The primary senses of humans are vision, hearing touch, taste, and smell (Abram, 2012). However, for other animal species, their predominant sense may be stronger or different to ours (Nielsen, 2018). As a result, animals under human care may be unintentionally placed in environments that are not best suited for their sensory abilities which could negatively impact their welfare (Nielsen, 2018). In captive settings such as zoos, enclosures designed to enhance the visibility of animals on display/to promote visitor satisfaction may compromise the animal’s needs (Davey, 2006). Therefore, humans must consider an animal’s sensory abilities and ensure the removal of stressful sensory inputs for animals that are under human care (Nielsen, 2018).
Environmental enrichment can be defined as the stimulation of the brain through its social and physical surrounding. As a result, it is a common method that is utilized in improving the welfare of captive animals (Young, 2013). The primary motives for applying enrichment are to promote species-specific behaviors and reduce abnormal repetitive behaviors such as stereotypes (Young, 2013; Wells, 2009). Food enrichment is one of the most common forms of enrichment in captive settings, for it is considered to be easy to apply (Robbins & Marguilis, 2016). Other types of enrichment can include enclosure alterations and adding accessories or sensory inputs (Young, 2013). According to Leone & Estevez (2008), environmental enrichment is beneficial both to the welfare of the animal and economically, through better time and budget spending, thereby resulting in a win-win situation.
Auditory stimulation is a form of acoustic enrichment that has received increased attention and application within captive settings (Kogan, Schoenfeld-Tacher & Simon, 2012). Auditory stimulation can be divided into two categories: natural sounds and other types of auditory signals, such as music (Wells, 2009). When applied correctly, acoustic enrichment has the ability to positively influence a captive animal’s welfare (Williams, Hoppitt & Grant, 2017). Contrastingly though, an inappropriate auditory stimulus can cause the undesired effect of stress and agitation (Wallace et al., 2013; Robbins & Margulis, 2014).
Auditory stimuli have been applied as an enrichment to several animal species with varying degrees of effectiveness (Wells, 2009; Snowdon, Teie & Savage, 2015). Many studies on humans note the benefits of listening to classical music, which includes an increase in wellbeing and a reduction in stress and anxiety (Wells, 2009; Williams Hoppitt & Grant, 2017; Barcellos et al., 2018). The benefits to humans are often the reason for classical music being selected in acoustic enrichment studies in non-human animals. Some of the species that acoustic enrichment has been tested in include: shelter dogs (Canis lupus familiaris) (Kogan, Schoenfeld-Tacher & Simon, 2012), captive gorillas (Gorilla gorilla gorilla) and birds (Musophaga rossae, Colius striatus and Lamprotornis superbus) (Robbins & Margulis, 2014; Robbins & Margulis, 2016), laboratory zebrafish (Danio rerio) (Barcellos et al., 2018), and captive parrots (Psittaciformes) (Williams, Hoppitt & Grant, 2017).
Two such studies which were performed simultaneously assessed the impacts of acoustic enrichment on zoo-kept Western lowland gorillas which shared their enclosure with three bird species (Lady Ross’s turacos, speckled mousebirds and superb starlings) (Robbins & Margulis, 2014; Robbins & Marguilis, 2016). The animals were exposed to four treatments: (1) no auditory stimuli (control), (2) rainforest sounds, (3) classical music and (4) rock music. The study found that the gorillas reduced their levels of stereotypy during the rainforest sounds treatment however their levels of stereotypy increased during the classical music and rock music treatments (Robbins & Margulis, 2014). The response of the birds to the sounds treatments differed considerably to that of the gorillas’. The enrichment led to an increase in flight and vocalization behavior which varied between each bird species and treatment (Robbins & Margulis, 2014).
