Stress-induced Behaviour in Rams of Three Different Sheep (Ovis aries) Breeds: Indicator of Welfare?
STRESS-INDUCED BEHAVIOUR IN RAMS OF THREE
DIFFERENT SHEEP (Ovis aries) BREEDS: INDICATOR OF
WELFARE?
SAMANTHA E. C. ENGELDAL
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
DECLARATION OF AUTHENTICITY
I, Samantha E. C. Engeldal, hereby declare that all information in this
document entitled:
‘STRESS-INDUCED BEHAVIOUR IN RAMS OF THREE DIFFERENT
SHEEP (Ovis aries) BREEDS: INDICATOR OF WELFARE?’
has been obtained and presented in accordance with academic rules and
ethical conduct. I also solemnly declare that this thesis was composed by myself
through guidance of my supervisory committee. This work has not been submitted
for the awards of any other academic degree, diploma, certificate or other
professional qualification except as specified. As required by academic rules, all
material and results that are not original to this work have been clearly and fully
cited and referenced.
Bogor, December 2012
Samantha E.C. Engeldal
NRP D151118051
ABSTRACT
SAMANTHA E.C. ENGELDAL. Stress-induced Behaviour in Rams of Three
Different Sheep (Ovis aries) Breeds: Indicator of Welfare? Under supervision of
RONNY RACHMAN NOOR and SUBANDRIYO.
Growing importance of and concern for the welfare of farm animals within
production systems has been the basis for an enormous amount of scientific
studies. The goal of the present study was to investigate whether both vocal and
social behaviour of sheep, under specific stress-inducing situations, could be used
as an indicator of the animals’ welfare status. Two separate experiments were
carried out with 2-3 year old adult rams. The animals were of three breeds,
namely Barbados Blackbelly Cross, Local Garut and Composite Garut. In the first
experiment twelve clinically healthy animals, four from each breed, were
subjected to three different levels of social isolation. The animals were held
completely alone, in the presence of a human and alone in a group pen adjacent to
a pen with conspecifics. During the isolation sessions both vocal and locomotive
behaviour of each animal were recorded. The recorded calls were acoustically
analyzed using specialized acoustic software. The results showed that the levels of
isolation were characterized by very specific behavioural responses with an
increased amount of locomotor activity and vocalization in partially isolated
animals. The animals that were completely isolated showed a higher amount of
inactive behaviour. No specific differences were found in the behaviour of
animals that were held completely alone and the ones which were in the presence
of a human observer. Acoustic analysis of the recorded calls showed significant
differences in a number of temporal and structural features. Spectral analysis
revealed the most notable differences in the amount of sound energy integrated in
the calls. Differences were found in both locomotive and vocal behaviour based
on isolation level and breed. The second experiment focused on the effect of
stocking density on the social behaviour of newly regrouped rams. Thirty-six
animals were subjected to three different stocking density levels, namely low (3.2
m2/ram), medium (1.6 m2/ram) and high (0.8 m2/ram). Recorded data consisted of
frequencies of agonistic-, exploratory, locomotive-, aberrant-, inactive-, self-care-,
mating- and vocal behaviour. The results of this experiment showed that the
animals responded differently to the different stocking density levels. The highest
stocking density level was characterized by the highest number of inactive
behaviour and the lowest number of locomotor activity. There were also
significant differences found in the frequency of displayed behaviours based on
the amount of time the animals had spent within the new group settings. The
amount of agonistic-, mating- and exploratory behaviour was found to be
significantly higher on the day of regrouping as compared to the level of these
behaviours on the day after regrouping. Significant differences were also found in
the behavioural response of animals from different breeds. The results from both
experiments thus lead us to conclude that both vocal- and social behaviour of rams
are able to provide humans with important information on their affective state
which may be helpful in the design of production systems that are beneficial to the
animals their welfare.
Keywords: vocalization, behaviour, stress, sheep, animal welfare
SUMMARY
SAMANTHA E.C. ENGELDAL. Stress-induced Behaviour in Rams of Three
Different Sheep (Ovis aries) Breeds: Indicator of Welfare? Under supervision
of RONNY RACHMAN NOOR and SUBANDRIYO.
Animal domestication has played a central role in the development of
human civilization. Modern animal production systems are principally
characterized by a larger number of farm animals which are kept together in
reduced space. A great number of the management practices which are currently
applied in intensive systems along with the conditions under which the animals
are kept, are thought to have a negative influence on both physiological and
production traits of the animals. The perception that humans have a moral
obligation to ensure that the animals their welfare, which is thought to be the
extent to which the animals are able to successfully adapt to their environment, is
never excessively poor has become widespread. The attempts of an animal to cope
to its environment and the results of failure to cope can be measured. This
meaning that the welfare of an individual animal can be assessed in scientific
ways using different types of indicators. An appreciation of how to handle animals
appropriately necessitates knowledge of their behaviour.
The purpose of this study was to evaluate both vocal- and social
behavioural response of different breeds of sheep to situations which have been
found to be very stressful for this gregarious species, in an attempt to discover
non-invasive ways that might reveal information on the animals’ affective state. It
was also intended to discover whether the animals would differ in their
behavioural response based on their breed.
The research consisted of two separate experiments. A total of forty-eight
rams from three different sheep breeds were used throughout the entire study. The
following breeds were included: Barbados Blackbelly Cross (BC) (50% Local
Sumatera, 50% Barbados Blackbelly), Local Garut (LG) and Composite Garut
(KG) (50% Local Garut, 25% St. Croix, 25% Moulton Charollais). In the first
experiment twelve clinically healthy, 2-3 year old adult sheep were subjected to
different levels of social isolation. Each individual animal was kept alone without
visual- and tactile contact with conspecifics, kept in the presence of an observer
without visual – and tactile contact with conspecifics, and kept alone in a group
pen at a specific distance from conspecifics with whom visual-, acoustic- and
olfactory contact was possible. During a maximum of 15 minutes both vocal and
locomotive behaviour were recorded. High-pitched bleats were recorded using a
Digital Voice Recorder after which the calls were acoustically analyzed using the
acoustic software program Raven Pro 1.4. Thirty-six acoustic parameters were
calculated after which their values were subjected to statistical analysis.
Frequencies of locomotive behaviours were observed and recorded during 5
minutes per isolation session using a predefined ethogram.
For the second experiment thirty-six, clinically healthy, 2-3 year old sheep
were used. Four animals from the same breed were grouped and held at three
different stocking densities, namely 3.2 m2/animal, 1.6 m2/animal and 0.8
m2/animal. Based on a predefined ethogram agonistic-, self-care-, exploratory-,
mating-, aberrant-, locomotive-, inactive, and vocal behaviour of each individual
animal were recorded on two consecutive days. Random scan sampling with scan
lengths of sixty seconds were used to gather the behavioural data. Behaviours
were observed for 30 minutes at four different times of day, namely 07.00 am,
09.30 am, 12.00 pm and 14.30 pm.
The results from the first experiment showed that the animals were more
active during partial isolation compared to complete isolation. The frequency of
locomotive behaviours and vocalizations during partial isolation was also found to
be higher compared to that during complete isolation. Significant effects of
isolation level and breed on both temporal and structural acoustic properties were
found. Amplitude, power and time acoustic properties were found to affect
acoustic quality of vocal responses to isolation, whereas frequency related
properties were also found to differ significantly (P < 0.05) between breeds. From
spectrogram analysis, the patterns of energy distribution within the calls proved to
offer the most distinctive difference between isolation levels and breeds. Calls
uttered during complete isolation were all identified by a higher level of noiseenergy compared to calls uttered during partial isolation. It was concluded that the
acoustic analysis of calls uttered during social isolation of adult rams revealed
information on the affective state of the animals. This was found to be
predominantly expressed by both temporal and structural variations in acoustic
cues within distress calls and to differ per breed.
The results of experiment 2 showed that agonistic behaviour was observed
at the highest frequency throughout the entire study. Stocking density was found
to have a significant effect on exploratory-, locomotive- and standing behaviour.
The effect of breed caused significant differences in agonistic-, self-care-,
aberrant- and mating behaviour. Significant differences were also found between
day 1 and day 2 of regrouping for agonistic-, exploratory, self-care- and mating
behaviour. These results led to the conclusion that the animals’ behavioural
response to regrouping and space allowance was characterized by specific patterns
and that the three breeds do differ in their reactions to novel situations. It is
believed that the animals their welfare might be compromised by housing them at
high stocking densities.
Keywords: vocalization, behaviour, stress, sheep, animal welfare
Copyright © IPB 2012
All Rights Reserved
This work is deposited at the university library to be made available to borrowers
under rules of the library. Brief quotations from this thesis are allowable provided
that accurate acknowledgment of the source is made. Request for this manuscript
in whole or in part may be granted by Bogor Agricultural University when in its
judgment the proposed use of the material will be beneficial for educational
purposes. In all other instances, however, no part or all of this thesis may be
reproduced or transmitted in any form or by any means.
STRESS-INDUCED BEHAVIOUR IN RAMS OF THREE
DIFFERENT SHEEP (Ovis aries) BREEDS: INDICATOR OF
WELFARE?
SAMANTHA E.C. ENGELDAL
A thesis sumbitted to the Graduate School
of Bogor Agricultural University
in partial fullfillment of the requirements for the degree
Master of Science
in the Department of
Animal Science and Production Technology
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
External examiner: Prof. Dr. Ir. Cece Sumantri, M. Agr. Sc.
