Feather plucking in captive Aratinga auricapillus: influence of sex, stress, and temperament

doi:10.21203/rs.3.rs-5032694/v1

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Feather plucking in captive Aratinga auricapillus: influence of sex, stress, and temperament

https://doi.org/10.21203/rs.3.rs-5032694/v1

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Brazil is recognized for its biological megadiversity, particularly noted for the variety of psittacines (Order Psittaciformes). Among them is Aratinga auricapillus, a species in decline in the wild and involved in illegal trafficking, frequently found in Centros de Triagem de Animais Silvestres (CETAS) [trans. Wildlife Screening Centers]. Feather plucking is a psychogenic behavior directly related to stress that affects captive birds. This study aimed to evaluate the influence of sex, stress level, and temperament on psychogenic feather plucking in A. auricapillus captive in Bahia, Brazil. Two groups were formed: the Control Group, consisting of five healthy individuals, and the Test Group, with five individuals exhibiting feather plucking. Analyses included clinical evaluation, plumage analysis, molecular sexing, pathogen investigation, leukogram, and an open field test. The heterophil:lymphocyte ratio was used to determine the stress level. Temperament was assessed through the open field test, classifying the animals as either shy or bold. Data analysis indicated a statistically significant association (p = 0.04) of sex with feather plucking, with females being more affected. These findings are valuable for deepening the understanding of the factors influencing feather plucking in A. auricapillus. Understanding this behavior is essential for developing management and conservation strategies for these birds in captivity.

Captive birds

self-mutilation

animal behavior

leukogram

Psittaciformes

molecular sexing

The Psittacidae species are distributed throughout the tropical zones of the planet, with Brazil hosting the second largest diversity of species within this family. Among them is Aratinga auricapillus (red-fronted parakeet), currently in decline in the wild (IUCN 2024). A. auricapillus is among the psittacine species introduced into illegal trafficking within Brazilian territory, contributing to the increase in the number of psittacines rescued in seizures. Data from Santos et al. (2021) showed that the Psittaciformes order is the second most frequently admitted into the Centros de Triagem de Animais Silvestres (CETAS) [trans. Wildlife Screening Centers] of Bahia, institutions that predominantly receive animals seized from wildlife trafficking (Santos et al. 2021).

Trafficked animals tend to exhibit high levels of stress due to poor transportation and handling conditions, as well as the conditions of captivity itself. Highly stressed animals may show behavioral changes such as stereotypy, aggression, and self-destructive behaviors (Seibert 2006). One example is psychogenic feather plucking, a pathology characterized by self-destructive aggressive behavior directly linked to stress (Van Zeeland et al. 2009).

The CETAS and Zoological Parks, although having different objectives, house wild animals and have the responsibility to provide them with the highest possible welfare. Given that captive animals are subjected to more intense stress compared to their wild counterparts (Telles et al. 2015), it is important for these entities to adopt strategies to better manage the animals in their facilities, reducing stress by minimizing physical, behavioral, and psychological suffering (Molento 2007). To better understand this pathology and develop strategies to address the issue, the aim of this study was to evaluate the influence of sex, stress level, and temperament on psychogenic feather plucking in A. auricapillus captive in Bahia, Brazil.

Animal sampling and clinical evaluation

The study included ten adult golden-capped parakeets (A. auricapillus), nine from the CETAS of Vitória da Conquista, Bahia, Brazil, and one from the Municipal Park Zoo of Matinha, located in Itapetinga, Bahia, Brazil. This research is associated with the project “Health and Behavioral Assessment of Wild Birds – Contributions to Reintroduction,” approved by the Animal Ethics Committee of the Multidisciplinary Institute of Health at the Federal University of Bahia, protocol number 093/2021.

All golden-capped parakeet included in the study underwent a thorough clinical examination, focusing on (i) the identification of possible pathologies in the skin or feathers that were not psychogenic in nature and (ii) the presence of ectoparasites, which could potentially be mistaken for feather plucking. After a visual inspection of the integumentary system, feathers from the pectoral region were collected, immediately stored in sealed plastic bags, and subsequently analyzed using a DI 224 Digilab® stereoscopic microscope to identify the presence of ectoparasites and assess feather integrity (Telles et al. 2015).

