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Emir. J. Food Agric. 2015. 27 (4): 338-349
doi: 10.9755/ejfa.v27i4.19909
http://www.ejfa.info/
338
REVIEW ARTICLE
Male camel behavior and breeding management strategies: How to handle a
camel bull during the breeding season?
B. Padalino1, D. Monaco2and G. M. Lacalandra2
1Department of Veterinary Medicine, Di. Me.V, University of Bari "Aldo Moro", Valenzano (Bari), Italy
2Department of Emergency and Organ Transplantation (D.E.T.O.), Veterinary Clinics and Animal Production Section;
University of Bari "Aldo Moro", Valenzano (Bari), Italy
Abstract
The present article reviews male camel behavior and breeding management strategies, providing an insight into
the handling procedures and the most relevant welfare issues on these topics. Furthermore, it suggests some
procedures for rearing, handling and collecting semen from camel bulls, based on results that have been
achieved in the last twenty years and, recently, literature published with the aim of optimizing dromedary camel
breeding. Camels are seasonal breeders and their breeding season (BS) is confined to the coolest winter months
of the year; during the BS, also called “rutting period” or "rut", males exhibit morphological, behavioral and
endocrinological peculiarities. Short breeding season, low libido and high aggressiveness are still some of the
major cause of economic loss, poor reproductive performance and injuries, for camel breeding and industry.
The application of ethology to approach, to train and to study camel bulls may be useful in the future to improve
camel welfare and productive performances. Strong knowledge of animal learning and correct management
procedure could be useful for camel technicians, owners, breeders, but also for veterinarians and others
scientists.
Key words: Dromedary camel, Handling, Management, Sexual behavior, Welfare
Introduction
Male camel sexual behavior and physiology
The “Ethology” is the observation and
description of behavior that leads to improved
understanding of its mechanism, function,
development and evolution (McGreevy, 2004).
References about dromedary camel (DC) behavior
mainly described camels observed in field and
reared in extensive or semi intensive breeding
system (Gauthier-Pilters and Dagg, 1981; Dioli,
2013). Camels are seasonal breeders and their
breeding season (BS) is confined to the coolest
winter months of the year; during the BS, also
called “rutting period” or "rut", males exhibit
morphological, behavioral and endocrinological
peculiarities (Table 1; Padalino et al., 2013).
Depending on the genetic and health condition of
the sire, the geographical location and
environmental parameters, management and
nutritional factors, the duration of the breeding
season ranges from 2 to 6 months. Out of the
breeding season, usually, male camels lose their
libido, do not copulate with females, and show
testicular size and weight decrease and very low
blood testosterone level (Deen et al., 2008).
When a rutting male approaches a female in
estrous it sniffs her genital region, urine or feces,
then performs the typical flehmen gesture of
artiodactyls by lifting his head and curling back his
upper lip (Gauthier-Pilters and Dagg, 1981) (Figure
1). Another typical sign is a notably and profuse
secretion of the poll glands of the neck, which
contains androgen concentration similar to blood
(Ebada et al., 2012). Camels are the only ungulates
that copulates in a couched position; in nature the
mating usually takes around one hour, the
copulation time lasts about 10-20 minutes, with
ejaculation occurring three or four times (Al-
Hazmi, 2000). After each copulation, the male
generally falls sideways and then stands over the
female, blowing out his soft palate “dulaa”, doing
flehmen, sniffing, touching and biting her neck
(Yagil and Etzion, 1980) (Figure 2). During the BS
dromedary bulls increase pacing and anxiety,
Received 10 May 2014; Revised 03 February 2015; Accepted 14
February 2015; Published Online 01 April 2015
*Corresponding Author
Barbara Padalino
Department of Veterinary Medicine, University of Bari "Aldo
Moro", Str. prov. per Casamassima, km 3, 70010 Valenzano
(Bari), Italy
Email: barbara.padalino@uniba.it
B. Padalino et al.
339
becoming very aggressive towards other males and
humans; due to this aggressiveness rutting camels
are usually tied with ropes and kept in single pens
or boxes and their handling is considered very
difficult over this period (Abu-Zidan et al., 2012).