ACKNOWLEDGEMENTS
A profound and genuine love for animals together with the increasing
importance of animal welfare within the modern farming industry, were the
motivation for investigating the way in which farm animals behave in stressful
situations. By using animal behaviour as an indicator of the animals’ affective
state, an attempt can be made to create such farming environments which support
their overall welfare.
My journey in pursuit of a Master of Science degree has been very
insightful, energized by numerous special moments. Each and every experience
which I have had throughout these past two years has led me to view life in an
entirely new light, of which an increased amount of respect for nature and its
perfect natural order is just one result. In short, my time spent in Indonesia can be
summed up by the words: ‘Without GOD, I am not’. Through HIS mercy I have
been blessed with Spiritual Guides and Ancestors who provide me with divine
insight, guidance and protection at all times. For this I am so grateful. THEY are
the sole reason for this achievement.
My parents have always encouraged me to pursue my dreams. I have been
blessed with a Mother who has always motivated and supported me throughout
my educational journey. The example she has set for me through her own life
fostered my enthusiasm and has also been the basis for all of the success I have
been fortunate to experience so far. My father instilled in me two traits: a strong
work ethic and to always strive for the best results. They have both taught me that
final victory ALWAYS comes to the one who stays connected and perseveres. For
this I am so grateful. I would not have reached this level had it not been for their
uninterruptible love, care, encouragement and prayer.
Words of gratitude are due to my family and friends for always taking an
interest in what I have been doing and offering me their much-valued support. I
would thank you from the bottom of my heart, but for you my heart has no
bottom.
I would also like to thank my head supervisor, Prof. Ronny Rachman
Noor. Without his willingness to take me under his supervision I might not have
had some of the wonderful experiences that I have had. He has provided me with
supreme counseling while exploring a topic that I am very passionate about. I am
thankful to him for his guidance, advice and encouragements throughout my
study. I have learned a lot from him during my research, which greatly increased
my skills in the field. His supervision challenged me intellectually and has helped
enrich my knowledge.
I would also like to acknowledge, Prof. Subandriyo for his support and
constructive criticism throughout this project.
I am sincerely thankful to Dr. Rarah R. A. Maheswari for pleasantly
welcoming me to the Department of Animal Science and Production Technology.
She has always treated me as a part of “her team” and has guided and advised me
whenever needed. I will always be grateful for the kindness and understanding she
has shown to me. Moreover, I will always remember the long, insightful talks we
have had in her laboratory.
My sincere appreciation is hereby offered to Dr. Eko Handiwirawan for
the help and encouragement given to me during the course of my research. Your
inexhaustible patience, excellent insight and support throughout my time spent in
Indonesia will always be greatly valued.
I am very grateful to everyone I have met at the Indonesian Research
Institute for Animal Production, especially the technicians who assisted me during
the collection of my data. The support and assistance received from Bapak
Sumantri, Pak. Koesma, Pak. Tohir, Pak. Njurjaja and Pak. Maplani in carrying
out my research will always be greatly appreciated.
I would like to convey my gratitude to all the staff at IPB for their
enormous and continuous support, patience and help throughout my study.
Finally, I would like to thank each and every person, not mentioned by
name, that I have met in Indonesia. Each word and experience has helped to
support, shape and form me in one way or another and for that I will always be
very grateful.
DEDICATION
This thesis is dedicated to all of the sheep that have participated in this
study. I will always have many fond memories of them. It is my sincere wish that
the results from this study will aid in improving their position within the animal
production industry.
AUTOBIOGRAPHY
The author was born in the month December in Paramaribo, Suriname.
After having finished all of the basic education levels, the author was admitted to
the Anton de Kom University of Suriname (ADEK). In the year 2009 the author
graduated with a Bachelor’s Degree in Animal Science.
In 2010 the author attained her teaching certificate for becoming a licensed
teacher. In that same year she was awarded a scholarship under the Developing
Countries Partnership Program to further her studies in Indonesia at Bogor
Agricultural University. The author successfully completed the Master’s program
in the Department of Animal Science and Production Technology in 2012.
TABLE OF CONTENTS
Page
LIST OF TABLES .......................................................................................... xiii
LIST OF FIGURES ........................................................................................ xiv
LIST OF APPENDICES ................................................................................. xv
GENERAL INTRODUCTION .......................................................................
Background to the Study .......................................................................
Purpose of the Study ..............................................................................
Significance of the Study .......................................................................
Hypothesis .............................................................................................
1
1
4
5
5
LITERATURE REVIEW ..............................................................................
Systematics and Distribution of Sheep ...................................................
Barbados Blackbelly Cross .....................................................................
Local Garut ............................................................................................
Composite Garut ....................................................................................
Importance of Animal Behaviour ...........................................................
Behaviour, Welfare and Environmental Design . ...................................
Motivation and Stress in Farm Animals .................................................
Relations of Vocalization to Animal Welfare .......................................
Vocalization Analysis ............................................................................
7
7
7
8
8
9
11
15
17
21
EFFECT OF DIFFERENT LEVELS OF SOCIAL ISOLATION
ON THE ACOUSTICAL CHARACTERISTICS OF
SHEEP VOCALIZATION .............................................................................
Abstract ..................................................................................................
INTRODUCTION .................................................................................
MATERIAL AND METHODS .............................................................
Location and Time of the Study ....................................................
Study Subjects and Housing..........................................................
Isolation Procedures ......................................................................
Recorded Behaviour .....................................................................
Bleat Recordings ...........................................................................
Bleat Analysis ...............................................................................
Data Analysis and Statistics ..........................................................
RESULTS AND DISCUSSION ............................................................
Behavioural Parameters.................................................................
Vocalization and Call Measures ..................................................
Breed Differences of Acoustic Structure of High Bleats ..............
CONCLUSIONS .....................................................................................
REFERENCES........................................................................................
23
23
24
27
27
27
27
28
29
29
34
35
35
41
45
53
55
IMPACT OF STOCKING DENSITY AND INFLUENCE OF
BREED ON THE BEHAVIOUR OF NEWLY REGROUPED
ADULT RAMS ...............................................................................................
Abstract ...................................................................................................
INTRODUCTION ..................................................................................
MATERIAL AND METHODS .............................................................
Location and Time of the Study ....................................................
Study Subjects and Housing ..........................................................
Experimental Setup and Procedure ..............................................
Behavioural Parameters .................................................................
Data Analysis.................................................................................
RESULTS AND DISCUSSION .............................................................
Behavioural Budget .......................................................................
Effect of Space Allowance on Behaviour of Rams ......................
Breed Effect ..................................................................................
Impact of Day of Regrouping on Ram Behaviour .........................
Vocal Behaviour ............................................................................
CONCLUSIONS .....................................................................................
REFERENCES ........................................................................................
61
61
62
65
65
65
65
66
68
69
69
70
72
75
78
81
83
GENERAL DISCUSSION .............................................................................. 87
RECOMMENDATIONS ................................................................................. 91
REFERENCES ................................................................................................ 93
APPENDICES ................................................................................................. 103
LIST OF APPENDICES
Page
1
Values of acoustic parameters based on isolation level ........................... 105
2
Values of acoustic parameters based on breed......................................... 106
3
ANOVA test results from the GLM procedure for comparison
of acoustic parameters for isolation level and breed ................................ 107
4
Output of Duncan’s multiple range test for isolation level ...................... 117
5
Output of Duncan’s multiple range test for breed ................................... 122
6
Output of Kruskall-Wallis test ................................................................. 126
7
Output of Mann-Whitney U test .............................................................. 129
8
Descriptive statistics for behavioural categories ..................................... 136
LIST OF TABLES
Page
1
An operational defination of animal welfare developed
in the Welfare Quality Project (Welfare Quality 2009) ......................... 12
2
Scheme for judging welfare indicators in animal management
and housing systems ............................................................................... 13
3
Experimental design of isolation procedures .......................................... 28
4
Frequencies of observed behaviours at different levels of isolation ...... 35
5
Breed differences in frequencies of observed behaviours
at different levels of isolation ................................................................. 37
6
Comparison of acoustic parameters of high-pitched bleats
at different levels of isolation ................................................................. 42
7
Comparison of acoustic parameters of high-pitched bleats
from different breeds ............................................................................. 46
8
Experimental design. Number of animals per breed group
and per stocking density ......................................................................... 66
9
Ethogram used for studying behaviour of rams at various
stocking densities ................................................................................... 67
10
Pooled behavioural categories ............................................................... 68
11
Frequencies of displayed behaviour at different
stocking densities ................................................................................... 70
12
Influence of breed on ram behaviour ..................................................... 72
13
Influence of day of regrouping on ram behaviour ................................. 76
LIST OF FIGURES
Page
1
Adult rams of the breeds Barbados Blackbelly Cross
and Local Garut .......................................................................................
8
2
Adult rams of the breed Composite Garut .............................................