The findings from Robbins & Margulis (2014)’s gorilla study contrasted with that of previous studies assessing the behavioral response of gorillas to acoustic enrichment. Wells, Coleman & Challis (2006) found that gorillas exhibited a higher frequency of locomotion to rainforest sounds, which is suggestive of agitation, whereas the rainforest treatment in Robbins & Margulis (2014)’s study had the opposite effect on the gorillas. A reason for the contrasting results between the studies could be that although the treatments of each study were both equally considered to be ‘rainforest sounds’, the sounds played would not have been the same as different CD tracks would have been used. Additionally, the Robbins & Margulis (2014) study did not state at which decibel (dB) the treatments were played to the gorillas, which could have an effect on their behavioral response. To make accurate assessments on the response of an animal to auditory stimuli, the dB should always be included. The studies were also performed at different study sites which could have differing levels of ambient noise.
The behavioral response of the birds in the Robbins & Margulis (2016) study are difficult to analyze as few studies have investigated the effect of acoustic enrichment on birds. The limited number of studies that have been performed were on different bird species. When studying the effect of auditory enrichment on zoo-housed parrots, Williams, Hoppitt & Grant (2017) found that preening increased across all six treatments, however, calm vocalizations were not exhibited during pop music or talking radio treatments. To assess the most appropriate acoustic enrichment for a particular species, a study would have to be performed on the target species, rather than applying the results from a different species. As stated by Robbins & Margulis (2016), acoustic enrichment for captive birds has been a largely unexplored area, which needs further study.
Zebra finches (Taeniopygia guttata) are small birds native to Australia that are now considered to be domesticated due to its popularity as a pet (Mello, 2014). They are also used in laboratory studies (Nager & Law, 2010) and therefore importance should be placed on ensuring optimal welfare for the subjects if used in research (Fenwick, Griffin & Gauthier, 2009). Few studies have investigated the effects of enrichment to zebra finch welfare. One such study conducted by Mello (2014) investigated the behavior of zebra finches in cages of different sizes and enrichment. However, a study on the impact of auditory stimuli to zebra finch behavior has yet to be performed. As zebra finches are auditory-sensitive animals, it is important to understand how the surrounding acoustic environment can impact their welfare.
Therefore, this study is aimed at investigating the behavioral responses of zebra finches to acoustic enrichment. The objective was to measure the frequency of fear and social behavioral responses of the zebra finches exposed to three auditory conditions, those being ambient sounds, human voices, and classical music. Fear responses can be a measure of the lowered welfare state, which has been seen in equines (Swann, 2006). As noted by Mello (2014) zebra finches are social and gregarious animals, therefore if they exhibit social behavior, this would be an indicator of good welfare (Yeates & Main, 2008). Based on literature that shows that humans and animals can respond positively to classical music (Kogan, Schoenfeld-Tacher & Simon, 2012; Barcellos et al., 2018), it was hypothesized that acoustic enrichment affects the frequency of different behaviors shown by zebra finches.
As captive animals will be used within this study, the impacts that this study could have on the subject’s welfare must be taken into consideration. The subjects may be exposed to stimuli which they perceive as stressful and therefore negative. By exposing the study subjects to different auditory stimuli, the knowledge gained from the outcome could aid in the understanding of the appropriate needs of the zebra finch. The motive of the study is to determine what the optimal auditory stimuli is for zebra finches to ensure appropriate care and management.
Subjects and Study Site
The study was performed at a large-bird breeding facility, using a population of 100 captive-reared zebra finches (Taeniopygia guttata) of an even sex ratio.
Procedure
The experiment was divided into three sound treatments per trial, those treatments being: 1) ambient sounds in the aviary (i.e. control); 2) human voices talking at 50dB, and 3) classical music (Vivaldi’s ‘Spring’) played at 50dB. For each trail, 10 birds of each sex were randomly selected and released into a large aviary, where they were exposed to one of the three sound treatments for two days. At the end of the trial, the birds were returned to their normal housing facility for at least two days, before the start of another trial. A total of 30 trials were performed with each bird being used for exactly six trials in differing groups and random treatments.
