R E V I E W Open Access
Review of human-animal interactions and their
impact on animal productivity and welfare
Humans and animals are in regular and at times close contact in modern intensive farming systems. The quality of
human-animal interactions can have a profound impact on the productivity and welfare of farm animals.
Interactions by humans may be neutral, positive or negative in nature. Regular pleasant contact with humans may
result in desirable alterations in the physiology, behaviour, health and productivity of farm animals. On the contrary,
animals that were subjected to aversive human contact were highly fearful of humans and their growth and
reproductive performance could be compromised. Farm animals are particularly sensitive to human stimulation that
occurs early in life, while many systems of the animals are still developing. This may have long-lasting impact and
could possibly modify their genetic potential. The question as to how human contact can have a positive impact
on responses to stressors, and productivity is not well understood. Recent work in our laboratory suggested that
pleasant human contact may alter ability to tolerate various stressors through enhanced heat shock protein (hsp)
70 expression. The induction of hsp is often associated with increased tolerance to environmental stressors and
disease resistance in animals. The attitude and consequent behaviour of stockpeople affect the animals’ fear of
human which eventually influence animals’ productivity and welfare. Other than attitude and behaviour, technical
skills, knowledge, job motivation, commitment and job satisfaction are prerequisites for high job performance.
Keywords: Animal welfare, Fear, Human-animal interactions, Productivity, Stress
Farm animals have undergone the process of domestica-
tion, a continuing genetic process aimed at modifying
the animal’s behaviour, anatomy and physiology to suit
mankind’s specific needs . Hence, domestic animals
should be adapted to man and captive environment.
However, many farm animals still perceive contact with
humans as an alarming predatory encou nter and sudden
changes in their physical and social environment as a
frightening experience [2,3]. In modern production sys-
tems, there are regular periods of contacts between
humans and animals such as during feeding and cleaning.
Animals may respond to tactile, visual, olfactory, gustatory
and auditory stimuli from humans. Even with considerable
automation in intensive farming, animals are still subjected
to some degree of human contact. The behaviour of
stockpersons is an important factor in determining the de-
gree of animals’ fear in humans and consequently the
quality of the human-animal interaction . Fear for
humans is a major source of stress and may result is poor
productivity in farm animals. This subject has been exten-
sively reviewed previously [4-7].
The quality of human-animal interaction can have a
profound impact on many facets of an animal’s physi-
ology and behaviour. Interactions by humans may be
neutral, positive or negative in nature. Regular positive
contact with humans is desirable in bot h mammalian
and avian species . On the other hand, farm animals
that were handled aversively were highly fearful of
humans, distressed and consequently their welfare and
productivity will be compromised . There have been
considerable reports of attempts to alter the physiology,
behaviour and performance pigs, poultry and cattle
through regular positive contact with humans at both la-
boratory and farm levels [6,9]. The aim of this paper is
to review some of the research that shows impact of
human-animal interactions on the productivity an d wel-
fare of farm animals.
Institute of Tropical Agriculture, and Department of Animal Science,
Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor, Malaysia
JOURNAL OF ANIMAL SCIENCE
© 2013 Zulkifli; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25
The concept of human-animal inter actions
According to Estep and Hetts , human-animal inter-
actions can be defined as the degree of relatedness or
distance between animal and humans. A relationship de-
velops between the stockperson and an animal in his /
her care. The relationship requires mutual individual
recognition. Animals may respond to tactile, visual, ol-
factory, gustatory and auditory stimuli from humans.
The quality of human-animal interactions will determine
whether the influence on an animal’s physiology and be-
haviour is desirable or otherwise . There is the ques-
tion of whether animals can discriminate one human to
another human. Literature regarding the ability of farm
animals to recognise individual people is inconsistent. A
number of experiments suggested that farm animals re-
spond the same way to different people. Hemsworth 
compared the response of pigs to two different
stockpersons which differed markedly in their nature of
contact with pigs. The authors concluded that pigs were
unable to differentiate between different people and
aversive handling by one person made the animals fear-
ful of all people. Jones  indicated that chicks that
had been habituated to one person by a regimen of regu-
lar handling also showed less fear of similarly dressed
but otherwise dissimilar people. On the contrary, other
studies showed that pigs [13,14], laying hens  and
sheep  were able to recognise individual people.
Rybarczyk  suggested that dairy cows may recognise
people by their faces .