9
3
Assessment of welfare and consequences of lack of welfare ................ 16
4
Neuronal, anatomical and functional elements of call
production in animals ............................................................................ 19
5
Frequency of locomotor activity by animals from different
breeds at different levels of social isolation ........................................... 39
6
Frequency of standing by animals from different breeds at
different levels of social isolation .......................................................... 40
7
Frequency of vocalizations per breed group at different levels
of social isolation .................................................................................... 41
8
Representative spectrographs of high-pitched bleats from the same
Barbados Blackbelly Cross ram while (A) completely alone,
(B) with observer and (C) partially isolated ........................................... 48
9
Representative spectrographs of high-pitched bleats from the same
Local Garut ram while (A) completely alone, (B) with observer
and (C) partially isolated ......................................................................... 49
10
Representative spectrographs of high-pitched bleats from the same
Composite Garut ram while (A) completely alone, (B) with observer
and (C) partially isolated ......................................................................... 50
11
Frequency of observed behaviours throughout the experiment ............. 66
12
Frequency of vocalizations at different stocking densities
on day 1 and day 2 of regrouping .......................................................... 78
13
Frequency of vocalizations per breed group at different
stocking densities ................................................................................... 78
LIST OF APPENDICES
Page
1
Values of acoustic parameters based on isolation level ........................... 105
2
Values of acoustic parameters based on breed......................................... 106
3
ANOVA test results from the GLM procedure for comparison
of acoustic parameters for isolation level and breed ................................ 107
4
Output of Duncan’s multiple range test for isolation level ...................... 117
5
Output of Duncan’s multiple range test for breed ................................... 122
6
Output of Kruskall-Wallis test ................................................................. 126
7
Output of Mann-Whitney U test .............................................................. 129
8
Descriptive statistics for behavioural categories ..................................... 136
GENERAL INTRODUCTION
Background to the Study
There is no better way of generating progress and development than by
looking beyond the boundaries of one’s current knowledge. For centuries
mankind has attempted to subject nature to obeying its rules in order to fulfill its
boundless needs. We are now, however, approaching an era in which change is
essential. Humans are becoming increasingly aware of the importance of
understanding and respecting both the animal and plant kingdom in order for us to
survive. In the development of human civilization the farming of animals has
played an important part. Animals have been used by humans for many purposes
including the production of food, clothing, draught power, companionship,
recreation, scientific research and education. In all cases some degree of
modification of genetics and/or environment of the species concerned has taken
place. According to Leaver (1999) those responsible for the animals and society as
a whole, have a duty to ensure that the welfare of animals is not unacceptably
compromised in these processes.
The feeling that man has a moral obligation to ensure that the welfare of
animals which are kept on farm is never poor has become widespread. At present
animals can no longer be considered machines that can be manipulated at will for
human purposes. It is believed by an increasing number of researchers (Duncan
1993; Whittaker et al. 2012) that because animals are sentient, their welfare
matters. The welfare of an animal depends on how it perceives the situation with
which it is confronted and on how it perceives itself in that situation (de Jong et
al. 2012). According to Fraser and Broom (1997) the attempts of an animal to
cope and the result of failure to cope to its surroundings can be measured. Hence
welfare can be assessed in a precise scientific way using a variety of indicators.
Knowledge of animal behaviour may be more important today as intensive
husbandry systems place animals in environments far removed from those they
were originally selected for, and even more distantly removed from those their
wild ancestors were adapted to (Lawrence & Rushen 1993). It is believed by
Fraser and Broom (1997) that many of the current animal husbandry problems are
2
not soluble by investigating nutrition, body physiology, or disease control but
require investigations of the behaviour of the animals before progress can be made
towards a solution. Behaviour can be defined as that which animals do to interact
with, respond to, and control their environment. An appreciation of how to handle
animals thus necessitates knowledge of behaviour, which is generally the animal's
"first line of defense" in response to environmental change. As such, careful
observations of behaviour can provide us with a great deal of information about
animals' requirements, preferences, dislikes, and internal states (Mench & Mason
1997).
Over the last few decades, scientists have made huge progress in
understanding how animals perceive their environment and the feelings prompted
by this perception. Investigating the modern farming environments and
management strategies which livestock are subjected to might help determine
where mismatches exist (Leone & Estevez 2008). Substantial new knowledge of
the behaviour of livestock under intensive husbandry systems is therefore needed
to assess these systems of management. This knowledge can be applied in the
animal production industry in order to improve production and welfare. Whittaker
et al. (2012) stated that space provided to animals is one easily recognizable
aspect of husbandry systems that is perceived by the public to imply that welfare
is poor. According to them features such as the structural characteristics of the
environment or social aspects of the group (such as group size or density) must be
considered to establish meaningful recommendations on how to create the most
beneficial environment for animals. Craig (1981) suggested that in many instances
it may be easier to modify an animal’s environment to provide or eliminate some
key stimulus than to use artificial selection to exploit a favorable behaviour or
eliminate an unfavorable one. When decisions are taken about methods in animal
husbandry, animals should be considered as individuals and their responses to
their environment should be evaluated and understood.
The vast majority of farmed animals is gregarious and reacts heavily to
being separated from group-mates. Much research has focused on the potential
role played by conspecifics in the elicitation of emotions. This is valid both for
mammals and birds (Boissy & Le Neindre 1997). Animal behaviour is rarely
3
given a great deal of consideration in the design of housing systems and
equipment, even though behaviourally inappropriate design can lead to injury and
other welfare problems (NRAES 1995). A careful description of the behaviour
patterns or a sequence of behaviours of animals offers the possibility to identify
all of the relevant components and to link their performance to the wider context
of the physical and biological environment of the animal (Scott 2005).
Particular states of mood or emotion may be accompanied by specific
behaviours, vocalization being one of them. Hence, in farm animals vocalizations
may supply us with hints on their well-being in an easy way, given that the
meanings of the respective calls are well-established. Then, it is possible to judge
acoustically uttered current needs and impaired welfare by non-invasive, possibly
even automatized continuous monitoring in farm-housing. Vocalizations may also
modulate emotions of the receivers such that welfare may also be affected in
conspecifics hearing distress utterances. For these reasons, the analysis of farm
animal vocalization has gained increasing interest in the last years and a variety of
attempts to decode the meaning have been made. According to Manteuffel et al.
(2004) future bioacoustical research for welfare assessment should focus on
comprehensive studies of a broad spectrum of species specific distress
vocalizations.
Sheep (Ovis aries) are a highly adaptable and versatile domestic species,
which has made them a critically important resource in human societies around
the world (Meadows et al. 2005). According to statistical data on the Indonesian
livestock sector, the amount of sheep raised for production purposes has increased
significantly in the past five to six years. The size of the national sheep population
was estimated at 8,979,849 animals in 2006. In 2010 this amount had increased to
10,915,000 (Direktorat Jenderal Peternakan 2010). It was reported by Johannes
and Budisatria (2011) that, in South East Asia, Indonesia has the largest small
ruminant population. According to them the rapid growth of the local population
serves as a major impulse for further increasing the number of small ruminants.
Although the welfare of farm animals has been of concern, and a focus for
research for decades, this has concentrated on those species generally farmed
intensively (pigs, poultry and latterly, dairy cows). As a species traditionally
4
managed extensively, sheep have received relatively little attention from a welfare
perspective (Dwyer 2009). Recently, Veissier et al. (2012) found that the
emotional responses of sheep to a threatening event are influenced by the animal’s
social environment. Therefore, sheep are likely to form social standards of
emotional responses according to their rank in hierarchy which makes them a
perfect candidate species for behavioural studies.
The general breeding strategy for any production environment is to match
genetic potential to the feeding and management system (Bradford 1993). In order
for farmers to increase the productivity of their livestock with the use of limited
resources, it is important for them to facilitate the needs of their animals as much
as possible. More precise welfare assessments need to consider specific
behavioural response of genetic lines, as different lines react differently when
facing environmental challenges (McGary et al. 2003). Behaviour, like
physiology and anatomy, is part of the general functioning an make-up of an
animal. An interesting question in the context of animals’ genetical background
concerns how differences in genotype and in the environment result in differences
in behaviour (Broom 1981).
Farmers and the food industry have the responsibility of meeting the
demands of the consumers for high welfare products and quality products by
adjusting their farming systems. Research in the area of animal behaviour will
therefore be able to provide farmers with important information for developing
better livestock management systems and designing captive environments catering
to the specific needs of each breed, which will automatically result in an
improvement of the production level of the local animals.
Purpose of the Study
The purpose of this study was formulated as follows:
1. To discover whether, and if so, to what extend the vocal output of sheep is
influenced by the stressfulness of different levels of social isolation
2. To determine whether there are differences in the vocal behaviour of different
breeds of sheep
5
3. To analyze the impact of farming practices i.e. regrouping and housing (space
allowance) on sheep behaviour
4. To assess the degree of variability in behaviour between sheep breeds
5. To discover amount of time needed for newly regrouped animals to establish
affinity and affiliative relationships
Significance of the Study
The output of this research is aimed at providing livestock farmers with a
valuable, less invasive and convenient method for assessing overall welfare of
sheep, in which behaviour can serve as a key indicator for the animals’
motivational state and welfare status. It is also hoped that the results of the study
will be able to provide valuable information about the optimum stocking density
and regrouping method for different breeds of sheep.
Hypothesis
The hypothesis that was tested during this study is that the acoustic output
of sheep is affected by their motivational state and that the quality of the vocal
repertoire differs per breed. The prediction was that the vocalizations of the sheep
would reflect the stress response induced by different levels of social isolation. It
was therefore thought that the quality of the vocal output would differ depending
on the intensity of the stressor and on the breed. It was also hypothesized that the
animals’ behaviour would be affected by the novelty of the new housing
conditions and amount of space available per animal. It was predicted that the
frequency of agonistic behaviour would be higher on the first day right after
regrouping and that the amount of agonistic behaviour displayed would differ per
breed.