Male camels have been traditionally reared
under semi extensive conditions and kept in herds
with 40 to 60 mature females, while, nowadays, in
order to improve their reproductive performances,
male camels are often reared in breeding centers. In
the latter case, they are used for selective mating or
for semen collection, the latter used for artificial
insemination (Skidmore et al., 2013) or for the
development of assisted reproductive technologies
(e.g. Freezability studies, In vitro Fertilization, etc.)
(El Bahrawy et al., 2013; Skidmore et al., 2013;
Russo et al., 2014).
Unfortunately, Skidmore (2011) reported that
males kept in herds tended to start breeding earlier
and that the rutting period was longer than that of
confined males, so there is the need to investigate
the relationship between confinement and sexual
behavior, as well as early rutting enhancement
systems. Consequently, the major complains for
housed camels bred for semen collection are: low
libido and mating desire, short breeding season and
high variability in term of semen quality and
quantity (El-Hassanein, 2003; El-Bahrawy 2005).
Latter abnormal behaviors could be related to low
animal wellbeing.
Indeed, intensive production system could
affect animal welfare, which is considered related
to animal’s needs, concentrating on nutrition,
behavior, reproduction, physical and social
environment (Waran, 2007). With respect to the
actual well-being of the animal, most issues are
centered on how the animal "feels" when managed
within a specific level of confinement, during
special agricultural practices and handling
(Swanson, 1995). In the last twenty years many
papers have been published about the effects of
intensive management on livestock behavior and
welfare (Hanskell et al., 2003; Babu et al., 2004)
and ethologists have already standardized the study
of their behavior, proposing how to measure it in
other species (Martin and Bateson, 1993). An
“Ethogram” is a detailed description of the
behavioral features of a particular species and
collected behaviors are distinguished according to
their duration in: “events” and “states” (McGreevy,
2004). The events are behaviors of instantaneous
duration (e.g. vocalizations), which are best
described by their frequency, while the states are
behaviors of relatively long duration (e.g. feeding),
which can be best described by their total or
average duration. Therefore, a correct ethogram
should include the frequency of events and the
duration of states (McDonnel, 2003). In 1974,
Altmann wrote an observer’s guide where sampling
methods for use in direct observation of human and
animal behavior are presented.
Table 1. Description of typical sexual behavior in male dromedary camel (Padalino et al., 2013).
Behavior
Definition
Sniffing
The dromedary male sniffs female perineal region and/or the vulva
Nervousness
Increased pacing, anxiety and sound loading
Flehmen
After sniffing the female vulva the male raises the head and curl the upper lip for few
seconds
Grinding of
teeth/whistling
The male moves the lower jaw on left and right side, with closed mouth, grinding the tee th
and producing a typical squeaking/whistling sound
Yawning
An involuntary sequence consisting of mouth opening, deep inspiration, brief apnea and
slow expiration
Urinating
The dromedary male assume the urinating position, with spread hind leg and emits small
quantities of urine
Opened legs
Before, during and after urination the sire stands with opened hind legs
Tail flapping/beating
The tail is held under the prepuce and then it is beaten up and down 4 to 5 times, spreading
urine over the croup and surrounding areas
Poll gland secretion
The occipital poll glands become thick and large and produce a tarry and dark secretion that
colors occipital area and first part of the neck
Neck Rubbing
The male rubs the neck, particularly the occipital area, on walls, trees, fence bars etc
Blathering
Emission of typical metal and gurgling sounds
Dulaa extrusion
Exteriorization of the soft palate, usually named "Dulaa"
Emir. J. Food Agric. 2015. 27 (4): 338-349
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340
Figure 1. Dromedary camel flehmen: male dromedary camel usually show flehmen after sniffing dam's perineum.
Figure 2. Male dromedary camel extruding his "dulaa" after mating.
Since the behavior of camel reared in semi
intensive system have been poorly investigated and
due to the need of relating the behaviors (i.e. libido,
mating time, semen quantity and quality) with other
parameters (i.e. climatic factors, husbandry, diets),
Padalino et al. (2013), recently, proposed the
following procedures to collected data about male
dromedary camel worldwide.