Modifying the stress and fear reactions in animals
through human-animal interactions
Stress can be defined as any disruption of an animal’s
homeostatic equilibrium requiring the animal to make
some responses to maintain its psycho-physiological in-
tegrity . The life of a farm animal is constantly chal-
lenged by an array of factors that may evoke stress
responses. Overcrowding, extreme tempera tures, social
disruption, unfamiliar sounds, unfamiliar or uncaring
handlers, feed and water restriction, injection with anti-
gens, disease are common environmental factors that
may disrupt homeostasis. Biological reactions to stress
comprise changes in behaviour, neuroendocrine system,
autonomic nervous system and immune system . In
many stressful events, the first line of defence is behav-
ioural response, which is biologically economic. When
the biological system fails to cope with the stressor(s)
and behavioural activity is suppressed, an animal de-
pends on the integrative capacities of nervous and endo-
crine systems. Regardless of whether the stimulus is
threatening or not, two distinct pathways inv olving
interlocking physiological reactions will be evoked. T he
first pathway comprises the sympathetic adreno-medullary
(SA) system that is responsible for the increase in the
synthesis and release of cathecolamines (adrenaline and
noradrenaline). T he SA system reaction is manifested by
immediate increases in blood pressure, muscle tone, nerve
sensibility, respiration rate and blood sugar. Although the
system may have dramatic physiological consequences, it is
short term. Activation of the hypothalamic-pituitary-
adrenal a xis is a longer adjustment to environmental
fluctuations. Sensory inputs cause the rele ase of
corticotrophin-releasing hormone form the hypothal-
amus. The neurohormone stimulates the anterior pitu-
itary gland to release adrenocorticotrophin hormone
that elicit s the adrenal cortex to relea se glucocorticoids
(cortisol and corticosterone). Glucocorticoids are known
to modulate immune response, shift metabolism, influ-
ence growth, and alter behaviour . Changes in the cir-
culating levels of cortisol or corticosterone are routinely
used to measure an animal’s response to stress.
Stress and fear are not synonymous but the latter may
contribute to overall stress, particularly if the frightening
stimulation is intense, prolong ed or inescapable [21,22].
According to Jones , fear is an emotional (psycho-
physiological) response to perceived danger. Gray 
defined fear as a form of emotional reaction to a stimu-
lus that the animal works to termina te, escape from, or
avoid. High levels of fear not only represent a state of
suffering but they are also a powerful and potentially
damaging stressor. Two of the commonest and poten-
tially frightening events encountered by farm animals
are sudden chan ges in their social or physical environ-
ment and their exposure to people . Animals probably
perceive a new unfamiliar environment with a degree of
uncertainty that acts as a psychological stimulus. In pigs,
short-term exposure to a novel environment indu ced
both behavioural and emotional reactions such as increased
locomotive activity and escape attempts, vocalization, and
as well as hormonal responses . Novel environment is a
potent fear- and stress-elicitor in all animals. Zulkifli et al.
, and Zulkifli and Siti Nor Azah  noted elevation of
heterophil / lymphocyte ratios (HLR) 24 h following trans-
fer of chicks to new home cages. Translocation of chicks
from the hatcher to brooding cages or pens may result in
behavioural inhibition and panic .
The predominant response of the domestic fowl to
humans is thought to be one of fear . Naive chickens
may perceive contact with humans as an alarming
predatory encounter. It is comm on for farm animals to
display fear-related behaviour in the presence of humans
such as withdrawal from or avoidance of humans, im-
mobility such as freezing or crouching [9,21]. Fear of
humans in farm animals can be measured by home cage
avoidance test, box plus experimenter and approachin g
human test . The approaching human test is useful
for commercial poultry flocks raised in floor pens. An
experimenter can film the withdrawal responses of
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25 Page 2 of 7
chickens as he walks slowly through a chicken house.
Orientation away and withdrawal from the approaching
human may be equated with fear levels. It is well docu-
mented that procedures with high human involvements,
such as catching, loading and unloading can evoke both
stress and fear reactions which may compromise chick-
ens’ welfare [28-30]. Hemsworth and Gonyou  indi-
cated that pigs exhibited marked avoidance of humans
following imposition of daily negative interactions as lit-
tle as 15 to 30 s.