6
7
LITERATURE REVIEW
Systematics and Distribution of Sheep
Domesticated sheep (Ovis aries) belong to the tribe Caprini (Shackleton &
Shank 1984). Following Mesolithic mans’ domestication of the sheep
approximately 8000–9000 years ago (Ryder 1984), selection has proceeded on
traits such as coat color, environmental tolerance, wool characteristics, and meat
and milk production. The result is a spectrum of phenotypic differences between
breeds (Meadows et al. 2005).
According to Sodiq and Tawfik (2004) Indonesia has various indigenous
sheep breeds distributed throughout its different tropical environments which are
well suited for intensive and extensive exploitation. Throughout the years
different crossbreeding programs have been used in the hope of creating the ideal
animal, one which is well adapted to the various environmental conditions and
thus able to produce optimally. It is believed that there are two distinct types of
sheep in Indonesia: thin-tailed - and fat-tailed sheep (Edey 1983). In the hope of
improving the production of local animals, certain temperate breeds such as
Merino, Suffolk, Suffas, Dorset and, more recently, Barbados Blackbelly and
St.Croix were introduced to Indonesia (BPPT 2007).
Barbados Blackbelly Cross
Barbados Blackbelly sheep are a breed of hair sheep. Although there can
be little doubt that the Barbados Blackbelly has African ancestry, there is
compelling evidence that the breed originated and evolved on the Island of
Barbados. The fleece color of these animals ranges from light tan to a dark
mahogany red, with black breed markings on the face, legs, belly, inguinal region,
chin, and chest (BBAI 2011). The animals of this breed are believed to be more
tolerant than other sheep breeds to internal parasites (CARDI 2006). A composite
breed, named Barbados Blackbelly Cross was created by crossing Barbados
Blackbelly sheep with animals from the breed Local Sumatera. This composite
breed is believed to possess the combined attributes of adaptation to widespread
environments and high reproductive efficiency (BBPT 2007).
8
Local Garut
Local Garut, a breed indigenous to Indonesia, is believed to have
originated from a crossing between Merino sheep, Kaapstad sheep and animals
from a breed local to Indonesia (Merkens & Soemirat 1926). Garut sheep possess
certain characteristics which make them very suitable for use in livestock
production systems, one of which is their adaptability to novel environments
(BPPT 2007). Under rural conditions, Garut sheep are generally raised on a small
scale as an additional source of income (Bradford & Inounu 1996). Due to its
rather dominant temperament, animals of this breed have been known to be used
for fighting purposes (Edey 1983).
Figure 1 Adult rams of the breeds Barbados Blackbelly Cross (left) and
Local Garut (right). Source: private collection of the author
Composite Garut
St. Croix, a species of sheep known for its rather large size, high
adaptability to hot climates and ability to sustain a good production level under
poor feeding conditions together with Moulton Charollais, famous for its high
milk production, large body size and rapid growth rate, were used to create a
composite breed (Sodiq & Tawfik 2004). The before mentioned two breeds were
crossed with the previously described breed Local Garut to create the breed
Composite Garut. The animals of this composite breed are believed to have a very
rapid growth rate and a high ability to adapt to tropical conditions (BPPT 2007).
9
Figure 2 Adult rams of the breed Composite Garut
Source: private collection of the author
Importance of Animal Behaviour
Farm animals are kept to produce food an other essentials for humans, and
the farmers need to make profit from their enterprises. It is therefore necessary
that the difference between the value of what animals produce and the costs that
the farmer incurs for this production is sufficiently high. By taking animal
behaviour into account, such optimization may be easier to achieve (Jensen 2009).
Initially, before animal domestication, man used his knowledge of wild animal
behaviour to hunt them successfully. Later, whether by design or accident, he used
behaviour traits, particularly social ones, as key criteria in his selection of and
success with domestic animals (Tennessen & Hudson 1981).
Broom (1981) believes that behaviour, like physiology and anatomy, is
part of the general functioning of an animal. The term ethology is often used for
the observation and description of behaviour with the objective of finding out how
biological mechanisms function (Fraser & Broom 1997). Behaviour is the aspect
of an animal’s phenotype that involves the presence or absence of definable motor
activities, vocalizations and odor production by means of which it conducts its
daily affairs of self-maintenance and social interaction. Like other phenotypic
traits, behaviour is the outcome of environmental and genetic causal agents
(Banks 1982). Fletcher (1992) explained that research on animal behaviour has an
inherently integrative nature, for it gathers together questions and methodologies
across levels of analysis, across levels of explanation and across diverse taxa.
Behavioural studies are of great importance in increasing our understanding and
10
appreciation of animals. In addition to providing knowledge about the diversity
and complexity of behaviour in nature, such studies also provide information
crucial to improvements in the welfare of animals maintained in laboratories,
agricultural settings and zoos, and as companion animals (The Association for the
Study of Animal Behaviour 2003).
According to Fraser and Broom (1997) there are two types of questions
which can be asked when trying to understand a particular kind of behaviour.
These are: “How does it work?” and “Why does it happen?” The answers to the
first question refer to the mechanisms underlying the behaviour which cause it to
occur at the time of observation and with the form which is seen. The answers to
the second question refer to the way in which this behaviour has arisen in the
species under observation. The authors have suggested that since all behaviour
depends on the genetic information in an animal and environmental factors will
always affect the expression of genes, it is not useful to try to distinguish between
instinctive and innate behaviour and which is environmentally determined. The
questions of interest here, concern how differences in genotype and in the
environment result in differences in behaviour.
It was mentioned by Arney (2009) that sheep are an attractive animal for
scientific research on behaviour due to the facts that they are docile, have a
(relatively) short flight distance and are gregarious. In sheep, several studies have
been carried out concerning the behavioural reactivity of animals to a novel
environment. Breed differences are known to exist in several behaviours, such as
selection of lambing sites (Alexander et al. 1983; Poindron et al. 1984), openfield behaviour and reaction to the presence of a dog (Torres-Hernandez &
Hohenboken 1997). It is possible that the breed differences found in open-field
tests reflect genotypic variations in reactivity of animals to various stressful
situations according to Le Neindre et al. (1993).
Abnormal behaviour may be the first indicator that there is a problem with
an individual sheep, or the whole flock. Such abnormal behaviours observed in
sheep include: lethargy, becoming uninterested in feeding, increased vocalization,
isolation of individuals from the flock, restlessness and an increased respiration
rate (Arney 2009). Recent work by Wemelsfelder (2007) has found that,
11
irrespective of professional expertise, observers' interpretation of animals'
behavioural expressions, including their emotional state, are in close agreement.
This includes assessments of sheep.
In an attempt to emphasize the importance of behavioural studies Fraser
and Broom (1997) even stated that every farmer, every veterinary surgeon and
indeed all those who have an interest in livestock production need to know about
farm animal behaviour in order for them to carry out their job properly. Research
on the behaviour of farm animals is thus relevant and needed for animal
production enterprises to be carried out effectively and economically.
Behaviour, Welfare and Environmental Design
It has been stated by Rollin (1995) that society is currently demanding that
agriculture be modified to reduce suffering and to accommodate the physical and
psychological needs of animals, as determined by their biological natures.
According to the author the aim of research into animal welfare that will be
undertaken in the future therefore, must be primarily to improve the well-being of
animals, presumably within the constraints of economic reality. This, in turn,
means that research should be directed toward making production systems
“animal-friendly”, so as to alleviate suffering and increase animal happiness. To
date there is no consensus on the definition of welfare, however definitions have
been proposed based on the ability of the animals to perform natural behaviour,
the animals’ subjective experiences, or the biological functioning of the animals
(Dwyer 2008).
Table 1 gives an operational definition of animal welfare developed in the
Welfare Quality Project (2009). At present the innovations in management are
principally characterised by larger livestock numbers kept together in markedly
reduced space. Such conditions have effects on disease transmission and they
require considerable physological and behavioural adaptation. It has been
assumed that farm animals are, in certain cases, able to adapt to the environmental
restrictions, but that both adaptation and failure to adjust are recognisable in the
behaviour of animals (Fraser & Broom 1997).
12
Table 1 An operational definition of animal welfare developed in the Welfare
Quality Project (Welfare Quality 2009)
Principle
Good feeding
Good housing
Good health
Appropriate
behaviour
No.
1
2
3
Welfare criterion
Absence of prolonged hunger
Absence of prolonged thirst
Comfort aroused resting
4
5
Thermal comfort
Ease of movement
6
Absence of injuries
7
Absence of disease
8
Expression of social behaviours
Example of potential measures
Body Condition Score
Access to water
Frequency of different lying
positions, standing up and lying
down behaviour
Panting, shivering
Slipping or falling, possibility
of exercise
Clinical scoring of integument,
carcass damage, lameness
Enteric problems, downgrades
at slaughter
Evidence of routine mutilations
such as tail docking and
dehorning,
stunning
effectiveness at slaughter
Social licking, aggression
Expression of other behaviours
Good human-animal relationship
Positive emotional state
Play, abnormal behaviour
Approach or avoidance tests
Novel object test
Adapted from Rushen et al. (2011)
The welfare of different farm animal species has been a scientific issue for
a relatively long time, generating a significant quantity of information related to
welfare of different farm animal s
DIFFERENT SHEEP (Ovis aries) BREEDS: INDICATOR OF
WELFARE?
