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UNIVERSIDAD POLITÉCNICA DE MADRID

ESCUELA TÉCNICA SUPERIOR DE INGENIEROS AGRÓNOMOS

NEW SYSTEMS OF MANAGEMENT TO IMPROVE

THE HEALTH AND WELFARE OF RABBITS IN

FARM CONDITIONS

TESIS DOCTORAL

Clara Alfonso Carrillo

INGENIERO AGRÓNOMO

2015

DEPARTAMENTO DE PRODUCCIÓN ANIMAL

ESCUELA TÉCNICA SUPERIOR DE INGENIEROS AGRÓNOMOS

NEW SYSTEMS OF MANAGEMENT TO IMPROVE

THE HEALTH AND WELFARE OF RABBITS IN

FARM CONDITIONS

Nuevos sistemas de cría y manejo para mejorar la salud y

bienestar de conejos de granja


AGRICULTURAL ENGINEER

SUPERVISORS

Paloma García Rebollar Dr. INGENIERO AGRÓNOMO

Ana Isabel García Ruiz Dr. INGENIERO AGRÓNOMO

A mi familia

AGRADECIMIENTOS

Parece mentira pero no lo es!... después de muuuucho mucho tiempo de trabajo y

“sufrimiento” pero también de alegrías, diversión y aprendizaje hemos logrado terminar

ésta tesis!!

Solo tengo palabras de agradecimiento y cariño hacia toda esa gente que me ha rodeado

y apoyado y no me gustaría olvidarme de ninguno de ellos en éste gran momento.. pero

como me conozco y la ayuda ha sido infinita… Mil gracias a todos los que estáis leyendo

éstas palabras.

Gracias Directoras:

Paloma, tu gran ayuda, dedicación, comprensión, cariño y valiosos consejos han

sido más de lo que me merezco.. te estaré eternamente agradecida.

Anabel, mil gracias por creer en mí. Tu inestimable ayuda y sabios consejos pero

sobre todo tu cariño, amistad y tu infinita paciencia conmigo me han hecho crecer en

todos los sentidos…una gozada estar siempre a tu vera.

Carlos De Blas, me siento afortunada, tu incalculable ayuda, apoyo y comprensión han

sido un regalo para mí. Todo un placer contar con tu paciencia y un gran privilegio

contar con tu sabiduría.

Miguel Ibáñez, tu asesoramiento en estadística ha sido vital en ésta tesis….y en mi vida!

Me has transmitido una pasión por los “números” que ni yo me lo creo.

Erika, mejor que tú no lo sabe nadie.. gracias por soñar con las conejas y no volverte

loca. Nadie me podría haber ayudado más y mejor.

Álvaro y Paco, vuestra valiosa ayuda a pie de granja ha sido inmejorable. Es un placer

trabajar con vuestra profesionalidad y disfrutar de vuestra amistad.

A mi equipo de Nanteros, Enrique, Bea y Manolo, me habéis facilitado muchísimo el

poder compaginar trabajo y tesis, no sabéis lo que eso ha valido para mí. Gracias por

vuestra paciencia y comprensión.

Thanks to Leo Den Hartong and to Pedro Pérez de Ayala for your confidence.

Compañer@s y amig@s de mí siempre “PRRC”, no hay un equipo mejor que el nuestro.

Millones de gracias a tod@s, pero especialmente a:

Mis chicas: Rosa (my Prety), Lauri, Andrea, Eva, Bea, Gema.. me habéis hecho

mucho más fácil y llevadero esta fase de mi vida con nuestras mini thesis en el café,..

chicas, tenéis mucho arte!.

A los más “buenorros” de la granja, Jon y Alberto, gracias por estar siempre

ahí,..tenemos que tirar ese muro, que en vuestro despacho huele a ciencia de la buena.

A Ángela… se me puede olvidar tu cumpleaños, pero nunca se me olvidará tu

apoyo, ánimo e insistencia.

Twan, Adam and Grace thanks for all …I feel more comfortable talking in

English thanks to you!

Cibele, me has ayudado más de lo que te crees, aunque no te des cuenta!

Ángel, aunque no lo creas tus conciertos matutinos con tu “voz angelical” me ha

animado las mañana en las que me levantaba con mal pie.

Susana, me has dado esa “vidilla” que tanto necesitaba en la recta final, gracias.

Santi, entre tú y yo nunca han hecho falta las palabras, por lo que no te digo na!

Tengo que dar las gracias por haber conocido durante esta etapa de mi vida a un grupo

de personas que aunque con algunas no tenga el placer de tener cerca, son y serán

siempre inolvidables: Álvaro, Irene, Jose Luis, Jose Carlos, Rubén, Álvarito, Julito, Jano,

María y Mercedes. Chicos con vosotros ser becaria ha sido una de las experiencias más

bonitas de mi vida.

Familia Pérez Bonilla, se acabó!!! Gracias por todo el apoyo, ánimo y cariño que me

dais. Me ha tocado la lotería con todos vosotros!....Adriano, cómo me hubiera gustado

darte la noticia cara a cara!.. De todas formas sé que te has enterado porque te siento

siempre muy cerca.

Familia, todos mis logros tanto profesionales como personales son gracias a vosotros.

Soy la persona más afortunada del mundo por tener unos hermanos y unos padres como

vosotros. OS QUIERO.

Adriano, sobran las palabras pero.. gracias por tu inagotable insistencia, entusiasmo y

paciencia. Gracias a tus desayunos, lavadoras, cenas, mimos, ratos de tele y cambios de

pañal. Gracias por compartir tu vida conmigo, porque simplemente me haces feliz… pero

sobre todo gracias por haberme dado lo más importante de mi vida, nuestro pequeño

Héctor. Os adoro.


INDEX RESUMEN ......................................................................................................................... 1

ABSTRACT ....................................................................................................................... 5

CHAPTER 1: INTRODUCTION AND OBJECTIVES ................................................................ 9

1. Introduction: Animal welfare in rabbit production .................................................. 10

1.1. Animal Welfare Definition ............................................................................. 10

1.2. Welfare assessment ......................................................................................... 11

1.2.1. Physiologic measurements ...................................................................... 11

1.2.2. Behavioural measurements ...................................................................... 12

1.2.3. Pathological and productive measurements ............................................. 13

1.3. Legislation for Animal Welfare on rabbit production ...................................... 14

1.4. Alternatives to improve Rabbit Welfare .......................................................... 15

1.4.1. Management practices ............................................................................. 15

1.4.2. Housing system ....................................................................................... 15

2. Objectives .............................................................................................................. 16

3. References .............................................................................................................. 17

CHAPTER 2: EFFECT OF TYPE OF CAGE ON THE BEHAVIOUR PATTERN OF RABBIT

DOES AT DIFFERENT PHYSIOLOGICAL STAGES ............................................................... 22

1. Introduction ............................................................................................................ 23

2. Material and methods ............................................................................................. 24

2.1. Animals and housing ...................................................................................... 24

2.2. Feed ................................................................................................................ 24

2.3. Behavioural observations ................................................................................ 25

2.4. Statistical methods .......................................................................................... 25

3. Results ................................................................................................................... 25

3.1. Location ......................................................................................................... 25

3.2. Posture............................................................................................................ 27

3.3. Functional behaviours ..................................................................................... 28

4. Discussion .............................................................................................................. 33

5. Conclusions ............................................................................................................ 36

6. References .............................................................................................................. 37

CHAPTER 3: DEVELOPMENT OF SIMPLIFIED SAMPLING METHODS OF BEHAVIOURAL

DATA IN RABBIT DOES .................................................................................................... 40

1. Introduction ............................................................................................................ 41

2. Material and methods ............................................................................................. 42

2.1. Animals and housing ...................................................................................... 42

2.2. Feed ................................................................................................................ 42

2.3. Behavioural measurements ............................................................................. 43

2.4. Experimental design ....................................................................................... 43


3. Results ................................................................................................................... 45

3.1. Location ......................................................................................................... 45

3.2. Posture............................................................................................................ 45

3.3. Functional behaviours ..................................................................................... 46

4. Discussion .............................................................................................................. 47

5. Conclusions ............................................................................................................ 48

6. References .............................................................................................................. 51

CHAPTER 4: EFFECT OF LATE WEANING AND USE OF ALTERNATIVE CAGES ON

PERFORMANCE OF DOES, SUCKLING AND FATTENING RABBITS UNDER EXTENSIVE

REPRODUCTIVE MANAGEMENT ...................................................................................... 53

1. Introduction ............................................................................................................ 54

2. Material and Methods ............................................................................................. 55

2.1. Animal, housing and management .................................................................. 55

2.2. Feeding ........................................................................................................... 56

2.3. Controls .......................................................................................................... 56


3. Results ................................................................................................................... 57

3.1. Body weight and body composition of does .................................................... 57

3.2. Rabbit doe and litter performance ................................................................... 60

3.3. Feed intake and feed conversion ratio ............................................................. 61

4. Discussion .............................................................................................................. 64

4.1. Weaning age ................................................................................................... 64

4.2. Type of cage ................................................................................................... 66

5. Conclusions ............................................................................................................ 68

6. References .............................................................................................................. 69

CHAPTER 5: GENERAL DISCUSSION ............................................................................... 74

General Discussion ........................................................................................................ 75

References ..................................................................................................................... 83

CHAPTER 6: GENERAL CONCLUSIONS AND IMPLICATIONS............................................ 89

General Conclusions and Implications ............................................................................ 90

INDEX OF TABLES AND FIGURES

CHAPTER 2: EFFECT OF TYPE OF CAGE ON THE BEHAVIOUR PATTERN OF RABBIT

DOES AT DIFFERENT PHYSIOLOGICAL STAGES

Table 1. Ethogram of behaviours used per category ...................................................... 26

Table 2. Location of does at 2 physiological stages housed in conventional and

alternative cages over 24h period ................................................................................... 26

Table 3. Duration and frequency of different postures performed by rabbit does at two

physiological stages housed in conventional and alternative cages over 24h period. ....... 28

Table 4. Duration and frequency of main functional behaviour performed by lactating

and gestating does in conventional and alternative cages over 24 h period. ..................... 29

Table 5. Duration and frequency of functional behaviours performed by lactating and

gestating does housed in conventional and alternative cages over 24h period. ................ 31

Figure 1. Proportion of time spent by rabbit does at different physiological stages in

different locations housed in conventional and alternative cages throughout the day....... 27

Figure 2. Evolution throughout the day of time spent lying and sitting by lactating and

gestating does as average. And frequencies performing different postures:hyperactivity

in lactating does and standing in gestating does. ............................................................. 29

Figure 3. Evolution throughout the day of time spent performing different behaviours

by lactating and gestating does as average: resting, eating, drinking and grooming. ........ 30

Figure 4. Evolution throughout the day of time spent by rabbit does interacting-with-

kits in conventional cages or in alternative cages . .......................................................... 32

Figure 5. Evolution throughout the day of proportion of rabbit does nursing per hour in

conventional and alternative cages ................................................................................. 32

CHAPTER 3: DEVELOPMENT OF SIMPLIFIED SAMPLING METHODS OF BEHAVIOURAL

DATA IN RABBIT DOES40

Table 1. Ethogram of behaviours used per category ...................................................... 26

Table 2. Comparison of the simplified methods with the reference method on the time

spent by does on different locations. ............................................................................... 45

Table 3. Comparison of the simplified method with the reference method on the time

spent by does in different postures in two physiological stages . ..................................... 45

Table 4. Comparison of the simplified methods with the reference method on the time

spent by does performing different functional behaviours in two physiological stages .... 47

Figure 1. Frequency and duration of video recordings of different sampling methods.

Black sections show recording periods. .......................................................................... 43

Figure 2. Estimation error of different simplified behavioural methods .......................... 50

CHAPTER 4: EFFECT OF LATE WEANING AND USE OF ALTERNATIVE CAGES ON

PERFORMANCE OF DOES, SUCKLING AND FATTENING RABBITS UNDER EXTENSIVE

REPRODUCTIVE MANAGEMENT53

Table 1. Effect of weaning age and type of cage on body weight and body composition

of does at different points of lactation phase. .................................................................. 58

Table 2. Effect of weaning age and type of cage on reproductive parameters, mortality

of animals and litter traits. .............................................................................................. 62

Table 3. Effect of weaning age and type of cage on feed intake and feed conversion

ratio during the first five reproductive cycles. ................................................................. 63

Figure 1. Conventional cages......................................................................................... 56

Figure 2. Alternative cages ............................................................................................ 56

Figure 3. Fat and energy body content of the body at 46 days after parturition of does

subjected to standard and late weaning throughout the three first reproductive cycles ..... 59

Figure 4. Effect of standard and late weaning on mortality of young rabbits from 3 to

46 days of age throughout the five reproductive cycles ................................................... 60

Figure 5. Effect of standard and late weaning on litter size at 59 days of age

throughout the five reproductive cycles. ......................................................................... 61

Figure 6. Effect of standard and late weaning on litter weight at 59 days of age

throughout the five reproductive cycles... ....................................................................... 63

Resumen

1

RESUMEN

Resumen

2

Resumen El objetivo general de esta Tesis Doctoral fue evaluar nuevos sistemas de alojamiento y

cría de conejos de granja, estudiando tanto parámetros comportamentales (experimento 1)

como productivos y reproductivos (experimento 3). Además, se evaluaron diferentes

técnicas de muestreo con el fin de optimizar el tiempo empleado para el estudio del

comportamiento animal (experimento 2).

En el experimento 1, se estudió el comportamiento de conejas alojadas en dos tipos de

jaulas (TJ), convencionales vs. alternativas con una plataforma elevada, en distintos

estados fisiológicos (EF), lactantes y gestantes. Se observó el comportamiento de 12

conejas reproductoras con grabaciones de una duración de 24 h continuas.

Independientemente del EF y TJ, las conejas pasaron gran parte de su tiempo sobre el

reposapatas (57,7 %, de media). Sin embargo, debido al uso de la plataforma (23,0% del

tiempo, de media), las conejas lactantes permanecieron un 36,6 % menos de tiempo

(P<0,001) sobre el reposapatas y las gestantes un 27,0% menos (P<0,001) sobre el

enrejillado en jaulas alternativas que en convencionales. En las jaulas alternativas, las

conejas podían adoptar la postura “levantada”, sin embargo ésta fue observada solamente

en conejas gestantes una media de 4,6 veces al día. Las conejas bebieron con mas

frecuencia en jaulas convencionales que en alternativas (24,6 vs 19,1 veces al día;

P<0,05). Se observó una mayor duración y frecuencia del comportamiento “interactuando

con compañeras” en conejas gestantes alojadas en jaulas convencionales (276 s/d y 4,6

veces/d; P<0,05). La frecuencia de “interactuando con gazapos” fue menor en jaulas

alternativas que en convencionales (2,4 vs 8,6 veces al día; P<0,01). La hora del día

afectó al comportamiento de las conejas, teniendo un comportamiento menos activo

durante las horas centrales del día. Durante las horas de oscuridad, las conejas estuvieron

más inquietas realizando comportamientos como ‘encabritarse’ o amamantar,

coincidiendo éstos en el tiempo en el cual las conejas pasaron más tiempo en la

plataforma. Las conejas utilizaron frecuentemente la plataforma, independientemente del

estado fisiológico. En la fase de lactación, las conejas utilizaron la plataforma para huir

de los intentos de mamar por parte de los gazapos cuando éstas no estaban receptivas. El

uso de la plataforma puede dar lugar a problemas higiénicos debidos tanto por la

acumulación de heces sobre ella como por la caída de heces y orina sobre los animales

que están en la parte inferior. La ausencia de estereotipias por parte de las conejas tanto

Resumen

3

en jaulas alternativas como en convencionales no sugiere una falta de bienestar debida al

sistema de alojamiento.

En el experimento 2, se compararon distintos métodos de observación simplificada con

respecto un método de referencia usando grabaciones continuas de 24 h para la

evaluación del comportamiento de conejas en distintos estados fisiológicos (gestantes y

lactantes) alojadas en dos tipos de jaulas (convencionales y alternativas). Se analizaron un

total de 576 h de grabaciones continuas de 24 h en 12 conejas reproductoras al final del

periodo de lactación y en las mismas conejas después del destete. Los comportamientos

observados se clasificaron en tres categorías independientes (localización en la jaula,

postura y comportamientos funcionales). Se utilizaron grabaciones continuas de 24 h

como método de referencia para validar otros cuatro métodos de observación

simplificados, utilizando grabaciones de distinta duración y frecuencia a lo largo del día.

Métodos regulares: corto y largo con 2.4 y 8 h de observación respectivamente, y

métodos irregulares: corto y largo con 6 y 8 h de observación, respectivamente. Como

resultado, se observó que independientemente del sistema de alojamiento, el mejor

método para reducir el tiempo de observación necesario para evaluar el comportamiento

de conejas reproductoras depende del tipo de variable a estudiar y del estado fisiológico

de las conejas. En gestantes, los métodos irregulares no fueron adecuados para estimar

comportamientos de larga duración tales como tumbada, sentada, descansando y

acicalándose. Sin embargo, en ambos estados fisiológicos, los métodos regulares fueron

precisos para los comportamientos de los grupos localización y postura y para

comportamientos funcionales de larga duración. Por otro lado, los coeficientes de

variación de los comportamientos poco frecuentes realizados principalmente durante el

periodo de oscuridad fueron muy altos, y el método irregular largo obtuvo los menores

errores de estimación para éstos comportamientos.

En el experimento 3, se estudió el efecto de un uso combinado de lactaciones largas

(hasta 46 días) con jaulas alternativas sobre los parámetros productivos y reproductivos

de 104 conejas y sus camadas durante cinco ciclos reproductivos. La mitad de las conejas

fueron alojadas en jaulas polivalentes convencionales (39 cm x 100 cm x 30 cm) y la otra

mitad en jaulas polivalentes alternativas (39 cm x 100 cm x 60 cm), con una plataforma

elevada. Dentro de cada grupo de alojamiento, la mitad de las conejas se destetaron a 32

días y la otra mitad a 46 días tras el parto. Las lactaciones más largas afectaron

negativamente al peso (P<0,001), contenido en grasa y energía (P<0,05) de las conejas al

final del periodo de lactación, pero éste efecto disminuyó con el número de partos. La

Resumen

4

fertilidad, prolificidad y la mortalidad de las conejas no fue afectada por la duración de la

lactación. El destete tardío dio lugar a un mayor tamaño y peso de la camada al final del

periodo de crecimiento (8,9 y 11,3 %, respectivamente) y a un menor índice de

conversión por jaula durante el todo el periodo experimental (13,5 %) con respecto al

destete convencional (P<0,001). Éstos resultados fueron paralelos a la menor mortalidad

global (12,6 vs 17,6 %; P<0,05) observada en gazapos con destete tardío. Las diferencias

en los parámetros productivos con las distintas edades al destete sólo fueron observadas

en los ciclos con peor estado sanitario (tercer y quinto ciclo), en los cuales el destete

tardío redujo la mortalidad. El tipo de jaula no afectó al peso de la coneja, condición

corporal, mortalidad, fertilidad ni tamaño de camada durante los cinco primeros ciclos

reproductivos. Sin embargo, el peso de la camada y el índice de conversión a los 21 días

de edad fueron 4,2% mayor (P<0,001) y 5,0% menor (P<0,005) en animales alojados en

jaulas alternativas que en jaulas convencionales. A día 59 las jaulas alternativas dieron

lugar a camadas más pesadas (P<0,01); sin embargo, éste efecto fue influenciado por la

densidad alcanzada en cada ciclo, ya que cuando la densidad de los animales fue menor

que 40kg/m2 (tercer y quinto ciclo), el efecto del tipo de jaula sobre el peso de la camada

no fue significativo. De los resultados obtenidos se puede concluir que el uso combinado

de lactaciones más largas y jaulas con mayor superficie disponible con una plataforma

elevada podría ser una alternativa para mejorar el bienestar animal en determinadas

situaciones productivas.