There is considerable report to suggest that regular
positive human contact is a powerful and reliable
method to dampen stress and fear reactions in pigs ,
dairy cows , goat s , and poultry [26,34,35]. Al-
Aqil et al.  subjected broiler chicks to a pleasant
physical contact daily for 30 s from 1 to 28 d of age. The
authors found that those chickens had lower HLR,
plasma le vels of corticosterone (CORT), and shorter
tonic immobility (TI) duration than their neglected
counterparts following road transportation. Jones 
suggested that the benefit of regular handling was specif-
ically reducing birds’ fear of humans rather than through
any effect on their underlying fearfulness. However, dur-
ing transit chickens may be exposed to an array of
stressful and fearful stimuli including thermal extremes,
acceleration, vibration, motion, impacts, feed and water
deprivation, social disruption and noise . Similarly,
Lyons  reported that early human contact not only
influenced behavioural responses to humans but also to
novel stimuli. Hence, the findings of Lyons , and Al-
Aqil et al.  showed that regular pleasant human con-
tact may attenuate nonspecific underlying fearfulness in
There is evidence that poultry are also sensitive to vis-
ual contact with humans [26,38,39]. Zulkifli et al. 
reported that visual contact procedure involving the ex-
perimenter standing in the centre of a pen (with no
attempted physical contact with birds) for 10 min twice
daily from 0 to 3 wk reduced fear and stress reactions to
handling and crating. Jones  demonstrated that vis-
ual contacts without tactile interaction was more effect-
ive in reducing fear of humans than picking up and
stroking the birds. Visual contact is obviously mor e feas-
ible and practical than physical contact in commercial
poultry flocks. There is, however, limited documented
work on visual contact with humans, on stress and fear
responses in non-avian species.
One of the earliest studies on the effect of early age
stimuli on physiological stress response was by Levine
 who reported that infantile stimulation through
handling elicited long lasting alterations of the adreno-
cortical function in rodents. When adults, these rats had
lower CORT both basally and during recovery, after
withdrawal of stressors than those that were not
handled, Gross  suggested that stimulation which
occur early in life while many systems of the animals are
still developing may have long lasting impact and could
possibly modify expression of their genetic potential.
Studies in pigs demonstrated that early handling during
the first eight wk of life increased the approach behav-
iour of pigs to an experimenter in a standard test from
10 to 24 wk of age . Zulkifli et al.  compared the
effect of regular visual contact from 0 to 3 wk, 0 to 6 wk
and 3 to 6 wk in chickens subjected to crating at 42 d of
age. Chickens subjected to visual contact from 3 to 6 wk
showed longer TI durations and higher HLR in response
to crating than those interacted at other ages. Based on
these studies, it appears that early age human contact
may have long-term effects. On the other hand, Jones
and Waddington  reported that fear of humans in
20-day-old chicks was equally reduced irrespective they
were handled from 0 to 9, 10 to 18, or 0 to 18 d of age.
It is not clear whether the quality of human contact
experienced by animals at an early age can be modified
by subsequent pleasant or unpleasant interaction with
humans. This is critical under commercial setting be-
cause there will be variation both between and within
stockpersons in their behaviour toward farm animals.
Al-Aqil et al.  subjected chicks to either a combin-
ation of pleasant-unpleasant or unpleasant-pleasant
physical contacts from 1 to 14 d and 15 to 28 d of age,
respectively. Based on HLR and CORT reactions to road
transportation, the authors concluded that the benefits
of early age positiv e human contact can be modified by
subsequent unpleasant experience with humans. The au-
thors also indicated that chickens which had experienced
pleasant human contact early in life may perceive the
presence of huma ns as a signal for continuous positive
interaction. Hence, subsequent exposure to unpleasant
human contact may result in disappointment with con-
sequent elicitation of the physiological stress response.
Effect of human-animal interactions on animal
There is substantial evidence of a negative relationship
between underlying fearfulness and productivity in farm
animals [4,5]. Because positive interaction can reduce
fear of humans, such practice may enhance productivity
of farm animals. Gross and Siegel  postulated that
positive human contact may reduce the resources other-
wise required by animals to respond to their human asso-
ciates and that resources can be utilised for productivity.
In poultry, some authors [44-46] reported a significant im-
provement in weight gain and feed efficiency in positively
handled chickens. The enhanced disease resistance and
immune response in those studies could be associated
with the stress modulating effect of human contact. How-
ever, others demonstrated that positive tactile interaction
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25 Page 3 of 7
either had negligible  or negative effect  on growth
performance. Nature of the physical contact, breed and
age differences may have accounted for the discrepancies.
Zulkifli et al.  reported that regular visual contact, irre-
spective of age, had no effect on weight gain, feed intake,
FCR and mortality rates of broiler chickens. Zulkifli
and Siti Nor Az ah  compared the effe ct s of phys -
ical and visual contact s and showed only the former
was beneficia l in enha ncing growth performance. Phys -
ical contact which involved picking up and stroking
the chickens appeared to be more “interactive” than
visual contact in broiler chickens. In laying hens, however,
Barnett et al.  showed that regular visual contact
which reduced the subsequent avoidance behaviour of lay-
ing hens improved egg production.