SAMANTHA E. C. ENGELDAL
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
DECLARATION OF AUTHENTICITY
I, Samantha E. C. Engeldal, hereby declare that all information in this
document entitled:
‘STRESS-INDUCED BEHAVIOUR IN RAMS OF THREE DIFFERENT
SHEEP (Ovis aries) BREEDS: INDICATOR OF WELFARE?’
has been obtained and presented in accordance with academic rules and
ethical conduct. I also solemnly declare that this thesis was composed by myself
through guidance of my supervisory committee. This work has not been submitted
for the awards of any other academic degree, diploma, certificate or other
professional qualification except as specified. As required by academic rules, all
material and results that are not original to this work have been clearly and fully
cited and referenced.
Bogor, December 2012
Samantha E.C. Engeldal
NRP D151118051
ABSTRACT
SAMANTHA E.C. ENGELDAL. Stress-induced Behaviour in Rams of Three
Different Sheep (Ovis aries) Breeds: Indicator of Welfare? Under supervision of
RONNY RACHMAN NOOR and SUBANDRIYO.
Growing importance of and concern for the welfare of farm animals within
production systems has been the basis for an enormous amount of scientific
studies. The goal of the present study was to investigate whether both vocal and
social behaviour of sheep, under specific stress-inducing situations, could be used
as an indicator of the animals’ welfare status. Two separate experiments were
carried out with 2-3 year old adult rams. The animals were of three breeds,
namely Barbados Blackbelly Cross, Local Garut and Composite Garut. In the first
experiment twelve clinically healthy animals, four from each breed, were
subjected to three different levels of social isolation. The animals were held
completely alone, in the presence of a human and alone in a group pen adjacent to
a pen with conspecifics. During the isolation sessions both vocal and locomotive
behaviour of each animal were recorded. The recorded calls were acoustically
analyzed using specialized acoustic software. The results showed that the levels of
isolation were characterized by very specific behavioural responses with an
increased amount of locomotor activity and vocalization in partially isolated
animals. The animals that were completely isolated showed a higher amount of
inactive behaviour. No specific differences were found in the behaviour of
animals that were held completely alone and the ones which were in the presence
of a human observer. Acoustic analysis of the recorded calls showed significant
differences in a number of temporal and structural features. Spectral analysis
revealed the most notable differences in the amount of sound energy integrated in
the calls. Differences were found in both locomotive and vocal behaviour based
on isolation level and breed. The second experiment focused on the effect of
stocking density on the social behaviour of newly regrouped rams. Thirty-six
animals were subjected to three different stocking density levels, namely low (3.2
m2/ram), medium (1.6 m2/ram) and high (0.8 m2/ram). Recorded data consisted of
frequencies of agonistic-, exploratory, locomotive-, aberrant-, inactive-, self-care-,
mating- and vocal behaviour. The results of this experiment showed that the
animals responded differently to the different stocking density levels. The highest
stocking density level was characterized by the highest number of inactive
behaviour and the lowest number of locomotor activity. There were also
significant differences found in the frequency of displayed behaviours based on
the amount of time the animals had spent within the new group settings. The
amount of agonistic-, mating- and exploratory behaviour was found to be
significantly higher on the day of regrouping as compared to the level of these
behaviours on the day after regrouping. Significant differences were also found in
the behavioural response of animals from different breeds. The results from both
experiments thus lead us to conclude that both vocal- and social behaviour of rams
are able to provide humans with important information on their affective state
which may be helpful in the design of production systems that are beneficial to the
animals their welfare.
Keywords: vocalization, behaviour, stress, sheep, animal welfare
SUMMARY
SAMANTHA E.C. ENGELDAL. Stress-induced Behaviour in Rams of Three
Different Sheep (Ovis aries) Breeds: Indicator of Welfare? Under supervision
of RONNY RACHMAN NOOR and SUBANDRIYO.
Animal domestication has played a central role in the development of
human civilization. Modern animal production systems are principally
characterized by a larger number of farm animals which are kept together in
reduced space. A great number of the management practices which are currently
applied in intensive systems along with the conditions under which the animals
are kept, are thought to have a negative influence on both physiological and
production traits of the animals. The perception that humans have a moral
obligation to ensure that the animals their welfare, which is thought to be the
extent to which the animals are able to successfully adapt to their environment, is
never excessively poor has become widespread. The attempts of an animal to cope
to its environment and the results of failure to cope can be measured. This
meaning that the welfare of an individual animal can be assessed in scientific
ways using different types of indicators. An appreciation of how to handle animals
appropriately necessitates knowledge of their behaviour.
The purpose of this study was to evaluate both vocal- and social
behavioural response of different breeds of sheep to situations which have been
found to be very stressful for this gregarious species, in an attempt to discover
non-invasive ways that might reveal information on the animals’ affective state. It
was also intended to discover whether the animals would differ in their
behavioural response based on their breed.
The research consisted of two separate experiments. A total of forty-eight
rams from three different sheep breeds were used throughout the entire study. The
following breeds were included: Barbados Blackbelly Cross (BC) (50% Local
Sumatera, 50% Barbados Blackbelly), Local Garut (LG) and Composite Garut
(KG) (50% Local Garut, 25% St. Croix, 25% Moulton Charollais). In the first
experiment twelve clinically healthy, 2-3 year old adult sheep were subjected to
different levels of social isolation. Each individual animal was kept alone without
visual- and tactile contact with conspecifics, kept in the presence of an observer
without visual – and tactile contact with conspecifics, and kept alone in a group
pen at a specific distance from conspecifics with whom visual-, acoustic- and
olfactory contact was possible. During a maximum of 15 minutes both vocal and
locomotive behaviour were recorded. High-pitched bleats were recorded using a
Digital Voice Recorder after which the calls were acoustically analyzed using the
acoustic software program Raven Pro 1.4. Thirty-six acoustic parameters were
calculated after which their values were subjected to statistical analysis.
Frequencies of locomotive behaviours were observed and recorded during 5
minutes per isolation session using a predefined ethogram.
For the second experiment thirty-six, clinically healthy, 2-3 year old sheep
were used. Four animals from the same breed were grouped and held at three
different stocking densities, namely 3.2 m2/animal, 1.6 m2/animal and 0.8
m2/animal. Based on a predefined ethogram agonistic-, self-care-, exploratory-,
mating-, aberrant-, locomotive-, inactive, and vocal behaviour of each individual
animal were recorded on two consecutive days. Random scan sampling with scan
lengths of sixty seconds were used to gather the behavioural data. Behaviours
were observed for 30 minutes at four different times of day, namely 07.00 am,
09.30 am, 12.00 pm and 14.30 pm.
The results from the first experiment showed that the animals were more
active during partial isolation compared to complete isolation. The frequency of
locomotive behaviours and vocalizations during partial isolation was also found to
be higher compared to that during complete isolation. Significant effects of
isolation level and breed on both temporal and structural acoustic properties were
found. Amplitude, power and time acoustic properties were found to affect
acoustic quality of vocal responses to isolation, whereas frequency related
properties were also found to differ significantly (P < 0.05) between breeds. From
spectrogram analysis, the patterns of energy distribution within the calls proved to
offer the most distinctive difference between isolation levels and breeds. Calls
uttered during complete isolation were all identified by a higher level of noiseenergy compared to calls uttered during partial isolation. It was concluded that the
acoustic analysis of calls uttered during social isolation of adult rams revealed
information on the affective state of the animals. This was found to be
predominantly expressed by both temporal and structural variations in acoustic
cues within distress calls and to differ per breed.
The results of experiment 2 showed that agonistic behaviour was observed
at the highest frequency throughout the entire study. Stocking density was found
to have a significant effect on exploratory-, locomotive- and standing behaviour.
The effect of breed caused significant differences in agonistic-, self-care-,
aberrant- and mating behaviour. Significant differences were also found between
day 1 and day 2 of regrouping for agonistic-, exploratory, self-care- and mating
behaviour. These results led to the conclusion that the animals’ behavioural
response to regrouping and space allowance was characterized by specific patterns
and that the three breeds do differ in their reactions to novel situations. It is
believed that the animals their welfare might be compromised by housing them at
high stocking densities.
Keywords: vocalization, behaviour, stress, sheep, animal welfare
Copyright © IPB 2012
All Rights Reserved
This work is deposited at the university library to be made available to borrowers
under rules of the library. Brief quotations from this thesis are allowable provided
that accurate acknowledgment of the source is made. Request for this manuscript
in whole or in part may be granted by Bogor Agricultural University when in its
judgment the proposed use of the material will be beneficial for educational
purposes. In all other instances, however, no part or all of this thesis may be
reproduced or transmitted in any form or by any means.
STRESS-INDUCED BEHAVIOUR IN RAMS OF THREE
DIFFERENT SHEEP (Ovis aries) BREEDS: INDICATOR OF
WELFARE?
SAMANTHA E.C. ENGELDAL
A thesis sumbitted to the Graduate School
of Bogor Agricultural University
in partial fullfillment of the requirements for the degree
Master of Science
in the Department of
Animal Science and Production Technology
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
External examiner: Prof. Dr. Ir. Cece Sumantri, M. Agr. Sc.