Abstract

5

ABSTRACT

Abstract

6

Abstract

The general aim of this PhD Thesis was to evaluate new housing and husbandry systems

of farmed rabbits, studying behavioral (experiment 1), productive and reproductive

(experiment 3) parameters. Moreover, different sampling techniques were evaluated in

order to optimize the assessment of rabbit behaviour (experiment 2).

In experiment 1, the behaviour of rabbit does housed in two different types of cage (TC),

conventional vs. alternative with an elevated platform, at different physiological stages

(PS), lactation and gestation was to study. Behavioural observations were carried out on

12 commercial rabbit does using continuous 24 hour video recording. Independently of

PS and TC, rabbit does spent most of their time on foot mats (57.7 %, as average).

However, due to the use of platforms (23.0% of time, as average), lactating does spent

36.6% less time (P<0.001) on foot mats and gestating does spent 27.0% less (P<0.001)

time on wire mesh in alternative cages than in conventional cages. Alternative cages

allowed for standing posture but this behaviour was only observed in gestating does (4.6

times a day, as average). Frequency of drinking was higher in conventional than in

alternative cages (24.6 vs. 19.1 times a day; P<0.05). Gestating does housed in

conventional cages reached the highest duration and frequency of interacting with

neighbours (276 s/d and 4.6 times/d; P<0.05). The frequency of interacting with kits was

lower in alternative than in conventional cages (2.4 vs. 8.6 times a day; P<0.01). Does’

behaviour was influenced by hour of day, being less active at the midday hours. During

dark hours rabbit does more frequently performed restless behaviour such as

hyperactivity or nursing, matching the time at which rabbit does spent more time on the

platform. The platform was frequently used by rabbit does, independent of their

physiological state, and during late lactation phase, when mothers were not receptive to

nursing, does housed in alternative cages used the platform as a mean to flee from kids

trying to suckle. The use of the platform might lead to hygienic problems due to retained

faeces on the platform and faeces and urine falling onto animals located in the lower part

of the cage. Stereotypies were not observed in any housing system, therefore

conventional cages do not suggest lack of animal welfare.

In experiment 2, it was compared the results of different simplified sampling methods of

behavioural data with respect to reference records of 24-h in order to assess rabbit does

behaviours at different physiological stages (gestation and lactation) in animals housed in

two types of cages (conventional and alternative). A total of 576 h of continuous video of

Abstract

7

12 rabbit does at the end of lactation and on the same females after weaning were

analysed. The behavioural observations were studied using three independent categories

of classification (location in the cage, posture and functional behaviours). Continuous

behavioural recordings of 24 h were considered as the reference method to validate

another 4 sampling methods of data collection by aggregated video recordings of

different frequency and duration (regular short and long methods with 2.4 and 8 h of

observation respectively, and irregular short and long methods with 6 and 8 h of

observation, respectively). The current results showed that, independently of housing

system, the best method to reduce the total observation time required to assess rabbit does

behaviour depends on the trait studied and physiological stage of does. In gestating does,

irregular methods were not suitable to estimate behaviours of long duration such as lying,

sitting, resting and grooming. However, in both physiological stages, regular methods

were accurate for location behaviours, postures and functional behaviours of long

duration. Instead, for the study of infrequent behaviours performed mainly during dark

period, where coefficients of variation were high, the irregular long method led to the

lowest mean estimation errors.

In experiment 3, the effects of the combined use of long lactation periods (46 days) with

alternative cages on the reproductive and growth performance of 104 rabbit does and

their litters during five consecutive reproductive cycles were studied. Half of does were

housed in conventional polyvalent cages (39 cm x 100 cm x 30 cm) and the other half in

alternative polyvalent cages (39 cm x 100 cm x 60 cm), with a raised platform. Half of

the rabbit does in each type of cages were weaned at 32 and the other half at 46 days after

parturition. Longer lactations affected negatively to body weight (P<0.001), fat and

energy content (P<0.05) of rabbit does at the end of the lactation period, but this effect

decreased with the number of parturitions. Fertility, prolificacy and doe mortality were

not affected by lactation length. Late weaning led to higher litter size (by 8.9 %) and litter

weight (by 11.3 %) at the end of growing period and lower feed conversion ratio per cage

during the overall experimental period (13.5 %) than standard weaning (P<0.001). These

results were parallels to a lower mortality (12.6 vs 17.6 %; P<0.05) of young rabbit

weaned later during the overall experimental period. Differences in performances at

different weaning ages were only observed during cycles with worst health status (third

and fifth cycles) in which late weaning decreased mortality. Type of cage did not affect

doe body weight and body condition, mortality, fertility, prolificacy and litter size during

the five firsts reproductive cycles. Nevertheless, at day 21 litter weight and feed

Abstract

8

conversion ratio were 4.2 % higher (P<0.001) and 5.0 % lower (P<0.005) in animals

housed in alternative than in conventional cages. Alternative cages also led to heavier

litters at 59 days (P<0.01); however, this effect was influenced by density reached in each

cycle, as when the density of animals was lower than 40 kg/m2 (cycles three and five),

the difference of litter weight between alternative and conventional cages was not

significant. From the results obtained it can be concluded that the combined use of longer

lactations and cages with higher available surface with a raised platform could be an

alternative to improve animal welfare in some productive situations.

Chapter 1: Introduction and objectives

9

CHAPTER 1: INTRODUCTION AND OBJECTIVES

CHAPTER 1:

INTRODUCTION AND OBJECTIVES


10

Introduction: Animal welfare in rabbit production

1.1. Animal Welfare Definition

Interest and public concern about the welfare of animals is increasing in recent years.

This is a multi-faceted issue which involves important scientific, ethical, economic and

political dimensions (Lund et al., 2006). According to Hughes (1976), the term of ‘animal

welfare’ is a condition of perfect physical and mental integrity in which the animal is in

complete harmony with the surrounding environment. Thereafter, several definitions of

‘animal welfare’ have been proposed, which are not uniformly defined in the literature

due to different societal attitudes towards animals. Then, three main approaches have

been followed in order to define welfare level (Duncan and Fraser, 2000):

• “Physiologic”: Emphasizes the biological functioning of organisms, such as

growth and reproduction, as well as health and behaviour.

• “Psychologic”: Consider feelings or emotions as key elements in determining the

quality of life, increasing the positive feelings (comfort and pleasure) and

decreasing the negative ones (pain and suffering).

• “Natural”: Emphasizes that animals should be allowed to live according to their

natural attitudes and behaviour.

The concept of welfare involves issues as the concepts of ‘suffering’ and ‘need,’ as well

as the ‘five freedoms’ which are more related to animal husbandry and management by

man (Carenzi and Verga, 2009). Suffering occurs “when unpleasant subjective feelings

are acute or continue for a long time because an animal is unable to carry out the actions

that would normally reduce risks to life and reproduction in those circumstances”

(Dawkins, 1990). According to Fraser and Broom (1997) “the general term ‘need’ is used

to refer to a deficiency in an animal which can be remedied by obtaining a particular

resource or responding to a particular environmental or bodily stimulus.”

The knowledge about the animals needs is related to the proposal of giving animals some

‘freedoms’ (Brambell Report, 1965), revised by the FAWC (1993) according to which

animals are under welfare circustances when are protected and free from 1) thirst, hunger

and malnutrition, 2) discomfort with unsuitable housing and inclement weather, 3) pain,

injury and disease, 4) fear and distress, and, finally, 5) can freely express the behavioural

pattern typical of their species.


11

Therefore, the different aspects of the concept of animal welfare should always be taken

into consideration in studies on animal science. However, although the first three

freedoms are easily identified and measured, the latter two freedoms are difficult to

measure objectively with simple techniques, due to its complex nature and lack of

scientific information.

1.2. Welfare assessment

Faced with a stressful situation, the central nervous system of animals organizes a

biological defense which consists of four general categories: behavior, the autonomic

nervous system, the neuroendocrine axis and the immune system (Moberg, 1985; 1998).

These four categories of responses constitute the biological defenses of the animal for

dealing with a stressor and are responsible for the biological changes that occur during an

animal attempt to cope with stress. However, due to differences in the extent of

physiological and behavioural responses to problems, the welfare assessment requires the

joint evaluation of several indicators of different type. Some indicators are most relevant

to short-term problems, like heart-rate and plasma cortisol concentration which are

appropriate for assessing welfare during human handling or a brief period of adverse

physical conditions but not during long-term conditions. However, some measures of

behaviour, immune system function and disease incidence are more appropriate for long-

term problems (Broom, 2011).

From a practical standpoint, the welfare problems found in intensive rabbit production are

partly similar to those observed for other livestock species. Thus, the main welfare

indicators used for livestock (physiological, behavioural, pathological and productive

indicators) may also be used for rabbits and have been previoulsy defined by many

authors (Verga, 2000; Hoy and Verga, 2006; Broom, 2000).

1.2.1. Physiologic measurements

A prolonged stress condition implies a series of alterations in homeostatic equilibrium

that leads to changes in physiological assets (Broom, 1993). Thus, there are some

physiological measurements which are used to assess animal welfare. Depending on the

stressor, different physiological indicators can be measured (Knowles and Warriss,

2000): illness: leucocyte evaluation; hungry: free fatty acids, β- hydroxybutyrate, glucose

or urea; thirst: osmolarity, total proteins, albumins or hematocrit; physical exercise, fear

and excitation: creatine kinase, lactate dehydrogenase, heart rate, breath rate, adrenal


12

activity or hematocrit. Some of these indicators are evaluated comparing a basal level and

its fluctuation with over time.

One of the drawbacks of including stress measurements in welfare studies is that the

sampling techniques to obtain these parameters, such as blood sampling or attaching

electrodes to the animal, are also invasive and stressful in themselves. Some of these

methods have been replaced wit less invasive procedures. For example, radiotelemetry

offers the possibility of recording physiological variables, such as heart rate and blood

pressure, at a distance with minimal interference to the animal. Moreover, it is now

possible to take glucocorticoid measurements from samples of saliva, urine and faeces.

1.2.2. Behavioural measurements

The most biologically economical response to cope with a stressful situation is the

behavioural change, as an individual may be able to simply remove itself from the

stressor (Broom, 2000). Moreover, the fact that an animal avoids an object or event, gives

information about its feelings and hence about its welfare. The stronger the avoidance the

worse the welfare whilst the object is present or the event is occurring (Broom, 2011).

Additionally, the evaluation of behavioural changes is non-invasive and can be used to

measure welfare at the farm (Scott et al., 2001) where the level of stress could be affected

by social and environmental factors. However, the observation of a large number of

animals at the same time to assess different behaviours demands a high degree of labour,

equipments and time. Thus, although continuous recording is the most accurate method

for behavioural measurements, it is difficult to conduct if a large number of animals and a

wide type of behaviours are studied. Therefore, in many cases it is necessary to use

simplified observation methods to reduce the time required to study animal behaviours.

Sampling techniques have already been described by Altmann (1974); however, these

techniques have not been validated in farm domestic rabbits yet.

Regarding behavioural measurements, the presence of abnormal behaviours, called

'stereotypies', which are characterized by the fact of being repetitive and devoid of

purposes (Lawrence and Rushen, 1993), may indicate a condition of poor welfare

(Podbercheck et al., 1991), since manifest themselves as a result of a condition of chronic

stress (Van Zutphen et al., 1993). Some examples of stereotypies in rabbits, are biting the

cage (Stauffacher, 1992) or beat the hind leg on the floor of the cage (Verga, 2000).

Useful information on adaptation and welfare of rabbits can also be obtained by

observing their behavior when they are subjected to so-called "test of reactivity", during


13

which the animal reaction is measured, as the fear of animals towards humans or a new

environment. The test of tonic immobility is used to evaluate the anti-predatory response

and, therefore, the fear of the animal towards humans (Carli, 1982; Ferrante et al., 1992;

Trocino et al., 2004 and 2008). During this test, the rabbit is located on the back inside a

wooden structure delegated to maintain the balance, into a state pseudocatatonico (tonic

immobility), and the time spent on this position is mesasured and is usually positively

correlated with the level of fear of animal. The test of open-field, instead measure the fear

of the animal towards an unknown environment (Meijsser et al., 1989; Ferrante et al.,

1992; Xiccato et al., 1999). The bibliography regarding the interpretation of the behavior

of animals during the test of open-field is multiple, because the reasons for the same

behavior can be different (De Passillé et al., 1995; Rushen, 2000). For example, the

locomotor activity of the rabbit placed within a fence during the test of open-field may

depend on the need to explore the new environment in search of food and shelter, or the

instinct to escape from a predator. In any case, a high locomotor activity and exploratory

during this test are considered indicative of a good adaptation of the animal, whereas an

increase of the times of freezing and immobility represents an adaptive response of the

passive type and is considered negative. Other techniques to measure the feelings of the

animals are the preference tests, where the animal is allowed to choose between certain

aspects of its environment, and the assumption is that the animal will chose according to

how it feels. Motivation tests measure the “work” or “price” to get something or to gain

access to its preferred choice (Duncan, 2005).

Other significant indicators of acute stress, due for example to transportation or handling

practices, may be evaluated looking at other behaviours, such as feeding activity (Finzi et

al., 1986) or social and maternal behaviour (Verga et al., 1978; Lehman, 1991).

1.2.3. Pathological and productive measurements

The autonomic nervous system and the neuroendocrine system modulate many of the

biological functions that are known to be severely impacted by stress; such as

reproduction, immune competence, and metabolism (Moberg, 1985).

Pathological conditions, productive and reproductive performance are the most easily

perceptible welfare indicators but must be interpreted with caution. Unsuitable sanitary

conditions decrease welfare, whereas on the other hand, prolonged chronic stress causes a

higher susceptibility to pathologies due to reduced immune response (Broom, 1993;

Koolhaas et al., 1993). Mortality rate is a simple indicator of animal welfare; however,


14

some diseases do not cause the death of animals and may affect productive performance.

Therefore, the study of performance variables (live weight gain, feed conversion ratio,

fertility, etc.,) can help to assess animal welfare. Conversely, under extensive rearing

conditions, low productive and reproductive performance could be achieve without being

necessarily associated to poor animal welfare conditions. On the other hand, under

intensive conditions, the highest performance values may be obtained but do not fulfil

biological animal requirements. Diseases, injury, movement difficulties and growth

abnormalities all are indicators of poor welfare. Physical pain is the state of suffering that

probably reduces welfare the most in animal husbandry (Duncan, 2005). The evaluation

of injuries such as bruises and abrasions due to badly designed environment can be used

as a way to study pain. Another parameter which can indicate pain it is the weakness of

bones, as if animal’s bones are easily breakable there will be considerable pain and the

welfare will be seriously impaired.

1.3. Legislation for Animal Welfare on rabbit production

In recent years, animal welfare has become established as one of the criteria used to

decide on whether a system is sustainable and whether product quality is good. Thus, it

has implied some changes in European legislation for the livestock industry. The main

issues which are being considered in the new legislations for the protection of animals

kept for farming purposes are the management during transport, the time of slaughter and

the care during the rearing. Although European regulation on these issues exist (Council

Regulation 1/2005/EC; Council Regulation 1099/2009/EC; Council Directive 98/58/EC),

there is currently no Community legislation laying down specific welfare standards for

commercial rabbit production. Therefore, the Standing Committee of the European

Convention for the protection of animals kept for farming purposes has been preparing

recommendations to ensure the welfare of rabbits in commercial farms but they have not

been adopted yet. According to the report of the scientific panel on Animal Health and

Welfare (AHAW) from the European Food Safety Authority (EFSA, 2005), the current

production techniques, and in particular housing systems, do not respect certain of the

rabbit’s fundamental biological characteristics, however, there is a lack of information on

the basis of establishing reliable recommendations to improve rabbit welfare. So, to carry

out further researches, mainly about rabbit husbandry and management practices are an

important issue.


15

1.4. Alternatives to improve Rabbit Welfare

1.4.1. Management practices

Nowadays the sanitary status of the rabbit farm is disputed. The replacement rate of does

is at present around 100-120 % in commercial rabbit farms (Coutelet, 2011; Pascual,

2010; Sánchez del Cueto et al., 2012) but also, high rates of mortality are observed in

fattening rabbitries, especially since the emergence of Epizootic Rabbit Enteropathy

(Licois et al., 2006). This situation requires feasible alternatives to the use of antibiotics

to attenuate this problem. Thus, a delay of the weaning age may help to decrease

fattening mortality in poor hygienic conditions (Romero et al., 2009) due to the protective

role of rabbit milk against some pathogens (Gallois et al., 2007) and to the higher weight

and age at weaning (Lebas 1993; Morisse, 1987). However, long lactations can

exacerbate the deficit body energy of does, impairing the lifespan of rabbit does (Xiccato

et al., 2005). A strategy to improve the reproductive life of the rabbits does could be a

delay of the insemination postpartum (i.e: from 11 to 25 days post partum), reducing

body energy deficit, increasing fertility and improving welfare of the rabbit does (Cervera

et al., 1993; Partridge et al., 1984; Xicatto et al., 2005). Thereby, an extensive

reproductive system in combination with a long lactation period (more than 35 days)

could be an alternative to improve the reproductive activity of does while improving

growing rabbit welfare.

1.4.2. Housing system

Regarding the housing system from a well being point of wiew, the available space and

provision of adequate environment are highly important (Verga, 2000). The report of

EFSA (2005) emphasized the need of providing enough space to ensure the possibility of

movement, giving the opportunity to express the natural animal behaviour and to reduce

stress. However, not all naturally occurring behaviour is desirable in farm animals.

Behaviours strongly associated to wild rabbits, as hiding under cover or alertness posture

to evade predators (Moreno et al., 1996), should not be used as indicator variables for

measuring stress of farmed rabbits under different housing conditions. The study of rabbit

behavior on commercial farms is fundamental to understand rabbits requirements and the

consequent adaptation to intensive rearing housing conditions (Trocino and Xiccato,

2006). One of the strategies applied to overtake the lack of available surface in

commercial cages was to increase the standard cage dimensions, with its corresponding

increment cost. The increased available surface of commercial cages to allow animals to


16

express their natural behaviour modifying the current cage dimension is one of the

aspects most concerned to farmers, due to the investment required.

