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Effect of Sound Enrichment in Captive Zebra Finches (Taeniopygia Guttata) Behaviour

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Published: 8th Feb 2020 in Biology

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Effect of sound enrichment in captive zebra finches (Taeniopygia guttata) behaviour

ABSTRACT

Zebra finches (taeniopygia guttata) are small passerines birds widely used as laboratory animals and are kept in captivity for scientific purposes, taking away most of their natural behaviours.  Considering that the constant human manipulation could detriment the welfare of the birds leading to them developing negative behaviours (like over-preening), environmental enrichment is an important tool to be used. Many studies have been done on humans, in which classical or relaxing music offer a significant positive effect in human’s health; few studies of sound enrichment have been done on animals, and many of that number show versatile and contradictory results. In this experiment, we evaluate the response of zebra finches to three different sound environments (ambient sound, classical music and human voices), with the objective to find out if sound enrichment could affect their fear or social behaviour. From a total of 100 birds, 20 of them (10 males and 10 females) were randomly selected for each trial (30 trials in total) and their behaviour was marked every 3 minutes for 2 hours. Our results showed a positive effect of classic music in fear behaviour, where birds developed less frequency of fear behavioural measurement. We cannot generalize our findings as some limitations were found during the process of the experiment.   However, music could easily be considered as an enrichment tool with low-cost implementation and no infrastructure requirements but, it is important to mention that from our literature review, even if some author described a positive effect of music as an enrichment tool, some other ones mention it as having negative effects. So whichever environmental enrichment is provided, a prior evaluation has to be done to ensure that this activity is enhancing the animal´s welfare and not affecting their health and behaviour.

  1. INTRODUCTION

Zebra Finches (taeniopygia guttata) are small passerines originating from Australia and are one of the most widely used passerine for avian research because of its rapid acclimation and all year round reproduction. These birds possess a strong sexual dimorphism; males are provided with a bright red beak, white cheeks with black strips and a white abdomen, while the female´s body is grey and their beak is not as vivid a red colour as the males are (Morris, 1954). This dimorphism not only applies for the appearance but also in vocal production, where only males produce songs. Young finches learn their songs from their tutors (fathers), while the females develop song preferences by listening to male tutors. Both male and female develop a distance call, which are used to alarm, identify, or locate other birds (Scully et al, 2017). During the courtship dance of these monogamous birds, the male sings continuously, repeating once and again the same song phrase; the dance is never performed without the song. While the courtship goes ahead, the song is changed into a call which is answered in a similar way by the female. The song phrase is unmusical for the human ear (Morris, 1954). Yamahachi et al (2017) mentions that song rate is positively correlated with the male´s body condition, he also mentions that in zebra finches high singing rate is equivalent to good welfare.

Zebra finches have been breed in captivity for many generations, and are very popular as a pet (Jacobs et al, 1995). Captive birds are provided with food, water, care, a safe place to live and even roommates, taking away all their natural instincts and behaviour. This is the main reason why we should provide enrichment environments to these animals to keep them physically and physiologically active, develop instincts and prevent boredom (Gray, 2017), but overall, ensuring a good quality life. In captivity, it is important to manage the group very carefully, not only for numbers but also for weight. There are situations where one bird is dominant to another, and the subordinate bird flees from the spot it occupied as the dominant one approaches. However, it is not very clear if this subordinate behaviour can lead to some birds to show a homosexual behaviour, where males perform the female behavioural courtship patterns (pseudofemale) and females perform the male behaviour courtship pattern (pseudomale), the reversed sexual roles have been reported in many different species of bird (Morris, 1954).

