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Establishing Stress Behaviors in Response to Manual Restraint in Cockatiels (Nymphicus hollandicus).

Abstract: Avian patients are presented commonly to veterinarians for preventive and disease-induced care. Physical examinations commonly are used to assess the overall patient, but this requires manual restraint, which often leads to increased stress and subsequent deleterious effects. To develop a noninvasive evaluation of the stress response in cockatiels (Nymphicus hollandicus), we evaluated the behavior of 26 juvenile cockatiels during their normal daily routine and after an acute stressful event (manual restraint and physical examination). Nonstressed behavior budgets were established by performing quantitative ethograms using 10-minute focal animal sampling methods with point samples recorded every 5 seconds. The ethograms then were repeated after a > 10-minute restraint period for physical examination and venipuncture. Plasma corticosterone levels at baseline (<3 minutes) and after stress (>10 minutes) were compared to accompanying behaviors. Plasma corticosterone levels significantly increased after restraint. Overall, reactionary behaviors and inactivity increased, while locomotion, feeding, interaction with the environment, and displays of aggression decreased in the stressed birds. Maintenance behaviors were not significantly different before and after restraint, but the subjective character changed, with stressed birds displaying an increase in behaviors that were short in duration with minimal decrease in vigilance. Our results will be helpful to develop a method of quantifying stress in companion avian patients by using behavioral indicators. However, further study into specific behaviors of significance is needed.

Key words: corticosterone, stress, behavior, ethogram, avian, psittacine, cockatiel, Nymphicus hollandicus


Evaluation of stress in avian patients has long been recognized as an important part of patient care for clinical practitioners. (1,2) The ability to assess a patient's stress level and adapt accordingly is beneficial in clinical practice as it helps to improve safety for the patient. While a physical examination ultimately is necessary, initial observation of basic parameters, such as stance within the carrier and respiratory rate, can give insight into stress levels. (1,2) Because no standardized criteria for stress evaluation are readily available in a clinical setting, a practitioner may unwittingly cause additional stress in an already compromised bird and cause unintended harm or even death. Therefore, identifying and quantifying stress by using behavioral criteria will allow practitioners or clinical staff to allow the patient time to recover before handling or provide the patient with frequent breaks during a physical examination to minimize the stress response as much as possible.

Corticosterone and glucose levels, heart rate, and skin temperature via infrared thermography all have been used to quantify stress. (3-9) However, these methods often are invasive in birds, requiring capture

and restraint, and resulting in a stress response in the process of obtaining the necessary samples. While glucose levels and heart rate are readily available in the clinical setting, increases in either of these criteria may not always reflect a stress-induced state, as both are regulated and affected by multiple other systems. (3-5) Infrared thermography is a newer method that has not been studied or established in many avian species, and it requires visible bare skin, limiting evaluation to the areas of the head, eyes, and feet. Further investigation to determine its use in evaluating stress responses in avian species is warranted but not practical at this time. (6-9)

The most well-established and commonly used method of stress evaluation is to measure corticosterone levels. (10,11) Corticosterone concentrations can be measured in plasma, feathers, or feces. Plasma corticosterone levels can be used to evaluate baseline stress levels and the acute stress response, but measurement bears the disadvantage of inducing stress because of the necessary capture, restraint, and venipuncture. (11) Methods to measure fecal and feather corticosterone concentrations were developed to be noninvasive, but these only provide evaluation of chronic stress. (12,13) Furthermore, these methods do not give clinicians instantaneous assessment of stress because samples must be assayed by a diagnostic laboratory. (10)