The ten birds were divided into two groups based on the presence or absence of feather plucking. The first group - Control Group - consisted of five healthy animals with no feather abnormalities, while the second group - Test Group - consisted of five animals exhibiting psychogenic feather plucking. Both groups underwent the same experiments to compare the influence of the same factors on psychogenic feather plucking.

Feather evaluation

The feather evaluation of all golden-capped parakeet was conducted to record the body areas with the highest incidence of feather plucking. Photographic records were made following the physical restraint of the birds for analysis. The evaluations were performed subjectively, following the ten-point scoring system proposed by Meehan et al. (2003) and adapted by Telles et al. (2015). This system is based on the assessment of feathers, plumes, and skin lesions observed in five different body parts: chest/flank, back, legs, wings, and tail. Each area is scored from 0 (maximum degree of feather loss) to 2 (minimum degree of feather loss), and the sum of these sub-scores forms the final score ranging from 0 to 10, where 0 represents maximum feather damage and 10 represents intact plumage.

Biological sample collection and molecular analyses

Blood samples were collected by clipping the toenails using specialized clippers as described by Silva et al. (2021) and Fraga et al. (2023). The collected blood was used for DNA extraction and blood smear preparation. The portion intended for accessing genetic material was utilized for molecular sexing, following the DNA extraction (Smith and Burgoyne 2004) and PCR protocols (Vucicevic et al. 2012) adapted by Antonio et al. (2021a), using primers 2550F (5’-GTTACTGATTCGTCTACGAGA-3’) and 2718R (5’-ATTGAAATGATCCAGTGCTTG-3’) (Fridolfsson and Ellegren 1999).

For the health evaluation, sterile swabs from Goodwood Medical Care® (Dalian, LN, China) were used to collect cloacal material, which was stored in autoclaved Falcon tubes containing 2 ml of injection-grade water. Two pathogens were investigated: Chlamydia psittaci and Circovirus sp. For the detection of C. psittaci, the protocol optimized by Mirabal-Santos et al. (2023) was followed using primers CPF (5’-GCAAGACACTCCTCAAAGCC-3’) and CPR (5’-CCTTCCCACATAGTGCCATC-3’) designed by Hewinson et al. (1997). Infection with Circovirus was assessed using the primer pair P2 (5'-AACCCTACAGACGGCGAG-3') and P4 (5'-GTCACAGTCCTCCTTGTACC-3') developed by Ypelaar et al. (1999), with the PCR conditions used by Bert et al. (2005).

Leukogram and stress level determination

From the blood smears stained with rapid panotic stain, hematological evaluations were conducted involving: (i) total leukocyte count (using the indirect method), (ii) differential leukocyte count, and (iii) total platelet count. The stress level was determined based on the heterophil:lymphocyte (H:L) ratio. All calculations related to the counts and stress level used formulas standardized by Campbell (2015). The reference values for leukocyte evaluation are from the studies of Silva (2010), Vaz et al. (2015) and Mello et al. (2016).

Temperament Determination

To determine the temperament of each animal, the "open field test" was conducted, characterizing temperament based on behavioral analysis in response to a new environment. Each of the ten birds was tested individually only once, as repeating the test could lead to habituation and consequently a change in temperament (Perals et al. 2017; Silva et al. 2021).

The temperament test took place from 10 a.m. to 3 p.m. over two consecutive days and involved the following steps: (i) removing the bird from the aviary with a capture net; (ii) placing it in a cage covered with a cloth to prevent prior visual exposure to the new environment; (iii) transporting the cage to a closed room unfamiliar to the bird; (iv) placing the cage on a table; (v) waiting five minutes for habituation; (vi) removing the cloth and opening the cage (at this point, the researcher left the room). The bird's reactions to the new environment were filmed for 10 minutes. Subsequently, the videos were analyzed by a single observer to characterize the temperament. The criterion used to determine temperament was whether or not the bird exited the cage, classifying each animal as bold or shy, respectively (Silva et al. 2021).