According to Hemsworth and Coleman , fear of
humans may be considered as one of the major factors
for depressed growth and reproductive performance in
commercial pigs. Hemsworth et al.  subjected gilts
to either pleasant or unpleasant human contact three
times per week for 2 min in duration from 11 to 22 wk
of age. The authors noted gilts in the pleasant handling
treatment had significantly better weight gain but not
feed efficiency than those in the unpleasant handling
treatment. Unpleasant physical contact with humans re-
duced testicle size and delayed co-ordinated mating re-
sponse in boars when compared to those subjected to
positive handling by humans. In the similar study, gilts
in the unpleasant treatment showed a lower pregnancy
rate than those in the pleasant treatment. Work by
Paterson and Pearce , and Pearce et al. , how-
ever, suggested that the growth response of pigs
housed in groups wa s not affected by regular aversive
handling by humans. There is a possibility that pigs
raised in large groups may receive psychological pro-
tection from members of the group.
There have been relatively few human contact and
productivity studies in other farm animals. Rushen et al.
 showed that pleasant human contact had negligible
effect on milk yield but reduced some behavioural signs
of agitation in dairy cattle that were stressed due to
milking in an unfamiliar environment. The authors con-
cluded that human contact is not sufficient to reduce
neuroendocrine reaction to novelty / isolation stress.
Effect of human-animal interactions on animal health
The immune system, once considered an autonomous sys-
tem, is integrated with other physiological systems and is
sensitive to regulation of the brain . Because human
contact may result alterations in brain physiology and
morphology  it is possible that immune response and
disease resistance will be affected. It is well established
that farm animals encountering challenging conditions
often show some degree of immunosupression [54-57].
Chronic activation of the hypothalamic-pituitary-adrenal
axis and the sympathetic-adrenal-medullary axis results
chronic production of corticosteroids and cathecolamines,
respectively. Lymphocytes, monocytes or macrophages
and granulocytes, exhibit receptors for corticosteroids and
cathecolamines, which can alter cellular trafficking, prolif-
eration, cytokine secretion, antibody production and cyto-
lytic activity .
Because fear is a potent stressor, reducing fear of
humans in farm animals through positive human contact
may enhance the health of animals. Other than poultry
there is a lack of information on the effect of human
contact on the immune response and disease resistance
in farm animals. Gross and Siegel [44,59,60] reported
that chickens habituated to humans through pleasant
contact were more resistant to Escherichia coli and
Staphylococcus aureus infections and had greater anti-
body production against erythrocyte antigens than those
that were ignored. Zulkifli et al.  indicated that regu-
lar visual contact from 0 to 3, an d 0 to 6 wk of age may
improve antibody production against Newcastle disease
vaccine. Similarly, Barnett et al.  showed that hens
subjected to regular pleasant human contact had im-
proved cell-mediated immune response to a mitogen
when compa red to the chickens that received negative
human contact. The benefit of human contact improving
disease resistance and immune res ponse could be a ssoci-
ated with its effect on modulating physiological stress
How do positive human-animal interactions improve
animal productivity and welfare?
There is the question of how positive human-animal
interaction can improve productivity and modify physio-
logical stress response of farm animals. At any particular
time, resources available to an individual are finite.
Hence, competition for resources between body func-
tions such as growth, reproduction and health will al-
ways occur . The resources required to respond to
prolonged and severe stress may be significant. Gross
and Siegel  suggested that habituation to humans re-
duces the resources otherwise needed by the bird to re-
spond to subsequent human contact, and these resources
could be used either for coping ‘with other environmental
stressors of for productivity.
Jones  suggested that regular human contact exerts
its effect by specifically reducing chickens’ fear of
humans. For example regular handling failed to influ-
ence chicks’ reactions to unfamiliar places and objects
[61,62]. On the contrary, Lyons  reported that early
human contact not only influenced behavioural reaction
of goats to human exposure but also a range of novel
stimuli. Al-Aqil et al.  showed that regular pleasant
human contact reduced stress and fear reactions to road
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25 Page 4 of 7
transportation in broiler chickens. Although road trans-
portation involved handling by humans, it is a multifac-
torial process which include feed and water deprivation,
noise, vibration, thermal extremes, social disruption,
crowding and restriction of movements . Fluck 
suggested that handling of chicks decreased forebrain
aminobutyric acid (GABA) receptors and in vitro GABA
release from brain tissues. Hence, it appears that re-
duced chickens’ fear to humans is not the only possible
explanation for the benefit of a positive human-animal
interaction on farm animals.