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Going back to enrichment facilities, housing conditions for animals have always been mentioned as one of the mayor concerns in animal welfare (Collins et al, 2008); for example, Jacobs et al (1995) demonstrated that larger enrichment cages allow zebra finches to deliver a natural behaviour spending more time flying and singing. Also large aviaries allow birds for more social interaction, which is important in this situation as these birds are naturally social and in the wild they live in big congregations (Gray, 2007), carrying out activities like allopreening (grooming another bird), which plays an important role in their social life, reducing stress and reinforcing pair bonds (Villa et al, 2016).  However, this kind of facility can easily turn into a stress and fear environment when the birds need to be caught.  Said this, it is important to reduce the stress for handling. Collins et al (2008) mentioned that domestic chickens (Gallus gallus domestic) reduce their fear for humans only through regular visual contact.  Fear is one of the undesirable emotions which detriments the welfare (Jones & Waddington, 1992).

Many studies on humans have found that listening to relaxing or classic music can be beneficial to their health, such as by decreasing anxiety, increasing prosocial behaviour or decreasing blood pressure among others (Kogan et al, 2012). Few studies have explored the effect of music on animals, like in chimpanzees (Wallace et al, 2013), rabbits (Peveler & Hickman, 2018), dogs (Kogan et al, 2012), psittacines (William et al, 2017) and chickens (Campo et al, 2005). Some of these studies experiment with classic music (Kogan et al, 2012), natural sounds (Robinson & Margulis 2016) or noise (Campo et al, 2005). No matter what kind of audio enrichment we are providing, we have to record the behaviour of the animals in their natural environment to find out and understand all the subtle changes that can occur as not all the animals respond in the same way in front of stimuli and we have to be very careful to not affect their behaviour in a negative way.

From an ethical point of view, the human being is responsible for looking after the animals kept in captivity under their care, however for a scientific researcher this responsibility is increased as these animals are the most important part of their research; by providing environmental enrichment we are helping the animals to increase their ability to cope with behavioural challenge like been surrounded by humans and experimental manipulation (Gray, 2017). For this, it is extremely important to bring to these animals the best living conditions available to ensure their well-being and to provide an environment that satisfies their behavioural requirements, mimicking the conditions found in their natural habitat.

As I mentioned before, many of the studies which reveal the positive effect of music have been done with humans and this is likely the “main point” of the misunderstanding. Consciously or unconsciously, most of the time, we pretend to understand an animal´s well-being from an anthropomorphic point of view, assuming if humans like it animals will as well. In this case, the objective of this study is to find out if auditory enrichment affects social behaviour or fear behaviour in zebra finches (Taeniopygia guttata), addressing two hypothesis: ¿Does sound treatment affects the fear behaviour in zebra finches?, ¿Does sound treatment affects the social behaviour in zebra finches?.

2. METHODS

2.1 Subjects

A total of 100 birds (Taeniopygia guttata) were observed during this study (50 males and 50 females), all of them kept in a large bird-holding facility. We don’t know for sure the age of the birds or how many adults and how many juveniles took part in the study. All the birds were captive-reared with no prior experience to background noise, other than the vocalization of conspecifics and ambient ventilator noise. As part of the study, all the animals were selected at random for each Trial (Ambient sound, human voices and classical music), and back to the bird-holding facility after that. Each bird was tested more than once at different trials. Each bird has a one colour ring on each leg with easily readable identification and also zebra finches, male and female, are well defined by the colours of their feathers and external characteristics (Appendix1).

2.2 Behaviour

In order to evaluate two specific behaviour aspects, ¨FEAR¨ and ¨SOCIAL¨ a small ethogram (Table 1) was created.

Table 1: An ethogram describing the two behaviours to be evaluate

Behaviour

Criteria description

Fear

  • Retreating to high perches
  • Clumping together

Social

  • Allopreening
  • Interaction with other birds

2.3 Ethical approval

We don’t have the details about the Ethical approval for this study.

2.4 Auditory enrichment

Three conditions of auditory enrichment were used in this study:  ambient sound, human voices and classical music (Antonio Vivaldi’s Concert N° 1, “Spring”).  The two last ones were played at 50 decibels.