On the second day of each trial, the behaviors of the birds were recorded over a two-hour observation period. The observer recorded the frequency that each individual spent displaying social behaviors and fear behaviors, using instantaneous sampling. A timer beeped every 3 minutes and the observer identified each bird and recorded which target behavior they performed at that time. Once the behaviors of each bird had been recorded, the observer waited for the next beep. For identification purposes, all birds wore a colored leg ring on each leg, with a colored thread hanging from each ring.
Results
Data Visualization
Figure 1: Fear against sex
From figure 1 above, it is evident that the mean of the level of fear for both male and female zebra finches are the same. However, it can be seen that the female have a greater variance in their level of fear compared to the male zebra finches.
Figure 2: Fear against sound
It can be observed that the mean of the level of fear is highest in ambient sound while lowest for the classic music among the female zebra finches. On the other hand, for male zebra finches, the level of fear is highest for the voices while lowest for the classic music. Hence, it is evident that the fear levels are different among the different genders of the bird which is also impacted by the different types of sound.
Figure 3: Social level against sound
From figure 3, it can be seen that there is not so much difference between means of the social levels of the female birds with respect to the three types of sound. However, for the male birds, a different scenario is seen where classic music makes the male birds more social compared to the ambient sound and the voices. The ambient sound makes them very anti-social compared with the other types of sound.
Figure 4: Fear against mass
The level of fear with regards to mass can be observed not to have any significant difference. However, it can be seen that the variance of fear with respect to mass is highest among the females compared to the males.
Figure 5: Social against Mass
With regards to social levels, their difference in mean can be seen to be very minimal where females tend to be more social compared to the male birds. The variance of social levels can also be seen to be varying greatly for the male birds compared to the female birds.
Figure 6: Fear against Mass with regards to sound
The ambient sound stirs a great level of fear compared to the other two type of sound for both male and female zebra finches. Consequently, the opposite can be seen for the classic music type. The human voices stir the same level of fear to both male and female zebra finch, unlike the other sound type which had varying level of fear to the two genders of the birds.
Figure 7: Social levels against mass with regards to sound
The means of the social levels can be seen to be all similar for both genders and all the sound types with regards to mass. The social level means can, however, be seen to vary greatly between the males and the females with regards to the mass of the birds.
Research Question 1: Does acoustic enrichment influence the frequency of fear behavior?
The developed hypothesis to answer this question is as shown below:
H0: Acoustic enrichment affects the frequency of fear behavior
H1: Acoustic enrichment does not affect the frequency of fear behavior
ANOVA
Before the data was analyzed, several assumptions were tested to ensure that they were met. The assumptions include; the residuals have to be normally distributed, there should be independence of observations and there should be homogeneity of variance.
The data was tested to determine whether it met all the assumptions of ANOVA.
Figure 8: Normal Q-Q Plot
From figure 8 above, it can be concluded that the residuals appear to be normally distributed since they follow a diagonal line. Moreover, the residuals do not appear to have a non-linear pattern. A similar observation can be seen for the residuals as shown in figure 9 below.
Figure 9: Normality of residuals
Figure 10: Independence of residuals
Figure 10 shows that there is the independence of observations through the residuals. Thus, there is no relationship between the groups.
Figure 12: Test for homoscedasticity
It can be seen from figure 12 that there is a variance in fear between the three groups. However, the variance is similar between the sound group and the voices group. Thus, the data meets the assumption of having homogeneity of variances.
ANOVA Model 1 Output
Table 1: ANOVA with Satterthwaite’s method
From table 1, it can be seen that sound has a significant effect on the level of fear among the bird species of zebra finches (p < 0.05). Sex and mass, on the other hand, do not have a significant effect (p > 0.05). However, the sound has a significant effect on the level of fear among zebra finches with regards to sex (p < 0.05) unlike with mass (p > 0.05).
Table 2: Backward reduced random-effect
Consequently after carrying out the backward reduced random-effect, it can be seen that the interaction between sound and sex continued to remain statistically significant (p < 0.05) while mass and the interaction between mass and sound remained insignificant (p > 0.05).