B. Padalino et al.
341
Ethogram for camel general behavior
To fill this kind of ethogram the best record
technique may be the “Focal animal sampling”:
observing each camel, reared in his single box or
pen, for a fixed time window. It should include as
states: feeding, rumination, standing, resting,
standing with head outside the box, walking; while
as events: head outside/looking through the
window, legs movement, number of steps, head up,
head down, explorative behavior (sniffing), sound
emission, defecation, urination, scratching,
occipital glands scratching, yawning, teeth
grinding, blatering, dulaa extrusion, flehem, tail
beating/flapping, open legs. As intensive housing
system may limit the normal expression of animal
behavior, even camels could develop stereotypy
(Padalino et al., 2014) (a stereotypy is a repeated,
relatively invariant sequence of movements that has
no obvious function - McGreevy, 2004), therefore
this kind of abnormal behavior should be included
in the recorded states or events, accordingly with
their duration.
Ethogram for camel sexual behavior
As the major stimulus for expressing sexual
behavior is the presence of the partner (Houpt,
2011), it is essential to bring a female in estrus,
near the box, for a limited time window (e.g. 12
min). The sampling rule could be a behavior
sampling and, during female presence, the
observers must note down the occurrence of
following behaviors: sniffing, flehmen, whistling,
urination, dulaa extrusion, tail flapping.
Furthermore the grade of salivary production,
nervousness, poll gland secretion should be scored
(absent, low, high, very high) (Figure 3).
Camel sexual behavioral score
After the female passage the observers may
score the camel sexual behavior according to
Table 2.
In addition, since it is reported that a stud male
is capable of mating with and fertilizing an estrus
female at any time of the year (Al-Qarawi, 2005)
and Skidmore (2011) stated that the presence of
female led to the increase of male’s libido and of its
behavioral signs, Fatnassi et al. (2014a) tried to
stimulate the enhancement of the rutting period
stimulating males through a female parade. Latter
authors concluded that dam could provide a good
olfactory and visual cue stimulating the onset of
rutting behavior in housed male bulls. Thus,
accordingly with their experience, it seems that the
assessment of male camel behavior during female
parade by means of an ethogram represents a useful
tool to monitor camel bull sexual behavior. Fatnassi
et al. (2014b) work is a proof that the ethological
approach is useful and could be easily adopted by
camel industry in other countries.
Handling procedures
One definition of learning is "a process in
which an individual's experience results in a
relatively permanent change in behavior"
(McGreevy and McLean, 2010). As a process,
learning is not directly measurable, what can be
measured is what has been remembered as a result
of learning (i.e. when the association is
remembered). Learning theory establishes clear
guidelines and training protocols for correct
training practices and methods of behavior
modification. It is truly fascinating, easy to relate to
and really quite simple to understand (McGreevy
and McLean, 2010).
Animals are able to learn by “non associative”
or “associative” processes.
Non-associative learning occurs when exposure
to a single stimulus results in either habituation or
sensitization. Both are fundamental to effective
animal-training and are interconnected at almost
every stage of training. Habituation is learning to
not respond to a repeated stimulus that has no
consequences. Whereas, sensitization is the
opposite of habituation in that there is an increase
in a response after repeated presentation of the
stimulus by itself: the stimulus has to be
intrinsically unpleased or aversive. For example, if
while completing his training, a police horse is
involved in a road accident every day for a month,
he would reliably become sensitized to motor
vehicles and perhaps even become phobic so that
just the sound or sight of them, might be sufficient
to send him into a flight response (McGreevy,
2004).
Emir. J. Food Agric. 2015. 27 (4): 338-349
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342
Figure 3. Recording of focal animal sampling ethogram of male camel sexual behavior during female passage: using
"positive reinforcer" the female accept this procedure easily and she does not need any kind of restraint.
Table 2. Behavioral criteria for scoring the sexual behavior of male dromedary camel during a female passage (Padalino
et al., 2013).
Behavioral Score
Criteria
1: not interested
The male does not show any sexual behavior parameters.
2: low interested
The male goes near the female and shows low frequency of sniffing and flehmen.
3: interested
The male goes near the female, it shows sniffing, flehmen, grinding of teeth/ whistling,
yawning.
4: high interested
The male goes near the female, it shows sniffing, flehmen, grinding of teeth/ whistling,
yawning (more than 3) , urination and tail raising. It is very agitated, stands with open
legs, poll glands secretion and neck rubbing are observed.
5: excited
Like 4, but the male shows blatering and dulaa extrusion, is very excited, stands with open
legs, high poll glands secretion and neck rubbing are observed.