To enhance the accuracy of the temperament classification method, the parameter used to define temperament (cage exit) was supplemented with: (i) duration of freezing (the time from the moment the cage was opened until the first movement of any body part) and (ii) latency to the first step (the period from the opening of the cage until the first step taken).

Statistical analysis

Statistical analysis was conducted using both exploratory and inferential methods. The Shapiro-Wilk test was employed to assess which numerical variables followed a normal distribution. To compare temperament and stress level, as well as feather plucking and stress level, the Welch’s t-test was used. For associations between non-parametric data, the Mann-Whitney test was applied. Fisher’s exact test was used for other association tests. Statistical significance was considered for p-values ≤ 0.05, and all analyses were performed using R software, version 4.1.0 (R Core Team 2022).

Clinical evaluation

The clinical evaluation of the animals confirmed psychogenic feather plucking in members of the Test Group. Some of these individuals also presented skin lesions. In the feather analysis, no ectoparasites were found; however, a difference in feather integrity was observed between the Test Group and the Control Group. In the Test Group, wear was noted on the vexillum (the upper part of the contour feathers – Lovette and Fitzpatrick 2016), whereas in the Control Group, the vexillum was intact. This indicates that the animals not only engage in feather plucking but also cause wear on the feathers that remain on the body (Fig. 1).

Feather evaluation

The feather evaluation, based on the scoring system, allowed for the assessment of areas with feather plucking, including injured areas formed by plucking (Fig. 2). The mean and standard deviation of the scores for the Test Group were: chest 1.25 ± 0.43; back 0.95 ± 0.41; legs 1 ± 0.35; wings 1.8 ± 0.27; and tail 1.2 ± 0.44. The back and legs were the most affected areas, while the wings were the least affected. The Control Group scored 2 in all body parts.

Molecular analyses

None of the birds tested positive for the pathogens investigated (Chlamydia psittaci and Circovirus). The sex determination revealed that out of the 10 animals, 6 (60%) were males and 4 (40%) were females (Fig. 3).

Regarding the composition of the groups, 100% (n = 4) of the females belong to the Test Group, while 16.7% (n = 1) of the males are in this group, and 83.3% (n = 5) are in the Control Group (Fig. 4). Fisher's exact test resulted in p = 0.04, indicating a significant association between sex and feather plucking.

Leukogram and stress level

It was not possible to analyze the blood smear of one animal because the slide preparation was unsatisfactory, potentially compromising the results. Most of the counts showed a slightly higher average for the Test Group, except for the averages of lymphocytes and thrombocytes (Table 1).

Table 1

Leukocyte values for the Test Group (with feather plucking) and Control Group (without feather plucking) in *Aratinga auricapillus*.
Leukocyte parameter	Test Group (mean ± standard deviation)	Control Group (mean ± standard deviation)
Total Leukocytes	15.16 ± 1.84 (x10³/µL)	13.95 ± 0.95 (x10³/µL)
Monocytes	0.98 ± 0.20 (x10³/µL)	0.94 ± 0.33 (x10³/µL)
Heterophils	8.83 ± 0.89 (x10³/µL)	7.70 ± 0.66 (x10³/µL)
Lymphocytes	4.44 ± 0.72 (x10³/µL)	4.69 ± 0.90 (x10³/µL)
Eosinophils	0.89 ± 0.34 (x10³/µL)	0.59 ± 0.19 (x10³/µL)
Basophils	0.00 ± 0.00 (x10³/µL)	0.00 ± 0.00 (x10³/µL)
Heterophil:lymphocyte ratio (H:L)	1.99 ± 0.20	1.69 ± 0.48
Thrombocyte	15.12 ± 1.06 (x10³/µL)	15.40 ± 1.27 (x10³/µL)

Given the normality of the data, Welch's t-test was used to examine the association between the stress level (H:L) and feather plucking. The analysis yielded a p-value of 0.691, indicating no significant association. However, the observation of the medians suggests that, despite the lack of significant variation in the statistical analysis, the stress level in the Test Group was higher than that in the Control Group (Fig. 5).