Table 3: ANOVA
From the final model in table 3, it can be seen that the effect of sound treatment is statistically significant (p < 0.05). However, sex treatment is not statistically significant. On the other hand, there was a statistically significant effect on the level of fear with regards to the interaction between sound and sex.
Figure 13: Visual effects
From figure 13 it can be seen that the variation between the fear levels is high in ambient sound and human voices. Consequently, the variation between the two groups is greater among the female compared to the male. However, the fear levels are least in a classic music. More so, the variation is greatest among the males compared to the females.
Research Question 2: Does acoustic enrichment influence the frequency of social behavior?
The developed hypothesis to answer this question is as shown below:
Ha1: Acoustic enrichment affects the frequency of social behavior
H01: Acoustic enrichment does not affect the frequency of social behavior
ANOVA model 2
Similarly to model 1, prior to the data analysis, several assumptions were tested to ensure that they were met. The assumptions include; the residuals have to be normally distributed, there should be the independence of observations and there should be the homogeneity of variance.
Figure 14: Normal Q-Q Plot
From figure 14 above, it can be concluded that the residuals appear to be normally distributed since they follow a diagonal line. Moreover, they do not appear to have a non-linear pattern. A similar observation can be seen for the residuals as shown in figure 15 below.
Figure 15: Normality of Residuals
Figure 16: Independence of residuals
It is evident that there is the independence of observations through the residuals as shown in figure 16 above. Thus, there is no relationship between the groups.
Figure 17: Test for homoscedasticity
It is clear that there is no difference in the variation in social levels between the three groups. Hence, the data meets the assumption of having homogeneity of variances.
ANOVA Model 2 Output
Table 4: ANOVA with Satterthwaite’s method
From the summary of the model in table 4 above, it can be seen that none of the variables has a statistically significant effect on social levels. The same can also be said for the interactions of the three variables, sound and sex, and sound and mass.
Table 5: Backward reduced random-effect table
Consequently, after carrying out the backward reduced random-effect, it can be seen that there was no significant effect of sound treatment on the social behavior of the zebra finches (p > 0.05). Consequently, it was also observed that there was no significant effect of sex and mass on the social behavior of the zebra finches (p > 0.05).
Figure 18: Model 2 Visual effects
From figure 18, it can be seen that the variation of social behavior with respect to sound and sex does not differ significantly. Thus, it can be concluded that sound does not impact the level of social behavior among the zebra finches.
The study was aimed at investigating the behavioral responses of zebra finches to acoustic enrichment. Consequently, the main objective was measuring the frequency of fear and social behavioral responses of zebra finches exposed to the three auditory conditions of ambient sounds, human voices, and classical music.
Does acoustic enrichment influence the frequency of fear behavior?
Having met all the assumptions of ANOVA, the data was passed through the ANOVA process and the results were obtained. It was found out that sound has a significant effect on the level of fear among the zebra finches, unlike mass. Consequently, it was also established that the interaction of sound and sex also has a significant effect on the fear behavior of the zebra finches. Hence, we reject the null hypothesis and conclude that acoustic enrichment does affect the frequency of fear behavior.
Does acoustic enrichment influence the frequency of social behavior?
Similarly to model 1, the data met all the assumptions and ANOVA analysis was carried out. It was established that none of the variables nor the interactions had a significant effect on the social levels of zebra finches. Thus, we choose to not reject the null hypothesis and conclude that acoustic enrichment does not affect the frequency of social behavior.
Assessing the most appropriate acoustic enrichment for a particular species requires for a study to be performed on the targeted species instead of applying the results from a different species. In this study, it was found out that acoustic enrichment does influence the frequency of fear behavior and not social behavior. However, the result differs with the results of Williams et al. (2017) which found out that preening (a social behavior) increased across all six treatment unlike in this study where the social behavior was not affected in any of the three treatments. Conversely, the results could be compared with the results of Robbins & Margulis (2004) which found out that acoustic enrichment led to an increase in flight and vocalization behavior. The behavior in flight and vocalization can be linked to the factor of fear in which a lack of it leads to complacency among the birds while the presence of it leads to the bird being in a panic.