When living organisms are exposed to thermal stresses,
the synthesis of most proteins is retarded but a group of
highly conserved proteins known as heat shock proteins
(hsp) are rapidly synthesized . In a heat shocked cell,
hsp may bind to heat sensitive proteins and protect them
from degradation, or may prevent damaged proteins from
immediately precipitating and permanently affecting cell
viability. It has been documented that stressors other than
thermal stressors, for example feed restriction, confine-
ment in crates, transportation and social isolation [65-68]
may also elicit hsp 70 response in poultry. The induction
of hsp is often associated with increased tolerance to en-
vironmental stressors and disease resistance [65,69].
Al-Aqil et al.  subjected broiler chickens to either
pleasant or unpleasant negative human handling from
1 to 28 d of age. Following 3 h of road transportation,
the chickens had lower heterophil / lymphocyte ratios ,
shorter TI duration and greater hsp 70 expression
than those that were ignored or handled unplea santly.
Thus, it can be concluded that pleasant human contact
may alter ability to tolerate road transportation stress
through enhanced hsp 70 expression.
The impact of stockmanship on animal productivity and
The factors commonly emphasised to improve farm ani-
mals’ productivity are genetics , housing, nutrition, and
health. There is, however, less emph asis on the quality of
stockmanship. The way a stockperson carry out his or
her routine animal care tasks may contribute to the
overall relationship that animals have with humans and
determine the relationship is positive, negative or neu-
tral. Review of research in commercial pig and dairy
farms showed a significant sequential relationships be-
tween stockpeoples’ attitudes and behaviour towards ani-
mals and the fear of humans and productivity [70,71].
However, there is limited work in the poultry industry.
Cransberg et al  investigated the relationship between
stockperson attitude and behaviour, bird behaviour and
productivity in 24 commercial broiler chicken farms. Un-
like findings in pigs and dairy cattle, the authors failed to
find a relationship between stockpeoples’ attitude and be-
haviour. Although sequential relationships between human
behaviour, bird behaviour and production were noted by
the authors the magnitude of these relationships were not
as substantial as found in pig and dairy industries. The lack
of physical contact between stockperson and chickens and
the large number of chickens managed by the stockpeople
explanations for the results . On the contrary, close
physical contact between stockpeople and animals is com-
The attitude of a stockperson holds about animals will
strongly influence their behaviour to wards animals .
The attitude and consequent behaviour of stockpeople
affect the animals’ fear of human which eventually influ-
ence animals’ productivity and well-being. Other than at-
titude and behaviour, technical skills, knowledge, job
motivation, commitment and job satisfaction are prereq-
uisites for high job performance. Hence, proper selection
and formal training of stockpeople are critical. Today,
many countries, including Malaysia, are facing labour
shortage in the agriculture sector. This may limit the
capacity to select high potential stockpersons. Another
possible limiting factor is the inadequate educational
background of the stockpeople which may restrict their
ability to be trained formally . Thus, the content of
the training programme has to be easily comprehensible
by the target group. It is a lso critical that the animal
industry recognizes and apprec iates the stoc kpeoples’
role in determining animal performance and welfare.
Better financial rewards and cle ar career pathway for
stockpeople would contribute to better motivation and
The preceding discussion clearly highlights the oppor-
tunity to improve productivity and welfare of farm ani-
mals through positive human-animal interaction s. Most
of the pre vious findings on human-animal interaction
were based on laboratory studies. More on-farm studies,
particularly in poultry, are required before appropriate
operational strategies can be formulated for overall ease
and feasibility of implementation in commercial settings.
Factors such as genetic background, housing system,
prior experience and individual variation may determ ine
how an animal respond to human contact. The precise
physiological mechanisms underpinning the effect of
human-animal interactions on productivity and welfare
of farm animals are unclear, although changes in ability
to express heat shock proteins may be considered a pos-
sible route of action. The quality of stockmanship may
markedly influence the productivity and welfare of farm
animals. In intensive animal productions systems the
tasks of managing and monitoring intensively-raised ani-
mals have been increasingly replaced by the use of modern
technologies such as automation and surveillance cameras.
Such technologies are labour-saving but opportunities for
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25 Page 5 of 7
animals to interact with humans will be limited and
thus, may exacerbate their natural fear of humans. A
more regular visual contact with animals is necessary
to dampen underlying fearfulness and physiological
stress in farm animal. Hence, the attitude and behav-
iour of the stockpeople towards farm animals have to
be empha sised.
The author declares that he has no competing interests.
Received: 3 May 2013 Accepted: 4 July 2013
Published: 15 July 2013
1. Siegel PB: Behavior-genetic analyses and poultry husbandry. Poult Sci
2. Suarez SD, Gallup GG Jr: Open-field behaviour in chickens: the
experimenter is a predator. J Comp Physiol Psycho 1982, 96:432–439.