Behavioral indicators of stress have been established and used to develop behavioral stress scoring systems for many species, including dogs, (14,15) cats, (15,17) and horses. (18) These systems have been used in clinical veterinary practice and are used as one basis for the Low Stress Handling Certification. (14,18) These behaviors often are categorized as fight, flight, freeze, and fidget. (15) While many avian practitioners have developed an understanding of avian behavior and response to stress, there is a paucity of information defining such behavioral indicators of stress in companion avian species in a clinical setting, and available information often is limited to anecdotal reports. (1,2,19) The development of a scoring system for avian patients would allow veterinary staff to improve current care and handling techniques. Welfare of food-production avian species as well as wildlife species focuses on the impact of human presence, responses to novel objects, or environmental changes. Behavioral responses, such as decreases in movement as well as increases in avoidance, vigilance, aggressive displays, submissive behaviors, and feather ruffling are commonly observed. (20,23) Captive European starlings (Sturnus vulgaris) demonstrated a decrease in preening and nearly significant increase in aggressive displays after diverse acute stressors, including an auditory stressor and antagonistic human disturbance. (3) Based on this result and the concept that stress results in behavioral changes aimed at increasing an individual's chance of survival, (20) we hypothesized that the stress created by capture, restraint, and physical examination would result in increased plasma corticosterone levels in cockatiels (Nymphicus hollandicus) and a measurable change in behaviors. Specifically, an increase in resting, aggressive, and reactionary behaviors categorized as stress behaviors and a decrease in locomotion, feeding, environmental interaction, and maintenance behaviors categorized as luxury behaviors would occur in response to stress (Table 1).

Materials and Methods


Twenty-six juvenile (5-7 months old; 15 males, 9 females, 2 unknown sex) cockatiels were observed. All cockatiels were of the following color morphs: grey (n = 15), split to pied (n = 9), or light pied (n = 2). An intake physical examination was performed, and individualized colored zip-tie leg bands were placed on each bird for identification purposes. The cockatiels were relatively naive to handling at time of intake and were sedated before use to teach handling techniques to a class of veterinary students before the study protocol. The birds were given a 1-month period free of any handling before starting the study protocol.

The birds were divided randomly into 4 groups, with 2 groups of 6 and 2 groups of 7 birds, and housed by group in separate 3 x 5 x 6-foot metal wire aviaries with natural branch perches. Birds were maintained on a 12-hour day-night photoperiod, with the lights on at 8:00 am and off at 8:00 PM. The room temperature was maintained between 23.9[degrees]C and 26.7[degrees]C (75[degrees]-80[degrees]F) and the humidity at 20% to 50%. The diet consisted of a seed mixture (Kaytee Forti-Diet Pro Health Cockatiel Food with Safflower; Kaytee Products, Inc, Chilton, WI, USA), as well as an extruded formulated diet (Zupreem Naturals Budgerigar, Premium Nutritional Products, Inc, Shawnee, KS, USA), fed out of plastic bowls. At time of intake, the diet consisted of a seed mix, and before starting the study protocol, a gradual transition to an extruded formulated diet was begun. Dietary transition was halted when clinical signs of illness were observed in the flock. The transition was restarted at the end of the protocol. Enrichment was provided in the form of destructible toys made from popsicle sticks, straws, and twine. The aviary floors, and food and water dishes were cleaned daily in the mornings at 8:00 AM. The birds were allowed a month to acclimate to the wire aviaries before any handling or video recording occurred to minimize or eliminate the stress of a new environment as a confounding factor on the minimal stress observations and plasma corticosterone levels.

Group fecal Gram's stains and wet mounts were performed randomly based on availability of fresh samples at the daily wellness checks. Results of fecal Gram's stains revealed Macrorhabdus ornithogaster presence in all groups. Cockatiels that displayed any signs of clinical illness, including but not limited to melena, vomiting, regurgitation, cachexia, undigested material in the droppings, or that died during the protocol period were excluded from the study. A total of 2 birds (1 from each group of 7 birds) were excluded from the study because of clinical signs of Macrorhabdus species, including cachexia in both birds and death of 1 bird.