Associative learning occurs when a animal
creates an association between two stimuli or a
behavior and a stimulus. There are two forms of
associative learning: the classical and the operant
conditioning. The classic conditioning was defined
by Pavlov in 1927 as the process whereby the
unconditionated or conditionated response becomes
elicited from a conditioned stimulus. Another
definition of classical conditioning is “the
acquisition of a response to a new stimulus by
association with an old one” (McGreevy, personal
communication).
Operant conditioning is distinguished from
Pavlovian conditioning in that operant conditioning
deals with the modification of a “voluntary
behavior” through the use of consequences. For
example, a cat can learn to direct its behavior to get
out of the cage by pressing a lever (Thorndike,
1898). In another experiment, mice had to press a
lever to obtain food (Skinner, 1938). The cat and
the mice learned a behavior to get reward. The cat
tries to get out because being locked in a cage
(stimulus) is a discomfort, for which it performs a
certain behavior (response) to exit (reinforcement).
In the same way, hungry mice (stimulus) perform
the behavior of pressing the lever (response) to
obtain food (reinforcement). Escape and food are
both reinforcements. The reinforcement needs to be
something biologically relevant for the animal, such
as the removal of discomfort or the appearance of
food, so the animal is highly motivated to obtain it.
Therefore, operant conditioning works by giving or
taking away rewards or punishments when the
animal performs a desired/undesired behavior,
respectively (Kratzer et al., 1977) through the
chain: stimulus - response - reinforcement (Pavlov,
B. Padalino et al.
343
1927). "Reinforcer" and "punishment" are applied
in animal training, the first used for increasing the
occurrence of the desired behavior and the second
for limiting the occurrence of the undesired one.
We can apply a positive reinforcer adding a reward
or a negative reinforcer removing aversive
stimulus. We can apply a positive punishment
adding an aversive stimulus or, in the case of
negative punishment, removing a positive
reinforcing stimulus. It has been found that
punishment is often used incorrectly in animal-
training, particularly when not immediately
contingent with the undesired behavior (McGreevy
and McLean, 2010). Incorrect use of punishment
can affect the animal behavior, desensitizing the
animal to the punishing stimulus and creating
fearful associations (Mills, 1998). Non-associative
and associative learning processes in the animals
must be taken in account to be successful in
handling and training (Murphy and Arkins, 2007).
To know the animal learning abilities is important,
to apply the rules of the "classical and operant
conditioning method" for handling and training
dromedary bulls, particularly during the breading
season, when they become more aggressive and can
be dangerous toward other males and humans.
Camels, as other animals, must associate the
relationship between behavior and
punishment/reinforcement within 3-5 seconds and
usually they could quickly learn. By this method
camel bulls’ handling could become easy, and
injuries and accidents, both for humans and
animals, could be prevented and avoided.
Moreover, animals, which could properly
understand human requests, are usually calmer and
less stressed by any handling procedure, so in a
better welfare living condition.
Semen collection method
Semen collection could be carry out by
different methods: electro-ejaculation, by using an
artificial vagina (AV) and a female teaser, or by
using AV and one El-Hassanein camel dummy.
For collection by electro-ejaculation, the male
camel kneels down and its front legs are tied to the
shoulder and neck. The male is forced to turn on its
side and its hind legs are tied together (from the
shin region) to facilitate receiving semen in the
rubber cone and collection tube. Collection may be
done with or without sedation with detomidine
hydrochloride (30 - 35 mg/Kg B.W., IV, or 70 - 80
mg/Kg B.W., IM). A bovine probe (2 inches, 12
volts and 180 mA) is introduced rectally, after
lubrication with jelly, and two sets of stimulation
are generally used, each of 10–15 pulses of 3–4 s
duration with a rest of 2 - 3 minutes in between.
Ejaculation often occurs after about 15 minutes of
manipulation. Semen obtained by electro-
ejaculation is often reduced in volume and has high
percentage of dead and tail-less spermatozoa and
sometimes is contaminated with urine, due to the
short duration of ejaculation (El-Hassanein, 2003).
In addition, the use of electro-ejaculation for semen
collection does not respect animal welfare and has
other many disadvantages: consuming a lot of time
and many workers to restraining the bull, sedation
or general anesthesia of the animal, possible
injuries to the bulls, sensitization of the bulls
toward humans and consequently fear of humans,
inability of male to mount normally (El-Hassanein,
2003; Skidmore et al., 2013).