Temperament analysis

The "open field" test revealed that 6 (60%) animals were shy, and 4 (40%) were bold. The shy animals exhibited a longer latency time for the first step and more freezing behavior compared to the bold ones (Table 2). Given the abnormality of the data, the Mann-Whitney test was applied to examine the correlation between temperament and (i) freezing behavior and (ii) latency to the first step. Correlating temperament with freezing behavior yielded a p-value of 0.02, indicating a positive association. Correlating temperament with latency to the first step yielded a p-value of 0.01, also indicating a positive association.

Table 2

Time (in seconds) of the variables analyzed in the "open field" test between groups with Shy or Bold temperament in *Aratinga auricapillus*.
Variable	Shy	Bold
Duration of freezing	12.6 (s)	0.5 (s)
Latency to the 1st step	316.16 (s)	1.75 (s)

By correlating the temperament data between the Test and Control Groups using Fisher's exact test, a p-value of 1 was obtained. In the Test Group, 60% were shy and 40% were bold, and the same pattern was observed in the Control Group. Therefore, no positive correlation between feather plucking and temperament was found.

When associating sex and temperament of the individuals, it was observed that 77% (n = 3) of the females were shy and 33% (n = 1) were bold. Among the males, 50% (n = 3) were shy and 50% (n = 3) were bold. Fisher's exact test yielded a p-value of 0.5, indicating no significant association. However, an exploratory analysis suggests that the majority of females are shy, as three out of four females showed this result in the "open field" test.

Feather plucking encompasses all types of self-mutilation involving feathers, including chewing, biting, and/or pulling them out (Van Zeeland et al. 2013; Kinkaid et al. 2013). In some cases, feather plucking can cause damage to the skin and tissues, hypothermia, infection, or bleeding (Meehan 2003; Van Zeeland 2016). In the present study, in addition to feather plucking, skin lesions and structural alterations in feathers were identified in animals from the Test Group. When viewed under a stereomicroscope, the feathers showed wear on the vexillum, indicating that the animals were engaging in feather chewing, which corroborates the previously observed data and literature.

Assessing the extent of feather damage is crucial as feathers are involved in flight, protection, thermal insulation, waterproofing, camouflage, mobility, and identification of mating partners (Cardoso 2010; Pough et al. 2008; Oliveira 2019). Van Hoek and King (1997) report that in psittacines, the pectoral region is the most affected area by feather plucking. This finding does not align with the observations in the present study, where the back and legs were the most affected body parts.

Many factors are associated with feather plucking behavior: (i) genetic factors, such as sex; (ii) socioenvironmental factors, such as stress levels; (iii) neurobiological factors, such as age; and (iv) even the rearing conditions, as animals raised by their parents have a lower chance of exhibiting feather plucking (Kinkaid et al. 2013; Garner et al. 2006; Van Zeeland et al. 2009). Considering this, since the animals in the Test Group (the group with feather plucking) were housed at CETAS and were mostly rescued from wildlife trafficking, many of these factors described in the literature could have contributed to the development of such self-destructive behavior. However, it was not possible to test the correlation of many of these factors in the present study due to a lack of information regarding these trafficked animals. Despite this, of the two aforementioned factors that could be evaluated (stress levels and sex), only sex showed a statistically significant difference.

In some bird species, feather coloration differences indicate the sex of the animal, distinguishing between males and females (Vieira et al. 2009). However, this plumage distinction does not apply to psittacines (Sick 1997). There are various techniques for sexing birds, including laparoscopy, nuclear magnetic resonance imaging, and molecular sexing. Among these methods, molecular sexing is the most reliable and recommended for identifying the sex of birds, as it is highly accurate, non-invasive, and not influenced by age or sexual maturation. Thus, this method was chosen for sex determination in the present study, and all individuals were sexed to explore the possible relationship between sex and temperament, which was found to be true (Antonio et al. 2021b; Vieira et al. 2012).