In commercial conditions, reproductive does are usually housed individually in

polyvalent cages where the available surface is large, but this varies depending on litter

age. Moreover, late weaning decreases the available floor surface per animal, which

results in a negative perception of animal welfare (Vanhonacker et al., 2009). One

alternative for maintaining or even increasing floor surface per doe with late weaning

management is to use a two-floor cage including a communicating platform inside and

increasing the cage height (Finzi et al., 1996). Thus, increasing the size of breeding cages

could offer more comfortable housing and more possibilities for locomotion of rabbit

does (EFSA, 2005) but this need to be demostrated. Results from the experiments

conducted so far increasing cage size (horizontally or vertically) are not conclusive

(Szendrő and McNitt, 2012) and the interaction of late weaning management with type of

cage is still unknown.

2. Objectives

i) To study if adult rabbit does at two physiological stages (late gestation and

late lactation) perform different behavioural pattern showing a higher welfare

level when they are housed in alternative cages with a raised platform.

ii) To study if some simplified sampling techniques of behavioural data can be

used as accurate method to assess rabbit does behaviours at different

physiological stages (gestation and lactation) housed in two type of cages

(conventional and alternative).

iii) To study if a delay of the weaning age of rabbit housed in alternative cages

improves their welfare status using productive and reproductive parameters of

does and their litters.


17

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Chapter 2: Effect of type of cage on the behavior pattern

22

CHAPTER 2: EFFECT OF TYPE OF CAGE ON THE

BEHAVIOUR PATTERN OF RABBIT DOES AT

DIFFERENT PHYSIOLOGICAL STAGES

CHAPTER 2:

EFFECT OF TYPE OF CAGE ON THE BEHAVIOR

PATTERN OF RABBIT DOES AT DIFFERENT

PHYSIOLOGICAL STAGES

(Experiment 1)

PUBLISHED IN:

World Rabbit Science 22:59-69.

doi: 10.4995/wrs.20141396


23

1. Introduction

Since 1996, the Standing Committee of the European Convention for the protection of

animals kept for farming purposes has been preparing recommendations to ensure the

welfare of rabbits in commercial farms. According to the report of the scientific panel on

Animal Health and Welfare (AHAW) from the European Food Safety Authority (EFSA,

2005) there is a lack of information in order to establish reliable recommendations to

improve rabbit welfare. After this report most of the published studies have been run with

fattening rabbits (Prinz et al., 2008a, 2008b; Ribikauskas et al., 2010; Szendro et al.,

2012) and few studies evaluated behaviour in rabbit does under farming conditions.

Regarding the housing system, the EFSA report emphasized the need for providing

enough space to ensure the animal opportunity to move and express their natural

behaviour. However, not all naturally occurring behaviour is desirable in farm animals.

Behaviour strongly associated with wild rabbits, for example hiding under cover or

alertness posture to evade predators (Moreno et al., 1996), have been used as indicator

variables for measuring stress of farmed rabbits under different housing conditions.

However, differences between wild and domestic behaviour are not necessarily indicative

of animal suffering (Dawkins, 1990). Traditionally, alertness behaviour such as sitting on

hindlimbs has been considered a natural behaviour indicative of improved welfare.

Following this, Morton et al. (1993) advised the use of sufficiently high cages (75 cm) to

allow the rabbit to sit upright without its ears touching the top of the cage (lookout

position). However, the importance of this behaviour in the current commercial housing

system with a lack of predators is questionable. In fact, Princz et al. (2008a) observed

that the commonly used 30-35 cm high cages were satisfactory for growing rabbits

although, such research has not been performed with adult rabbits where differences in

body size and space allowances could affect behavioural activities.

The increase in the available surface of commercial cages to allow animals to express

their natural behaviour is the most concerning aspect for farmers, due to the investment

required. In farm conditions, reproductive does are usually housed individually in

polyvalent cages and the available surface is large, but it varies depending on litter age.

One solution for maintaining the number of does while increasing floor surface is to use a

two-floor cage including a communicating platform inside and increasing the cage height

(Finzi et al., 1996). The increased available surface of these alternative cages could be a

way for improving welfare of farmed rabbits. However, there is not enough information


24

to ensure that conventional cages used in commercial conditions impair rabbit does’

welfare.

A comparative study of the behaviour of rabbit does housed in conventional and

alternative cages could demonstrate if there is any welfare improvement in alternative

cages or if conventional cages are adequate.

The aim of this trial was to study the behavioural pattern of adult rabbit does at two

physiological stages (late gestation and late lactation), housed in two types of cages

(conventional vs. alternative).

2. Material and methods

2.1. Animals and housing

All experimental procedures were approved by the Ethics Committee of the Polytechnic

University of Madrid and were in compliance with the Spanish guidelines for the care

and use of animals in research (Spanish Royal Decree 1201/2005).

The study was carried out at the Poultry and Rabbit Research Centre of Nutreco, in

Toledo, Spain. A total of 12 multiparous rabbit does (Oryctolagus cuniculus) in their

fourth reproductive cycle from a hybrid maternal line (Hy-Plus) were used. Animals

weighed on average 4.5 kg live weight, and were inseminated 25 days after kindling,

being kits weaned 32 days after kindling. All animals were housed in the same artificially

lighted room. The light:dark cycle was 15:9 h (light interval from 06:00 to 21:00 h and

dark interval from 21:00 to 06:00 h). From the first artificial insemination, half of the

rabbit does were individually housed in alternative polyvalent cages (385 mm x 995 mm

x 600 mm) with one wire platform (381 mm x 310 mm) raised at 400 mm from the floor.

The other half of animals was individually housed in conventional polyvalent cages (385

mm x 995 mm x 300 mm). All the cages were equipped with a feeder and a nipple

drinker placed in the lower level and a foot mat (perforated plastic plate) in the middle of

the floor. Heating, cooling and forced ventilation systems allowed the building

temperature to be maintained between 20 and 23 ºC throughout the experiment.

2.2. Feed

Throughout the study, rabbits were fed ad libitum with a commercial pelleted diet.

Triplicate chemical analysis of feed was performed according to AOAC procedures


25

(2004), and the average composition on as fed basis was: crude protein 18.6%, ether

extract 3.8%, starch 22.0%, crude fibre 14.4% and ash 8.2%.

2.3. Behavioural observations

The observations were performed on two different days with the same does, at the end of

the lactation period (24 days after parturition) with eight kits per litter, and one week

before next parturition (3 days after weaning in pregnant not lactating does). All females’

records were captured simultaneously for 24 h. While recording behaviour nobody

entered the room to avoid disturbances on rabbit does’ behaviour. Behaviour was

recorded by infrared video cameras (VCB-3380/Sanyo) and a LED infrared reflector (IR-

880/12D) placed on bars 2 m above the cages. Video recordings were analysed in their

entirety by one trained person viewing at double speed, the data was then entered into the

computer using “The Observer XT 8.0” software (Noldus Information Technology,

Wageningen). Observations were classified into three exclusive categories (location,

posture and functional behaviours) and into each category, different behaviours were

assigned according to the ethogram described in Table 1. Frequency and duration

performing different behaviours per hour were recorded.

2.4. Statistical methods

Behavioural measurement effects were analysed in a completely randomized design by

using a mixed model with repeated measures, with type of cage (TC), physiological stage

(PS), time of day (Td) and their interactions as fixed effects and hour of the day as a

repeated variable. Rabbit does nested to TC was included in the model as a random

effect. When effects were significant, a t-test was used to make pairwise comparisons to

separate means of the interaction TC x PS. Values are reported as average duration

(seconds per hour and doe) and average frequency (number of times performing an

activity per hour and doe) of each of the behaviours studied ± standard error. Normal

distribution of residuals and variance homogeneity of the data was tested and no

transformations were made. All analyses were performed using SAS (2008).

3. Results

3.1. Location

Time spent by does visiting each cage location over a period of 24 h is presented in Table

2. The effect of time of day (Td) and its interaction with type of cage (TC) and


26

physiological stage (PS) is also shown in this table. To further illustrate the interaction,

additional information is shown in Figure 1.

Table 1. Ethogram of behaviours used per category (location, posture and functional behaviours).

Table 2. Location of does at 2 physiological stages (lactating and gestating) housed in conventional and alternative cages over 24h period (mean ± s.e).

Conventional Alternative P-value

s/h Lactating Gestating Lactating Gestating TC PS TCxPS Td TdxTC TdxPS

Platform - - 903±93 750±86 - NS - <0.001 - NS

Foot mats 2940±55a 1893±78b 1865±92b 1604±84b <0.05 <0.001 <0.001 NS NS NS

Wire mesh 660±55c 1707±78a 831±67c 1246±87b NS <0.001 <0.001 <0.05 NS <0.1

NS: no significant (P>0.1). TC: type of cage. PS: physiological stage. Td: Time of day. Main values are represented in Figure 1.a,b,c Means with different superscripts in the same row differ significantly at P<0.05.

Location

On platform (only in alternative cages)

On foot mats

On wire mesh

Posture

Lying Trunk on ground, forelimbs and hindlimbs tucked under the body

or outstretched

Sitting Forepaws on ground with the forelimbs straight, the thorax and

abdomen visible

Standing Sitting on hindlimbs with both forepaws off the ground

Hyperactivity Hopping in circles around itself or quickly running around in the

cage

Functional

behaviours

Resting Sitting or lying without carrying out any activity

Eating Consumption of feed from the feeder, gnawing the pellet

Drinking Drinking water from nipple drinker

Caecotrophy

Rabbit doe bowed down, pushed the head between hind legs and

ingested caecotrophs (soft faeces) directly from the anus.

Afterwards they rose, and chewed intensively for a few moments.

Grooming Licking, scratching or nibbling of the body

Interacting with

Neighbours

Physical contact with animals from the adjacent cage by biting,

sniffing, licking and removing hair

Interacting with

Kits

Physical contact of the rabbit does with the kits by licking or

pushing them with the head

Nursing Rabbit doe lying with belly exposed and kits suckling

Sniffing Smelling surroundings, with movement of head

Paw scraping Rapid scratching with the forelegs on the floor or feeder

Gnawing Biting wire-net, cage and feeder


27

0%

20%

40%

60%

80%

100%

Lac

tatin

g do

es

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60%

80%

100%

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Conventional Alternative

Ges

tatin

g do

es

Time of the day (h:m)Time of day (h:m)

Rabbit does spent most of the time on foot mats and subsequently on wire mesh (on av.

57.7 and 30.9%, respectively). These times depended on interaction between TC and PS

(P<0.001). In conventional cages, time spent on foot mats by lactating does and on wire

mesh by gestating does was relatively longer than in any other combination of treatments.

Animals placed in alternative cages spent on average, 23.0% of their time on the platform

and this time was not influenced by PS.

The time spent on platform and wire mesh depended on Td (P<0.001 and P<0.05,

respectively). From 17:00 to 01:00 h, rabbit does stayed a longer time on the platform

than on wire mesh (35.0 vs. 19.6% respectively), whereas from 08:00 to 15:00 h minimal

values (on av. 7.1%,) on the platform were reached (see Figure 1).

3.2. Posture

The effect of TC and PS on duration and frequency of different postures by rabbit does is

presented in Table 3. The effect of Td and its interaction with TC and PS is also shown in

this table; additional information is given in Figure 2.

Figure 1. Proportion of time spent by rabbit does at different physiological stages (lactating and gestating) in different locations, wire mesh ( ), foot mats ( ) and platform ( ), housed in conventional and alternative cages throughout the day.


28

Mainly, rabbit does lie (78.4%) and for the remaining time were in the sitting position

(21.4%). TC did not affect (P>0.05) any of these postures. On average, lactating does

spent 2.8% more time lying and 9.3% less time sitting than gestating does (P<0.05).

Frequencies of these postures were also affected by PS (P<0.001), as the values were

higher in lactating than in gestating does (7.57 vs. 6.25; s.e=0.20 and 8.20 vs. 6.61;

s.e=0.21 times/h for lying and sitting respectively). The standing posture was not

performed in conventional cages and it was only observed in gestating does housed in

alternative cages with a frequency of 0.19 times per hour. Hyperactivity was only

observed when rabbit does shared the cage with kits, to flee from kits, with an average

value of 0.21% of the day and a frequency of 0.24 times/h.

Most of these postures were dependent on Td (P<0.001). Does spent most of their time

lying and sitting during light and dark hours, respectively, with the lowest frequencies of

these behaviours occurring from 10:00 to 16:00 h. Standing and hyperactivity were

mainly observed from 19:00 to 24:00 h (see Figure 2).

Table 3. Duration (s/h, mean ± s.e) and frequency (number of times per hour; n/h) of different postures performed by rabbit does at two physiological stages (lactating and gestating) housed in conventional and alternative cages over 24h period.

n.d: not detected. NS: no significant (P>0.10). TC: type of cage. PS: physiological stage. Td: Time of day. Main values are presented in Figure 2.

3.3. Functional behaviours

Duration and frequency of different functional behaviours that rabbit does demonstrated

over a period of 24 h are shown in Table 4 and 5.


Lactating Gestating Lactating Gestating TC PS TCxPS Td TdxTC TdxPS

Duration, s/h

Lying 2829±32 2773±47 2892±29 2794±43 NS <0.05 NS <0.001 NS NS

Sitting 761±32 826±47 701±29 787±42 NS <0.05 NS <0.001 NS NS

Standing - - n.d 18.3±8.8 - NS - NS - NS

Hyperac. 9.03±2.97 n.d 5.95±1.51 n.d NS <0.001 NS <0.001 NS <0.001

Frequency, n/h

Lying 7.69±0.25 6.59±0.23 7.44±0.23 5.89±0.19 NS <0.001 NS <0.001 NS NS

Sitting 8.64±0.31 6.79±0.35 7.76±0.33 6.42±0.34 NS <0.001 NS <0.001 NS <0.001

Standing - - n.d 0.19±0.05 - <0.05 - <0.05 - <0.01

Hyperac. 0.24±0.06 n.d 0.22±0.04 n.d NS <0.001 NS <0.001 NS <0.001


29

0.0

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Fre

quen

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tand

ing

and

hype

ract

ivity

Dur

atio

n ly

ing

and

sitt

ing

(s/h

)

Time of day (h:m)

Figure 2. Evolution throughout the day of time (s/h) spent lying ( ) and sitting ( ) by lactating and gestating does as average. And frequencies performing different postures: hyperactivity in lactating does ( ) and standing in gestating does housed in alternative cages ( ).

For most of the time (on av. 78.9%) does were resting (Table 4). Lactating does spent

more time resting (P<0.05) and with a higher frequency (P<0.001) than gestating does

(2889 vs. 2797 s/h; s.e=39 and 8.03 vs. 6.44 times/h; s.e=0.13, respectively). The other

main activities performed were eating, drinking and grooming (8.69, 1.65 and 9.08% of

the day with a frequency on av. of 2.10, 0.91 and 3.38 times/h, respectively, Table 4).

Table 4. Duration (s/h, mean ± s.e) and frequency (number of times per hour; n/h) of main functional behaviour performed by lactating and gestating does in conventional and alternative cages over 24 h period.



Duration, s/h

Resting 2835±32 2776±47 2942±28 2813±41 NS <0.05 NS <0.001 NS NS

Eating 358±19 304±25 319±19 270±22 <0.1 <0.05 NS <0.001 NS NS

Drinking 87.6±6.9a 48.1±5.5b 56.7±6.0b 45.1±5.2b <0.1 <0.01 <0.05 <0.001 NS NS

Grooming1 270±18 414±32 241±17 383±27 NS <0.001 NS <0.001 NS NS

Frequency, n/h

Resting 7.84±0.25 6.70±0.23 8.21±0.27 6.18±0.20 NS <0.001 NS <0.001 NS NS

Eating 2.86±0.13 1.56±0.1 2.63±0.14 1.36±0.08 NS <0.001 NS <0.001 NS <0.001

Drinking 1.17±0.08 0.92±0.08 0.87±0.08 0.67±0.06 <0.05 <0.05 NS <0.001 NS NS

Grooming1 3.60±0.15 3.54±0.19 2.97±0.15 3.38±0.17 <0.1 NS NS <0.001 NS <0.001

NS:non-significance (P>0.10). a,b,c Means with different superscripts in the same row differ significantly at P<0.05. TC: type of cage. PS: physiological stage. Td: Time of day. Main values are presented in Figure 3. 1Caecotrophy is included


30

0

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s/h

Time of day (h:m)

The time spent eating by rabbit does was affected by TC (P<0.1) and PS (P<0.05), with

higher values in conventional than in alternative cages (331 vs. 295 s/h; s.e=12.8) and in

lactating than gestating does (339 vs. 287 s/h; s.e=13.4). Frequency of eating was also

higher in lactating than gestating does (2.75 vs. 1.46 times/h; s.e=0.09; P<0.001). Does

spent more time drinking and with a higher frequency in conventional than in alternative

cages (by 33.4 and 34.8%; P<0.1 and P<0.05, respectively) and in lactating than in

gestating does (by 54.9 and 28.9%; P<0.01, respectively), but the effect of TC on time

spent drinking was only significant in the case of lactating animals (87.7 vs. 56.7 s/h;

s.e=7.6). Due to the difficulty in distinguishing between grooming and caecotrophy, both

were analysed together and in the present trial these functional behaviours are

collectively referred to as grooming. Time spent on grooming behaviour varied with PS

(P<0.001), as gestating does reached values 56.0% higher, on average, than lactating

does. Does performed grooming behaviour with a higher frequency (P<0.1) in

conventional than in alternative cages (3.58 vs. 3.18; s.e=0.13).

This group of functional behaviours was affected by Td (P<0.001). Resting behaviour

was observed mainly from 10:00 to 19:00 h while other behaviour reached minimum

values (see Figures 3). Concurrent with the soft faeces intake period, a peak of grooming

was observed from 09:00 to 10:00 h.

Figure 3. Evolution throughout the day of time (s/h) spent performing different behaviours by lactating and gestating does as average: resting1

/2.5 ( ), eating ( ), drinking1x2 ( ) and grooming ( ). (1In the figure,

resting and drinking values were divided and multiplied by 2.5 and 2, respectively).


31

Other behaviour such as interacting with neighbours and kits, nursing and sniffing were

also observed (0.12, 0.21, 0.48 and 0.05% of the day, respectively; see Table 5). Duration

and frequency of interacting with neighbours varied depending on the interaction between

PS and TC (P<0.05), showing higher values in conventional than in alternative cages

(5.92 vs. 2.78 s/h; s.e=1.62 and 0.10 vs. 0.08 times/h; s.e=0.03), but this effect was only

significant in gestating does. Time spent interacting with kits was not affected by TC,

although an interaction of Td with TC was observed (P<0.05), as in conventional cages

this behaviour was observed during more time throughout the day, except from 23:00 to

03:00 h when higher values in alternative than in conventional cages were observed

(Figure 4). The frequency of this behaviour was higher in conventional than in alternative

cages (0.36 vs. 0.10 times/h; s.e=0.06; P<0.01). Time spent nursing was not affected by

TC; however, TC had effect on proportion of does nursing per hour (P<0.05), showing

higher values does housed in conventional than alternative cages. This effect depended on

Td (P<0.1), as both alternative and conventional cages nursing behaviour was mainly

observed from 20:00 to 22:00 h, but in conventional cages the period was longer than in

alternative cages (see Figure 5). Sniffing behaviour was observed more frequently in

alternative than in conventional cages (0.01 vs. 0.07; s.e=0.01; P<0.1) and it was not

affected by PS.