For each corticosterone sample, a total of 0.5 to 1 mL of whole blood was collected by venipuncture of the right jugular vein with a 26-gauge, 0.5-inch needle and 3-mL Luer lock syringe. Baseline samples were obtained within 3 minutes of entering the animal room before the daily cleaning and feeding routine. This was accomplished by having one handler capture the birds from a single aviary, then immediately hand them off to other handlers for venipuncture, while the first handler captured more birds. Samples were collected from all birds in a single aviary per day, with a minimum of 2 days between blood collections to allow the corticosterone levels of birds to return to baseline before the next sample collection. (24) Any baseline samples obtained after 3 minutes were not used in this study, as corticosterone levels can increase in plasma samples as early as 3 minutes after the induction of stress. (25,26) On a separate day, samples were collected after 10 minutes of handling to assure adequate time for a stress response. Whole blood samples were placed in a 2-mL glass heparin tube and centrifuged at 3300 rpm for 10 minutes, then plasma was separated, placed in plastic sample tubes, and frozen at -20[degrees]C (-4[degrees]F) until shipment. Samples were shipped overnight on dry-ice to the Texas A&M Veterinary Medical Diagnostic Laboratory (College Station, TX, USA). All study activities were approved by the University of Illinois Institutional Animal Care and Use Committee (IACUC 16169).

Video recording equipment

Video recordings were made using GoPro Hero4 Session Video Cameras (GoPro Inc, San Mateo, CA, USA). The resolution was set at 1080 pixels (1920 X 1080) with frame rate set to 30 frames per second and a wide viewing angle. After the acclimation period and before the baseline corticosterone sample collection, the cameras were placed on top of the enclosures for 3 days to allow the birds to become accustomed to the presence of the devices. The cameras then were mounted in the upper front left corner of the aviaries for 24 hours before recording. The devices recorded to Sandisk Extreme 16 gigabyte microSD cards (Western Digital Technologies Inc, Milpitas, CA, USA). The videos were viewed using a VLC media player (Version 2.2.6, VideoLAN, Paris, France) to allow the observer to zoom in and out on the focus animal.

Plasma corticosterone analysis

Plasma corticosterone analysis was performed by radioimmunoassay at the Texas A&M Veterinary Medical Diagnostic Laboratory Endocrinology Section. The assay is specific for corticosterone, 07120102 MP BioMedicals Corticosterone Double Antibody RIA Kit (MP BioMedicals, LLC, Santa Ana, CA, USA). Samples were performed in duplicate with coefficient of variation (CV) <7.0 repeated for verification. The interassay CV was 6.25 to 8.38, with the intra average for the samples being 3.28. An initial set of four samples was collected for validation of the corticosterone assay in cockatiels before the start of the experiment.


Quantitative ethograms were performed using interval focal animal sampling (27) during a 10minute video segment of the cockatiels in the aviaries. Interval sampling was chosen, as it has been shown to be more efficient with more data collected per set timeframe than continuous sampling. (27) A total of 34 behaviors were recorded. The behaviors assessed were determined by observing the videos of the cockatiels in the aviaries, using the ad libitum sampling method (28) and defined using previously established definitions. (29,31) All behaviors were classified into a behavioral category (Table 1). The ethograms were developed based on previously established ethograms for cockatiels and other psittacine species. (29,31) Behaviors were measured every 5 seconds for 10 minutes, and a single behavior was counted once at each time point of 5 seconds. The total numbers of each behavior during the 10minute observation time frame were recorded.

Establishing normal behaviors

Video of each group of birds was recorded for a 2-hour duration between 9:00 AM and 11:00 AM on a single day. Video recording was started by a person entering the room, then time was given before observations to allow birds to calm after the person left the room. During the recording period, no personnel entered the room to eliminate any potential stress effect due to human presence. Baseline corticosterone samples were obtained at 9:00 am on a separate day to the ethogram, within 3 minutes of entering the aviary room, to minimize the effects of daily photoperiod variation on the corticosterone levels. (32,33)

Establishing stress behaviors

The same camera setup was repeated as described previously. To decrease the effects of daily variances in corticosterone levels, stressed recordings were performed between 9:00 am and 12:00 PM. (32,33) Stress was induced by restraint and handling of the birds for physical examination and venipuncture. Each bird was restrained and handled for 10 to 13 minutes before venipuncture. (34) The birds then were released back into the aviaries and video recorded for a minimum of 10 minutes after release of the last bird in each aviary.