3. Jones RB: Fear and distress.InAnimal Welfare. Edited by Appleby MC,
Hughes BO. Wallingford: CAB International; 1997:75–88.
4. Hemsworth PH, Coleman GJ: Human-Livestock Interactions: The Stockperson
and the Productivity and Welfare of Intensively Farmed Animals. Wallingford:
CAB International; 1998.
5. Hemsworth PH, Gonyou HW: Human contact.InAnimal Welfare. Edited by
Appleby MC, Hughes BO. Wallingford: CAB International; 1997:205–218.
6. Hemsworth PH: Human–animal interactions in livestock production. Appl
Anim Behav Sci 2003, 85: 185–198.
7. Waiblinger S, Boivin X, Pedersen V, Tosi MV, Janczak AM, Visser EK, Jones RB:
Assessing the human-animal relationship in farmed species; A critical
review. Appl Anim Behav Sci 2006, 101:185–242.
8. Jones RB: Fear and adaptability in poultry: insights, implications and
imperatives. Wld’s Poult Sci J 1996, 52:131–174.
9. Hemsworth PH, Barnett JL: Human-Animal Interactions and Animal Stress.
In The Biology of Animal Stress. Edited by Moberg GP, Mench JA.
Wallingford: CAB International; 2000:309–315.
10. Estep DQ, Hetts S: Interactions, relationships and bonds: the conceptual
basis for scientist-animal relations.InThe Inevitable Bond-Examining
Scientist-Animal Interactions. Edited by Davis H, Balfour AD. Cambridge:
CAB International; 1992:6–26.
11. Hemsworth PH, Coleman GJ, Cox M, Barnett JL: Stimulus generalization:
the inability of pigs to discriminate between humans on the basis of
their previous handling experience. Appl Anim Behav Sci 1994, 40:129–142.
12. Jones RB: Ontogeny of the response to humans in handled and non-
handled female domestic chicks.
Appl Anim Behav Sci 1995, 42:261–269.
13. Tanida H, Nagano Y: The ability of miniature pigs to discriminate stimuli
between a stranger and their familiar handler. Appl Anim Behav Sci 1998,
14. Koba Y, Tanida H: How to miniature pigs discriminate between people?
The effect of exchanging cues between a non-handler and their familiar
handler on discrimination. J Anim Sci 1997 2001, 61:239–252.
15. Davies H, Taylor A: Discrimination between individual humans by
domestic fowl. Br Poult Sci 2001, 42:267–279.
16. Boivin X, Desprès Nowak R, Nowak R, Tournadre H, Le NP: Discrimination
between shepherds by lambs reared under artificial conditions. J Anim
Sci 1997, 75:2982–2898.
17. Rybarczyk P, Koba Y, Rusehn J, Tanida De Passille H: Recognition of people
by dairy calves using colour of clothing. Appl Anim Behav Sci 2000,
18. Zulkifli I: Stress and disease development.InDiseases of Poultry in
Southeast Asia. Edited by Zamri-Saad M. Serdang: UPM Press; 2006:1–8.
19. Moberg GP: Biological response to stress: Implications for animal welfare.
In Biology of Animal Stress: Basic Principles and Implications for Animal
Welfare. Edited by Moberg GP, Mench JA. Wallingford: CAB International;
20. Moberg GP: Biological response to stress: Key to assessment of animal
well-being? In Animal Stress. Edited by Moberg GP. Bethesda, Maryland:
American Physiological Society; 1985:27–49.
21. Jones RB: The assessment of fear in the domestic fowl.InCognitive
Aspects of Social Behaviour in the Domestic Fowl. Edited by Zayan R. Duncan:
IJH: Amsterdam: Elsevier; 1987:40–81.
22. Craig JV, Adams AW: Behaviour and well-being of hens (Gallus
domesticus) in alternative housing environments. Wld’s Poult Sci J 1984,
23. Gray JA: The Psychology of Fear and Stress. Cambridge, England: Cambridge
University Press; 1987.
24. Dantzer R, Mormède P: Stress in domestic animals: A
psychoneuroendocrine approach.InAnimal Stress. Edited by Moberg GP.
Bethesda, Maryland: American Physiological Society; 1985:81–96.
25. Zulkifli I, Dunnington EA, Gross WB, Larsen AS, Martin A, Siegel PB:
Responses of dwarf and normal chickens to feed restriction, Eimeria
tenella infection and sheep red blood cell antigen. Poult Sci,
26. Zulkifli I, Siti Nor Azah A: Fear and stress reactions, and the performance
of commercial broiler chickens subjected to regular pleasant and
unpleasant contacts with human beings. Appl Anim Behav Sci 2004,
27. Jones RB: The tonic immobility reaction of the domestic fowl. Wlds’ Poult
Sci J 1986, 42:82–96.