ACKNOWLEDGEMENTS
A profound and genuine love for animals together with the increasing
importance of animal welfare within the modern farming industry, were the
motivation for investigating the way in which farm animals behave in stressful
situations. By using animal behaviour as an indicator of the animals’ affective
state, an attempt can be made to create such farming environments which support
their overall welfare.
My journey in pursuit of a Master of Science degree has been very
insightful, energized by numerous special moments. Each and every experience
which I have had throughout these past two years has led me to view life in an
entirely new light, of which an increased amount of respect for nature and its
perfect natural order is just one result. In short, my time spent in Indonesia can be
summed up by the words: ‘Without GOD, I am not’. Through HIS mercy I have
been blessed with Spiritual Guides and Ancestors who provide me with divine
insight, guidance and protection at all times. For this I am so grateful. THEY are
the sole reason for this achievement.
My parents have always encouraged me to pursue my dreams. I have been
blessed with a Mother who has always motivated and supported me throughout
my educational journey. The example she has set for me through her own life
fostered my enthusiasm and has also been the basis for all of the success I have
been fortunate to experience so far. My father instilled in me two traits: a strong
work ethic and to always strive for the best results. They have both taught me that
final victory ALWAYS comes to the one who stays connected and perseveres. For
this I am so grateful. I would not have reached this level had it not been for their
uninterruptible love, care, encouragement and prayer.
Words of gratitude are due to my family and friends for always taking an
interest in what I have been doing and offering me their much-valued support. I
would thank you from the bottom of my heart, but for you my heart has no
bottom.
I would also like to thank my head supervisor, Prof. Ronny Rachman
Noor. Without his willingness to take me under his supervision I might not have
had some of the wonderful experiences that I have had. He has provided me with
supreme counseling while exploring a topic that I am very passionate about. I am
thankful to him for his guidance, advice and encouragements throughout my
study. I have learned a lot from him during my research, which greatly increased
my skills in the field. His supervision challenged me intellectually and has helped
enrich my knowledge.
I would also like to acknowledge, Prof. Subandriyo for his support and
constructive criticism throughout this project.
I am sincerely thankful to Dr. Rarah R. A. Maheswari for pleasantly
welcoming me to the Department of Animal Science and Production Technology.
She has always treated me as a part of “her team” and has guided and advised me
whenever needed. I will always be grateful for the kindness and understanding she
has shown to me. Moreover, I will always remember the long, insightful talks we
have had in her laboratory.
My sincere appreciation is hereby offered to Dr. Eko Handiwirawan for
the help and encouragement given to me during the course of my research. Your
inexhaustible patience, excellent insight and support throughout my time spent in
Indonesia will always be greatly valued.
I am very grateful to everyone I have met at the Indonesian Research
Institute for Animal Production, especially the technicians who assisted me during
the collection of my data. The support and assistance received from Bapak
Sumantri, Pak. Koesma, Pak. Tohir, Pak. Njurjaja and Pak. Maplani in carrying
out my research will always be greatly appreciated.
I would like to convey my gratitude to all the staff at IPB for their
enormous and continuous support, patience and help throughout my study.
Finally, I would like to thank each and every person, not mentioned by
name, that I have met in Indonesia. Each word and experience has helped to
support, shape and form me in one way or another and for that I will always be
very grateful.
DEDICATION
This thesis is dedicated to all of the sheep that have participated in this
study. I will always have many fond memories of them. It is my sincere wish that
the results from this study will aid in improving their position within the animal
production industry.
AUTOBIOGRAPHY
The author was born in the month December in Paramaribo, Suriname.
After having finished all of the basic education levels, the author was admitted to
the Anton de Kom University of Suriname (ADEK). In the year 2009 the author
graduated with a Bachelor’s Degree in Animal Science.
In 2010 the author attained her teaching certificate for becoming a licensed
teacher. In that same year she was awarded a scholarship under the Developing
Countries Partnership Program to further her studies in Indonesia at Bogor
Agricultural University. The author successfully completed the Master’s program
in the Department of Animal Science and Production Technology in 2012.
TABLE OF CONTENTS
Page
LIST OF TABLES .......................................................................................... xiii
LIST OF FIGURES ........................................................................................ xiv
LIST OF APPENDICES ................................................................................. xv
GENERAL INTRODUCTION .......................................................................
Background to the Study .......................................................................
Purpose of the Study ..............................................................................
Significance of the Study .......................................................................
Hypothesis .............................................................................................
1
1
4
5
5
LITERATURE REVIEW ..............................................................................
Systematics and Distribution of Sheep ...................................................
Barbados Blackbelly Cross .....................................................................
Local Garut ............................................................................................
Composite Garut ....................................................................................
Importance of Animal Behaviour ...........................................................
Behaviour, Welfare and Environmental Design . ...................................
Motivation and Stress in Farm Animals .................................................
Relations of Vocalization to Animal Welfare .......................................
Vocalization Analysis ............................................................................
7
7
7
8
8
9
11
15
17
21
EFFECT OF DIFFERENT LEVELS OF SOCIAL ISOLATION
ON THE ACOUSTICAL CHARACTERISTICS OF
SHEEP VOCALIZATION .............................................................................
Abstract ..................................................................................................
INTRODUCTION .................................................................................
MATERIAL AND METHODS .............................................................
Location and Time of the Study ....................................................
Study Subjects and Housing..........................................................
Isolation Procedures ......................................................................
Recorded Behaviour .....................................................................
Bleat Recordings ...........................................................................
Bleat Analysis ...............................................................................
Data Analysis and Statistics ..........................................................
RESULTS AND DISCUSSION ............................................................
Behavioural Parameters.................................................................
Vocalization and Call Measures ..................................................
Breed Differences of Acoustic Structure of High Bleats ..............
CONCLUSIONS .....................................................................................
REFERENCES........................................................................................
23
23
24
27
27
27
27
28
29
29
34
35
35
41
45
53
55
IMPACT OF STOCKING DENSITY AND INFLUENCE OF
BREED ON THE BEHAVIOUR OF NEWLY REGROUPED
ADULT RAMS ...............................................................................................
Abstract ...................................................................................................
INTRODUCTION ..................................................................................
MATERIAL AND METHODS .............................................................
Location and Time of the Study ....................................................
Study Subjects and Housing ..........................................................
Experimental Setup and Procedure ..............................................
Behavioural Parameters .................................................................
Data Analysis.................................................................................
RESULTS AND DISCUSSION .............................................................
Behavioural Budget .......................................................................
Effect of Space Allowance on Behaviour of Rams ......................
Breed Effect ..................................................................................
Impact of Day of Regrouping on Ram Behaviour .........................
Vocal Behaviour ............................................................................
CONCLUSIONS .....................................................................................
REFERENCES ........................................................................................
61
61
62
65
65
65
65
66
68
69
69
70
72
75
78
81
83
GENERAL DISCUSSION .............................................................................. 87
RECOMMENDATIONS ................................................................................. 91
REFERENCES ................................................................................................ 93
APPENDICES ................................................................................................. 103
LIST OF APPENDICES
Page
1
Values of acoustic parameters based on isolation level ........................... 105
2
Values of acoustic parameters based on breed......................................... 106
3
ANOVA test results from the GLM procedure for comparison
of acoustic parameters for isolation level and breed ................................ 107
4
Output of Duncan’s multiple range test for isolation level ...................... 117
5
Output of Duncan’s multiple range test for breed ................................... 122
6
Output of Kruskall-Wallis test ................................................................. 126
7
Output of Mann-Whitney U test .............................................................. 129
8
Descriptive statistics for behavioural categories ..................................... 136
LIST OF TABLES
Page
1
An operational defination of animal welfare developed
in the Welfare Quality Project (Welfare Quality 2009) ......................... 12
2
Scheme for judging welfare indicators in animal management
and housing systems ............................................................................... 13
3
Experimental design of isolation procedures .......................................... 28
4
Frequencies of observed behaviours at different levels of isolation ...... 35
5
Breed differences in frequencies of observed behaviours
at different levels of isolation ................................................................. 37
6
Comparison of acoustic parameters of high-pitched bleats
at different levels of isolation ................................................................. 42
7
Comparison of acoustic parameters of high-pitched bleats
from different breeds ............................................................................. 46
8
Experimental design. Number of animals per breed group
and per stocking density ......................................................................... 66
9
Ethogram used for studying behaviour of rams at various
stocking densities ................................................................................... 67
10
Pooled behavioural categories ............................................................... 68
11
Frequencies of displayed behaviour at different
stocking densities ................................................................................... 70
12
Influence of breed on ram behaviour ..................................................... 72
13
Influence of day of regrouping on ram behaviour ................................. 76
LIST OF FIGURES
Page
1
Adult rams of the breeds Barbados Blackbelly Cross
and Local Garut .......................................................................................
8
2
Adult rams of the breed Composite Garut .............................................