Statistical analysis

Descriptive statistics and frequencies were tabulated for continuous variables (plasma Cortisol concentrations) and categorical variables (behaviors). Normality was assessed by the Shapiro-Wilks test. Differences in plasma Cortisol levels before and after handling by sex and cage number were tested by the repeated measures analysis of variance (ANOVA). A Wilcoxon signed rank test for related samples was used to test the difference in the number of instances an individual exhibited each behavior in the categories (locomotion, resting, aggression, reactionary, maintenance, feeding, environmental interaction) before and after handling. The behavior categories then were regrouped as either luxury (locomotion, feeding, maintenance, environmental interaction) or stress (resting, aggression, reactionary), and the analysis was repeated. All statistical analyses were performed using commercial software (SPSS version 24, IBM Statistics, Chicago, IL, USA).


Corticosterone levels increased significantly after handling (P < .001; Table 2; Fig 1). There was no effect of sex (P = .69) or cage number (P = . 11) on the change in corticosterone levels. Overall, instances of luxury behaviors decreased significantly (P < .001), and instances of stress behaviors increased significantly (P < .001). Specifically, exhibitions of locomotion (P < .001), aggression (P = .001), feeding (P = .002), and environmental interaction (P < .001) decreased significantly, while exhibitions of reactionary (P < .001) and resting (P = .007) behaviors increased significantly. There was no difference in exhibition of maintenance behavior (P = .98) before and after handling.


Based on the significant increase in plasma corticosterone levels and disruption of normal behaviors, the protocol of capture and restraint for physical examination used in this study elicited a stress response. Significant behavioral changes were associated with this stress response including increased reactionary and resting behaviors as well as decreased locomotion, feeding, interaction with environment, and aggression when stressed. These results were consistent with our overall hypothesis that when the cockatiels are stressed, time spent in behaviors not necessary to maintain homeostasis and life will decrease, while time spent in behaviors that might increase chances survival will increase. Interestingly, aggressive behaviors that we expected to increase in frequency actually decreased, and maintenance behaviors that were expected to decrease were not significantly affected.

European starlings and trumpeter swans (Cygmis buccinator) have demonstrated a significant or near significant increase in aggressive behaviors in response to stressful stimuli, while the cockatiels in this study displayed decreased aggressive behavior. (4,23) The cause for the decrease rather than increase in aggressive behavior is not clear, because of the complex nature of aggression and the various possible motivations for aggressive behavior, including fear, conditioning, territorial, or resource-related motivators. (19,33) The interval sampling method used in this study did not allow for assessment of such motivators; rather, a continuous study design would be necessary to allow assessment of the initial stimulus called antecedent, resulting behavior, and end effect on the individual, called consequence. Additionally, this study only looked at 1 type of stress stimulus, restraint and physical examination, while additional types of stressful stimuli were not evaluated and could be motivation for aggression. Aggressive behavior only occurred on average once per baseline ethogram, so this decrease, while statistically significant, may not be of clinical significance. Further study to develop a better understanding of the relationship between stress and aggressive behavior in cockatiels would allow practitioners to better adapt to decrease the stress level of individual birds in the clinical setting.

While the frequency of demonstrated maintenance behaviors did not change significantly in the stress observations, a change in the quality of maintenance behaviors displayed was observed. Certain maintenance behaviors, such as burst preening and plumage shaking, occurred more frequently during the stressed observations. Such behaviors were of short duration with minimally decreased vigilance, which was defined as a state of increased awareness of an individuals' surrounding with decrease in stimulus threshold required to illicit a response. While some of these behaviors also were seen during the baseline observations, they occurred less frequently and were noted to follow altercations with other birds. These altercations often occurred over access to a resource, such food or perching location, and might represent a mild social stimulus. Birds with lower plasma corticosterone levels devoted more time to grooming, such as actively preening with attention paid to feather maintenance and scratching their heads. We recorded a total of 34 behaviors in the 7 behavior categories, but did not have the statistical power to differentiate specific behaviors. Specific behaviors are necessary to develop a behavioral stress scoring system for this species, and studies that evaluate specific behaviors will enhance captive care and handling aimed at improving animal health.