Table 5. Duration (s/h, mean ± s.e) and frequency (number of times per hour; n/h) of functional behaviours performed by lactating and gestating does housed in conventional and alternative cages over 24h period.



Duration, s/h

I.Neighbours 0.34±0.34b 11.5±3.08a 1.71±0.93b 3.84±1.29b NS <0.01 <0.05 NS NS NS

Int. Kits 7.38±1.47 - 7.59±2.52 - NS - - <0.01 <0.05 -

Nursing 25.3±7.7 - 9.40±3.7 - NS - - <0.001 NS -

Sniffing 3.28±1.86 0.07±0.07 2.35±1.06 1.33±0.52 NS NS NS NS NS NS

Scraping n.d(4) 29.2±9.60 n.d 21.8±8.97 NS <0.01 NS NS NS NS

Gnawing 2.89±1.14b 17.2±5.2b 9.90±2.84b 61.8±13.8a <0.1 <0.001 <0.05 <0.001 NS <0.05

Frequency, n/h

I.Neighbours 0.01±0.01c 0.19±0.03a 0.04±0.01bc 0.11±0.03b NS <0.01 <0.05 <0.01 NS NS

Int. Kits 0.36±0.06 - 0.10±0.02 - <0.01 - - <0.01 NS -

Nursing1 0.14±0.03 - 0.05±0.02 - <0.05 - - <0.001 <0.1 -

Sniffing 0.01±0.01 0.01±0.01 0.05±0.01 0.08±0.02 <0.1 NS NS NS NS NS

Scraping n.d 0.18±0.06 n.d 0.14±0.06 NS <0.01 NS NS NS NS

Gnawing 0.10±0.03b 0.26±0.05b 0.19±0.05b 0.57±0.09a <0.1 <0.001 <0.1 <0.001 NS <0.05

nd: not detected. NS:non-significance (P>0.10). a,b,c Means with different superscripts in the same row differ significantly at P<0.05.TC:type of cage. PS: physiological stage.Td: Time of day. Main values effects are presented in Figures 4 and 5. 1 Proportion of does nursing per hour.


32

Figure 4. Evolution throughout the day of time (s/h) spent by rabbit does interacting-with-kits in

conventional cages ( ) or in alternative cages ( ).

Behaviours such as paw scraping and gnawing were performed during 0.35 and 0.62% of

the day with a frequency on av. of 0.17 and 0.28 times per hour, respectively (Table 5).

Paw scraping was only observed in gestating does and did not depend on TC. An

interaction between TC and PS (P<0.05) was observed for time and frequency of

gnawing behaviour, with the highest time and frequency of performing gnawing by

rabbits housed in alternative cages was only significant for gestating does (17.2 vs. 61.8

s/h; s.e=10.7 and 0.26 vs. 0.57 times/h; s.e=0.08, for conventional vs. alternative cages,

respectively).

Figure 5. Evolution throughout the day of proportion of rabbit does nursing per hour in conventional ( ) and alternative cages ( )


33

4. Discussion

Under commercial farm conditions, location preference by rabbit does varied depending

on housing. Results showed that when a raised platform is available, rabbit does spent

23% of their time, on average, on the platform (Table 2). This result agrees with a

previous study using two-floor cages (Mirabito, 2007), where lactating does spent 28% of

time, on average, on the upper floor. A higher value, 53% of the time on the raised

platform, was reported by Finzi et al. (1996). In the present trial the time spent by does

on the platform was independent of their PS, indicating that the use of the platform was

not related to the available surface that is larger in gestating does than in lactating ones

because of the presence of the kits. The time that does spent on the platform, which is

inaccessible for kits, was higher from 17:00 to 01:00 h and especially between 21:00 to

23:00 h (Figure 1). Also a peak in nursing behaviour was observed in this period, being

the proportion of does nursing per hour lower in animals housed in alternative than in

conventional cages (Figure 5). This is in agreement with Selzer et al. (2004), who found

that most nursing events occurred between 20:00 and 22:00 h, whereas a decrease in

nursing activity was observed in the early morning. They also found that nursing activity

tended to decrease moderately with increasing size of cage and with the provision of

enrichment (an elevated seat for the doe in the get-away-cage or a tunnel at the entrance

to the nest box). During this time which both peak nursing and higher use of platform

happened, does exhibited a higher regularity of hyperactivity, a symptom of restlessness

(Figure 2). This overlap could be due to the fact that the 24 day old kits are not satisfied

with the milk provided for them and as a result seek more from the mother, in response

does flee from them. These results and the lower proportion of does nursing per hour

observed in alternative suggest that the platform was used as an escape by rabbit does in

the late phase of the lactation period, when they are tired and the kits still wanted to

suckle. This result is in agreement with Mirabito (2007), who showed that the time spent

on the platform by nursing does increased between the second and fourth week after

parturition (from 20 to 35%), in parallel to the emergence of the kits and the removal of

the nest boxes.

According to the results obtained, rabbit does showed a clear preference for foot mats

above wire mesh floors in conventional and alternative cages, especially when kits close

to the weaning age were present (Table 2). Under these conditions, does have less room,

competing with kits for the most comfortable place. These results confirm those obtained

by Princz et al. (2008b), who reported that growing rabbits preferred plastic nets covering


34

wire mesh floors. Moreover, Rosell and de la Fuente (2009) showed a positive

relationship between the use of foot mats and animal welfare after finding a significant

reduction in the prevalence of sore hocks in farms where foot mats were used. It follows

that these findings suggest a higher level of comfort and welfare for rabbit does reared on

this type of flooring and with a raised platform at the end of lactation period. Noteworthy;

the use of platforms raise hygiene issues due to the accumulation of faeces and

subsequently faeces and urine falling onto animals located in the lower part of the cage.

Some alternatives to prevent this problem have been studied by Finzi et al. (1996), who

trained animals to excrete in the lower part of the cage by preventing access to the

platform during the first two days. Drip trays were also used leading to animals spreading

more evenly in the cage without the risk of soiling from above (Szendro et al., 2012).

Frequently, the welfare of rabbits reared under commercial conditions has been evaluated

by comparing their functional behaviours with those observed in wild rabbits. However,

the natural behavioural repertoire includes activities that are adaptions to adverse

conditions, for example, hiding from predators or displaying the alert position (standing

on its hindlimbs) considered as an indicator for variable or poor welfare (Dawkins, 2008).

Under commercial conditions, this position is not possible as the height of standard cages

used in Europe varies between 29 and 40 cm (Trocino and Xiccato, 2006) and, depending

of the rabbit’s size, a minimum of approximately 75 cm high is required (Morton et al.,

1993). In addition, as mentioned by Princz et al. (2008a), the relevance of this behaviour

in the commercial cage system may be limited due to the lack of predators. Accordingly,

in the current trial, height of alternative cages (60 cm) was enough to perform standing

posture and it was rarely observed. The individual variation in the standing posture

among animals was high, and it was exclusively performed to eat and smell retained

faeces on the platform. Martrenchar et al. (2001) reported that in cages without enclosed

ceilings, animals performed standing behaviour less than 0.7% of the time of the day.

However, they concluded that certain behaviour can be important even if they are rarely

practised. In an open field study (testing the behaviour of animals that are otherwise

housed in different cage systems, compared under the same stimuli and environment),

Hansen and Berthelsen (2000) found that rabbits previously housed in the conventional

cage system (40 cm of height) performed the standing posture significantly more time

(3.4 vs. 2.6%) than rabbits housed in alternative cages (80 cm of height). Regarding the

height of the cage, Princz et al. (2008a) reported that the commonly used height in

commercial cages (30-35 cm) was satisfactory for growing rabbits. In the present trial,


35

does housed in conventional (30 cm high) and alternative cages (40-60 cm) showed times

spent on the comparable postures as lying and sitting were not significantly different.

These results suggest comfort in this posture irrespective of the height of the cage.

In the current study, rabbit does spent most of their time lying and the duration of this

behaviour was not affected by the TC. Generally when animals were lying (mainly during

the light period, Figure 2) they were resting, and this is the reason why the duration for

both types of behaviour was almost the same. Gunn and Morton (1995) and Fernández-

Carmona et al. (2005) observed that rabbits spent more time resting and sleeping during

the light period and were more active during the dark period. In this work, most of the

functional behaviours were also observed mainly during the dark period (Figures 3, 4 and

5) and when rabbit does were sitting. Frequency of certain behaviour while sitting was

lower in alternative cages, such as drinking, grooming (P<0.1), interacting with

neighbours (only in gestating does) and with kits, indicating that animals might be more

restless in conventional than in alternative cages. Frequent changes of behaviours have

been described as a sign of increased stress in animals (Lehmann, 1987; Hughes and

Duncan, 1988) that can show abnormal behaviour, such as bar-biting, excessive

grooming or other stereotypic activities (Morton et al., 1993; Love, 1994). Hansen and

Berthelsen (2000) found that females were more restless in conventional cages, showing

excessive grooming, bar-gnawing and timidity with respect to those housed in alternative

cages with a platform. However, in the present trial the mean values of these behaviours

were not so excessively high, and for example, grooming included caecotrophy which is

natural behaviour and not a stereotypic activity. The current data showed that duration

and frequency of gnawing were higher in alternative than in conventional cages and

especially in the gestation phase. An explanation might be based on the fact that after

weaning, rabbit does are more quiet but also more bored, an available platform may lead

to distraction such as biting the bars or smelling droppings retained on the platform. In

addition, the use of enriching elements such as straw or “toys” could be an option to

minimize the stress and boredom of gestating does housed in cages. Similarly, María et

al. (2005) found an improvement of rabbit does welfare (enlarging the spectrum of

behaviour) through the use of enrichment elements as wooden toys with different shapes,

straw or a tube of PVC. Lidfors (1997) also found that male laboratory rabbits showed

less abnormal behaviour when different objects were available in the cage, presenting

alternative activity to alleviate boredom.


36

Contrary to expectation, in the present work lactating does spent more time resting than

gestating does (Table 4) the most obvious explanation for this being the less available

surface in the lactating phase. Ribikauskas et al. (2010) also observed lower activity in

growing rabbits housed in wire cages with a higher density than in those housed in pens

with more functional space. However, in the current study the shorter resting time in

gestating does might also be due to nervousness a result of being close to the parturition

date, leading to the prevalence of longer and higher frequency of activities such as

grooming, interacting with neighbours, paws scraping and gnawing.

5. Conclusions

Rabbit does under commercial conditions will maintain their circadian behavioural

pattern depending on their PS and housing system. The platform is frequently used by

rabbit does, independently of their physiological state (with or without kits) or the

available space in the cage. Additionally, the platform is used as an escape by rabbit does

in the late phase of the lactation period, when they are tired and the kits still wanted to

suckle. The PS of rabbit does exert a stronger influence than the TC on the duration and

frequency spent performing functional behaviours. After weaning, in the proximity of the

parturition day, rabbit does are more restless than lactating does and therefore, the

addition of enrichment elements could provide extra stimulus during this period. An

increase of cage height to allow rabbit does to perform standing posture, without placing

a platform would not improve rabbit does welfare status, as this behaviour has no real

function in a controlled, predator free environment. Moreover, conventional cages with

30 cm height seem to be satisfactory for rabbit does, since stereotypies were not

observed. In addition, care should be taken when implementing the use of platforms as

they are associated with hygiene issues such as faeces and urine falling onto animals

located in the lower part of the cage.


37

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Dawkins M.S. 2008. The science of animal suffering. Ethology, 114: 937-945.

EFSA (European Food Safety Authority). 2005. The impact of the current housing and


Journal, 267: 1–137.

Fernández-Carmona J., Solar A., Pascual J.J., Blas E., Cervera C. 2005. The behaviour of

farm rabbit does around parturition and during lactation. World Rabbit Sci., 13: 253-

277.


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Gunn D., Morton D.B. 1995. Inventory of the behaviour of New Zealand White rabbits in

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Hansen L.T., Berthelsen H. 2000. The effect of enviromental enrichement on the

behaviour of caged rabbits (Oryctolagus cuniculus). Appl. Anim. Behav. Sci., 68:

163-178.

Hughes B.O., Duncan I.J.H. 1988. The notion of ethological ‘need’, models of motivation

and animal welfare. Anim. Behav., 36: 1696–1707.

Lehmann M. 1987. Interference of a restricted environment — as found in battery cages

— with normal behaviour of young fattening rabbits. In Auxilia T. (Ed), Rabbit

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Publishing, Luxembourg, Brussels, pp. 257-268.

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conejas reproductoras alojadas en jaulas individuales. In Proc.: XXX Symposium de

Cunicultura, ASESCU, 18-20 May, Valladolid, Spain, pp. 71-76.


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Martrenchar A., Boilletot E., Cotte J.P., Morisse J.P. 2001. Wire-floor pens as an

alternative to metallic cages in fattening rabbits: influence on some welfare traits.

Anim. Welfare, 10: 153–161.

Mirabito L. 2007. Logement et bien-être du lapin plus de questions que de réponses ?.

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Moreno S., Villafuerte R., Delibes M. 1996. Cover is safe during the day but dangerous at

night: the use of vegetation by European wild rabbits. Can. J. Zool., 74: 1656–1660.

Morton D.B., Jennings M., Batchelor G.R., Bell D., Birke L., Davies K., Eveleigh J.R.,

Gunn D., Heath M., Howard B., Koder P., Phillips J., Poole T., Sainsbury A.W.,

Sales G.D., Smith D.J.A., Stauffacher M., Turner R.J. 1993. Refinements in rabbit

husbandry. Second report of the BVAAWF/FRAME/RSPCA/UFAW joint working

group on refinement. Lab. Anim., 27: 301-329.

Princz Z., Radnai I., Biró-Németh E., Matics Z., Gerencsér Z., Nagy I., Szendro Z.

2008a. Effect of cage height on the welfare of growing rabbits. Appl. Anim. Behav.

Sci., 114: 284-295.

Princz Z., Dalle Zotte A., Radnai I., Bíró-Németh E., Matics Z., Gerencsér Z., Nagy I.,

Szendrő Z. 2008b. Behaviour of growing rabbits under various housing conditions.

Appl. Anim. Behav. Sci., 111, 342-356.

Ribikauskas V., Ribikauskienė D., Skurdenienė I. 2010. Effect of housing system (wire

cages vesus group-housing) and in-house air quality parameters on the behavior of

fattening rabbits. World Rabbit Sci., 18: 243-250.

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pododermatitis in domestic rabbit does. Anim. Welfare, 18: 199-204.

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SAS Institute Inc., Cary, NC, USA.

Szendro Zs., Matics Zs., Odermatt M., Gerencse Zs., Nagy I., Szendro I., Dalle Zotte A.

2012. Use of different areas of pen by growing rabbits depending on the elevated

platforms’ floor-type. Animal, 6: 650–655.

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different housing conditions. Appl. Anim. Behav. Sci., 87: 317-324.


39


on housing systems. World Rabbit Sci., 14: 77–93.

Chapter 2: Development of simplified sampling methods

40

CHAPTER 3: DEVELOPMENT OF SIMPLIFIED

SAMPLING METHODS OF BEHAVIOURAL DATA IN

RABBIT DOES

CHAPTER 3:

(EXPERIMENT 2)

SECOND REVIEW IN:

World Rabbit Science

DEVELOPMENT OF SIMPLIFIED SAMPLING METHODS

OF BEHAVIOURAL DATA IN RABBIT DOES


41

1. Introduction

In rabbits, as in other species, welfare conditions may be measured using behavioural,

physiological, pathological and productive indicators. Behavioural observation

techniques are appropriate to determine space allowances and to identify and evaluate

abnormal conducts that could be associated to an impairment of welfare in farmed

animals (stereotypies).

Continuous record is the most accurate method for behavioural measurements, but it is

difficult to conduct due to time needed if a large number of animals and a wide type of

behaviours are studied. Thus, in many cases it is necessary to design simplified

observation methods. Sampling techniques have been described by Altmann (1974), to

reduce the time required to study animal behaviour. However, these techniques should be

validated to ensure proper collection and interpretation of the data. A good estimation of

duration of an activity is obtained if the observation period lasts long enough and if the

interval between the samples is not too long (Broom and Fraser, 2007). Depending on

frequency and length, the limitations and advantages of different types of simplified

observation methods of animal behaviour have been examined by Arnold-Meeks and

McGlone (1986), Martin and Bateson (1993), Mann (1999) and Mitlöhner et al. (2001).

These techniques have been studied in animal species such as mice, swine, primates,

cattle or cetaceans. Rabbits show an important nocturnal activity and the use of visible

light to control rabbits’ behaviour can lead to alterations in circadian periodicity that lead

to disturbances of conducts. In addition, the presence of an observer can influence

behavioural patterns of rabbits. Nowadays, infrared observation techniques allow a

continuous view of the animals for 24 h, without disturbing them overnight and not

affecting their behaviour. Different record frequencies and lengths have been used in

behavioural rabbit research, as one every 15 min throughout 24 h (Morisse and Maurice,

1997), one min every hour throughout 24 h (Morisse et al., 1999), 15 min at the end of

the light period and at the beginning and in the middle of the dark period (Chu et al.,

2004), instantaneous observations (scan sampling) with a frequency of 5 min during 6 h

for the light period and 6 h for the dark period (Princz et al., 2008) or 5 min in the

morning and 5 min in the afternoon (Mugnai et al., 2009). However, these techniques

have not been validated in farmed domestic rabbits yet.


42

The aim of this study was to compare the results of different simplified sampling

techniques of behavioural data with respect to reference records of 24-h on the

assessment of rabbit does behaviours at different physiological stages (gestation and

lactation) housed in two type of cages (conventional and alternative).

2. Material and methods

2.1. Animals and housing

All the experimental procedures were approved by the Ethics Committee of the

Polytechnic University of Madrid and were in compliance with the Spanish guidelines for

the care and use of animals in research (Boletín Oficial del Estado, 2013).


Toledo, Spain. A total of 12 multiparous rabbit does (Oryctolagus cuniculus) in their

fourth reproductive cycle from a hybrid maternal line (Hy-Plus) were used. Animals

weighed on average 4.5 kg live weight, and were inseminated 25 d after kindling, being

kits weaned 32 d after kindling. All animals were housed in the same artificially lighted

room. The light:dark cycle was 15:9 h (light interval from 06:00 to 21:00 h and dark

interval from 21:00 to 06:00 h). From the first artificial insemination, half of the rabbit

does were individually housed in alternative polyvalent cages (385×995×600 mm) with a

wire platform (381×310 mm) raised at 400 mm from the floor. The other half of animals

was individually housed in conventional polyvalent cages (385×995×300 mm). All the

cages were equipped with a feeder and a nipple drinker placed in the lower level and a

foot mat (perforated plastic plate) in the middle of the floor. Heating, cooling and forced

ventilation systems allowed the building temperature to be maintained between 20 and 23

°C throughout the experiment.

