethogram Validation.
https://doi.org/10.1371/journal.pone.0037486.s002
(DOC)
Acknowledgments
We thank the Zhongke Experimental Animal Co. Ltd. for providing the facilities to conduct the field observation and Professor Zhigang Jiang for detailed discussions on the Posture-Action-Environment system.
Author Contributions
Conceived and designed the experiments: FX LX XL QL. Performed the experiments: FX LX XL QL TW YJ FK LF. Analyzed the data: FX QZ. Contributed reagents/materials/analysis tools: PX FX YJ FK. Wrote the paper: FX KC PX.
References
- 1. Cappenter S (2000) Behavioral science claims the decade. Monitor on Psychology 31: 22–24.
- 2. Almond R, Kupfer DJ (1969) Psychiatric inpatient research. Social system and planning issues. J Nerv Ment Dis 149: 398–407.
- 3. Allen C, Bekoff M (1995) Function natural design and animal behavior: philosophical and ethological considerations In: Thompson, N.S. (Ed),. Perspectives in Ethology 11: 1–46.
- 4.
Beauchamp TL, Childress JF (1994) Principles of Biomedical Ethics, 4th edn. Oxford Univ Press. pp. 12–45.
- 5. Broom DM (1991) Animal welfare: concepts and measurement. J Anim Sci 69: 4167–4175.
- 6. Dawkins MS (1990) From an animal's point of view: motivation, fitness and animal welfare. Behav Brain Sci 13: 54–61.
- 7. Duncan IJH (1993) Welfare is to do with what animals feel. J Agric Environ Ethics 6(Suppl 2): 8–14.
- 8.
Duncan IJH, Fraser D (1997) Understanding animal welfare. In: Appleby MC, Hughes BO, editors. Animal Welfare CAB International. pp. 19–31.
- 9. Huntingford FA (1984) Some ethical issues raised by studies of predation and aggression. Anim Behav 32: 210–215.
- 10.
Regan T (1983) The Case for Animal Rights. University of California Press. pp. 20–32.
- 11.
Rollin BE (1992) Animal Rights and Human Morality. pp. 21–40. Revised edition Prometheus Books.
- 12. Stafleu FR, Grommers FJ, Vorstenbosch J (1996) Animal welfare: evolution and erosion of a moral concept. Anim Welfare 5: 225–234.
- 13. Tannenbaum J (1991) Ethics and animal welfare: the inextricable connection. J Am Vet Med Assoc 198: 1360–1376.
- 14. Thorpe WH (1969) Welfare of domestic animals. Nature 224: 18–20.
- 15. Wood-Gush DGM (1973) Animal welfare in modern agriculture. Brit Vet J 129: 167–174.
- 16.
Martin PBP (1993) pp. 1–200. Measure Behavior, An introduction Guide 2nd Edition.
- 17.
Lehner PN (1996) pp. 1–60. Handbbok of Ethological Method 2nd Edition.
- 18. Skinner SW, Lockard JS (1979) An ethogram of the liontail macaque (Macaca Silenus) in captivity. Applied Animal Ethology 5: 241–253.
- 19. Adams MR, Kaplan JR, Koritnik DR, Weaver DS, Bond MG (1984) Erectile Failure in Cynomolgus Monkey with Atherosclerosis of the Arteries Supplying the Penis. Journal of Urology 131: 571–573.
- 20. Jolly A (1966) Lemur Social Behavior and Primate Intelligence-Step From Prosimian to Monkey Intelligence Probably Took Place in a Social Context. Science 153: 501–510.
- 21. William T, McKinney J, Suomi SJ, Harlow HF (1971) Vertical -Chamber Confinement of Juvenile-Age Rhesus Monkeys. Arch Gen Psychiatry 26: 1313–1320.
- 22. Zhang J, Zhao DP, Li BG (2010) Postconflict behavior among female Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in the Qinling Mountains China. Current Zoology 56: 222–226.
- 23. Yamada K (2010) Social intelligence in Old World monkeys: ecological and developmental view. Japanese Journal of Animal Psychology 59: 199–212.
- 24. Mears CE, Harlow HF (1975) PLAY - EARLY AND ETERNAL. Pro Natl Acad Sci U S A 72: 1878–1882.
- 25. Jiang ZG (2000) Behavior coding and ethogram of the Pere David's Deer. Acta Theriologica Sinica 20: 1–12.
- 26. Bakeman R, Quera V (2000) OTS: a program for converting Noldus Observer data files to SDIS files. Behav Res Methods Instrum Comput 32: 207–212.
- 27. Noldus LPJJ, Trienes RJH, Hendriksen AHM, Jansen H, Jansen RG (2000) The Observer Video-Pro: New software for the collection, management and presentation of time-structured data from video tapes and digital media files. Behavior Research Methods, Instruments & Computers 32: 197–206.