From the results, it can be seen that more research need to be carried out on zebra finches to determine a consistent result. Future researchers may opt to replicate these finding by including more sample into their research. Consequently, they should expand their focus from just the three acoustic sound type and include more similar to Robbins & Margulis (2016) research.
References:
Abram, D., 2012. The spell of the sensuous: Perception and language in a more-than-human world. Vintage.
Barcellos, H.H., Koakoski, G., Chaulet, F., Kirsten, K.S., Kreutz, L.C., Kalueff, A.V. and Barcellos, L.J., 2018. The effects of auditory enrichment on zebrafish behavior and physiology. PeerJ, 6, p.e5162.
Davey, G., 2006. Relationships between exhibit naturalism, animal visibility and visitor interest in a Chinese Zoo. Applied Animal Behaviour Science, 96(1-2), pp.93-102.
Fenwick, N., Griffin, G. and Gauthier, C., 2009. The welfare of animals in science: How the “Three Rs” ethic guides improvements. The Canadian Veterinary Journal , 50 (5), p.523.
Kogan, L.R., Schoenfeld-Tacher, R. and Simon, A.A., 2012. Behavioral effects of auditory stimulation on kenneled dogs. Journal of Veterinary Behavior: Clinical Applications and Research, 7(5), pp.268-275.
Leone, E.H. and Estevez, I., 2008. Economic and welfare benefits of environmental enrichment for broiler breeders. Poultry Science, 87(1), pp.14-21.
Mello, C.V., 2014. The zebra finch, Taeniopygia guttata: an avian model for investigating the neurobiological basis of vocal learning. Cold Spring Harbor Protocols.
Nager, R.G. and Law, G., 2010. The zebra finch. The UFAW handbook on the care and management of laboratory and other research animals, pp.674-685.
Nielsen, B.L., 2018. Making sense of it all: The importance of taking into account the sensory abilities of animals in their housing and management. Applied Animal Behaviour Science.
Robbins, L. and Margulis, S.W., 2014. The effects of auditory enrichment on gorillas. Zoo biology, 33(3), pp.197-203.
Robbins, L. and Margulis, S.W., 2016. Music for the birds: effects of auditory enrichment on captive bird species. Zoo biology, 35(1), pp.29-34.
Snowdon, C.T., Teie, D. and Savage, M., 2015. Cats prefer species-appropriate music. Applied Animal Behaviour Science, 166, pp.106-111.
Swann, W.J., 2006. Improving the welfare of working equine animals in developing countries. Applied Animal Behaviour Science, 100(1-2), pp.148-151.
Wallace, E.K., Kingston?Jones, M., Ford, M. and Semple, S., 2013. An investigation into the use of music as potential auditory enrichment for moloch gibbons (Hylobates moloch). Zoo biology, 32(4), pp.423-426.
Wells, D.L., 2009. Sensory stimulation as environmental enrichment for captive animals: a review. Applied Animal Behaviour Science, 118(1-2), pp.1-11.
Wells, D.L., Coleman, D. and Challis, M.G., 2006. A note on the effect of auditory stimulation on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science, 100(3-4), pp.327-332.
Williams, I., Hoppitt, W. and Grant, R., 2017. The effect of auditory enrichment, rearing method and social environment on the behavior of zoo-housed psittacines (Aves: Psittaciformes); implications for welfare. Applied Animal Behaviour Science, 186, pp.85-92.
Yeates, J.W. and Main, D.C., 2008. Assessment of positive welfare: a review. The Veterinary Journal, 175(3), pp.293-300.
Young, R.J., 2013. Environmental enrichment for captive animals. John Wiley & Sons.
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