2.2. Feed

Rabbits were fed ad libitum with a commercial pelleted diet (Cunilactal, NANTA, S.A.,

Spain). Triplicate chemical analysis of feed was performed according to AOAC

International (2000) procedures, and the average composition on as fed basis was: crude

protein 18.6%, ether extract 3.8%, starch 22.0%, crude fibre 14.4% and ash 8.2%.


43

Method

R2.4

R8

I6

I8

Hour 2:00 3:00 4:00 5:00 6:00 7:0020:00 21:00 22:00 23:00 0:00 1:0014:00 15:00 16:00 17:00 18:00 19:008:00 9:00 10:00 11:00 12:00 13:00

2.3. Behavioural measurements

The observations were performed on the same does at the end of the lactation period (24

days after parturition) with eight kits per litter, and one week before next parturition

(three days after weaning in pregnant not lactating does). All females’ records were

captured simultaneously for 24 h per day. While recording behaviour nobody entered into

the room to avoid disturbances on rabbit does behaviour. Behaviours were recorded by

infrared video cameras (VCB-3380/Sanyo) and a LED infrared reflector (IR-880/12D)

placed on bars 2 m above the cages. Video recordings were analysed in their entirety by

one trained person viewing at double speed, the data was then entered into the computer

using “The Observer XT 8.0” software (Noldus Information Technology, Wageningen).

Observations were classified into three exclusive categories (location, posture and

functional behaviours) and into each category behaviours were assigned according to the

ethogram described in Table 1. Grooming and caecotrophy behaviours were considered

as one due to difficulty in distinguishing them, and were just referred to as grooming.

2.4. Experimental design

Continuous video-records obtained during 24 h (reference method) were cutting out in

sequences of different frequency and length, in order to decrease total observation time.

The choice of the length and frequency of the recordings depended upon several

considerations such as, the duration, frequency and distribution of throughout the day of

the broad range of rabbit behaviours. Thereby, a total of four new videos (simplified

sampling methods) were designed considering records of different length (2 min or 2 h)

in regular frequencies throughout the day (every 20 min or 6 h) and records of 1 h with a

higher frequency during the activity period of rabbits. Specifications of these methods

were as follows (Figure 1):

Figure 1. Frequency and duration of video recordings of different sampling methods. Black sections show recording periods.


44

• Regular-short method (R2.4): records for the first 2 min out of every 20 min. Total

recorded time: 2.4 h/d.

• Regular-long method (R8): records for the first 2 h out of every 6 h. Total recorded

time: 8 h/d.

• Irregular short 6h method (I6): records for 1 h, twice during the rest period and 4

times during the active period . Total recorded time: 6 h/d.

• Irregular long 8h method (I8): records for 1h, twice during the rest period 6 times

during the active period. Total recorded time: 8 h/d.

To represent behaviour over the whole day, the time recorded at each behavioural

category during the different recording sequences was multiplied by the appropriate

factor depending on frequency and duration of them in each selected method. In regular

methods (R2.4 and R8), time of each behaviour recorded during each sequences (2 min

and 2 h) were multiplied by 10 and 3 respectively, and in irregular methods (I6 and I8) by

6 in both cases during rest period sequences and 3 and 2 during the active period

sequences, respectively.


Behavioural measurements effects were analysed in a completely randomized design by

using a mixed model with repeated measures, with type of cage, physiological stage,

observation method and their interactions as fixed effects and physiological stage within

type of cage as the repeated term. Rabbit does nested to type of cage was included in the

model as a random effect. Only the effect of methods and their interactions with type of

cage and physiological stage are shown, as type of cage and physiological stage effects

were discussed in a previous article (Alfonso-Carrillo et al., 2014). When method effect

and their interactions were significant, a Dunnet test was used to make pairwise

comparisons using reference method as control treatment. Traits values are reported as

average duration (min per day and doe) ± standard error. All analyses were performed

using SAS (2008). Estimation errors of different simplified sampling methods are

represented as:

��ℎ�� − ��ℎ��

��ℎ��100


45

3. Results

3.1. Location

No significant effect of observation method and their interactions with physiological

stage and type of cage was detected on the time spent by rabbit does on different

locations (Table 2). According to values obtained with the reference method, females

spent on average 57.6, 30.9 and 23.0% of the day on foot mats, wire bars and platform,

respectively, and the estimation errors observed using simplified methods were low (on

average 1.06, 1.52 and 1.66 %, respectively; Figure. 2).

Table 2. Comparison of the simplified methods with the reference method on the time (min/d ± s.e) spent by does on different locations.

Methods1 Reference R-2.4 R-8 I-6 I-8 P value

Foot mats 829±63 841±68 831±68 824±62 845±62 0.952

Wire bars 445±49 433±52 449±49 444±47 455±46 0.962

Platform2 331±81 331±82 321±83 343±83 331±76 0.827

R-2.4: regular short; R-8: regular long; I6: irregular short; I8: irregular long.1Interactions method x type of cage and method x physiological stage were not significant.2Only does housed in enriched cages were considered.

3.2. Posture

The effect of observation methods and the comparison of the simplified sampling

methods with the reference one on the time spent by does performing different postures

are shown in Table 3.

Table 3. Comparison of the simplified method with the reference method on the time (min/d ± s.e) spent by does in different postures in two physiological stages (gestating and lactating).


Lying 1129±11 1142±12 1116±14 1107±19* 1116±19 0.003

G2 1113±18 1136±19 1097±22 1057±29*** 1073±27** <0.001

L3 1145±9 1149±16 1135±16 1156±15 1161±17 0.305

Sitting 308±11 294±13 318±15 328±19* 320±19 0.003

G2 323±20 298±21 337±23 379±30*** 363±27** <0.001

L3 292±9 289±16 301±17 279±15 275±17 0.327

Standing2,4 7.0±6.8 12.1±9.7 11.4±11.1 9.4±8.9 11.1±3.5 0.337

Hyperactivity3 3.0±0.6 1.3±0.8 4.3±2.1 3.5±1.1 3.2±0.8 0.291

R-2.4: regular short; R-8: regular long; I6: irregular short; I8: irregular long. 1Interaction method x type of cage was not significant. Means differ significantly respect to reference method at *P<0.05; **P<0.01;*** P<0.001, respectively. 2,3Interaction of method x physiological stage was significant and only gestating or lactating does were considered, respectively. 4Only does housing in alternative cages were considered.


46

The method of observation affected the estimation of the time spent in lying and sitting

postures (P<0.05); the differences among the simplified sampling methods with the

control were independent of type of cage, but were affected by physiological stage

(P<0.001). According to reference method, gestating and lactating does spent on average

77.3 and 79.5 % of the day lying and 22.4 and 20.3 % sitting, respectively. In lactating

does, the estimates reached by simplified methods for both postures did not differ to the

reference method; however, in gestating does, the estimates of the irregular methods were

significant different to the reference method in both postures (P<0.001 and P<0.01 for I6

and I8, respectively).

The standing posture was only observed in gestating does housed in alternative cages

with an average value of 0.49 % of the day. Hyperactivity was only observed when rabbit

does share the cage with kits, to flee from kits, with an average value of 0.21 % of the

day. Both postures were not affected by the observation method, but simplified methods

reached high estimation errors (57.1 and 30.8 % for standing and hyperactivity postures

on average, respectively; Figure. 2).

3.3. Functional behaviours

The effect of observation methods and the comparison of the simplified sampling

methods with the reference one on the time spent by does performing different functional

behaviours are shown in Table 4.

The effect of observation methods on functional behaviours was always independent of

the housing system. For resting, grooming, eating and gnawing, the effect of observation

methods varied with the physiological stage, as differences between some simplified

sampling methods with the reference method were observed in gestating but not in

lactating does. In gestating does, irregular methods, I6 and I8, underestimated by 4.7 and

3.9 % (P<0.001 and P<0.01) resting behaviour and overestimated by 20.0 and 22.5 %

(P<0.001 and P<0.01) grooming behaviour, respectively, with respect to the reference

method. The irregular method I6 also led to higher gnawing values in gestating does (by

44.9 %, P<0.05) than the reference method. For the eating behaviour, the regular short

method in gestating does led to a lower values than the reference method (115±9 vs

96±11 min/d; P<0.01).

Estimations of time spent in the other functional behaviours analysed such as drinking,

sniffing, nursing, interacting with neighbour and kits and paw scraping did not differ


47

from values obtained with the reference method. Average values registered for these

behaviours in the reference and simplified sampling methods were 1.65 vs 1.69, 0.05 vs

0.06, 0.48 vs 0.51, 0.12 vs 0.14, 0.21 vs 0.24 and 0.71 vs 0.86 % of de day, on average

respectively.

Table 4. Comparison of the simplified methods with the reference method on the time (min/d) spent by does performing different functional behaviours in two physiological stages (gestating and lactating).


Resting 1136±11 1146±20 1119±18 1119±13 1122±14 0.013

G2 1117±19 1138±30 1097±26 1064±20*** 1073±23** <0.001

L3 1155±10 1153±14 1142±15 1174±17 1171±15 0.128

Grooming 131±10 135±15 140±14 144±12 147±13 0.231

G2 160±15 157±22 173±21 192±19** 196±19** 0.001

L3 102±5 113±10 107±8 97±11 99±10 0.619

Drinking5 23.8±2.4 19.0±3.1 27.1±2.5 25.2±4 26.1±3.5 0.022

Eating 125±6 114±7 125±7 120±8 120±7 0.206

G2 115±9 96±11** 115±12 119±9 116±9 0.013

L3 136±8 133±9 135±8 121±11 125±10 0.167

Sniffing 0.72±0.27 0.43±0.79 1±0.51 1.43±0.34 0.87±0.35 0.248

Nursing4 6.92±2.47 3.88±3.55 10.52±1.43 8.78±3.27 6.33±4.79 0.133

Interacting-

neighbour4 1.73±0.64 2.02±0.83 2.17±0.66 1.87±0.73 1.73±0.63 0.931

Interacting-

kits3 3.02±0.84 4.75±0.86 3.45±0.97 2.17±1.86 3.17±1.29 0.291

Gnawing 9.22±3.28 11.08±4.42 8.78±4.69 13.1±4.34 10.52±2.77 0.289

G2 15.8±6.0 21.3±7.9 14.3±8.4 22.9±7.7* 18.6±4.9 0.032

L3 2.60±0.91 0.72±1.55 3.32±0.48 3.45±0.54 2.45±1.78 0.905

Paw scraping2 10.2±7.0 13.1±10.3 10.7±7.4 15.3±9.3 10.2±7.2 0.388

R-2.4: regular short; R-8: regular long; I6: irregular short; I8: irregular long. 1Interaction method x type of cage was not significant. Means differ significantly respect to reference method at **P<0.01;*** P<0.001, respectively. 2,3Interaction of method x physiological stage was significant and only gestating or lactating does were considered, respectively. 4Only does housing in alternative cages were considered.

4. Discussion

The wide range of behaviours that can be analysed in an animal study with their duration

and frequency during the day and even at different animal physiological stages evidenced

the need of validating simplified observation methods to assure the quality of these

studies. In the present study, the accuracy of simplified methods varied depending on the

physiological stage of does for behaviours as lying, sitting, resting, grooming and

gnawing. These findings show that when animals change of position or functional


48

behaviour more frequently as gestating does close to the parturition day, some of the

simplified methods, mainly the irregular ones, are not suitable to estimate behaviours

performed throughout the whole day. However, regular methods (R2.4 and R8) were

accurate for measuring behaviours of long length as lying, sitting, resting and grooming,

and the R2.4 method seems to be the most suitable one from a practical point of view.

Therefore, this result show that methods with short observation periods provide a useful

estimate of animal behaviour if the duration of the activity is long enough, as Broom and

Fraser (2007) asserted. Other methods similar to the regular short one used in this work,

as the scan sampling method, which describes animal behaviour at a fixed time interval

have been already validated in others species. Mitlöhner et al. (2001), in a study for

feedlot cattle, showed that scan sampling methods can provide an unbiased estimate of

percentage of time of behaviour when the interval between scans is short enough relative

to the duration of the behaviour, being intervals of 60 min too long for most of

behaviours studied. In this sense, scan sampling techniques have been used in the study

of rabbit behaviour and some of them with long intervals between observations,

regardless of the behaviour. Morisse and Maurice (1997), in a study of rabbit behaviour

used sequences of one min every 15 min to evaluate different behavioural groups;

however, Morisse et al. (1999), analysing the same group of behaviours lengthened

interval between sequences up to 60 min.

In the current work when studying behaviours performed on short time during the day

(hyperactivity, eating, drinking, nursing or social interactions), high estimation errors

were observed, mainly when using regular methods, being the irregular long method (I8)

the most accurate for these traits (Figure 2). This result might be explained by the longer

observation time from dusk until dawn, when rabbits are more active and performed with

higher frequency these kind of behaviours, as observed by Alfonso-Carrillo et al. (2014)

in a study of behaviour pattern of rabbit does throughout 24 h. Even so, the irregular long

method was not accurate enough for other short and infrequent behaviours such standing

or sniffing due to their high variation. It would be advisable an increase in the number of

replicates to get more reliable information for this type of behaviours.

5. Conclusions

Simplified behavioral sampling methods can been used to reduce the total observation

time required to assess different types of behaviours. However, depending on the


49

behaviour studied, some methods are more accurate than others. From a practical point of

view, the regular short method (R2.4) is the best option to study long duration

behaviours. For shorter length behaviours and due to the nocturnal activity of rabbits,

methods with longer records time during the dark period would be preferable. Because of

the high coefficient of variation of these later behaviours mentioned an increase in the

number of animals observed would be recommended.

Figure 2. Estimation error of different simplified behavioural methods


50


51

6. References

Alfonso-Carrillo C., Martín E., De Blas C., Ibáñez M.A., García-Rebollar P., García-Ruiz

A.I. 2014. Effect of cage type on the behaviour pattern of rabbit does at different

physiological stages. World Rabbit Sci., 22: 59-69. doi:10.4995/wrs.20141396

Altmann J. 1974. Observational study of behavior: Sampling Methods. Behaviour, 49:

227–267.

AOAC International, 2000. Association of Official Analysis Chemists. Official Method

of Analysis of the Association of Official Analytical Chemists International. 17th ed.

AOAC, Gaithersburg, MD.

Arnold-Meeks C.A., McGlone J.J. 1986. Validating techniques to sample behavior of

confined, young pigs. Appl. Anim. Behav. Sci., 16: 149–155. doi.org/10.1016/0168-

1591(86)90107-3

Boletín Oficial del Estado. 2013. Real Decreto 53/2013 por el que se establecen las

normas básicas aplicables para la protección de los animales utilizados en

experimentación y otros fines científicos, incluyendo la docencia. BOE-A-2013-

1337.

Broom D.M., Fraser A.F. 2007. Describing, Recording and Measuring Behaviour. In:

Broom, D.M., Fraser, A.F. (Eds.), Domestic Animal Behaviour and Welfare.

Cambridge University Press, Cambridge, U.K, pp. 17-26.

Chu L., Garner J.P., Mench J.A. 2004. A behavioral comparison of New Zealand White

rabbits (Oryctolagus cuniculus) housed individually or in pairs in conventional

laboratory cages. Appl. Anim. Behav. Sci., 85: 121-139. doi.org/10.1016/

j.applanim.2003.09.011

Mann J. 1999. Behavioral sampling methods for cetaceans: a review and critique. Marine

Mammal Sci., 15: 102-122. doi: 10.1111/j.1748-7692.1999.tb00784.x

Martin P., Bateson P. 1993. Recording Methods. In: Martin, P., Bateson, P. (Eds.),

Measuring Behaviour. An introductory guide, Cambridge University Press.

Cambridge, U.K, pp. 84-100.

Mitlöhner F.M., Morrow-Tesch J.L., Wilson S.C., Dailey J.W., McGlone J.J. 2001.

Behavioral sampling techniques for feedlot cattle. J. Anim. Sci., 79: 1189-1193.

Morisse J.P., Boilletto E., Martrenchar A. 1999. Preference testing in intensively kept

meat production rabbits for straw on wire grid floor. Appl. Anim. Behav. Sci., 64: 71-

80. doi.org/10.1016/S0168-1591(99)00023-4


52

Morisse J.P., Maurice R. 1997. Influence of stocking density or group size on behaviour

of fattening rabbits kept under intensive conditions. Appl. Anim. Behav. Sci., 54:

351-357. doi.org/10.1016/S0168-1591(96)01188-4

Mugnai C., Dal Bosco A., Castellini C. 2009. Effect of different rearing systems and pre-

kindling handling on behaviour and performance or rabbit does. Appl. Anim. Behav.

Sci., 118: 91-100. doi.org/10.1016/j.applanim.2009.02.007

Princz Z., Dalle Zotte A., Radnai I., Biró-Németh E., Matics Z., Gerencsér Z., Nagy I.,

Szendrő Zs. 2008. Behaviour of growing rabbits under various housing conditions.

Appl. Anim. Behav. Sci., 111: 342-356. doi:10.1016/j.applanim.2007.06.013

SAS. 2008. SAS/STAT User's Guide, version 9.3. SAS Inst. Inc., Cary NC,

Chapter 4: Effect of late weaning and use of alternative cages

53

CHAPTER 4: EFFECT OF LATE WEANING AND USE OF

ALTERNATIVE CAGES ON PERFORMANCE OF DOES,

SUCKLING AND FATTENING RABBITS UNDER

EXTENSIVE REPRODUCTIVE MANAGEMENT

CHAPTER 4:

EFFECT OF LATE WEANING AND USE OF

ALTERNATIVE CAGES ON PERFORMANCE OF DOES,

SUCKLING AND FATTENING RABBITS UNDER

EXTENSIVE REPRODUCTIVE MANAGEMENT

(Experiment 3)

PUBLISHED IN:

Livestock Science 167:425-434

doi: 10.1016/j.livsci.2014.05.018


54

1. Introduction

The requirements of farmed rabbit does have increased, because of intensification of the

reproductive rhythms leading to a wide overlapping between lactation and gestation, and

genetic selection programs focused on a higher productivity (Pascual, 2010). Limited

dietary intake, mainly in primiparous does, leads to a body energy deficit (Xiccato and

Trocino, 2010), decreasing the productivity of does and impairing the general health

status of the farm (Pascual et al., 2006). Thus, the replacement rate of does is at present

around 100-120 % in commercial rabbit farms (Coutelet, 2011; Sánchez del Cueto et al.,

2012). It has been reported by several authors (Cervera et al., 1993; Xiccato et al., 2005)

that a strategy to improve the reproductive life of the rabbits does could be a delay of the

insemination postpartum, reducing body energy deficit, increasing fertility and improving

welfare of the rabbit does. However, because the theoretical maximum number of

parturitions per year and per doe decreases, an extensive reproductive management

program could impair the profitability of rabbit farms compared to conventional

management. Otherwise, special care should be taken to avoid excessive deposition of fat

in extensive systems due to an increased length of the dry period (Castellini, 2007). On

the other hand, high rates of mortality are observed in fattening rabbitries, especially

since the emergence of epizootic rabbit enteropathy (Licois et al., 2006). A delay of

weaning age may help to decrease fattening mortality in poor hygienic conditions

(Romero et al., 2009) due to the protective role of rabbit milk against some pathogens

(Gallois et al., 2007) and to the higher weight and age at weaning (Lebas 1993). Although

Xiccato et al. (2005) found that longer lactations (25 vs. 21 days) can exacerbate the body

energy deficit of does, a lower impact of this effect might be expected when comparing

conventional with late weaning (32 vs. 46 days), because of the decrease in milk

production after four to five weeks of lactation. An extensive reproductive system in

combination with a long lactation period could thus be an alternative to improve the

reproductive performance of does while improving young rabbit performance.

