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Encouraging natural vibrissae movements in California sea lions (Zalophus californianus) using fish-catching as an

enrichment behaviour

Rachael Saxon14006064

BSc (Hons) BiologyFull Time

2017Field Based

Project Supervisor: Dr. Robyn Grant

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Contents

Abstract……………………………………………………………………………………………3

Introduction………………………………………………………………………………………4

Methods…………………………………………………………………………………………..6

Results…………………………………………………………………………………………….9

Discussion………………………………………………………………………………………14

Acknowledgments……………………………………………………………………………..18

References………………………………………………………………………………………19

�3Abstract

The welfare of captive marine mammals has become more of a concern in the eyes of the public in recent years. Enrichment is believed to improve the welfare of captive animals. The present study aims to mimic naturalistic behaviours of California sea lions (Zalophus californianus) using fish-catching as a behavioural enrichment device. The current study used three California sea lions which are housed at Blackpool Zoo to discover if fish-catching generated species-appropriate vibrissae, or whisker, movements. The results suggest that fish-catching does elicit the naturalistic whisker movements in the sea lions, however, all three sea lions did not generate the same response suggesting that the movements of the whiskers are dependent on the individual. This study has implications for zoological institutions that house California sea lions and can also provide an insight into developing new behavioural enrichment devices not just for captive California sea lions, but also for other captive species.

�4Introduction

In recent years the welfare of captive marine mammals has been called into question. A very public dispute between SeaWorld and Occupational Safety and Health Administration (OSHA) after the death of a high profile trainer, has caused the release of several books; Death at SeaWorld, Beneath the Surface (Kirby 2012, Hargrove and Chua-Eoan 2015), and an extremely popular documentary, Blackfish, that have populated the public eye causing more doubts to be raised about the welfare of not just captive whales and dolphins, but rather all marine mammals.

In order to better understand how to improve the welfare of captive California sea lions (Zalophus californianus) this study looked at producing naturalistic whisker movements using fish-catching as an enrichment behaviour. Whiskers, or vibrissae, function as tactile receptors and are used when sea lions hunt in the wild (Berta, Sumich et al. 2005). However, most research into whiskers has been carried out in phocids (Dehnhardt and Kaminski 1995, Dehnhardt, Mauck et al. 2001, Hanke, Wieskotten et al. 2013).

The Dehnhardt and Kaminski (1995) study looked at the sensitivity of mystacial whiskers of harbour seals when actively touching different sized objects. This particular study found that the seals could differentiate between different sized objects using just their whiskers. The Dehnhardt, March et al. (2001) study found that harbour seals were amazingly capable of following hydrodynamic trails generated by a miniature submarine.An issue with all these studies is that although harbour seals and California sea lions are closely related they are not the same species and do not exhibit the same behaviours or lifestyles, and therefore, the results from these studies may not apply to California sea lions.

For this reason, sea lions were used in the present study to discover if the results of the previous research on phocids could also be generalised to other pinnipeds such as the California sea lion. Whiskers were selected as the object of the present study as they are widely studied as a model of sensing (Mitchinson, Martin et al. 2007) and are part of the sea lions’ natural wild behaviour (Berta, Sumich et al. 2005).

It is well known that stress can cause a range of issues such as impairing immune function and suppressing reproductive function, as well as causing abnormal behaviours (Moberg

�5and Mench 2000). Reducing stress has been shown to improve the behaviour and welfare of animals in captive environments (Line, Markowitz et al. 1991, Carlstead, Brown et al. 1993).

The main aim of the present study is to discover if fish-catching elicited naturalistic whisker movements in three captive California sea lions housed at Blackpool Zoo. This was done by recording the movement of the sea lions when catching an incoming fish to observe the movements of the whiskers and head in relation to the fish.

�6Methods

AnimalsThe present study was conducted at the Active Oceans Arena in Blackpool Zoo, using three of the California sea lions (Zalophus californianus) that are housed there. The three sea lions used were Gina (female, 15 years old), Anya (female, 11 years old) and Elmo

(male, 8 years old). Gina and Anya are full sisters whereas Elmo is not related. The fish catching behaviour is natural to the sea lions as it is a currently used feeding method; therefore, no new behaviours were trained for the study. Furthermore, there were no sensory restrictions to the sea lions during the study; i.e. the sea lions were not blindfolded or made to wear a whisker sock, which were methods used in previous studies (Dehnhardt, Mauck et al. 2001, Gläser, Wieskotten et al. 2011, Hanke, Wieskotten et al. 2013) as a result there was no undue stress caused to the animals.