2.5 Procedure

The birds were evaluated under three different husbandry conditions (Ambient sound, human voices and classical music), all the birds were selected randomly for each trial. On the second day of the study, the 20 birds of each trial were observed and their behaviour was recorded. The behavioural criteria are described at Table 1. These observations were repeated every three minutes for a period of two hours and the experimenter recorded the performed behaviour of the bird at that moment. After the trial session the birds were brought back to the bird-holding facility for at least two days before the next trial session starts. The classical music and the human voices were played at 50dB. Each trial was repeated 10 times, giving a total of 600 entries (Table 2). Before running any results, we have to mention that trial 26- classic music hosted only females same as on trial 27-human voice. A similar situation occurs during trial 29-classic music with only males same as trial 30-human voices. It was not our intention to make a difference with these four trials, but we have to report all these findings as the results can be affected by it.

Table 2: Distribution of the bird under three different husbandry conditions (This pattern was repeated 10 times, except for trial 26, 27, 29, 30)

TRIAL

Zebra finches

Ambient sound

Human voices (50dB)

Classical music (50dB)

Male

10

10

10

Female

10

10

10

 

2.6 Data analysis

To examine the effect of sound in our response variables, fear and social behaviour, we used a program named RStudio (appendix 2). Variables such as mass and sex have also been tested. We used a standard diagnostic check to find out if the data is normally distributed, and then we plotted two mixed effect lineal models, one for each response variable, with mass, sex and sound as explanatory variables and trial and birds as random effects. An account of the total amount of time that each bird was observed performing a specific behaviour was recorded and marked as “social behaviour” or “fear behaviour”. We used model selection in order to create a simpler model using step function, and then we compared the complex and simple model using loglikelihood function. Finally, we assess the effect of the explanatory variables using the Anova function. 

3. RESULTS

The purpose of this study was to understand if auditory enrichment affects the fear or social behaviour in zebra finches.

Looking at our first research question, ¿Does acoustic enrichment affect the frequency of fear behaviour?  In the final model we got a significant effect of sound treatment in the frequency of fear behaviour (DF= 596,   F value= 455.4723, P value < 0.001). Also, we found no significant effect on sex into fear behaviour (DF= 596, F value = 0.0187, p value= 0.8914), however, the interaction between sound:sex shows a significant effect on fear behaviour (P value < 0.001).  In the boxplot (figure 1) we can see how classic music keeps a lower frequency of fear behaviour. We accept our alternate hypothesis (Ha1) where acoustic enrichment affects the frequency of fear behaviour.

Figure 1: Effect of sound treatment against fear behaviour

Our second research question was: ¿Does acoustic enrichment affect the frequency of social behaviour?  From the Anova, none of our explanatory variables (sound, sex, mass) or their interactions show significant effects on their social behaviour (Figure 2). Sound (DF = 591, F value = 0.2100, P value = 0.8107), Sex (DF = 591, F value = 0.3300, P value = 0.5659), Mass (DF = 591, F value = 0.1331, P value = 0.7154), sound:sex (DF = 591, F value = 7901, P value = 1678), sound:sex (DF = 591, F value = 0.1677, P value = 0.8457).  We reject our alternate hypothesis (Ha2) in which acoustic enrichment affects frequency of social behaviour.

Figure 2: Effect of sound treatment against social behaviour

4. DISCUSSION

There are many studies of audit enrichment in humans, few ones in animals, but not many in birds. We examined the effect of acoustic enrichment in zebra finches, with three different sounds (ambient sound, human voices and classical music) with the objective to see if the fear behaviour or the social behaviour might be affected. From all our variables (sound, sex and mass) we found that only sound affects the fear behaviour. Social behaviour was not affected at all in any of the three different sound treatments.

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From our result, classical music significantly affected the fear behaviour in zebra finches, reducing the frequency of behavioural measurement. Our findings did not agreed with Wallace et al (2013) who tested a group of eight Moloch Gibbons in a zoo facility, finding that six of them did not showed any changes, but the behaviour of the other two (1 male and 1 female) suggest that this music enrichment produces anxiety and stress. In our experiment, sex (male/female) itself did not show any significant effect in the bird´s behaviour, but the interaction of sound:sex did, perhaps due to the fact the zebra finches males and females develop different sound skills. We refer to this before, as the males are the ones who develop song and calls while the females develop only calls.