Late weaning decreases the available floor surface per animal, which results in a negative

perception of animal welfare (Vanhonacker et al., 2009). One solution for maintaining or

even increasing floor surface per doe with late weaning management is to use a two-floor

cage including a platform inside and increasing the cage height (Finzi et al., 1996).

Increasing the size of breeding cages could offer more comfortable housing and more

possibilities for locomotion of rabbit does (EFSA, 2005). However, the results from the


55

experiments conducted so far increasing cage size (horizontally or vertically) are not

conclusive (Szendrő and McNitt, 2012) and the interaction of late weaning management

with type of cage is not known.

The aim of this trial was to study does under extensive reproductive management,

(inseminated at 25 days after parturition), the effect of combined use of late vs. standard

weaning age (46 vs. 32 days) and alternative vs. conventional cages over five consecutive

reproductive cycles on performance of rabbit does and growing rabbits.

2. Material and Methods

2.1. Animal, housing and management

All experimental procedures were approved by the Animal Ethics Committee of the

Universidad Politécnica of Madrid and were in compliance with the Spanish guidelines

for the care and use of animals in research (Boletín Oficial del Estado, 2013).


Toledo, Spain. A total of 104 nulliparous rabbit does (Oryctolagus cuniculus) and their

litters from the first to the sixth parturition of a hybrid maternal line (Hy-Plus) were used.

At 18 weeks of age, does were distributed randomly in four groups in a factorial

arrangement with two housing systems and two weaning ages (32 and 46 days). The first

artificial insemination (AI) was performed at 19.5 weeks of age and thereafter all does

were inseminated at 25 days post partum (dpp). Non-pregnant females were re-

inseminated 56 days later. To induce ovulation, does were given an intramuscular

injection of 5 µg Lecirelin (FATRO S.p.A. Italy). All does were housed in naturally

lighted room except for five days before and three days after AI when a photoperiod of

16 h light and 8 h dark were established with artificial lighting. At birth, litter size was

standardized by cross-fostering (within each experimental group) to 7-8 or 9-11 kits in

primiparous and multiparous rabbit does, respectively. At weaning, the does were moved

to a clean room while their litters were kept in the cages where they were born. From the

first artificial insemination, half of the rabbit does were individually housed in

conventional polyvalent cages (39 cm x 100 cm x 30 cm) (Figure 1). The other half of the

animals were individually housed in alternative polyvalent cages (39 cm x 100 cm x 60

cm) with a wire platform (38 cm x 31cm) raised 40 cm from the floor (Figure 2). All the

cages were equipped with a feeder and a nipple drinker placed in the lower level and a

foot mat (perforated plastic plate) in the middle of the floor. Heating, cooling and forced


56

ventilation systems allowed the building temperature to be maintained between 18 and 23

ºC throughout the experimental period. Within each group of cages, half of the rabbits

were weaned at 32 days of age (standard weaning; SW) and the other half at 46 days of

age (late weaning; LW).

2.2. Feeding

Throughout the study, all does were fed ad libitum with the same commercial pelleted

diet (doe feed; DF). Non-lactating does were restricted to 150 g/d until 25 d of gestation

to avoid does fatness. After weaning, growing rabbits were fed with a commercial

pelleted diet (growing feed; GF). Triplicate chemical analysis of DF and GF diets were

performed according to AOAC (2000) procedures, and the average composition (%, as

fed) for DF and GF were respectively: moisture 10.4 and 10.3 %, crude protein 17.0 and

16.3%, ether extract 3.1 and 3.0%, starch 16.9 and 16.0 %, crude fiber 14.8 and 15.4 %,

neutral detergent fiber 32.1 and 34.5 %, acid detergent fiber 17.0 and 19.8 %, lignin 5.44

and 5.50 % and ash 6.2 and 7.2%. Doe and growing feeds included robenidine (60 ppm)

and diclazuril (1 ppm), respectively.

2.3. Controls

During the first six parturitions, fertility, number of kits born alive and stillborn were

recorded. During the first five reproductive cycles, litter size, litter weight and body

weight of does at 3, 21, 32, 46 and at 59 dpp were recorded. The feed intake of does

(from 3 to 21 dpp), of does and kits (from 21 to 32 and 32 to 46 dpp) and of growing

rabbits (from 46 to 59 days of age) were also controlled. From 32 to 46 days, feed intake

of does that had already been weaned was added to intake of their litter in order to

compare it with animals subjected to late weaning. Feed conversion ratio (FCR) was

Figure 1. Conventional cage: 1Drinker; 2 Foot mats; 3Feeder; 4Nest.

Figure 2. Alternative cage: 1Drinker; 2 Foot mats; 3Feeder; 4Nest; 5Platform.


57

calculated as the ratio of total feed intake and litter weight. Mortality of does and young

rabbits was registered during the overall experimental period. The body composition of

52 does was calculated during their first three cycles by bioelectrical impedance analysis

(BIA) according to multiple regression equations described by Pereda et al. (2007) to

estimate moisture, protein, fat and energy content in relation to live body weight. This

technique is based on measuring the resistance and reactance of the body when a weak

alternating current is passed through it.


Productive and reproductive traits were analysed in a completely randomized design by

using a mixed model with repeated measures (MIXED procedure of SAS, 2008), with

type of cage and weaning age as fixed effects and cycle as the repeated term. Lactating

does were considered as the experimental unit. Several covariance structures were tested

and selected according to the Sawa Bayesian information criterion. When the interaction

of main effects was significant, a t-test was used to make pairwise mean comparisons.

Means were considered significant different at P<0.05. Mortality of young rabbits and

fertility of does were analysed by using generalised linear mixed model with repeated

measures (GLIMMIX procedure of SAS, 2008) and mortality of does during whole

experimental period by using a generalised linear model (GENMOD procedure of SAS,

2008). In both cases, the statistical analysis was carried out using a binomial distribution

and the logit function for maximum likelihood estimation. Values of binomial traits

shown in tables were transformed using logit function.

3. Results

3.1. Body weight and body composition of does

Body weight (BW) of does increased from the first to the third cycle (4619 vs. 4868 g,

P<0.001) and afterwards remained stabilized. Body composition (BC) of does was also

affected by the number of reproductive cycle (P<0.001). At the time of the first

parturition, fat and energy content were higher than at the second and both increased by

third parturition (fat: 10.5, 4.26, and 8.41%; energy: 914, 605 and 795 kj/100g,

respectively). At 32 dpp, these traits were lower in the first than in the second and third

cycle (fat: 5.18, 9.50 and 8.20%; energy 641, 838 and 769 kj/100g). Moisture content was


58

always negatively related to fat content (at parturition: 6.53, 7.26 and 6.81% and at 32

days: 7.22, 6.75 and 6.93 %, respectively).

The effect of weaning age and type of cage on BW, body weight gain (BWG) and BC of

does at different points of lactation phase is shown in Table 1.

Table 1. Effect of weaning age and type of cage on body weight and body composition of does at different points of lactation phase.

Type of cage (C) Conventional Alternative SEMb P-value

Weaning agea (W) SW LW SW LW W C WxC

Doe body weightc, g

3 d 4699 4540 4686 4669 63 0.166 0.357 0.259

21 d 4903 4693 4924 4887 66 0.180 0.165 0.196

32 d 4906 4649 4903 4816 70 0.016 0.247 0.232

46 d 5021 4597 4950 4728 68 <0.001 0.664 0.175

Does body weight gainc, g

3 - 21 d 203 156 240 213 24 0.131 0.046 0.678

3 - 32 d 213 114 219 142 29 0.004 0.560 0.722

3 - 46 d 330 72 259 68 29 <0.001 0.189 0.247

3 - next parturition 49.5 26.4 49.7 40.4 25.1 0.520 0.776 0.784

Body compositiond

Moisture, %

3 d 67.6 69.4 696 68.2 1.01 0.834 0.692 0.136

32 d 69.1 70.4 69.2 69.9 1.03 0.333 0.846 0.731

46 d 69.5 72.1 70.4 74.2 1.26 0.016 0.236 0.644

Protein, %

3 d 18.0 18.1 18.0 18.1 0.08 0.322 0.762 0.948

32 d 17.9 17.9 18.0 18.0 0.09 0.968 0.363 0.735

46 d 17.8 18.1 17.8 17.7 0.19 0.739 0.443 0.337

Fat, %

3 d 8.72 7.16 7.02 7.99 0. 97 0.763 0.654 0.202

32 d 8.15 7.01 8.02 7.34 0. 96 0.352 0.915 0.809

46 d 7.78 5.30 6.94 3.74 1.16 0.020 0.309 0.761

Energy, kj/100g

3 d 817 743 735 791 43.2 0.827 0.693 0.138

32 d 775 715 769 740 43.5 0.315 0.830 0.722

46 d 746 631 707 551 53.3 0.015 0.273 0.705 aSW: standard weaning (at 32 d), LW: late weaning (at 46 d). bStandard error of the least squares means (n=26). cValues are means of the first five cycles. dValues are means of the first three cycles.

No significant interactions were observed between weaning age and cage type in

anytraits. At 32 and 46 dpp through the first five cycles, BW of does weaned later were

3.5 % (P<0.05) and 6.5 % (P<0.001) lower than does weaned at 32 days, respectively.


59

0

100

200

300

400

500

600

700

800

900

1000

0

2

4

6

8

10

12

14

1st cycle 2nd cycle 3rd cycle 1st cycle 2nd cycle 3rd cycle

Fat Energy

Ene

rgy,

kj/

100g

Fat

, %

******

Body weight gain from 3 to 32 and 3 to 46 dpp were also affected by weaning age

(P<0.01 and P<0.001, respectively). In LW group it was lower by 40.7 and 76.2 % than

in the SW group. However, from 3 to 32 days the difference between LW and SW was

only significant during the second and the fourth cycle (P<0.01). Weaning age of kits had

no effect on doe BW at 3 and 21 dpp, BWG from 3 to 21 dpp or from 3 dpp to three days

after the next parturition. Weaning age in the first three cycles affected BC at 46 dpp. LW

does had higher moisture content (4.8 %), and lower fat and energy content (38.6 and

18.7 %, respectively) than SW does (P<0.05). However, the difference between LW and

SW does for fat and energy content decreased from 4 to 1.7 % and from 184 to 80

kj/100g respectively, with the number of parturition (Figure 3). At 3 and 32 dpp no

significant differences between LW and SW for BC traits were observed.

Type of cage had an effect on BWG from 3 to 21 dpp (P<0.05), reaching higher values

animals housed in alternative than in conventional cages (227 vs. 180 g; Table 1).

However, BW, BC and BWG throughout the experimental period were not affected by

type of cage.

Figure 3. Fat and energy body content of the body at 46 days after parturition of does subjected to standard ( ) and late weaning ( ) throughout the three first reproductive cycles. Each data point is the least squares mean (LSM) ± standard error of means. Level of significance: ***=P<0.001


60

0.0

5.0

10.0

15.0

20.0

25.0

30.0

35.0

40.0

45.0

1st cycle 2nd cycle 3rd cycle 4th cycle 5th cycle

%

**

*

3.2. Rabbit doe and litter performance

The fertility depended on cycle number (P<0.001) with values from the second, third and

fourth cycles lower than the other cycles (96.2, 80.0, 85.4, 84.9, 96.8 and 95.6 % from

first to sixth parturition, respectively). The mortality of does and young rabbits from 3 to

59 days of age were low (14.6 and 17.4 %, respectively). Mortality of kits depended on

cycle (P<0.001), as mortality in the third and fifth cycles was higher than in the other

cycles (29.6 vs. 9.17 %, respectively) (Figure 4). Litter size born was also affected by

cycle (P<0.001), since it increased from 8.37 in primiparous does up to 12.3 in

multiparous. Litter size at 59 d, during the first, third and fifth cycles was lower

(P<0.001) (Figure 5) than during the second and fourth cycles (7.08, 8.01, 7.40, 9.06, and

6.60 rabbits per cage, from the first to the fifth cycle, respectively). Individual BW of kits

during the first cycle was lower than later litters but at 59 days of age, the highest and

lowest values were observed in first and the fifth cycles, respectively (2305 vs. 1853 g).

Figure 4. Effect of standard ( ) and late weaning ( ) on mortality of young rabbits from 3 to 46 days of age throughout the five reproductive cycles. Level of significance: **=P<0.01; *=P<0.05.


61

5.00

5.50

6.00

6.50

7.00

7.50

8.00

8.50

9.00

9.50

10.00


Lit

ter

size

(n)

Figure 5. Effect of standard ( ) and late weaning ( ) on litter size at 59 days of age throughout the five reproductive cycles. Each data point is the least squares mean (LSM) ± standard error of means. Level of significance: ***=P<0.001.

The effect of weaning age and type of cage on reproductive traits, mortality and growth

of young rabbits is shown in Table 2. No significant effects of treatments on fertility, doe

mortality, number of kits born alive and dead during the overall experimental period were

observed. Increasing weaning age from 32 to 46 dpp led to a decrease of mortality during

the period from 32 to 46 days (P<0.01). Overall mortality was higher in animals weaned

at 32 than at 46 days (P<0.01), but the effect was higher during the third and fifth cycles,

i.e. when the highest mortality rates were observed (Figure 4). At 46 and 59 days of age

litter size in LW was 5.3 and 8.9 % higher (P<0.001) than in SW group, respectively;

however, at 59 days the difference between SW and LW was only significant at the third

and fifth cycles (P<0.001) (Figure 5). From 32 to 46 and from 46 to 59, BWG of young

rabbits weaned at 46 days was 5.8 g/d higher (P<0.001) and 4.4 g/d lower (P<0.001)

respectively, than in rabbits weaned at 32 days. Litter weight at 59 dpp was thus 11.3 %

higher in LW than in SW (P<0.001), though weaning age had no effect during the first

and fourth cycles (Figure 6).

3.3. Feed intake and feed conversion ratio

Feed intake (FI) of lactating does and kits up to 32 days after parturition was lower

during the first (P<0.001) than during the other reproductive cycles (420 vs. 497 g/d).

When the fattening period was also considered, FI days was lower during the first and

fifth cycles than during the others (679 vs. 759 g/d; P<0.001). Feed conversion ratio was

***

***


62

affected by cycle. From 3 to 32 days of lactation, FCR was higher in the first than in the

other cycles (2.52 vs. 2.32; P<0.001). However, up to 59 days, values were lower during

the first, second and fourth cycles than during the third and fifth cycles (2.72 vs. 3.37;

P<0.001).

Table 2. Effect of weaning age and type of cage on reproductive parameters, mortality of animals and litter traits. Type of cage (C) Conventional Alternative

SEMb P-value


Fertilityc, % 93.9 91.9 87.9 92.9 - 0.678 0.339 0.116

Doe mortalityd, % 16.0 11.5 19.2 11.5 - 0.390 0.845 0.845 Total born, nc 11.4 11.8 11.9 11.4 0.40 0.835 0.872 0.257

Stillborn, nc 1.35 0.99 1.00 0.85 0.20 0.219 0.240 0.618 Young rabbit mortalitye, %

3-21 d 4.75 3.90 4.66 4.41 - 0.585 0.822 0.762 21-32 d 3.47 1.40 2.15 2.27 - 0.228 0.996 0.135

32-46 d 3.90 0.94 2.80 1.10 - 0.003 0.792 0.490 46-59 d 5.20 3.83 2.88 3.09 - 0.756 0.262 0.214 3-59 d 20.0 11.9 15.2 13.3 - 0.003 0.372 0.053

Litter sizee, n

3 d 9.29 9.22 9.21 9.38 0.09 0.616 0.627 0.163 21 d 8.82 8.84 8.88 8.91 0.13 0.870 0.634 0.965 32 d 8.47 8.70 8.74 8.63 0.13 0.655 0.455 0.197 46 d 8.03 8.70 8.32 8.51 0.13 <0.001 0.739 0.096 59 d 7.07 8.04 7.56 7.89 0.17 0.001 0.321 0.096

Litter weighte, g

3 d 817 842 825 848 15 0.077 0.624 0.942 21 d 2921 3040 3145 3135 50 0.275 0.002 0.200

32 d 6294 6666 6749 6678 112 0.184 0.040 0.051 46 d 10679 12480 11557 12686 211 <0.001 0.012 0.115

59 d 14161 16396 15730 16866 376 <0.001 0.008 0.147 aSW: standard weaning (at 32 d), LW: late weaning (at 46 d). bStandard error of the least squares means (n=26). cTotal doe mortality during six consecutive parturitions. dValues are means of the first six parturitions. eValues are means of the first five cycles.

There was no effect of type of cage on young rabbit mortality and litter size. At 21, 32, 46

and 59 days of age, animals housed in alternative cages had 5.4 (P<0.01), 3.6 (P<0.05),

4.7 (P<0.05) and 6.7 % (P<0.01) higher litter weights than animals housed in

conventional cages, respectively. Animals housed in alternative cages also had higher

individual BW at 21(by 4.2 %; P<0.05), 46 (by 3.5 %; P<0.01) and 59 days of age (by 3.6

%; P<0.001) than in conventional cages.


63

10

11

12

13

14

15

16

17

18

19

20


kg

Figure 6. Effect of standard ( ) and late weaning ( ) on litter weight at 59 days of age throughout the five reproductive cycles. Each data point is the least squares mean (LSM) ± standard error of means. Level of significance: ***=P<0.001; *=P<0.05.

The effect of treatments on FI and FCR through the first five cycles is shown in Table 3.

FI was higher at 46 dpp with the later weaning age (P<0.001) and over the whole

experiment (P<0.05) than with the earlier weaning age. Weaning age had an effect on

FCR (P<0.001). During the experimental period lower values were observed in the LW

than in the SW group (2.77 vs. 3.20).

Table 3. Effect of weaning age and type of cage on feed intake and feed conversion ratio during the first five reproductive cycles.