ApparatusThe sea lions were instructed to rest on their normally assigned platforms (Fig.1), which allowed their forelimbs to be raised. Fish were thrown to the sea lions individually after they performed a behaviour correctly so as to not affect their existing training. Filming took place inside

the main public display area of the Active Oceans Arena. The recordings were taken by hand to allow the camera to follow the movement of the sea lions. The positioning

Fig 2. Whisker tracking points

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Fig 1. a) Gina on her assigned platform b) Anya on her assigned platform c) Elmo on his assigned platform

�7of the camera allowed the whiskers to be viewed from the front of the subject. Recordings were taken on a waterproof GE DV1 Pocket Digital Camcorder (HD 1080p). This particular camera was chosen to reduce blurring during whisker movements.

Experimental proceduresThe three sea lions involved in the study were already desensitised to the recording apparatus due to previously partaking in a prior study (Milne and Grant 2014). The recordings were taken during showtimes as the fish catching is a natural part of public displays, and therefore the sea lions were not required to perform extra behaviours for the sole purpose of this study.

Video selection and analysisAll clips were examined to check their suitability for analysis. The videos required three characteristics in order to be suitable: i) all the whiskers needed to be visible throughout the entire clip. ii) enough lighting throughout the clip to see all the whiskers. iii) whiskers were defined and not blurred for the duration of the clip. There were a total of 117 videos (32 for Anya, 47 for Gina and 38 for Elmo) each with several catches per video. After examination, 10 clips were selected for each sea lion, meaning there were a total of 30 catches to be analysed. Each video was manually tracked using Manual Whisker Annotator (MWA) (Hewitt, Yap et al. 2016). Two whiskers were tracked on either side of the sea lion’s muzzle as well as the tip of the nose and middle of the upper jaw, and also the incoming fish. The whiskers that were tracked were the second from the front and the second from the back on each side of the muzzle. Three points were tracked on each whisker; the tip, the midpoint of the whisker and the root of the whisker, meaning there were 15 points in total tracked (Fig.2).Whisker offset is the mean whisker angle, which is calculated as the average of all the whisker positions on each side of the muzzle. Whisker amplitude is the difference between the maximum and minimum whisker positions and whisker asymmetry is calculated as the difference between the left and right whisker positions.

Statistical considerationsA Shapiro-Wilk test was carried out on all the results to discover if they are normally distributed or not. Following this a Kruskal-Wallis test was used to confirm these results and to discover whether we can confirm our hypothesis that the whiskers of the sea lions are affected by the incoming fish which they are receiving. To compare head orientation to

�8fish orientation and whisker asymmetry to fish orientation, a Wilcoxon Rank Sum Test was carried out. In order to provide a more in depth analysis of head orientation and whisker asymmetry compared to fish orientation, a Spearman’s rank correlation test was also carried out.

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Results

Sea lions exhibit differences between individuals when using whiskers during fish-catching.

Elmo had the smallest range of difference between his left and right whiskers for mean whisker offset (37.5°), whereas Gina had the highest range (50.5°) (Fig. 3). For mean

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Fig. 3. a) Boxplot of mean whisker offset (degrees) showing left and right whisker averages of the three sea lions. b) Boxplot of mean whisker amplitude (RMS) showing left and right whisker averages of the three sea lions. c) Boxplot of whisker curvature (degrees) showing left and right whisker averages of the three sea lions. d) Boxplot of mean whisker offset (degrees) showing the difference between the left and right whiskers of the three sea lions. e) Boxplot of mean whisker amplitude (RMS) showing the difference between left and right whiskers of the three sea lions.

�10whisker amplitude Elmo had the lowest range between the left and right whiskers (5.8°), whereas Anya had the largest (28.4°) (Fig.3).

In two of the three sea lions, the left whiskers had lowest average whisker offset (Anya left whiskers = 57.2°, Anya right whiskers = 63.3°; Elmo left whiskers = 106.6°, Elmo right whiskers = 118. 5°), which was mainly the side of the head that the incoming fish was appearing from in those two sea lions. However, Gina was the exception to this trend (left whiskers = 81.4°, right whiskers = 75.5°) (Fig. 3).