Previous studies have revealed no significant difference between sexes in baseline or stress-induced corticosterone levels in mature and juvenile captive birds of other species. (4) Similarly, no significant difference between sexes in baseline or stress-induced corticosterone levels were found in our study. This would be expected because the lack of sex hormone production in juvenile animals would result in decreases in significant sex differences in behavior related to sex hormone differentiation. Previous studies in cockatiels have demonstrated that mature male cockatiels demonstrate more aggressive behaviors than females in nonstressed environments. (31)

While there was confirmed shedding of M ornithogaster in the flock, positive birds were not excluded from the study unless they exhibited clinical signs of infection. Because of the common prevalence of M. ornithogaster found in some cockatiel flocks, (35,36) birds with subclinical infection were included in the study. (37) Chronic stressors, such as illness or infection, can decrease baseline corticosterone levels and the acute stress response, (26) but have not been evaluated in association with Macrorhabdus detection in cockatiels. Based on the fact that corticosterone level increases with stress were highly significant in this study, it is unlikely, that the presence of Macrorhabdus in the flock had a significant effect on the data obtained.

Our results showed that certain behaviors are significantly more frequent in cockatiels with high than in those with low corticosterone levels. The stress-induced behavior changes could be beneficial in developing an avian behavioral stress-scoring system. Such scoring systems are useful for clinical practitioners and veterinary staff working with dogs and cats, (14-17) and they are part of the basis of low-stress handling techniques. (15) Low-stress handling is even more critical when working with birds. While there are many challenges to the development of such a system, including the differences in natural behaviors of avian species, differences in the learned history of individual birds, and the subtler differences in quality of some behaviors, a scoring system could have clinical application. Further investigation into the variation of stress behaviors between avian species as well as response to more diverse or repetitive stressors is necessary for such a scoring system to be successful.

Katherine K. Turpen, DVM, Kenneth R. Welle, DVM, Dipl ABVP (Avian), Jennifer L. Trail, CVT, Seema D. Patel, BS, and Matthew C. Allender, DVM, MS, PhD, Dipl ACZM

From the Department of Veterinary Clinical Medicine (Turpen. Welle, Trail, Patel, Allender). University of Illinois College of Veterinary Medicine. 1008 W Hazelwood Dr. Urbana, IL 61802, USA.; and Wildlife Epidemiology Lab (Allender), University of Illinois College of Veterinary Medicine, 2001 S Lincoln Ave, Urbana. IL 61802, USA.


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Caption: Figure 1. Change in plasma corticosterone concentrations ([micro]g/mL) or number of instances of exhibiting a behavior in the 10 minutes before (pre) and after (post) handling of cockatiels (N=24) evaluated for response to stress.
Table 1. Behaviors recorded during observation of cockatiels
evaluated for stress behavior before and after restraint
and physical examination.

Behavioral       Behavior description              Behavior

Resting        Standing still on perch                --

               Standing still on aviary               --

               Standing still on                      --
               aviary floor

               Resting with head tucked               --
               under wing or on the
               back, or eyes closed

Aggression     Turn threat                 The aggressing aggressor
                                           bird quickly and
                                           abruptly directed
                                           anterior toward
                                           opponent, posture was
                                           erect, and head and neck
                                           were extended

               Bill gape                   Aggressor opened the
                                           beak with head directed
                                           toward opponent, but no
                                           contact was made

               Peck at                     Aggressor opened and
                                           closed beak while making
                                           pecking motion at
                                           opponent, head or whole
                                           body moved toward
                                           opponent but without
                                           actual contact

               Bill spar                   Aggressor engaged in
                                           short bouts in which
                                           beak made contact with
                                           beak of opponent bird