9
3
Assessment of welfare and consequences of lack of welfare ................ 16
4
Neuronal, anatomical and functional elements of call
production in animals ............................................................................ 19
5
Frequency of locomotor activity by animals from different
breeds at different levels of social isolation ........................................... 39
6
Frequency of standing by animals from different breeds at
different levels of social isolation .......................................................... 40
7
Frequency of vocalizations per breed group at different levels
of social isolation .................................................................................... 41
8
Representative spectrographs of high-pitched bleats from the same
Barbados Blackbelly Cross ram while (A) completely alone,
(B) with observer and (C) partially isolated ........................................... 48
9
Representative spectrographs of high-pitched bleats from the same
Local Garut ram while (A) completely alone, (B) with observer
and (C) partially isolated ......................................................................... 49
10
Representative spectrographs of high-pitched bleats from the same
Composite Garut ram while (A) completely alone, (B) with observer
and (C) partially isolated ......................................................................... 50
11
Frequency of observed behaviours throughout the experiment ............. 66
12
Frequency of vocalizations at different stocking densities
on day 1 and day 2 of regrouping .......................................................... 78
13
Frequency of vocalizations per breed group at different
stocking densities ................................................................................... 78
LIST OF APPENDICES
Page
1
Values of acoustic parameters based on isolation level ........................... 105
2
Values of acoustic parameters based on breed......................................... 106
3
ANOVA test results from the GLM procedure for comparison
of acoustic parameters for isolation level and breed ................................ 107
4
Output of Duncan’s multiple range test for isolation level ...................... 117
5
Output of Duncan’s multiple range test for breed ................................... 122
6
Output of Kruskall-Wallis test ................................................................. 126
7
Output of Mann-Whitney U test .............................................................. 129
8
Descriptive statistics for behavioural categories ..................................... 136
GENERAL INTRODUCTION
Background to the Study
There is no better way of generating progress and development than by
looking beyond the boundaries of one’s current knowledge. For centuries
mankind has attempted to subject nature to obeying its rules in order to fulfill its
boundless needs. We are now, however, approaching an era in which change is
essential. Humans are becoming increasingly aware of the importance of
understanding and respecting both the animal and plant kingdom in order for us to
survive. In the development of human civilization the farming of animals has
played an important part. Animals have been used by humans for many purposes
including the production of food, clothing, draught power, companionship,
recreation, scientific research and education. In all cases some degree of
modification of genetics and/or environment of the species concerned has taken
place. According to Leaver (1999) those responsible for the animals and society as
a whole, have a duty to ensure that the welfare of animals is not unacceptably
compromised in these processes.
The feeling that man has a moral obligation to ensure that the welfare of
animals which are kept on farm is never poor has become widespread. At present
animals can no longer be considered machines that can be manipulated at will for
human purposes. It is believed by an increasing number of researchers (Duncan
1993; Whittaker et al. 2012) that because animals are sentient, their welfare
matters. The welfare of an animal depends on how it perceives the situation with
which it is confronted and on how it perceives itself in that situation (de Jong et
al. 2012). According to Fraser and Broom (1997) the attempts of an animal to
cope and the result of failure to cope to its surroundings can be measured. Hence
welfare can be assessed in a precise scientific way using a variety of indicators.
Knowledge of animal behaviour may be more important today as intensive
husbandry systems place animals in environments far removed from those they
were originally selected for, and even more distantly removed from those their
wild ancestors were adapted to (Lawrence & Rushen 1993). It is believed by
Fraser and Broom (1997) that many of the current animal husbandry problems are
2
not soluble by investigating nutrition, body physiology, or disease control but
require investigations of the behaviour of the animals before progress can be made
towards a solution. Behaviour can be defined as that which animals do to interact
with, respond to, and control their environment. An appreciation of how to handle
animals thus necessitates knowledge of behaviour, which is generally the animal's
"first line of defense" in response to environmental change. As such, careful
observations of behaviour can provide us with a great deal of information about
animals' requirements, preferences, dislikes, and internal states (Mench & Mason
1997).
Over the last few decades, scientists have made huge progress in
understanding how animals perceive their environment and the feelings prompted
by this perception. Investigating the modern farming environments and
management strategies which livestock are subjected to might help determine
where mismatches exist (Leone & Estevez 2008). Substantial new knowledge of
the behaviour of livestock under intensive husbandry systems is therefore needed
to assess these systems of management. This knowledge can be applied in the
animal production industry in order to improve production and welfare. Whittaker
et al. (2012) stated that space provided to animals is one easily recognizable
aspect of husbandry systems that is perceived by the public to imply that welfare
is poor. According to them features such as the structural characteristics of the
environment or social aspects of the group (such as group size or density) must be
considered to establish meaningful recommendations on how to create the most
beneficial environment for animals. Craig (1981) suggested that in many instances
it may be easier to modify an animal’s environment to provide or eliminate some
key stimulus than to use artificial selection to exploit a favorable behaviour or
eliminate an unfavorable one. When decisions are taken about methods in animal
husbandry, animals should be considered as individuals and their responses to
their environment should be evaluated and understood.
The vast majority of farmed animals is gregarious and reacts heavily to
being separated from group-mates. Much research has focused on the potential
role played by conspecifics in the elicitation of emotions. This is valid both for
mammals and birds (Boissy & Le Neindre 1997). Animal behaviour is rarely
3
given a great deal of consideration in the design of housing systems and
equipment, even though behaviourally inappropriate design can lead to injury and
other welfare problems (NRAES 1995). A careful description of the behaviour
patterns or a sequence of behaviours of animals offers the possibility to identify
all of the relevant components and to link their performance to the wider context
of the physical and biological environment of the animal (Scott 2005).
Particular states of mood or emotion may be accompanied by specific
behaviours, vocalization being one of them. Hence, in farm animals vocalizations
may supply us with hints on their well-being in an easy way, given that the
meanings of the respective calls are well-established. Then, it is possible to judge
acoustically uttered current needs and impaired welfare by non-invasive, possibly
even automatized continuous monitoring in farm-housing. Vocalizations may also
modulate emotions of the receivers such that welfare may also be affected in
conspecifics hearing distress utterances. For these reasons, the analysis of farm
animal vocalization has gained increasing interest in the last years and a variety of
attempts to decode the meaning have been made. According to Manteuffel et al.
(2004) future bioacoustical research for welfare assessment should focus on
comprehensive studies of a broad spectrum of species specific distress
vocalizations.
Sheep (Ovis aries) are a highly adaptable and versatile domestic species,
which has made them a critically important resource in human societies around
the world (Meadows et al. 2005). According to statistical data on the Indonesian
livestock sector, the amount of sheep raised for production purposes has increased
significantly in the past five to six years. The size of the national sheep population
was estimated at 8,979,849 animals in 2006. In 2010 this amount had increased to
10,915,000 (Direktorat Jenderal Peternakan 2010). It was reported by Johannes
and Budisatria (2011) that, in South East Asia, Indonesia has the largest small
ruminant population. According to them the rapid growth of the local population
serves as a major impulse for further increasing the number of small ruminants.
Although the welfare of farm animals has been of concern, and a focus for
research for decades, this has concentrated on those species generally farmed
intensively (pigs, poultry and latterly, dairy cows). As a species traditionally
4
managed extensively, sheep have received relatively little attention from a welfare
perspective (Dwyer 2009). Recently, Veissier et al. (2012) found that the
emotional responses of sheep to a threatening event are influenced by the animal’s
social environment. Therefore, sheep are likely to form social standards of
emotional responses according to their rank in hierarchy which makes them a
perfect candidate species for behavioural studies.
The general breeding strategy for any production environment is to match
genetic potential to the feeding and management system (Bradford 1993). In order
for farmers to increase the productivity of their livestock with the use of limited
resources, it is important for them to facilitate the needs of their animals as much
as possible. More precise welfare assessments need to consider specific
behavioural response of genetic lines, as different lines react differently when
facing environmental challenges (McGary et al. 2003). Behaviour, like
physiology and anatomy, is part of the general functioning an make-up of an
animal. An interesting question in the context of animals’ genetical background
concerns how differences in genotype and in the environment result in differences
in behaviour (Broom 1981).
Farmers and the food industry have the responsibility of meeting the
demands of the consumers for high welfare products and quality products by
adjusting their farming systems. Research in the area of animal behaviour will
therefore be able to provide farmers with important information for developing
better livestock management systems and designing captive environments catering
to the specific needs of each breed, which will automatically result in an
improvement of the production level of the local animals.
Purpose of the Study
The purpose of this study was formulated as follows:
1. To discover whether, and if so, to what extend the vocal output of sheep is
influenced by the stressfulness of different levels of social isolation
2. To determine whether there are differences in the vocal behaviour of different
breeds of sheep
5
3. To analyze the impact of farming practices i.e. regrouping and housing (space
allowance) on sheep behaviour
4. To assess the degree of variability in behaviour between sheep breeds
5. To discover amount of time needed for newly regrouped animals to establish
affinity and affiliative relationships
Significance of the Study
The output of this research is aimed at providing livestock farmers with a
valuable, less invasive and convenient method for assessing overall welfare of
sheep, in which behaviour can serve as a key indicator for the animals’
motivational state and welfare status. It is also hoped that the results of the study
will be able to provide valuable information about the optimum stocking density
and regrouping method for different breeds of sheep.
Hypothesis
The hypothesis that was tested during this study is that the acoustic output
of sheep is affected by their motivational state and that the quality of the vocal
repertoire differs per breed. The prediction was that the vocalizations of the sheep
would reflect the stress response induced by different levels of social isolation. It
was therefore thought that the quality of the vocal output would differ depending
on the intensity of the stressor and on the breed. It was also hypothesized that the
animals’ behaviour would be affected by the novelty of the new housing
conditions and amount of space available per animal. It was predicted that the
frequency of agonistic behaviour would be higher on the first day right after
regrouping and that the amount of agonistic behaviour displayed would differ per
breed.