There were similar results for average whisker amplitude of the left and right whiskers. Again, Anya and Elmo had a lower average for the left whiskers in comparison to the right whiskers (Anya left whiskers = 26.9°, Anya right whiskers = 29.7°; Elmo left whiskers = 8.7°, Elmo right whiskers = 11.7°) Again, Gina was the exception to the trend (left whiskers = 18.6°, right whiskers = 17.3°) (Fig. 3).

The results for the Shapiro tests showed that the distribution of left and right whiskers for mean amplitude were not significantly different from normal (W = 0.94006, p-value = 01007; W = 0.90893, p-value = 0.01614 respectively). However, the distribution of the left minus the right whiskers was significantly different from normal (W = 0.73548, p-value = 7.086e-06).

There were similar findings from the Shapiro tests for mean offset, with both the left and right whiskers not being significantly different from normal (W = 0.9303, p-value = 0.05599; W = 0.9599, p-value = 0.3269 respectively) whereas, again the left minus right whiskers did have a distribution that was significantly different from normal (W = 0.80804, p-value = 0.0001168).

Sea lions use their whiskers as guidance during fish-catching behaviours.

The Kruskal-Wallis test showed that the whisker amplitude results were significantly different from normal when testing both the left and right whiskers, and so are not normally distributed, therefore we reject the null hypothesis and can say that the sea lion’s whiskers were affected by the incoming fish.Kruskal-Wallis chi-squared = 65.409, df= 3, p-value < 0.0001.

�11However, a Kruskal Wallis test showed that the results for the left minus right whiskers didn’t show a significant difference between the three sea lions (Kruskal-Wallis chi-squared = 2.2995, df = 2, p-value = 0.3167).

Another Kruskal-Wallis test showed that the whisker offset results for left and right whiskers were also significantly different from normal and were also not normally distributed. The sea lions whisker’s were also affected by the incoming fish.Kruskal-Wallis chi squared = 65.49, df = 3, p-value < 0.0001.However, when a Kruskal-Wallis test was run to compare the left minus right whiskers of all three sea lions, the results showed that the distribution wasn’t significantly different from normal and so there isn’t a difference in distribution between the three sea lions (Kruskal-Wallis chi-squared = 0.41931, df = 2, p-value = 0.8109).

Further Shapiro-Wilk tests were carried out on fish orientation, head orientation and whisker asymmetry and showed that all these results were differed significantly from

Fig 4. a) Scatterplot of fish orientation (degrees) against whisker asymmetry (degrees). b) Scatterplot of fish orientation (degrees) against head orientation (degrees). c) Line plot of head orientation (degrees), fish orientation (degrees) and whisker asymmetry (degrees) for all clips analysed. All three plots are showing Anya’s results.

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�12normal (w = 0.93786, p-value = 0.003305, w = 0.8931, p-value = 5.0473-05, w = 0.86425, p-value = 5.295e-06, respectively).

Whisker asymmetry has a stronger correlation to fish orientation than head orientation.

A Wilcoxon Rank Sum Test was carried out on Anya’s results for fish orientation, head orientation and whisker asymmetry. When comparing head orientation to fish orientation, the results showed significance (w = 1760, p-value = 0.2744). However, when comparing fish orientation to whisker asymmetry the results showed no significance (w = 161, p-value < 0.0001) (Fig. 4).

Anya was the only sea lion who didn’t show a significant result between fish orientation and whisker asymmetry. Gina had a higher significance when comparing fish orientation and whisker asymmetry (w = 2004, p-value < 0.0001) than when comparing fish orientation and head orientation (w = 1632, p-value < 0.0001) (Fig. 5).

Fig 5. a) Scatterplot of fish orientation (degrees) against head orientation (degrees). b) Scatterplot of fish orientation (degrees) against whisker asymmetry (degrees). c) Line plot of head orientation (degrees), fish orientation (degrees) and whisker asymmetry (degrees) for all clips analysed. All three plots are showing Gina’s movements.

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Elmo had similar results to Gina, with a higher significance for fish orientation and whisker asymmetry (w = 3108, p-value < 0.0001) than fish orientation and head orientation (w = 2785, p-value < 0.0001) (Fig. 6).

The Spearman’s rank correlation test showed that Anya was the only sea lion who had a significant result when comparing fish orientation to head orientation. Anya showed a positive correlation of 0.285%. Although all the sea lions didn’t show a significant result, the correlations were stronger for whisker asymmetry to fish orientation than head orientation to fish orientation.