It is also important to make a difference between noise and music. The former has shown many negative effects on animals, like stress and fear; Campo et al (2005) also refers to an experiment made by Stadelman (1958) where noise (80 – 118 decibels) made no difference on the effect of the growth of young chickens. However, he found in this study a violent behavioural response to intermittent noise (110 – 118dB); he also mentioned Hamm´s (1967) experiment, who found a decrease in egg production, attributing this result as a change in the hen´s behaviour, keeping themselves away from water and food due to noise stress. Campo et al (2005) found that hens exposed to noise were more stressed than the control group; also hens exposed to music were more fearful, suggesting that these stimuli could bring a negative effect on the bird´s welfare.  However, he also mentions that his results differ from those of many other authors, perhaps the type of music played, how long the exposure lasted or sound level decibels may all be relevant. Also, from my point of view, the use of different breeds of hens can affect in a way or even change the results, as it is well known that some breeds are easier to handle and others are more prone to a stress response.

On the other hand, Peveler and Hickman (2018) measured stress, testing faecal cortisol in male rabbits before and after music enrichment, finding less levels of cortisol in rabbits after 6 months of music enrichment. These findings can be used to improve the well-being of rabbits kept in laboratories, for example, or even kept as pets. Another positive result was found by  Kogan et al (2012) who proved that auditory stimulation (Classic music) can positively affect the well-being of shelter dogs by reducing stress levels and potentially increase the likelihood of adoption. A complete opposite result was found by Wallace et al (2017) who studied the role of music enrichment in a zoo facility in chimpanzees finding that chimpanzees show a little reaction to music by decreasing their social behaviour (playing and grooming),  in this case again, the finding suggest that music did not provide an enriching effect in chimpanzees.

Our other two sound treatments, ambient sound and human voices, did not show any significant difference (positive or negative) in fear or social behaviour, in contrast with Williams et al (2017), who mentions that pop music and talking radio reduces the level of calm vocalization to zero, indicating that these sounds may not be beneficial to parrots as vocalizations are part of their normal behaviour.  In this same study the preening behaviour was affected by rainforest sound, talking radio and classical music (in that order) showing an over-preening behaviour. Preening is part of their normal behaviour and help birds not only to socialize but also to keep themselves clean of ectoparasites (Villa et al, 2016).  However, over-preening is linked to stereotypy and feather-plucking. It is important to mention that we cannot generalize from Williams’s et al (2017) finding as this experiment took place with a small number of animals. Further research has to be done to provide a solid background. As we have found, the responses differs depending on the species, from good behaviour to stress and anxiety, so we cannot generalize and say that auditory enrichment is positive for animals as it is for humans. However, it is an excellent low-cost tool to environmental enrichment (prior evaluation),with no infrastructure requirements. We agree with Robinson & Margulis (2016) when they mention that auditory enrichment is underutilized, however, caution must be taken while selecting natural sounds, as call or song from conspecifics can be stressful and lead to negative behaviour like feather picking for example.

We found few limitations in this project that might affect the results. First of all, as the same birds were chosen randomly and used in different trials, it is a chance that the same bird was picked two times in a row. If so, it could be facing the same treatment again and may respond rapidly to the stimuli, or face another type of stimuli but still behaving with the prior stimuli. I would prefer to use each bird in only one sound treatment to be sure that there is no chance to cross over responses or behaviours. Another concern is, as these songbirds use their singing at the courtship dance, if we “enrich” the environment with any kind of sound, this disturbance might affect the courtship behaviour; we don’t have information (as it was not one of our parameters to record) about this behaviour during the experimental process. In the same way, we mentioned that young male birds learned their singing from the adult males; again this environmental enrichment with sound or music might affect that learning process.