A bovine AV of about 40 cm in length is
usually used for collecting semen from adult males
(over 10 years of age), while a shorter AV of about
30 - 35 cm length, is suggested for the collection
from younger males (less than 10 years of age). The
jacket of the AV is filled with water warmed to
about 55 - 60ºC (Skidmore et al., 2013).
During the last two years we have developed a
good method for semen collection procedure
(Padalino et al., 2013), then adapted and better
scheduled, explained in the following paragraphs.
During semen collection using AV it is of
fundamental importance that animals are not
disturbed particularly by unknown persons because
camel bulls are extremely territorial and tend to
defend their female herd toward other males or
humans. The semen procedure should be ritualized
and performed always in the same place. A
receptive female must be lead to a open paddock
near males’ stall and restrained in sternal
recumbence; once all operators are ready for the
semen collection, the door of the male’s stall are
opened and the male brought near the female. If the
male do not start copulating and walk around the
female on the collection area, it should be gently
again guided toward over the female, after 4
minutes; if he refuses, for three times, to approach
the female and to mate, it would be better to stop
the session, avoiding any kind of punishment and
negative association with the semen collection
procedure. If the bull start to copulates, it is
important that the approach of the technician to the
male is slow and cautious and that the penis is
gently guided into the artificial vagina. The
copulation must be not disturbed until the bull ends
and falls sideway. As one typical behavior is
standing near or over the female between two
copulations, the male can show this behavior for a
maximal time of 20 minutes. If the bull does not
Emir. J. Food Agric. 2015. 27 (4): 338-349
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344
want to copulate again after that time, it is better to
stop the session and bring the male into the stall.
Dromedary bulls usually copulates several times
during a semen collection session and sometimes
can start walking around; in this case, after 4
minutes of walking, it is useful to bring the male
near the female, in order to focus its attention on
the mating. Anyway, after three refuses, it would be
better to stop the session. A good semen collection
session should last approximately 45 minutes; such
session time provides many semen collections and
mimics the natural mating behavior thus avoiding
any kind of forcing. Sometimes, after the ending of
the collection session, the bull male could refuse to
leave the collection area and stands over the female
protecting her from intruders; in this particular
situation it is fundamental to avoid any positive
punishments on the male, and it is suggested to
untie the female and lead her far from the male. The
sexual attraction and mating desire, usually
decrease if the female is standing and not in the
couched position. Any stress or painful situation,
felt by the bull, during the collection/mating session
could be associated with the place or with the
procedure of collection thus compromising all
efforts of the trainers and the successful of the
subsequent collection session.
Following this recommendation, and applying the
classical and operant conditioning, dromedary camel
bulls could be well trained and accustomed to the
semen collection procedure their welfare
accomplished and large amount of good quality
semen (could be) easily collected. This procedure has
however some disadvantages, particularly related to
the welfare of the female teaser: injuries of the neck
and on the hump could be produced by the tight ropes
and by the male’s sternal pad. So, to avoid these
problems the females should be protected by a blanket
on her back (Figure 4) and the ropes should be
replaced by fine harness leather hobbles. The last
disadvantage is the discomfort of the technician who
must hold the artificial vagina for the whole duration
of the mating sitting beside the hind region of the
teaser female keeping his arm in a fixed position
(Figure 5).
A camel dummy with an AV inside was
conceived by El Hassanein (2003) trying to overcome
the above-mentioned disadvantages The dummy is in
the same shape and size of a female camel in sternal
decumbency and has a strong iron skeleton, with a
hollow core, to withstand the weight of the male
(about 400 - 500 Kg) during copulation. The iron
skeleton is covered with a strong smooth wooden
sheath that was the same symmetrical shape as a
normal female camel and the entire dummy surface,
in addition to the head and neck, are covered with a
camel hide (El-Hassanein, 2003). Anyway, the use of
the dummy require a particular training method for
the bulls, that is not standardized yet, as usually is
made for stallion, bulls and pigs.
Ethogram for mating behavior and libido score
Mating behavior could be recorded by a "Focal
animal sampling". In this case it is useful, the
mating time may be divided into three parts
according to the different states that the the male
could show: copulation/service time, standing
over/near the female time, walking around time.