6
7
LITERATURE REVIEW
Systematics and Distribution of Sheep
Domesticated sheep (Ovis aries) belong to the tribe Caprini (Shackleton &
Shank 1984). Following Mesolithic mans’ domestication of the sheep
approximately 8000–9000 years ago (Ryder 1984), selection has proceeded on
traits such as coat color, environmental tolerance, wool characteristics, and meat
and milk production. The result is a spectrum of phenotypic differences between
breeds (Meadows et al. 2005).
According to Sodiq and Tawfik (2004) Indonesia has various indigenous
sheep breeds distributed throughout its different tropical environments which are
well suited for intensive and extensive exploitation. Throughout the years
different crossbreeding programs have been used in the hope of creating the ideal
animal, one which is well adapted to the various environmental conditions and
thus able to produce optimally. It is believed that there are two distinct types of
sheep in Indonesia: thin-tailed - and fat-tailed sheep (Edey 1983). In the hope of
improving the production of local animals, certain temperate breeds such as
Merino, Suffolk, Suffas, Dorset and, more recently, Barbados Blackbelly and
St.Croix were introduced to Indonesia (BPPT 2007).
Barbados Blackbelly Cross
Barbados Blackbelly sheep are a breed of hair sheep. Although there can
be little doubt that the Barbados Blackbelly has African ancestry, there is
compelling evidence that the breed originated and evolved on the Island of
Barbados. The fleece color of these animals ranges from light tan to a dark
mahogany red, with black breed markings on the face, legs, belly, inguinal region,
chin, and chest (BBAI 2011). The animals of this breed are believed to be more
tolerant than other sheep breeds to internal parasites (CARDI 2006). A composite
breed, named Barbados Blackbelly Cross was created by crossing Barbados
Blackbelly sheep with animals from the breed Local Sumatera. This composite
breed is believed to possess the combined attributes of adaptation to widespread
environments and high reproductive efficiency (BBPT 2007).
8
Local Garut
Local Garut, a breed indigenous to Indonesia, is believed to have
originated from a crossing between Merino sheep, Kaapstad sheep and animals
from a breed local to Indonesia (Merkens & Soemirat 1926). Garut sheep possess
certain characteristics which make them very suitable for use in livestock
production systems, one of which is their adaptability to novel environments
(BPPT 2007). Under rural conditions, Garut sheep are generally raised on a small
scale as an additional source of income (Bradford & Inounu 1996). Due to its
rather dominant temperament, animals of this breed have been known to be used
for fighting purposes (Edey 1983).
Figure 1 Adult rams of the breeds Barbados Blackbelly Cross (left) and
Local Garut (right). Source: private collection of the author
Composite Garut
St. Croix, a species of sheep known for its rather large size, high
adaptability to hot climates and ability to sustain a good production level under
poor feeding conditions together with Moulton Charollais, famous for its high
milk production, large body size and rapid growth rate, were used to create a
composite breed (Sodiq & Tawfik 2004). The before mentioned two breeds were
crossed with the previously described breed Local Garut to create the breed
Composite Garut. The animals of this composite breed are believed to have a very
rapid growth rate and a high ability to adapt to tropical conditions (BPPT 2007).
9
Figure 2 Adult rams of the breed Composite Garut
Source: private collection of the author
Importance of Animal Behaviour
Farm animals are kept to produce food an other essentials for humans, and
the farmers need to make profit from their enterprises. It is therefore necessary
that the difference between the value of what animals produce and the costs that
the farmer incurs for this production is sufficiently high. By taking animal
behaviour into account, such optimization may be easier to achieve (Jensen 2009).
Initially, before animal domestication, man used his knowledge of wild animal
behaviour to hunt them successfully. Later, whether by design or accident, he used
behaviour traits, particularly social ones, as key criteria in his selection of and
success with domestic animals (Tennessen & Hudson 1981).
Broom (1981) believes that behaviour, like physiology and anatomy, is
part of the general functioning of an animal. The term ethology is often used for
the observation and description of behaviour with the objective of finding out how
biological mechanisms function (Fraser & Broom 1997). Behaviour is the aspect
of an animal’s phenotype that involves the presence or absence of definable motor
activities, vocalizations and odor production by means of which it conducts its
daily affairs of self-maintenance and social interaction. Like other phenotypic
traits, behaviour is the outcome of environmental and genetic causal agents
(Banks 1982). Fletcher (1992) explained that research on animal behaviour has an
inherently integrative nature, for it gathers together questions and methodologies
across levels of analysis, across levels of explanation and across diverse taxa.
Behavioural studies are of great importance in increasing our understanding and
10
appreciation of animals. In addition to providing knowledge about the diversity
and complexity of behaviour in nature, such studies also provide information
crucial to improvements in the welfare of animals maintained in laboratories,
agricultural settings and zoos, and as companion animals (The Association for the
Study of Animal Behaviour 2003).
According to Fraser and Broom (1997) there are two types of questions
which can be asked when trying to understand a particular kind of behaviour.
These are: “How does it work?” and “Why does it happen?” The answers to the
first question refer to the mechanisms underlying the behaviour which cause it to
occur at the time of observation and with the form which is seen. The answers to
the second question refer to the way in which this behaviour has arisen in the
species under observation. The authors have suggested that since all behaviour
depends on the genetic information in an animal and environmental factors will
always affect the expression of genes, it is not useful to try to distinguish between
instinctive and innate behaviour and which is environmentally determined. The
questions of interest here, concern how differences in genotype and in the
environment result in differences in behaviour.
It was mentioned by Arney (2009) that sheep are an attractive animal for
scientific research on behaviour due to the facts that they are docile, have a
(relatively) short flight distance and are gregarious. In sheep, several studies have
been carried out concerning the behavioural reactivity of animals to a novel
environment. Breed differences are known to exist in several behaviours, such as
selection of lambing sites (Alexander et al. 1983; Poindron et al. 1984), openfield behaviour and reaction to the presence of a dog (Torres-Hernandez &
Hohenboken 1997). It is possible that the breed differences found in open-field
tests reflect genotypic variations in reactivity of animals to various stressful
situations according to Le Neindre et al. (1993).
Abnormal behaviour may be the first indicator that there is a problem with
an individual sheep, or the whole flock. Such abnormal behaviours observed in
sheep include: lethargy, becoming uninterested in feeding, increased vocalization,
isolation of individuals from the flock, restlessness and an increased respiration
rate (Arney 2009). Recent work by Wemelsfelder (2007) has found that,
11
irrespective of professional expertise, observers' interpretation of animals'
behavioural expressions, including their emotional state, are in close agreement.
This includes assessments of sheep.
In an attempt to emphasize the importance of behavioural studies Fraser
and Broom (1997) even stated that every farmer, every veterinary surgeon and
indeed all those who have an interest in livestock production need to know about
farm animal behaviour in order for them to carry out their job properly. Research
on the behaviour of farm animals is thus relevant and needed for animal
production enterprises to be carried out effectively and economically.
Behaviour, Welfare and Environmental Design
It has been stated by Rollin (1995) that society is currently demanding that
agriculture be modified to reduce suffering and to accommodate the physical and
psychological needs of animals, as determined by their biological natures.
According to the author the aim of research into animal welfare that will be
undertaken in the future therefore, must be primarily to improve the well-being of
animals, presumably within the constraints of economic reality. This, in turn,
means that research should be directed toward making production systems
“animal-friendly”, so as to alleviate suffering and increase animal happiness. To
date there is no consensus on the definition of welfare, however definitions have
been proposed based on the ability of the animals to perform natural behaviour,
the animals’ subjective experiences, or the biological functioning of the animals
(Dwyer 2008).
Table 1 gives an operational definition of animal welfare developed in the
Welfare Quality Project (2009). At present the innovations in management are
principally characterised by larger livestock numbers kept together in markedly
reduced space. Such conditions have effects on disease transmission and they
require considerable physological and behavioural adaptation. It has been
assumed that farm animals are, in certain cases, able to adapt to the environmental
restrictions, but that both adaptation and failure to adjust are recognisable in the
behaviour of animals (Fraser & Broom 1997).
12
Table 1 An operational definition of animal welfare developed in the Welfare
Quality Project (Welfare Quality 2009)
Principle
Good feeding
Good housing
Good health
Appropriate
behaviour
No.
1
2
3
Welfare criterion
Absence of prolonged hunger
Absence of prolonged thirst
Comfort aroused resting
4
5
Thermal comfort
Ease of movement
6
Absence of injuries
7
Absence of disease
8
Expression of social behaviours
Example of potential measures
Body Condition Score
Access to water
Frequency of different lying
positions, standing up and lying
down behaviour
Panting, shivering
Slipping or falling, possibility
of exercise
Clinical scoring of integument,
carcass damage, lameness
Enteric problems, downgrades
at slaughter
Evidence of routine mutilations
such as tail docking and
dehorning,
stunning
effectiveness at slaughter
Social licking, aggression
Expression of other behaviours
Good human-animal relationship
Positive emotional state
Play, abnormal behaviour
Approach or avoidance tests
Novel object test
Adapted from Rushen et al. (2011)
The welfare of different farm animal species has been a scientific issue for
a relatively long time, generating a significant quantity of information related to
welfare of different farm animal s