5. REFERENCES

  • Campo JL, Gil MG & Dávila SG. 2005, Effects of specific noise and music stimuli on stress and fear levels of laying hens of several breeds, Applied Animal Behaviour Science 91:75-84
  • Collins SA, Archer JA & Barnard CJ. 2008, Welfare and mate choice in zebra finches: effect of handling regime and presence of cover, Animal Welfare 17:11-17.
  • Gray G. 2017 Enhancing welfare of zebra finches through the use of environmental enrichment. Animal Technology and Welfare 15:147150
  • Jacobs H, Smith N, Smith P, Smyth L, Yew P, Saibab P & Hau J. 1995, Zebra Finch Behaviour and Effect of Modest Enrichment of Standard Cages, Animal Welfare 4: 3-9
  • Jones RB & Waddington D. 1992, Modification of fear in domestic chicks, Gallus gallus domesticus, via regular handling and early environmental enrichment, Animal Behaviour 43:1021-1033.
  • Kogan LR, Schoenfeld-Tacher R & Simon AA. 2012, Behavioural effects of auditory stimulation on kenneled dogs, Journal of Veterinary Behavior: Clinical Applications and Research  7:268-275
  • Morris D.1954 The Reproductive Behaviour of the Zebra Finch (Poephila guttata), with Special Reference to Pseudofemale Behaviour and Displacement Activities, Behaviour 6:271-322.
  • Peveler J & Hickman D. 2018. Effects of Music Enrichment on Individually Housed Male New Zealand White Rabbits (Abstract), Journal of the American Association for Laboratory Animal Science: JAALAS Available online at: doi: 10.30802/AALAS-JAALAS-17-000153  
  • Robbins L & Margulis SW. 2016, Music for the birds: effects of auditory enrichment on captive bird species. Zoo Biology 35: 29-34
  • Scully EN, Hahn AH, Campbell KA, McMillan N, Congdon JV. & Sturdy CB. 2017, ZENK expression following conspecific and heterospecific playback in the zebra finch auditory forebrain, Behavioural Brain Research 331:151-158.
  • Villa SM, Goodman GB, Ruff JS & Clayton DH. 2016, Does allopreening control avian ectoparasites? Biol Lett. 12:20160362. Available online at: http://dx.doi.org/10.1098/rsbl.20160362
  • Wallace E, Altschul D, Körfer K, Benti B, Kaeser A, Lamberth S, Waller B, Slocombe K 2017. Is music enriching for group-housed captive chimpanzees (Pan troglodytes)?  Available online at: https://doi.org/10.1371/journal.pone.0172672
  • Wallace EK, KingstonJones M, Ford M & Semple S. 2013, An investigation into the use of music as potential auditory enrichment for moloch gibbons (Hylobates moloch), Zoo Biology 32:423-426.
  • Williams I, Will H, Grant R. 2017. The effect of auditory enrichment, rearing methods and social environment on the behaviour of zoo-housed psittacines (Aves: Psitaciformes): Implications for welfare, Applied Animal Behaviour Science 186:85-92.
  • Yamahachi H, Zai AT, Tachibana RO, Stepien AE, Rodrigues DI, Cavé-lopez S, Naryla G, Lee J, Huang Z, Höster H, Düring D, Hahnloser RHR. 2017. Welfare of zebra finches used in research. bioRxiv 154567 doi: https://doi.org/10.1101/154567

Appendix 1

Zebra finches: Male and Female external characteristics (taken from Morris, 1954)

Adult male

Bright red beak. Cheek white with black vertical margins. Ear-patch chestnut brown. Throat and breast finely barred with black and white, with a wide black band across the lower breast. Abdomen pure white. Flanks brown with white spots. Dorsal surface and wings grey. Upper tail coverts banded black and white. Rump white. Legs and feet orange.

Adult female

Grey over the whole body surface except for: Beak red, but less intense than male. Cheek white with black vertical margins. Up per tail coverts banded black and white. Rump white. Legs and feet orange

Appendix 2

 

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