28. Knowles TG, Broom DM: The handling and transport of broilers and spent
hens. Appl Anim Behav Sci 1990, 28:75–91.
29. Zulkifli I, Che Norma MT, Chong CH, Loh TC: Heterophil/lymphocyte and
tonic immobility reactions to pre-slaughter handling in broiler chickens
treated with ascorbic acid. Poult Sci 2000, 79:402–406.
30. Zulkifli I, Che Norma MT, Chong CH, Loh TC: The effects of crating and
road transportation on stress and fear responses of broiler chickens
treated with ascorbic acid. Arch fur Geflugelk 2001, 65:33–37.
31. Hemsworth PH, Barnett JL, Hansen C: The influence of handling by
humans on the behaviour, growth and corticosteroids in the juvenile
female pig. Hormones Behav 1981, 15:396–403.
32. Breuer K, Hemsworth PH, Coleman GJ: The effect of positive or negative
handling on the behavioural and physiological responses of
nonlactating heifers. Appl Anim Behav Sci 2003, 84:3–22.
33. Lyons DM, Price EO, Moberg GP: Individual differences in temperament of
domestic dairy goats: Constancy and change. Anim Behav 1988,
34. Zulkifli I, Gilbert J, Liew PK, Ginsos J: The effects of regular visual contact
on tonic immobility, heterophil/lymphocyte ratio, antibody and growth
responses in broiler chickens. Appl Anim Behav Sci 2002, 79:103–112.
35. Al-Aqil A, Zulkifli I, Hair Bejo M, Sazili AQ, Rajion MA, Somchit MN: Changes
in heat shock protein 70, blood parameters and fear-related behavior in
broiler chickens as affected by pleasant and unpleasant human contact.
Poult Sci 2013, 93:33–40.
36. Nicol CJ, Scott GB: Pre-slaughter handling and transport of broiler
chickens. Appl Anim Behav Sci 1990, 58:57–73.
37. Lyons DM: Individual differences in temperament of dairy goats and the
inhibition of milk injection. Appl Anim Behav Sci 1989, 22:269–282.
38. Jones RB: Reduction of domestic chick’s fear of humans by regular
handling and related treatments. Anim Behav 1993, 46:991–998.
39. Barnett JL, Hemsworth PH, Hennesy DP, McCallum TH, Newman EA:
The effects of modifying the amount of human contact on behavioural,
physiological and production responses of laying hens. Appl Anim Behav
Sci 1994, 41:87–100.
40. Levine S: Stress and behavior. Scientific Am 1967, 224:26–31.
41. Gross WB: Chicken-environment interactions.InEthics and Animals. Edited
by Miller HB, Williams WH: C. New Jersey: Human Press; 1983:329–337.
42. Hemsworth PH, Barnett PH, Hansen C: The influence of handling by
humans on the behavior, reproduction and corticosteroids of male and
female pigs. Appl Anim Behav Sci 1986, 15:303–314.
43. Jones RB, Waddington D: Attenuation of the domestic chick’s fear of
human beings via regular handling: in search of a sensitive period.
Appl Anim Behav Sci 1993, 36:1021–1033.
44. Gross WB, Siegel PB: Socialization as a factor in resistance to disease, feed
efficiency, and response to antigen in chickens. Am J Vet Res 1982,
45. Jones RB, H ughe s BO: Effectsofregularhandlingongrowthinmale
and female chicks of broiler and layer strains. Br Poult S c i 1981,
46. Collins JW, Siegel PB: Human handling, flock size and response to an E.
coli challenge in young chickens. Appl Anim Behav Sci 1987, 19:183–188.
Zulkifli Journal of Animal Science and Biotechnology 2013, 4:25 Page 6 of 7
47. Reichmann KG, Barram KM, Brock IJ, Standfast NF: Effects of regular
handling and blood sampling by wing vein puncture on the
performance of broilers and pullets. Br Poult Sci 1978, 19:97–99.
48. Freeman BM, Manning ACC: Stressor effects of handling on the immature
fowl. Res Vet Sci 1979, 26:223–226.
49. Paterson AM, Pearce GP: Boar-induced puberty in gilts handled pleasantly
or unpleasantly during rearing. Appl Anim Behav Sci 1989, 22:225–233.
50. Pearce GP, Paterson AM, Pearce AN: The influence of pleasant and
unpleasant handling and provision of toys on the growth and behavior
of male pigs. Appl Anim Behav Sci 1989, 23:27–37.