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Fig 6. a) Scatterplot of fish orientation (degrees) against head orientation(degrees). b) Scatterplot of fish orientation (degrees) against whisker asymmetry (degrees). c) Line plot of head orientation (degrees), fish orientation (degrees) and whisker asymmetry (degrees) for all clips analysed. All three plots are showing Elmo’s results.

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Discussion

The above results, although very mixed, show that the sea lions moved their whiskers at different angles, amplitudes and symmetries. Also, they also show that the orientation of the fish is more correlated to whisker asymmetry than it is to head orientation. When viewing the results without the use of statistical tests, there appeared to be a large difference between the sea lions. Furthermore, when a Kruskal-Wallis test was used, it showed that there was a difference between the sea lions when looking at their left and right whiskers separately rather than the asymmetry between them. Wilcoxon Rank Sum Tests showed that for Gina and Elmo there was a higher significance when comparing fish orientation to whisker asymmetry than when comparing fish orientation to head orientation. suggesting that the whiskers are providing the sensory information to enable the sea lions to catch the fish rather than the head. This is confirmed by another study that showed that whisker movements are more responsible for whisker positioning in sensorimotor tasks than the movements of the head (Milne and Grant 2014). However, Anya showed no significance when comparing fish orientation to whisker asymmetry but she did show a small significance when comparing fish orientation to head orientation. This suggests that most sea lions use their whiskers to guide objects such as fish into their mouths. However, this can not be generalised to all sea lions as Anya proved there are exceptions.

Being able to guide fish into their mouths is a vital skill for sea lions as it allows them to hunt for prey (Stephens, Beebe et al. 1973), the same is also true for other pinnipeds such as seals (Riedman 1990, Hyvarinen, Palviainen et al. 2009). Animals can actively regulate the movements and positions of their sensory organs to improve the quality of the sensory information they are receiving (Grant, Mitchinson et al. 2009). Therefore, vibrissae are an extremely important sensory system for pinnipeds; the whiskers are also possibly more of a sensing organ than eyes for certain phocids. The ringed seal (Pusa hispida saimensis) of Lake Saimaa in Finland has blind individuals that are otherwise healthy (Hyvärinen 1989). Dehnhardt and Kaminski (1995) suggest that Harbor seals can use their mystacial whiskers as efficiently as monkeys use their hands for active touch. Studies have shown that pinnipeds such as seals and sea lions follow hydrodynamic trails, created by the

�15movement of fish, as an important hunting strategy (Dehnhardt, Mauck et al. 2001). When comparing the California sea lion to the Harbor seal Gläser et al. (2011) discovered that although sea lions have non-specialised whiskers when compared to Harbor seals, they were still able to perform to a high level when following hydrodynamic trails. Hanke et al. (2013) found that sea lions are more sensitive to local water movements, or dipole stimuli, than Harbor seals.

Previous studies have shown that dynamic sensorimotor tasks have encouraged more whisker movements in California sea lions (Milne and Grant 2014) and if whisker movements are a natural behaviour of the sea lions (Gläser, Wieskotten et al. 2011) then these dynamic tasks are providing more enrichment to the captive sea lions. However, this particular study used ball-balancing as the enrichment behaviour; although this elicited intense whisker movements from the sea lions, ball-balancing is not a naturalistic behaviour that the sea lions would encounter in the wild.

The study by Milne and Grant (2014) found that the whiskers responded to the movement of the ball quicker than the head responded; the mean lag for the whiskers was 26.70ms, while the mean lag for the head was 129.03ms. This is similar to the current study as the whiskers are more responsive to the incoming fish than the head is. Furthermore, the Milne and Grant (2014) study also found similar differences between individuals. Their results stated that Anya also had the largest whisker amplitudes; 120° on the large ball whereas Gina and Elmo both had amplitudes under 100°, similar to the present study.

Providing more enrichment is a important aspect for any zoological institution to improve the welfare of the animals housed there (Markowitz and LaForse 1987, Forthman, Elder et al. 1992). Although studies have found that California sea lions have adapted well to life in captivity (Roberts and Demaster 2001), these studies also found that the ability of sea lions to survive and reproduce in captivity varied between institutions. Furthermore, certain studies have shown that captive pinnipeds have a higher level of illness than wild colonies. Forshaw and Phelps (1991) found that tuberculosis was more common in captive colonies than wild colonies of pinnipeds; while Dunn, Buck et al. (1984) also found that there were higher rates of candidiasis in captive pinnipeds.