               Peck                        Aggressor's beak rapidly
                                           closed on some part of
                                           recipient's body

               Wing extension              Perched aggressor had
                                           wings extended in
                                           vertical plane with head
                                           extended and body
                                           directed at opponent

               Wing flapping               Perched aggressor moved
                                           extended wings rapidly
                                           in vertical plane with
                                           head extended and body
                                           directed at opponent

               Sidle approach              Perched aggressor
                                           rapidly approached
                                           opponent with head
                                           extended and side of
                                           the body directed
                                           toward opponent

               Slow advance                Perched aggressor walked
                                           toward opponent, facing
                                           it, with head up

               Flight approach             Aggressor flew directly
                                           toward opponent

Reactionary    Avoidance                   Movement away from an
                                           individual or object

               Crouch                      Posture crouched low on
                                           perch, with plumage
                                           ruffled and head
                                           retracted, and focus
                                           directed at an
                                           individual or object

Locomotion     Moving laterally on         Use of beak and feet to
               perch                       move along a branch or

               Moving on aviary screen     Use of beak and feet to
                                           move across the aviary

               Moving on aviary floor      Use of feet to move
                                           across the floor of
                                           the aviary

               Flying or                   Use of wings to move
               preflight posturing         around the aviary

Maintenance    Preening                    Focused grooming or
                                           feather maintenance

               Burst preen                 Short duration grooming
                                           or feather maintenance
                                           with rapid return of
                                           focus to surroundings

               Allopreening                Behaviors involving
                                           contact between one
                                           individual's beak and
                                           any part of another
                                           individual, accompanied
                                           by grooming

               Shaking plumage             Rustling or shaking of
                                           feathers to settle them
                                           back into place

               Scratching                             --

               Stretching                             --

               Beak wiping                 Action of wiping the
                                           beak across a perch or
                                           other inanimate object

               Defecation                             --

               Yawning                                --

Feeding        Eating                                 --

               Drinking                               --

Interaction    Interacting with or                    --
with           inspecting toys,
environment    branches, or camera

               Biting aviary screen or                --

               Attempted foraging          Movement associated with
                                           feeding or foraging
                                           without actually feeding

Off screen/               --                          --
from view

Table 2. Plasma corticosterone concentrations ([micro]g/mL)
and behaviors (number [n]/10 minutes) exhibited before
(pre) and after (post) handling in cockatiels (N = 24)
evaluated for stress. Behaviors were measured every 5
seconds for 10 minutes and a single behavior was
counted once at each time point. Corticosterone levels
are reported as mean, 95% confidence interval, and
minimum and maximum values, while behaviors are
reported as median, interquartile range, and minimum
and maximum number of times/10 minutes.

Variable                   Pre         Post       P value

Corticosterone,            8.1         150.5       <.001
[micro]g/mL              5.5-10.7   100.4-200.6
                         0.8-18.7    8.8-145.5

Luxury, n/10 minutes        63           8         <.001
                          50-75        4-11

Stress, n/10 minutes        15          96         <.001
                           9-33       89-103

Locomotion, n/10            18           6         <.001
minutes,                   8-25         4-7
                          16-Jul       0-16

Maintenance, n/10           1            4          .98
minutes                    0-3          2-7
                           0-51        2-23

Feeding, n/10 minutes       0           NA         .002
                           0-13         --
                           0-66         --

Environmental               3           NA         <.001
interaction,               0-17         --
n/10 minutes               0-37         --

Resting, n/10 minutes       13          27         .007
                          10-25        20-38
                           0-70       16-109

Aggression, n/10            1            0         .001
minutes                    0-2          0-0
                           0-10         0-2         --

Reactionary, n/10           0           45         <.001
minutes                    0-0         34-58
                           0-43        0-86

Abbrev: NA, not applicable.
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Author:Turpen, Katherine K.; Welle, Kenneth R.; Trail, Jennifer L.; Patel, Seema D.; Allender, Matthew C.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2019
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