The higher tendency for feather plucking in females, as observed in the present study, has been noted in other research. Garner et al. (2006) established this relationship in Amazona amazonica. Kinkaid et al. (2013) reported that female Psittaciformes are three times more likely to develop feather-damaging behaviors than males. This may be related to stress levels, as previous studies have shown that females exhibit more signs of stress than males and that males are more sociable than females, with these two factors being associated with behavioral disorders such as feather plucking (Garner et al. 2006; Keller et al. 2015; Titulaer et al. 2012; Lopes et al. 2017).

Since feather plucking is closely related to behavioral characteristics, these can be influenced by the animals' stress levels (Keller et al. 2015; Garner et al. 2006; Titulaer et al. 2012; Lopes et al. 2017). Stress levels can be assessed through the measurement of glucocorticoids in feces (Costa et al. 2016; Owen and Lane 2006). However, this method has high variability and glucocorticoid levels can change rapidly due to stressful factors (Davis and Maney 2018). An alternative for determining stress levels is the use of the heterophil-to-lymphocyte ratio (H:L) (Davis et al. 2008). An increase in heterophil counts is associated with increased stress in animals, while a decrease in lymphocyte counts is related to high levels of glucocorticoids (Davis and Maney 2018). The H:L ratio has shown clear positive associations with stress levels in bird species such as Gallus gallus domesticus (Elston et al. 2000), Pygoscelis adeliae (Vleck et al. 2000), and Phoenicopterus sp. (Royer and Anderson 2014). In the present study, no statistically significant differences in H:L ratios were found between the Control and Test Groups, possibly reflecting the high general stress levels of captive wild birds, with some being more susceptible to feather plucking than others.

The "open field" test provides a simple, quick, safe, and inexpensive way to assess basic animal temperament, classifying them as shy or bold (Perals et al. 2017; Silva et al. 2021). According to Garner et al. (2006), Titulaer et al. (2012), and Lopes et al. (2017), feather plucking behavior can also be influenced by the animal's temperament, which could not be significantly observed in the present study, possibly due to the small sample size available. However, when evaluating temperament in relation to the animals' sex, it was possible to identify that the majority of females were classified as shy (70%). Similar findings were reported by Oers et al. (2005) and Titulaer et al. (2012) in studies of Parus major, and by Lopes et al. (2017) in Amazona aestiva. Bold animals exhibit more exploratory behaviors (Toms et al. 2010), which helps avoid elevated stress levels. In captivity, environmental enrichment designed to stimulate exploratory behavior has been shown to be an effective strategy for reducing feather plucking in psittacines of the genus Aratinga (Telles et al. 2015).

The present study demonstrated that in A. auricapillus, females are more affected by feather plucking. For the first time, the leukocyte profile of A. auricapillus, both with and without feather plucking, has been presented, contributing to the physiological knowledge of the species. Although statistically significant results were not obtained, the observation of medians regarding stress levels allowed us to infer that the stress level in the Test Group (with feather plucking) was higher than that in the Control Group (without feather plucking). Future work should focus on studying the influence of environmental enrichment on this species, as it has proven to be an effective tool for minimizing feather plucking damage in captive psittacines. We strongly encourage further studies using the methodology employed here and with a larger sample size to validate the findings of this research in a larger population.

Funding The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Competing Interest The authors have no relevant financial or non-financial interests to disclose.

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No competing interests reported.

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Feather plucking in captive Aratinga auricapillus: influence of sex, stress, and temperament

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Abstract

Figures

Introduction

Methods

Animal sampling and clinical evaluation

Feather evaluation

Biological sample collection and molecular analyses

Leukogram and stress level determination

Statistical analysis

Results

Clinical evaluation

Feather evaluation

Molecular analyses

Leukogram and stress level

Temperament analysis

Discussion

Declarations

References

Additional Declarations

Status:

Version 1