Previous studies have shown that enrichment decreases levels of cortisol or improves the function of the immune system. Line, Markowitz et al. (1991) found that by adding

�16manipulable devices to simplistic cages of adult, laboratory-housed rhesus macaques lowered cortisol concentrations to basal levels and also decreased abnormal behaviour. However, although this study shows that lowering cortisol concentrations lowered the incidence of abnormal behaviours, it occurred in using laboratory-housed animals which live in a different type of environment to the captive sea lions using in the present study. A study showed similar results in a zoo environment (Carlstead, Brown et al. 1993). Carlstead, Brown et al. (1993) showed that captive leopard cats (Felis bengalensis) had chronically elevated levels of cortisol when housed in the same building as tigers and lions. These levels dropped to baseline levels and stereotypical pacing decreased when the leopards were provided with a variety of hiding places and a mix of vegetation in their enclosures. An issue with these studies is that they are altering the living area of the captive individuals to provide enrichment, whereas the present study is using a behaviour to provide a physical enrichment.

There have been studies that have used more dynamic tasks to study whisker movements in seals and sea lions. Dehnhardt, Mauck et al. (2001) used a miniature ‘submarine’ that moved through the water allowed the seals to follow its hydrodynamic trail. The blindfolded seals could accurately follow the trail generated by the submarine. Gläser, Wieskotten et al. (2011) also did a similar study, however Gläser et al. studied California sea lions. Although, sea lions have non-specialised whiskers when compared to Harbor seals, the sea lions still revealed a good performance in following the hydrodynamic trails.

There have also been studies that have used more naturalistic enrichment in an ex-situ conservation environment. Markowitz and LaForse (1987) used artificial prey as an enrichment device for felines. In this study they used an artificial prey that allowed the servals (Felis serval) to physically ‘capture’ the prey. This generated species-specific behaviours. The issue with this study is that there was no link between whether these species-appropriate behaviours improved the welfare of the felines.

Smith and Litchfield (2010) carried out a case study that links the above aspects together. In their study they measured the amount of time the two Australian sea lions (Neophoca cinerea) spent engaged in pattern swimming to test the effectiveness of environmental enrichment. This study found that the male sea lion’s incidence of pattern swimming dropped from 45% to 25% when enrichment was introduced. On the other hand, the female sea lion showed no change. However, both the male and female sea lion did

�17exhibit more active behaviours when the enrichment was introduced to the environment. The study by Smith and Litchfield (2010) ties in with the present study because it showed that there are differences between individuals similar to the present study wherein one of the three sea lions studied did not show that the whiskers moved in response to the incoming fish.

For future research perhaps the best approach to examine the welfare of captive California sea lions, would be to use artificial prey as behavioural enrichment such as in the study by Carlstead, Brown et al (1993). This would provide the most naturalistic enrichment experience for the sea lions. Furthermore, it would then be appropriate to determine whether the introduction of the naturalistic enrichment decreases the concentration of cortisol in the sea lions when compared to sea lions before the enrichment was introduced. The reduction of cortisol signifies a decrease in stress, which then could lead to an improvement in welfare and health of the sea lions. This is important for not only zoological institutions but also for conservation. Increasing the welfare of the sea lions should improve the lifespan of the individuals involved. In addition to this, it is also possible that by mimicking natural hunting behaviours, if the captive individuals are required to be released into the wild then they should be more capable of living as a wild individual would. This could be vital for conservation as captive colonies could then replenish wild colonies if their numbers dramatically or rapidly drop. In this case, captive individuals could act as a reserve population that can help to restore biodiversity if the situation calls for it.

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AcknowledgmentsI would like to extend my greatest thanks to Alyx Milne for providing access to the fish-catching videos; and also to Robyn Grant for all her support throughout the duration of the project.