Moreover, to standardize the procedure, the sample
session may be scheduled at a predetermined time,
before starting: a maximal latency time (from when
the male is free to the first mating attempt) of 15
minutes, a maximal mating time of 45 minutes, a
maximal time between two copulations of 30
minutes, maximal standing over the female of 20
minutes and as previously mentioned, with
maximal three refuses to approach the female.
Finally, it is important to note down the frequency
of the following events: mounting attempts, number
of mounts, blatering, defecation, dulaa extrusion,
flehmen, jumping, neck-touching, sniffing, sound
emission, tail flapping, teeth-grinding and yawning.
Figure 4. An example of how to protect the dam's
back during a semen collection session.
In 1986, Chenoweth proposed a libido score
(from 1 to 10) to evaluate the breeding potential
of bulls used for semen collection. Sieme et al.
(2004) adapted this scoring for stallions (from 1
to 4: excellent, good, moderate, low) according
with their sexual interest and correlated it with
their fertility. Padalino et al. (2013) adapted
those scoring for dromedary camel bulls and
proposed a libido score from 0 to 5 (Table 3).
B. Padalino et al.
345
The libido could be easily scored, after the
evaluation of the filled ethogram.
Figure 5. Semen collection procedure.
Effects of different management system on
camel welfare
Captivity imposes to animal different kind of
constraints (e.g. limited space, social isolation) which
could alter behavioral repertoire and it is up to us, as
scientists, to evaluate enclosures and husbandry
practices for ensuring the optimal wellbeing of
animals and, consequently, their health status and
productivity. Moreover, it is important to remind that
the welfare notion includes physical (diseases or
wounds), but also psychological aspects (Dawkins,
2003), while “stress” has been defined as "the
inability of an animal to cope with his environment"
(Dobson and Smith, 2000).
In intensive management, animals are
confronted by a wide range of potentially
provocative environmental challenges (potential
stressors) that may adversely affect their living
(Morgan and Tromborg, 2007). Glucocorticoids
have been designated as the main hormones of the
stress because their level sharply rises in response
to stressful situations. One of their effects is the
decrease of the Leydig cells’ testosterone
production which finally affects the male’s libido
and fertility (Phillips et al., 1989; Orr et al., 1994).
Therefore, living and no-welfare conditions could
activate stress responses that can influence
reproduction (Moberg, 1987).
A feral camel bull, naturally would roam wide
areas of land, moving over pastures with his female
herd (Dörges et al., 1992), contrariwise a camel bull
kept isolation during intensive management, could
show abnormal behavior or breeding problems. As
mentioned above, El-Hassanein (2003), reported
that housed camel sires, bred for semen collection,
showed low libido and mating desire, short
breeding season and low reproductive
performances; these data were confirmed by El-
Bahrawy (2005), who stated that the signs of sexual
behavior in housed males varied, in strength and
frequency, within rutting months and within
individual camel bulls thus bearing to a variable
production in terms of semen doses.
Low sexual motivation/libido or poor mating
ability are common reproductive complaints also in
the breeding stallion. Sexual desire and mating
performance are complex traits affected by
management, psychological, hormonal and physical
factors (Stout, 2005) thus the evaluation of captive
animal’s welfare and its improvement through
management practices could be not only an ethic
issue but also a useful strategy in term of
productivity. Morel (2003) stated that many
problems encountered in the reproductive
management of the stallion could be overcome by
consistent discipline, and alleviating boredom
providing social interaction and activity. Dinger
and Noiles (1986) emphasized the importance of
exercise for reducing boredom due confinement
and social isolation. The same authors proved that
the improved basic fitness and muscle tone aids in
maintaining the physical and psychological well-
being of the stallion, with effects on libido,
performances and behavior (Dinger and Noiles,
1986). Performing observational studies on social
organization and reproductive behavior of equine
breeders under feral, semi-feral, and domestic
conditions, McDonnel (2000) concluded that
placing the stallion under the natural light with
chances to have social interaction with mares and to
perform lot of exercise, can improve reproductive
efficiency and fertility or overcome specific
breeding problems.
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346
Table 3. Libido score of male camels during mating (modified from Padalino et al., 2013).
Libido Score
Criteria
0: absent
Camel shows no sexual interest (latency time more than 15 minutes).
1: low
Camel approaches the female, sniffs her, mount on it, sit for copulation then dismount
(only 1 attempt to mount).