Type of cage (C) Conventional Alternative SEMb

P-value


Feed intake, g/d per cage

3 - 21d 369 371 380 385 6 0.611 0.053 0.886

21- 32 d 649 656 663 659 9 0.888 0.357 0.565

32 - 46 dc 836B 972A 955A 972A 16 <0.001 <0.001 <0.001

46 - 59 dd 957 996 1036 1036 23 0.389 0.013 0.403

3 - 59 dd 687B 731A 743A 745A 9.9 0.023 <0.001 0.040

Feed conversion ratio

3 - 21d 3.28 3.13 3.02 3.07 0.06 0.436 0.011 0.087

3 - 32 d 2.48 2.30 2.30 2.34 0.06 0.227 0.216 0.055

3 - 46 dc 2.79 2.32 2.61 2.24 0.08 <0.001 0.081 0.499

3 - 59 dd 3.30 2.82 3.09 2.71 0.09 <0.001 0.086 0.575

A, B Means in the same row with unlike superscripts differ (P<0.05). aSW: standard weaning (at 32 d), LW: late weaning (at 46 d). bStandard error of the least squares means (n=26). cFeed intake of does and growing rabbits was included. dFeed intake of does from 46 to 59 days was not included.

* ***

***


64

Type of cage affected FI during the periods from 32 to 46 (P<0.001), 46 to 59 (P<0.05)

and from 3 to 59 days of age (P<0.001). Animals housed in alternative cages consumed

6.6, 6.1 and 4.9 % more feed than those housed in conventional cages, respectively.

However, from 32 to 46 days and during the whole period, the lower values in

conventional cages were only observed in animals weaned at 32 days. The FCR from 3 to

21 dpp was 5.0 % (P<0.05) lower in alternative than in conventional cages.

4. Discussion

4.1. Weaning age

Lactation requires a great energy expenditure of the rabbit doe and is closely related to

some variables as body condition and fecundity. Moreover, animals with longer lactations

could have a higher susceptibility to diseases, as they show a fewer number of total

lymphocytes at the end of lactation (Guerrero et al., 2011). A higher body energy deficit

in does subject to longer lactations was observed in several trials where early and

standard weaning ages (21/23 vs. 32/35 days) were compared (Feugier and Fortun-

Lamothe, 2006; Xiccato et al., 2004). In the current trial, though the effect of an extended

lactation period led to a lower BW and body energy of does at 46 dpp, this effect

decreased from the first to the third reproductive cycle. Primiparous does are more

sensitive to energy deficits than multiparous does, where no relevant energy deficit seems

to occur during lactation phase (Pascual et al., 2013). This result is probably due to

limited intake capacity, as a relatively lower FI was observed in the first cycle during the

lactation period. Several authors demonstrated a relationship between feed and energy

intake and body energy deficit in lactating and pregnant does from their first to second

parturition (Fortun-Lamothe and Lebas, 1996; Xiccato et al., 1995). Despite the lower

body energy observed in LW does at 46 days of lactation, the recovery time from

weaning to the next parturition was enough to compensate the BW and body energy at the

next delivery. This ability to recover body reserves could explain the absence of weaning

effect in the current trial on fertility and mortality of does during the five breeding cycles,

as well as on BWG of suckling rabbits and FI until 21 or 32 days, which indicates similar

milk production in both treatments. These results could also be related to the extensive

reproductive rhythm used in the current trial (AI 25 dpp). Previous work showed a

significant improvement of BC, energy balance and fertility using extensive reproductive

rhythm, because it is better adapted to the physiology of rabbit does (Castellini, 2007).


65

Thus, when combining an extensive reproductive rhythm with LW, the long recovery

time after weaning (10 days) and the non-simultaneity of the main milk production phase

(up to 21 days) with pregnancy could be as important as an adequate body energy content

after weaning. In this way, Pascual et al. (2013) suggested that a short recovery time after

weaning and a large mobilization occurring at late pregnancy could be more responsible

for a negative balance of lactating-pregnant rabbit does during their first reproductive

cycle than the lactation effort. Martínez-Vallespín et al. (2012) did not observe a negative

effect of LW (42 dpp) on fertility rate in multiparous does when compared with

conventional management (AI at 11 dpp and weaning at 28 dpp). An even higher fertility

rate was obtained in primiparous does subjected to LW. Nonetheless, they found a

negative long term effect on litter weight mainly when extensive management was

combined with a less concentrated diet around weaning. In contrast, a trend towards a

higher kit body weight at 3 dpp with LW was observed in the current trial, which could

be related to differences in feed intake during late gestation (data not recorded).

According to Quevedo et al. (2006), one of the factors conditioning the energy intake

after weaning is the BC of the female, and an increase of energy intake that leads to a

heavier litter. Therefore, in the present trial it can be presumed that there was an increase

in feed intake by LW does after weaning, as lower energy and fat content were observed

at that moment. This would coincide with the late gestation phase, when the growth rate

of the fetuses is higher (Mocé et al., 2004), affecting the body weight of kits after

parturition. On the other hand, the difference between the litter weight of SW and LW at

the third dpp could be also due to the recovery time after weaning in the SW group (24

vs. 10 days, respectively), as a possible overfattening with lengthy dry period could have

negatively affected fetal growth, with a higher risk of metabolic diseases of does as

pregnancy toxaemia (Rosell, 2000). Other studies reported a higher risk of overfattening

in does inseminated post-weaning (26 dpp) which impaired the fertility rate (Castellini et

al., 2006).

Regarding growing rabbits, in the present trial the BW at 46 d of late weaned animals was

higher than rabbits weaned at 32 d (P<0.001) but was not different at the end of the

growing period. This result could be related to milk intake during late lactation phase.

According to Peaker and Taylor (1975), milk production at 32 days is still relevant. Lebas

(1969) found that the milk intake of kits during the sixth week of lactation was around

9.7% of the total milk intake. The difference at 46 d as compared to weaning could also


66

be related to a negative impact of feed switching of rabbits weaned at 32 days and high

energy content of lactation feed. Romero et al. (2009) also found higher BWG with late

weaning. However, they did not observe the compensatory effect during the second

growing period, probably due to a high incidence of epizootic rabbit enteropathy and the

positive effect of LW reducing mortality. A numerical reduction of mortality with longer

lactations was also observed by Martínez-Vallespín et al. (2012). In the present trial, late

weaning decreased mortality of growing rabbits but only during cycles with worse health

conditions, (second, third and fifth cycles). During these cycles, higher litter size, litter

weight, FI per cage and lower FCR with late weaning were observed. This fact could be

related to antibacterial effects of maternal rabbit milk found by several authors (Gallois et

al., 2007; Marounek et al., 2002). Furthermore, a slower transition period from milk to

feed intake could help to avoid gastrointestinal disorders caused by the sudden shift from

milk to exclusive solid feed intake (Fortun-Lamothe and Gidenne, 2000; Maertens and

De Groote, 1990).

Otherwise, late weaning decreases the available floor surface per animal, which results in

a negative perception of animal welfare (Vanhonacker et al., 2009). However, the

positive effect that late weaning seems to have on mortality under environments with

high health risk, can be associated to an improvement of animal welfare, even in

conventional cages with lower available floor surface.

4.2. Type of cage

As pointed out by Szendrő and Dalle Zotte (2011), effects of increasing the size of cages

(horizontally or vertically) are not conclusive. In the current trial, the type of cage did not

affect fertility, BW, BC and mortality of does, prolificacy or litter size throughout the

overall experimental period. Most of these results were similar to those observed in

literature (Bignon et al., 2012; Mikó et al., 2012; Mirabito et al., 2005). However,

Rommers and Meijerhof (1997) found higher numbers of kits born alive and weaned

using higher cages. Barge et al. (2008) and Masoero et al. (2003) found an impairment of

fertility with two-floor cages.

The growth of newborn rabbits depends mainly on the quantity and quality of the milk

ingested from the does, until at least around 20-25 days of age, when the consumption of

solid feed starts (Gidenne et al., 2002). During this period of milk dependency, higher

BW and BWG of young rabbits were observed in the current trial in alternative cages,


67

contrary to the results of Masoero et al. (2003), but in agreement with observed by Barge

et al. (2008) and Mikó et al. (2012). Results from the current study suggest higher milk

production of does housed in alternative cages, explaining the higher BWG of does

observed during first lactation period. Milk production could be associated with stress

level through adrenergic mechanisms. According to Alfonso-Carrillo et al. (2014) the

platform of the alternative cages is used as an escape by rabbit does in the lactation phase,

decreasing the stress caused by the kits at certain times, which could explain the increase

of milk production in this type of housing. Moreover, Mirabito (2003) found that the

nursing attempts by kits did not decrease in cages with platforms. The higher productivity

should imply an increase of the nutrient requirements of does, which could be related to

the increase of FI observed during this period in alternative cages. Higher feed

consumption might also be explained by an increase of exercise with the use of platform,

as it is used frequently throughout the day (Alfonso-Carrillo et al., 2014).

Regarding young rabbit mortality, Barge et al. (2008), observed lower kit mortality from

20 to 35 days using a platform in the cages in only one of the two strains studied. Mikó et

al. (2012) found a positive tendency of cage enlargement and height with a platform on

mortality up to 32 days. Although, in the current trial, the effect of type of cage on

mortality of young rabbits up to 32 days was not significant, mortality during the overall

growing period of animals weaned at 32 days was numerically higher in conventional

than in alternative cages. This result could be due to an easier spread of disease in cages

with less available area, because of the more frequent contact among animals in the same

cage.

Thus, in the growing period, an increase of the size of the area available in alternative

cages led to an increase of final BW, litter weight and FI of the animals. In agreement,

Lang and Hoy (2011) found higher BWG during the entire growing period in cages with

platforms than in cages without them but that difference was only observed in two of four

rounds. Other authors also found that the elevated platform resulted in a higher FI and

BWG from 29 to 46 days of age (Maertens et al. 2004) or higher BW at 36 and 63 days of

age (Jehl et al., 2003). Nevertheless, in both trials, at the end of fattening period (around

70 days), performance was not affected significantly by the use of platforms. Matics et al.

(2014) studied different housing conditions with or without elevated platforms, and

observed an impairment of growing performance with platform covered with straw-litter,

but no effect was found when a wire net platform was used. Postollec et al. (2008)


68

showed a significant reduction of BWG in enriched cages with elevated platforms;

however, these authors used larger cage compared with the alternative cages used in the

current trial, and physical activity could be greater. Princz et al. (2008) did not find any

effect of height of the cage (20, 30, 40 cm or open top) on BWG, FI or FCR in fattening

rabbits aged 5 to 11 weeks. Thus, the results from the current trial could be less related to

the height of the cage than to a decrease of density of animals, through the increase of

surface with the use of the platform (19.9 vs. 15.5 rabbits/m2; 40.1 vs. 32.1 kg/m2, in

conventional and alternative cages). This is in agreement with the impairment of growth

performance observed by Aubret and Duperray (1992), Lambertini et al. (2001) and

Villalobos et al. (2008) with increased densities of animals. Thus, Szendrő and Dalle

Zotte (2011), concluded in a review about the effect of housing conditions in growing

rabbits that the optimal stocking density was 16-18 rabbits/m2 (40-45 kg/m2).

5. Conclusions

According to the results of the current study, when facing situations with high sanitary

risk after weaning, the combined use of extensive reproductive rhythms with long

lactations and alternative cages increasing available surface with a raised platform could

be an alternative to improve animal welfare, decreasing mortality and increasing

performance of growing rabbits without detriment to the reproductive traits of rabbit

does. However, the economic impact of implementing this management procedure and

housing system on the profitability of rabbit farms should be taken into account.


69

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on the body fat and performance of rabbit doe. Reprod. Nutr. Dev. 46: 195-204.

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behaviour, performances and health status of young and reproducing rabbits. Ann.

Zootech., 49:517-529.

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enteropathogenic Escherichia coli infection. Clin.Vacc. Immunol., 14: 585-592.

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caecum of the rabbit around weaning: impact of a dietary fibre deficiency and of

intake level. Anim. Feed Sci. Technol. 99: 107-118.

Guerrero I., Ferrian S., Blas E., Pascual J.J., Cano J.L., Corpa J.M., 2011. Evolution of

the peripheral blood lymphocyte populations in multiparous rabbit does with two

reproductive management rhythms. Vet. Immunol. Immunopathol. 15: 75-81.

Jehl N., Meplain E., Mirabito L., Combes S. 2003. Incidence de trois modes de logement

sur les performances zootechniques et la qualité de la viande de lapin. In Proc.:

10èmes Journ. Rech. Cunicole, Paris, France, 181-184. Cuniculture Magazine, 30:

60-63.

Lambertini L., Vignola G., Zaghini G. 2001. Alternative pen housing system for fattening

rabbits: Effects of group density and litter. World Rabbit Sci. 9: 141-147.

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by growing rabbits. World Rabbit Sci., 19: 95-101.

Lebas F. 1969. Alimentation lactée et croissance pondérale du lapin avant sevrage. Ann.

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Licois D., Coudert P., Marlier D. 2006. Epizootic rabbit enteropathy. In: Maertens, L.,

Coudert, P. (Eds.), Recent Advances in Rabbit Sciences. Institute for Agricultural

and Fisheries Research, Melle, Belgium, pp. 163-170.

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to increase it. J. Appl. Rabbit Res., 13: 151-158.


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Maertens L., Tuyttens F., Van Poucke E. 2004. Group housing of broiler rabbits:

performances in enriched vs. barren pens. In Proc.: 8th World Rabbit Congress,

Puebla, Mexico, 1247-1250.

Marounek M., Skøivanová V., Savka O. 2002. Effect of caprilic, capric and oleic acid on

growth of rumen and rabbit caecal bacteria. J. Anim. Feed Sci., 11: 507-516.

Martínez-Vallespín B., Martínez-Paredes E., Ródenas L., Cervera C., Pascual J.J., Blas E.

2012. Effect of less concentrated weaning diet and an extensive reproductive

management on the long term rabbit doe performance at parturition. In Proc.: 10th

World Rabbit Congress, Sharm El-Sheikh, Egypt, 591-595.

Masoero G., Bergoglio G., Chicco R. 2003. Improved rabbit housing management for

female growth and reproduction. In Proc.: 54th European Association for Animal

Production, Rome, Italy, 199.

Matics Zs., Szendrő Zs., Odermatt M., Gerencsér Zs., Nagy I., Radnai I., Dalle Zotte A.

2014. Effect of housing conditions on production, carcass and meat quality traits of

growing rabbits. Meat Sci., 96, 41-46.

Mikó A., Szendrő Zs., Gerencsér Zs., Radnai I., Odermatt M., Nagy I., Matics Zs. 2012.

Performance of rabbit does in cages with or without elevated platform or plastic

footrest. In Proc.: 10th World Rabbit Congress, Sharm El-Sheikh, Egypt, 441-445.

Mirabito L. 2003. Logement et bien-être du lapin : les nouveaux enjeux. In Proc.: 10èmes

Journ. Rech. Cunicole, Paris, France, 163-172.

Mirabito L., Galliot P., Souchet C. 2005. Effet de la surface disponible et de

l'aménagement des cages sur les performances zootechniques et le comportement des

lapines. In Proc.: 11èmes Journ. Rech. Cunicole, Paris, France, 61-64.

Mocé M.L., Santacreu M.A., Climent A., Blasco A. 2004. The effect of divergent

selection for uterine capacity on fetal and placental development at term in rabbits:

Maternal and embryonic genetic effects. J. Anim. Sci. 82: 1046-1052.

Pascual J.J. 2010. The role of body condition on new feeding and breeding programmes

for reproductive rabbit does. In Proc.: 22nd Hungarian Conference on Rabbit

Production, Kaposvár, Hungary, 11-32. World Rabbit Sci. 19: 111-118

Pascual J.J., Savietto D., Cervera C., Baselga M. 2013. Resources allocation in

reproductive rabbit does: a review of feeding and genetic strategies for suitable

performance. World Rabbit Sci., 21: 123-144.

Pascual J.J., Xiccato G., Fortun-Lamothe L., 2006. Strategies for doe's corporal condition

improvement-relationship with litter viability and career length. In: Maertens, L.,


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Coudert, P. (Eds), Recent Advances in Rabbit Science. Institute for Agricultural and

Fisheries Research, Melle, Belgium, pp. 247-258.

Peaker M., Taylor J.C. 1975. Milk secretion in the rabbit: changes during lactation and

the mechanism of ion transport. J. Physio. 253: 527-545.

Pereda N., Rebollar P.G., Schwarz B.F., Arias-Alvarez M., Revuelta L., Lorenzo P.L.,

Nicodemus N. 2007. Study of body composition of rabbit does by means of

bioelectrical impedance. Part II Prediction equations. In Proc.: II Congreso Ibérico

de Cunicultura, Vila Real, Portugal, 17–20.

Postollec G., Boilletot E., Maurice R., Michel V. 2008. The effect of pen size and an

enrichment structure (elevated platform) on the performances and the behaviour of

fattening rabbits. Anim.Welfare. 17: 53-59.

Princz Z., Radnai I., Biró-Németh E., Matics Zs., Gerencsér Zs., Nagy I., Szendrő Zs.

2008. Effect of cage height on the welfare of growing rabbits. Appl. Anim. Behav.

Sci., 114, 284-295.

Quevedo F., Cervera C., Blas E., Baselga M., Pascual J.J. 2006. Long-term effect of

selection for litter size and feeding programme on the performance of reproductive

rabbit does. 1. Pregnancy of multiparous does. Anim. Sci. 82: 739-750.



Clostridium perfringens in the caecum, the incidence of Epizootic Rabbit

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153:131-140.

Rommers J., Meijerhof R. 1997. The effect of cage enlargement on the productivity and

behaviour of rabbit does. In Proc.: 10th International Symposium on Housing and

Diseases of Rabbits, Celle, Germany.

Rosell J.M. 2000. Enfermedades de menor presentación. Enfermedades metabólicas. In:

Rosell, J.M., (Eds), Enfermedades del conejo. Tomo II. Mundiprensa, Madrid,

Barcelona, México, pp. 399-454.


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Szendrő Zs, Dalle Zotte A. 2011. Effect of housing conditions on production and

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Szendrő Zs., McNitt J.I. 2012. Housing of rabbit does: Group and individual systems: A

review. Livest. Sci., 150: 1-10.

Vanhonacker F., Verbeke W., Van Poucke E., Buijs S., Tuyttens F.A.M. 2009. Societal

concern related to stocking density, pen size and group size in farm animal

production. Livest. Sci., 123: 16-22.

Villalobos O., Guillén O., García J. 2008. Effect of cage density on growth and carcass

performance of fattening rabbits under tropical heat stress conditions. World Rabbit

Sci., 16: 89-97.

Xiccato G., Parigi-Bini R., Dalle Zotte A., Carazzolo A., Cossu M.E. 1995. Effect of

dietary energy level, addition of fat and physiological state on performance and

energy balance of lactating and pregnant rabbit does. Anim. Sci., 61: 387-398.

Xiccato G., Trocino A. 2010. Energy and protein metabolism and requirements. In: De

Blas, C., Wiseman, J., (Eds), The Nutrition of the Rabbit. CAB International

Publising, Wallingford, UK, pp. 83-118.

Xiccato G., Trocino A., Boiti C., Brecchia G. 2005. Reproductive rhythm and litter

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weaning age on the performance and body energy balance of rabbit does. Livest.

Prod. Sci., 85: 239-251.