51. Rushen J, Munksgaard L, Marnet PG, Passillé D: Human contact and the
effects of acute stress on cows at milking. Appl Anim Behav Sci 2001,
52. Ader R, Cohen N: Psychoneuroimmunology: Conditioning and Stress. Ann.
Rev Psychol 1993, 44:53–85.
53. Meaney MJ, Bhatnagar S, Diorio J, Larocque S, Francis D, O’Donnell O,
Shanks N, Sharma S, Smythe J, Viau V: Molecular basis for the development
of individual differences in the hypothalamic-pituitary-adrenal stress
response. Cell Mol Neurobiol 1993, 13:321–347.
54. Blecha F: Immunomodulation: a means of disease prevention in stressed
livestock. J Anim Sci 1988, 66:2084–2090.
55. Griffin JF: Stress and immunity: a unifying concept. Vet Immunol
Immunopathol 1989, 20:263–312.
56. Zulkifli I, Siegel PB: Is there a positive side to stress? Wld’s Poult Sci J 1995,
57. Siegel PB, Gross WB: General principles of stress and well-being.In
Livestock Handling and Transport. Edited by Grandin T. Wallingford: CAB
58. Madden KS, Livnat S: Catecholamine action and immunologic reactivity.
In Psychoneuroimmunology II. Edited by Ader R, Felten DL, Cohen N. San
Diego: Academic Press; 1991:283–310.
59. Gross WB, Siegel PB: Influence of sequences of environmental factors on
the response of chickens to fasting and to Staphylococcus aureus
infection. Am J Vet Res 1982, 43:137–139.
60. Gross WB, Siegel PB: Socialization, the sequencing of environmental
factors, and their effects on weight gain and disease resistance of
chickens. Poult Sci 1983, 62:592–598.
61. Jones RB, Faure JM: The effects of regular handling on fear in the
domestic chick. Behav Proc 1981, 6:135–143.
62. Jones RB, Waddington D: Modification of fear in domestic chicks, Gallus
gallus domesticus via regular handling and early environmental
enrichment. Anim Behav 1992, 43:1021–1033.
63. Fluck E, Hogg S, Jones RB, Bourne R, File SE: Changes in tonic immobility
an dthe GABA: benzodiazepine system in response to handling in the
chick. Pharmacol Bio-chem Behav 1997, 58:269–274.
64. Etches RJ, John TM, Verrinder Gibbins AM: Behavioural, physiological,
neuroendocrine and molecular responses to heat stress.InPoultry
Production in Hot Climates. Edited by Daghir NJ. CAB International; 1995:31–66.
65. Zulkifli I, Che Norma MT, Israf DA, Omar AR: The effects of early-age food
restriction on heat shock protein 70 response in heat-stressed female
broiler chickens. Br Poult Sc 2002, 43:141–145.
66. Zulkifli I, Al-Aqil A, Omar AR, Sazili AQ, Rajion MA: Crating and heat stress
influences blood parameters and heat shock protein 70 expression in
broiler chickens showing short or long tonic immobility reactions. Poult
Sci 2009, 88:471–476.
67. Al-Aqil A, Zulkifli I: Changes in heat shock protein 70 expression and
blood parameters in transported broiler chickens as affected by housing
and early age feed restriction. Poult Sci 2009, 88:
68. Soleimani AF, Zulkifli I, Omar AR, Raha AR: Neonatal feed restriction
modulates circulating levels of corticosterone, and expression of
glucorticoid receptor and heat shock protein 70 in aged Japanese quail
exposed to acute heat stress. Poult Sci 2011, 90:1427–1434.
69. Liew PK, Zulkifli I, Hair-Bejo M, Omar AR, Israf DA: Effects of early age feed
restriction and thermal conditioning on heat shock protein 70
expression, resistance to infectious bursal disease and growth in male broiler
chickens subjected to chronic heat stress. Poult Sci 2003, 82:1879–1885.
70. Hemsworth PH, Barnett JL, Hansen Coleman GL: A study of the
relationships between the attitudinal and behavioural profiles of
stockpersons and the level of fear of humans and reproductive
performance of commercial pigs. Appl Anim Behav Sci 1989, 23:301–314.
71. Coleman GJ, Hemsworth PH, Hay M: Predicting stockperson behaviour
towards pigs from attitudinal and job-related variables and empathy.
Appl Anim Behav Sci 1998, 58:63–76.
72. Cransberg PH, Hemsworth PH, Coleman GL: Human factors affecting the
behaviour and productivity of commercial broiler chickens. Br Poult Sci 2000,
Cite this article as: Zulkifli: Review of human-animal interactions and
their impact on animal productivity and welfare. Journal of Animal
Science and Biotechnology 2013 4:25.
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