2: moderate
Camels approaches the female, sniffs, take position and copulates only 1 time (more than
30 minutes between two mounts).
2,5: medium
Camel mates more time, but the mating time is less than 45 min.
3: good
Camels copulates more time and between two mating stands over/near the female showing
flehmen, whistling, neck touching, but sometime spends time walking around (complete
mating time).
4: very good
Camels copulates more time and between two mating stands over/near the female showing
flehmen, whistling, neck touching, blatering, dulaa extrusion, tail beating and spends time
walking around sometime (complete mating time).
5: excellent
Like 4 but it walks around rarely (complete mating time).
Table 4. Stereotypical behavior of male dromedary camel (Padalino et al., 2014).
Behavior
Description
Head-shaking
"The camel raised his head to the vertical in a very fast movement (this behaviour included
a movement of the head up to 90°)"
Pacing in a circle
"The camel walked to the other side of his box (and sometimes stopped and looked through
the window), and walked again until he was at his initial position (by doing this the camel
always followed the same path which described a circle)"
Self biting” or "self-
mutilation
"The camel bitted his own forelegs (right or left) at different part of the legs (to the
shoulder to the feet)"
Bar-mouthing
"Licking, biting or playing with the lips on the bars"
In the framework of ENPI CBCMED
"PROCAMED" project (Promotion des systèmes
camelins innovants et des filières locales pour une
gestion durable des territoires sahariens du bassin
méditerraéen), Fatnassi et al. (2014b) studied and
compared the effects of following management
systems: i) housing in ingle box for 24 hours (H24),
ii) housing in single box for 23 hours with one hour of
free in the paddock (H23) and iii) housing in single
box for 22 hours and 30 min with 1 h of free in the
paddock time and 30 min of exposure to a female
camel's herd (ExF). One hour of paddock time was
chosen, as set out in a study by Freire et al. (2009)
who proved that one hour or regular exercise in a
paddock has positive effects on horse welfare.
However, to enhance the male camel breeding season,
30 minutes of exposure to females had already been
adopted by Bhakat et al. (2005).
During the above mentioned trial, camels
were filmed for thirty minutes mornings and
every evening during a female passage; the
videos were analyzed by two ethologists for
filling a focal sampling ethogram and for scoring
male sexual behavior during the female passage.
There were no statistical differences among H24
and H23, whereas EXF improved the sexual
behavior score of the male camels and their
behavioral repertoire. Traditional management
(H24) affects negatively sexual behavior of male
camels, causing also an increased production of
cortisol. From those preliminary data it seems
that the management system that allows
movements and the interaction with female (ExF)
had positive impact on camel rutting behavior
and welfare. So, Fatnassi et al. (2014b) proposed
the freedom to move and to express social
behavior as "behavioral needs" for camel reared
for semen collection, safeguarding their
wellbeing.
Moreover, when the male were kept daily long
in their stall, Padalino et al. (2014) identified and
targeted some stereotypical behavior in the male
dromedary camel (Table 4). Latter authors tried to
reduce their manifestation varying the management,
and suggested that when the male were reared with
one hour free for walking around and thirty minutes
of the exposition to the female herd the occurrence
of the stereotypies decreased.
B. Padalino et al.
347
Conclusion
The application of ethology to approach, to
train and to study camel bulls may be useful in the
future to improve camel welfare and consequently
their breeding performances and semen quality.
This review was for everyone who spends time
with camels and we wanted to share our approach
to camel management, handling and training in
order to move toward the best possible outcome for
humans and dromedary camels. Anyway, further
studies are needed regarding camel behavior,
welfare, management and breeding strategies to
identify dromedary "behavioral needs" and to
optimize reproduction performances: these are our
aims in the future.
Acknowledgement
This document has been produced with the
financial assistance of the European Union through
the ENPI CBCMED “PROCAMED” Project:
Promotion des systèmes camelins innovants et des
filières locales pour une gestion durable des
territoires saharienne: reference number:
I.B/1.1/493. The contents of this document are the
sole responsibility of Veterinary Clinics and
Animal Productions Section D.E.T.O. Bari, Italy,
and can under no circumstances be regarded as
reflecting the position of the European Union.
Author contributions
B. P., D. M. and G. M. L. conceived the work.
Figures were provided by D. M. B. P., D. M. and G.
M. L. wrote and revised the manuscript.
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