Chapter 5: General Discussion

74

CHAPTER 5: GENERAL DISCUSSION

CHAPTER 5:

GENERAL DISCUSSION


75

General Discussion

Nowadays, animal welfare raises interest world-wide and concretely there is a special

public concern about the farmed rabbit welfare due to different issues: 1) According to

the report of the European Food Safety Authority (EFSA, 2005), the current production

techniques, and in particular housing systems, do not respect certain of the rabbit’s

fundamental biological characteristics. 2) The sanitary status of the rabbit farm is

disputed, as the replacement rate of does is at present around 100-120 % in commercial

rabbit farms (Coutelet, 2011; Sánchez del Cueto et al., 2012), and high rates of mortality

are observed in fattening rabbitries, especially since the emergence of Epizootic Rabbit

Enteropathy (Licois et al., 2006). 3) There are different societal attitudes towards rabbit

meat production, e.g. in some countries rabbits are one of the most popular pets,

particularly for children. 4) Excessive influence of some groups lobbying for animal

rights without factual information. 5) There is no European regulation stipulating

requirements on stocking densities, group sizes or other housing conditions for growing

rabbits.

On the other hand, there is a lack of information for establishing reliable

recommendations and it is necessary to carry out research to improve and assess rabbit

welfare.

The assessment of rabbit welfare requires the joint evaluation of several indicators of

different type, physiological, behavioural, pathological and productive. According to

Broom (2011), behavioural and disease incidence are the most appropriate indicators for

assess long-term problems. Some diseases do not cause the death of animals and may

affect productive performance. Therefore, the study of performance variables (live weight

gain, feed conversion ratio, fertility, etc.,) also can help to assess rabbit welfare.

Behavioural observation techniques are appropriate to determine space allowances and

to identify and evaluate abnormal conducts that could be associated to an impairment of

welfare in farmed animals (stereotypies). However, due to the wide range of behaviours

that can be analysed in an animal study plus their duration and frequency throughout the

day and even at different physiological stages evidenced the need of using validated

simplified observation methods (as those used in Chapter 3) to ensure the quality of these

studies.


76

Some of the most important behaviours studied to evaluate the space requirements are the

different postures adopted by rabbits, as housing system should allow performing the

natural postures of their specie. Lying and sitting postures are behaviours of long length

and in this regard, Broom and Fraser (2007) asserted that observation methods with short

observation periods provide a useful estimate of animal behaviour if the duration of the

activity is long enough. Thus, as previously reported in Chapter 3, the R2.4 method

seems to be suitable from a practical point of view for these behaviours. According to the

results observed in Chapter 2, the time spent by rabbit does lying and sitting was similar

in both housing systems. These results show that conventional cages meet the height

requirements to sit up on their hind legs, as if they had been uncomfortable performing

this position in conventional cages, differences between housing systems would have

been found. However, conventional cages did not meet the height requirements of rabbit

does for standing up. Agreeing, Negretti et al. (2010) studied the height reached

performing different postures by four bucks and six does housed in a cage of one meter

height. The trial showed that most of the time (99.5% of the total occurrences) the rabbits

remained at a height lower than 40 cm and this height was only exceeded to perform

standing posture (0.5% of the total occurrences), being needed the use of the wall to reach

this height. Martrenchar et al. (2001) reported that in cages without enclosed ceilings,

animals performed standing behaviour less than 0.7% of the time of the day. Under

commercial conditions, this posture is not possible as the height of standard cages used in

Europe varies between 29 and 40 cm (Trocino and Xiccato, 2006) and depending on the

rabbit’s size a minimum of approximately 75 cm high is required (Morton et al., 1993).

Data from Chapter 2 showed that height of alternative cages (60 cm) was enough to

perform standing posture although it was rarely observed. The main problem to study this

posture is their high variability, as previously reported in Chapter 3, estimation errors

comparing different simplified observation methods varied from 34.3 to 72.9% and it was

exclusively performed to eat and smell retained faeces on the platform. Therefore, it

seems that rabbit does perform this posture as an entertainment rather than as need.

Moreover, as mentioned by Princz et al. (2008a), the relevance of this behaviour in the

current commercial cage system may be limited due to the lack of predators. In addition,

the absence of stereotypies at the conventional and alternative cages used in Chapter 2, 3

and 4, indicate that rabbit does were comfortable enough to easily perform essential

behaviours or functional activities as eating, caecothophy, drinking, grooming, suckling,

resting and walking.


77

Locomotory activity is another common behaviour used to assess the space requirements

and animal welfare. It has been observed a positive relationship between animal

locomotory activity and leg breaking strength in layer hens (Jendral et al., 2008; Knowles

and Broom, 1990; Norgaard Nilsen, 1990) and sows (Marchant and Broom, 1996),

decreasing the possibility of broken bones and avoiding entailed pain. This relationship

was not observed in broilers submitted both to a treadmill regime (Foutz et al., 2007) and

to movement around barriers for drinking and feeding (Bizeray et al., 2002), even though

the latter treatment significantly increased the diameter of the tibial diaphysis. Matics et

al. (2014) in a study comparing different housing systems also found stronger hind legs in

rabbits housed in pens with an elevated platform entailing higher locomotory activity. In

other similar studies performed in rabbits (Combes et al., 2003; Dal Bosco et al., 2002;

Dalle Zotte et al., 2009; Szendrő, et al., 2009a; 2009b) no significant differences were

observed. As previously reported in Chapter 2, the platform is used frequently throughout

the day by rabbit does, performing more physical exercise than in conventional cages, but

unfortunately leg breaking strength was not evaluated in this study.

On the other hand, an excessive physical activity could indicate restlessness, as for

example, animals fleeing from something or someone. In this regard, data from Chapter

2, showed that the 24 day old kits were not satisfied with the milk provided resulting in a

seek of more milk from their mother. In response, does flee from them, being the

platform the only escape they have to decrease the stress caused by the kits. On the other

hand, depending on the design of the elevated platforms the improvement of welfare

could be discussed, due to the hygiene problems, such as faeces accumulation on the

platform or urine and droppings falling onto the animal, and also due to higher handling

problems, increasing the incidence of broken legs and claws and sore hocks with wire net

platforms (according to opinion of Trouw Nutrition R&D staff with experience working

with alternative housing systems).

Locomotory activity is also assessed in the open-field test to evaluate fearfulness in

rabbits, and it has been accepted that greater locomotion reflects decreased fearfulness

(Hall, 1934). However, the interpretation of this test is complex and species dependent, as

more activity may also indicate a stronger motivation to explore the novel surroundings,

or to reinstate contact with conspecifics (Forkman et al., 2007; Gallup and Suarez, 1980;

Vandenheede et al., 1998). According to Buijs et al. (2015), discerning between these

different underlying causes for open-field behaviour is important, because whilst fear


78

clearly has a negative impact on welfare, the impact of a decreased need for exploration

or social contact is not so clear. In the last study, the development of open-field behaviour

in consecutive sessions was also evaluated. They conclude that the decrease in

locomotion over consecutive test sessions contradicts that this behaviour is exclusively

mediated by fearfulness in the rabbit, being the exploratory motivation the most accurate

interpretation. This greatly limits the usefulness of open-field locomotion as a welfare

indicator in this species. In addition, Princz et al. (2008b), in a study with growing rabbits

observed that despite the higher locomotory activity in animals housed in pens with

higher available surface (6.7% versus 3.8%), the frequency of aggressive behaviour

(measured by the number of ear lesions) was also increased (0.14% versus 0.01%).

Aggressive behaviour is another welfare indicator and this phenomenon is obviously

against animal welfare. From a welfare point of view there is a need of providing enough

space to ensure the animal can move and express their natural behaviour. But not all

naturally occurring behaviour is desirable in farm animals. Among wild rabbits,

aggressiveness is quite common and mainly among the youngest at the time of sexual

maturity, as well as, among females and among males from the start of the breeding

season until the population is balanced and the dominance rank order stablished. In

nature, subdominant animals can run away, but this is impossible on farms, even in the

largest pens (Szendrő and Dalle Zotte, 2011). Under extensive conditions (5 rabbits/m2),

alternative housing system in large pens (up to 70 animals) resulted in comparable growth

performance but aggressiveness was a problem being its frequency and severity related to

either group size or animal age (Bigler and Oester, 1996). Princz et al. (2005) observed

that frequency of ear lesions was higher in pens with 13 rabbits/0.83 m² than in cages

with 2 rabbits/0.12 m² (11.9 vs 5.6%). Szendrő et al. (2009b) found that the rate of ear

lesions was 3.5, 6.1 and 10.4% at the ages of 9, 10 and 11 weeks, respectively. Also a

close correlation between group size and the age of 11 weeks was detected increasing the

proportion of rabbits with ear lesions in the larger group. Szendrő and Dalle Zotte (2011)

showed that the frequency of injury increased in larger groups because an aggressive

animal can injure more group-mates in a larger group than in a smaller one. According to

the rabbit staff of the Poultry and Rabbit Research Centre of Trouw Nutrition, fights

without important injuries have been observed in growing rabbits after weaning due to

the different origin of the animals placed in one cage when starting a new study till the

new hierarchy is stablished. These fights after weaning could have a negative impact in


79

growing rabbits. Alfonso et al. (2007), in a study mixing or keeping litters, as such, after

weaning, reported that rabbits located keeping unalterable the litter showed a 3 and 7%

higher live weights at 46 days and weight gain, respectively, and a 5.5% lower feed

conversion rate than animals located by mixing litters. Moreover, during a trial carried

out at the Poultry and Rabbit Research Centre of Trouw Nutrition where the behaviour of

growing animals at the end of the lactation period but also at 61 days of age, was

registered during 24 hours, agonistic behaviours were not observed in conventional

neither alternative cages (data not published). Maertens and Van Herck, (2000) did not

observe aggressions in growing rabbits with access to gnawing material as wooden sticks

for a growing period lasting 6 weeks. Supporting this, , Princz et al. (2008b) studied

growing rabbit welfare by comparing groups, with or without gnawing sticks and they

observed that the rate of injured rabbits at 11 weeks of age was higher in the cages

without gnawing sticks. On the other hand, housing systems re-grouping female rabbits to

provide conditions similar to those of the wild rabbits (living in groups with a large area

for locomotion and social contact) may induce agonistic interactions resulting in high

rates of aggressiveness, competition for nest sites (increasing the cannibalism and

injures), and impairing body condition, productivity and lifespan of rabbit does (Szendrő

and McNitt, 2012.). Some alternative management procedures to reduce aggressive

behaviour caused by group housing have been studied by Andrist et al. (2014) masking

the group odours with alcohol or vinegar, or by Rommers et al. (2014) using hiding

places and straw.

Mortality and health status are the most evident welfare criteria. In Chapter 4, in an

extensive reproductive system of management (insemination at 25 days postpartum), a

decrease in the mortality rate of growing rabbits with a delay of weaning age up to 46

days of age was observed. Also, Romero et al. (2009) in poor hygienic conditions and

Martínez-Vallespín et al. (2012) observed that late weaning may help to decrease

mortality rate in the growing period, probably due to both the protective role of rabbit

milk against some pathogens (Gallois et al., 2007), as milk production at 32 days is still

relevant (Peaker and Taylor, 1975) and the higher weight and age at weaning (Lebas

1993). However, late weaning decreases the available surface per animal and could

compromise other welfare criteria as those allowing animals to express a wide range of

natural behaviours. Sometimes, important welfare criteria, as mortality and health status

are not in line with others welfare criteria as to allow animals expressing a wide range of


80

behaviours improving the welfare. Thus, although pen housing conditions permit the

rabbits to express a natural behaviour pattern as hopping, running or raising (Dal Bosco et

al., 2002; Maertens and Van Herck, 2000), the mortality rate is increased when large

groups size is used due to infectious pressure (Maertens and Van Herck, 2000; Jehl et al.,

2003). Also, some organic production systems (BioAustria, BioSuisse and Naturland)

suggest rearing rabbits on deep litter (at least 50% of the floor) to offer animals a more

comfortable floor, increasing the animal welfare; however, one of the most serious

problems posed by the use of deep litter is the risk of coccidiosis, which impairs health

conditions, raises mortality and lowers productivity. In the studies conducted by Dal

Bosco et al. (2000, 2002), mortality in deep litter groups was 5.8 and 3.8 times higher,

respectively, than in cages with wire net. Lambertini et al. (2001) also observed higher

mortality because of coccidiosis affection in rabbits reared on deep litter.

Perinatal mortality is an indicator of welfare status of rabbit does, as it is related with

anomalous maternal behaviours and an inadequate environment leading to hypothermia,

starvation, dehydration and cannibalism. Results from Chapter 4 indicated that alternative

cages did not improve perinatal mortality with respect conventional cages, and in both

systems values were low. Similar results were observed by Barge et al. (2008), who did

not observe any difference on rabbit mortality up to 35 days between cages with and

without platform. Mirabito (2005a; 2005b) compared three housing systems for

reproducing does: conventional individual cages, modified cages for two does, and pens

with net floors for four does. Reproductive performance was similar among groups, while

kit mortality was higher in collective pens than in individual or two-doe housing due to

several kindling taking place in the same nest.

Some productive parameters are welfare indicators, as they are often impaired by the

stress and poor health of animals originated from the housing system and handling. Stress

influences the endocrine pathways, inhibiting non-essential functions as reproduction and

growth for the maintenance and survival. Thus, variables as growth, milk production,

fertility rate or body condition, should also be measured to assess rabbit welfare. Mikó

et al. (2012) found a positive relationship between animals under poor welfare condition

using the severity of sore hocks and a decrease in the kindling rate. Data from Chapter 4

show that fertility rate was not affected by type of cage throughout the overall

experimental period. However, Barge et al. (2008) found an impairment of doe fertility

rate with the two-floor cages. Body condition of the doe shows the ability to cope energy


81

deficits during lactation phase and at late pregnancy being that related with lifespan.

Guerrero et al. (2010) and Ferrian et al. (2012) observed a positive correlation between

the body conditions of rabbit does and the population of B lymphocytes which were also

correlated with the lymphocyte populations of their litters. Recently, several in vivo

methods to determine the whole body composition of rabbits have been published: X-ray

computer tomography (Szendrő et al., 1992), magnetic resonance imaging tomography

(Köver et al., 1996), ultrasound measurements of the perirenal fat thickness (Pascual et

al., 2000), electrical body conductivity (Fortun-Lamothe et al., 2002) or biolectrical

impendance (Pereda et al., 2007; Saiz et al., 2013). As shown in Chapter 4, applying the

bioelectrical impedance method, the body energy of late weaned does at 46 dpp was

lower than in standard 35 dpp weaned does. Despite this the recovery time from weaning

to the next parturition was enough to compensate body energy deficit at the next delivery,

explaining the absence of weaning age effect on fertility and mortality of does during the

five breeding cycles. According to the results observed in Chapter 2 and 4, the weight of

lactating and growing rabbits housed in alternative cages was higher than in conventional

cages, probably due to both: 1) platform is used as an escape by rabbit does in the

lactation phase, decreasing the stress caused by the kits leading to an increase in milk

production; and 2) a decrease in the animal density, as the total available surface was

increased with the platform ( 40.1 vs. 32.1 kg/m2, in conventional and alternative cages,

respectively). In this sense, Mikó et al. (2014) concluded that the higher kit weight

observed at 21 and 35 days in cages with wire-mesh and plastic-mesh platforms

compared to those without platform was due to the lower disturbance of the sleeping kits

as a consequence of the lower number of visits made to the nest boxes. On the other hand,

Maertens and De Groote (1984) also observed, in the last weeks of the growing period,

that high stocking density affected negatively productive performance leading to an

impairment of animal welfare. These authors compared animal performance in groups

from 3 to 6 rabbits allocated in cages of 60x40 cm finding a reduction in daily weight

gain and feed intake when the stocking density was higher than 40 kg/m2 (at 19.3 and

23.2 rabbits/m2). Aubret and Duperray (1992), using cages of 46x77 cm with space

allowances ranging from 16.9 to 28.2 rabbits/m2 also found a reduction in the growth rate

when densities were above 19.8 rabbits/m2, and in the daily feed intake when they were

over 22.6 rabbits/m2.


82

The incidence of pododermatitis (sore hocks) and skin injuries are also commonly used to

evaluate the welfare status of the animals in different husbandry systems, as potential

cause of chronic suffering (EFSA, 2005). A scoring system with five levels to assess the

presence and severity of pododermatitis has been developed by Olivas et al. (2013). Some

authors have demonstrated that the installation of a plastic platform or slatted footrest on

the wire mesh play a significant role in the prevention and cure of sore hocks (Rossel and

De la Fuente, 2009; Mikó et al., 2014). In Chapter 2, it has been reported a clear

preference of rabbit does for foot mats above wire mesh floors in conventional and

alternative cages. Also, Princz et al. (2008b) in a study with growing rabbits housed at

different densities observed that the animals showed a preference towards the plastic nets

covering wire mesh floors (16 rabbits/m2, 62.5%; 12 rabbits/m2, 76.5%).


83

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Chapter 6: General Conclusions and Implications

89

CHAPTER 6: GENERAL CONCLUSIONS

AND IMPLICATIONS

CHAPTER 6:

GENERAL CONCLUSIONS

AND IMPLICATIONS


90

General Conclusions and Implications

• From the behaviour perspective, since stereotypies and agonistic behaviours have

not been observed, conventional and alternative cages can be perfectly used for

rabbit production. Therefore, the use of conventional cages does not imply a lack

of welfare and a potential upcoming ban of the use of this type of cages is not

justified.

• The physiological state of rabbit does exert a stronger influence than the type of

cage on the duration and frequency of functional behaviours, showing gestating

does more restlessness and boredom than lactating does. Therefore, after weaning

the animal welfare of gestating does could be compromised, and the addition of

enrichment elements could be a tool to prevent it.

• Standing posture is a behaviour without real fuction under predator free

environment. Moreover, it is scarcely performed by rabbit does and only in order

to smell or eat the feaces on the platform and therefore, an increase of cage height

just to allow it would not improve rabbit does welfare status.

• The platform of the alternative cages is used by rabbit does with and without kits

having in the late phase of the lactation a functional use. It could be used as an

enrichment element decreasing the stress caused by the kits and improving milk

production of rabbit does.

• The platform increases available surface of the cage decreasing final animal

density (<40kg/m2) without reducing the number of animals in the farm and

improving animal performance. Thus, platform can be used in commercial

conditions to increase the marginal profit of the rabbit farm.

• Platforms may lead to hygiene problems due to faeces accumulation in the upper

part of the platform or to faeces and urine falling down onto the animals located in

the lower part of the cage, so to develop new and different platform designs are

required to avoid these problems.

• Simplified behavioral sampling methods can used to reduce the total observation

time required to assess different types of behaviours.


91

• Regular observations of short length, as those used in the regular short method

(R2.4), are the best option from a practical point of view to accurate assess long

length behaviours.

• Due to the nocturnal activity of rabbits, methods with longer records time during

the dark period should be applied to asses short length behaviours.

• The use of extensive reproductive rhythms with long lactations would decrease

mortality and increase performance of growing rabbits without detriment to the

reproductive traits of rabbit does. However, the economic impact of implementing

this management procedure on the profitability of rabbit farms should be taken

into account.

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