�19Berta, A., J. L. Sumich and K. M. Kovacs (2005). Marine mammals: evolutionary biology, Academic Press.Carlstead, K., J. L. Brown and J. Seidensticker (1993). "Behavioral and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis)." Zoo Biology 12(4): 321-331.Carlstead, K., J. L. Brown and W. Strawn (1993). "Behavioral and physiological correlates of stress in laboratory cats." Applied Animal Behaviour Science 38(2): 143-158.Dehnhardt, G. and A. Kaminski (1995). "Sensitivity of the mystacial vibrissae of harbour seals (Phoca vitulina) for size differences of actively touched objects." Journal of Experimental Biology 198(11): 2317-2323.Dehnhardt, G., B. Mauck, W. Hanke and H. Bleckmann (2001). "Hydrodynamic trail-following in harbor seals (Phoca vitulina)." Science 293(5527): 102-104.Dunn, J. L., J. D. Buck and S. Spotte (1984). "Candidiasis in captive pinnipeds." J. Am. Vet. Med. Assoc 185: 1328-1330.Forshaw, D. and G. Phelps (1991). "Tuberculosis in a captive colony of pinnipeds." Journal of Wildlife Diseases 27(2): 288-295.Forthman, D. L., S. D. Elder, R. Bakeman, T. W. Kurkowski, C. C. Noble and S. W. Winslow (1992). "Effects of feeding enrichment on behavior of three species of captive bears." Zoo Biology 11(3): 187-195.Gläser, N., S. Wieskotten, C. Otter, G. Dehnhardt and W. Hanke (2011). "Hydrodynamic trail following in a California sea lion (Zalophus californianus)." Journal of Comparative Physiology A 197(2): 141-151.Grant, R. A., B. Mitchinson, C. W. Fox and T. J. Prescott (2009). "Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration." Journal of neurophysiology 101(2): 862-874.Hanke, W., S. Wieskotten, C. Marshall and G. Dehnhardt (2013). "Hydrodynamic perception in true seals (Phocidae) and eared seals (Otariidae)." Journal of Comparative Physiology A 199(6): 421-440.Hargrove, J. and H. Chua-Eoan (2015). Beneath the Surface :  Killer Whales, SeaWorld, and the Truth Beyond Blackfish, St Martin's Press.Hewitt, B., M. H. Yap and R. Grant (2016). "Manual Whisker Annotator (MWA): A Modular Open-Source Tool." Journal of Open Research Software 4(1).Hyvärinen, H. (1989). "Diving in darkness: whiskers as sense organs of the ringed seal (Phoca hispida saimensis)." Journal of Zoology 218(4): 663-678.Hyvarinen, H., A. Palviainen, U. Strandberg and I. J. Holopainen (2009). "Aquatic Environment and Differentiation of Vibrissae: Comparison of Sinus Hair Systems of Ringed Seal, Otter and Pole Cat." Brain Behavior and Evolution 74(4): 268-279.Kirby, D. (2012). Death at SeaWorld :  Shamu and the Dark Side of Killer Whales in Captivity, St Martin's Press.Line, S. W., H. Markowitz, K. N. Morgan and S. Strong (1991). "Effects of cage size and environmental enrichment on behavioral and physiological responses of rhesus macaques to the stress of daily events."Markowitz, H. and S. LaForse (1987). "Artificial prey as behavioral enrichment devices for felines." Applied Animal Behaviour Science 18(1): 31-43.Milne, A. O. and R. A. Grant (2014). "Characterisation of whisker control in the California sea lion (Zalophus californianus) during a complex, dynamic sensorimotor task." Journal of Comparative Physiology A 200(10): 871-879.Mitchinson, B., C. J. Martin, R. A. Grant and T. J. Prescott (2007). "Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact." Proceedings of the Royal Society of London B: Biological Sciences 274(1613): 1035-1041.Moberg, G. P. and J. A. Mench (2000). The biology of animal stress: basic principles and implications for animal welfare, CABI.

�20Riedman, M. (1990). The pinnipeds: seals, sea lions, and walruses, Univ of California Press.Roberts, S. P. and D. P. Demaster (2001). "Pinniped survival in captivity: annual survival rates of six species." Marine Mammal Science 17(2): 381-387.Smith, B. P. and C. A. Litchfield (2010). "An empirical case study examining effectiveness of environmental enrichment in two captive Australian sea lions (Neophoca cinerea)." Journal of Applied Animal Welfare Science 13(2): 103-122.Stephens, R., I. Beebe and T. Poulter (1973). "Innervation of the vibrissae of the California sea lion, Zalophus californianus." The Anatomical Record 176(4): 421-441.

�21With the exception of any statements to the contrary, everything presented in this report are the

result of my own efforts. No parts of this report have been copied from other sources (or have been cited explicitly if so). I understand that any evidence of plagiarism and/or the use of

unacknowledged third party data will be dealt with as a very serious matter. This work has not been submitted previously in any form to Manchester Metropolitan University or to any other institution

for assessment or any other purpose.

Signed................................................................... Date.............................