Widening the spotlight on genetic welfare problems: heritable
disorders in selectively bred reptiles.
Mark P Rose BSc MSc CBiol MSB. Student at The Royal (Dick) School of Veterinary Studies, The University of
Edinburgh, Easter Bush Campus, Midlothian EH25 9RG.
David L Williams MA VetMD PhD CertVOphthal CertWEL FHEA FSB FRCVS Department of Veterinary
Medicine, Univetsity of Cambridge CB3 0ES
Abstract
There is widespread and growing public and professional awareness of genetic disorders, and
their implications for health and welfare, associated with the artificial breeding selection of
companion animals. However, little research has been conducted to date into these issues in
captive-bred wild animals, such as reptiles, compared to the domestic companion animal
species. This is despite comparable if not greater numbers of reptiles now maintained in
captivity in the UK relative to domestic dogs, and the increasing popularity of atypical
colour/pattern variants of these species. The work presented here aims to raise awareness of
the potential for genetic welfare problems in reptiles among the animal welfare science
community, and stimulate further research in this field. Survey of expert opinion was used to
establish a description of a heritable disorder (‘wobble syndrome’) associated with a widely
propagated phenotype (the ‘Spider’ morph) of a popular captive species (the royal python),
and to provide an assessment of animal welfare impacts. Recommendations are made for
improved self-regulation of the herpetocultural community, and suitable avenues for further
investigation identified.
Introduction
Genetic disorders in captive bred animals
and their associated implications for health
and welfare, whilst long acknowledged
among veterinarians and welfare scientists
(see CAWC 2003), were brought to the
public spotlight by the 2008 BBC
documentary ‘Pedigree Dogs Exposed’
(APGAW 2009).
Since the airing of the programme,
advances have been made toward
addressing the issues raised, which have
no doubt been to some extent facilitated
by increased awareness among pet owners.
These advances include funding provision
for research into the prevalence of
inherited disorders in companion animals,
the establishment of the Advisory Council
on the Welfare Issues of Dog Breeding,
the continued development of screening
options for hereditary diseases and the
introduction of veterinary checks for 14
‘high profile’ dog breeds (Peck 2010;
RSPCA 2013). Public and professional
attention has continued to increase, with
dog breeding and welfare having received
prominent coverage in several British
newspapers (APGAW 2012) as well as
being cited as the leading welfare concern
of veterinary professionals in 2011 (PDSA
2011).
In their recent review of progress since the
documentary’s broadcast in tackling the
issues raised, the Associate Parliamentary
Group for Animal Welfare (2012) detailed
an Action Plan which, among other
measures, highlighted the need for
continued and enhanced engagement and
education of the public, thus empowering
them to make informed choices when
purchasing companion animals. Sharing
this goal, the Universities Federation for
Animal Welfare (UFAW) is developing an
online database of genetic diseases and the
associated impacts on animal welfare
(Kirkwood 2012). The number of
hereditary disorders detailed on the
UFAW database at the time of writing is
shown in Table 1. For each condition
listed on the website, discussion is made
of the clinical and pathological effects,
intensity and duration of welfare impact,
number of animals affected, diagnosis,
1
genetics, detectability and prospects for
the conditions’ elimination from the
respective breed or strain.
Table 1: Numbers of genetic welfare problems in different companion animals detailed within the
UFAW online database (UFAW 2012). Conditions were repeat-counted where they are associated
with multiple breeds/strains.
Companion Animal
Species/Taxon
Dogs
Birds
Cats
Fish
Rabbits
Horses
Guinea Pigs
Number of Breeds/Strains
A possible limitation to the progress that
has been made to date is the heavy bias in
focus toward disorders in the domestic
dog, as evident in Table 1. It is
undoubtedly important for welfare
scientists and other stakeholders to
allocate their finite resources with regard
for the number of individuals of a species
maintained in captivity, and the extent and
scale of their deviation from the ancestral
phenotype. However, there has as yet been
comparatively little consideration of the
health and welfare consequences in
captive wild animals subject to selective
breeding, such as reptiles. This is despite,
in the UK at least, comparable if not
collectively greater numbers of reptiles
being maintained as companion animals
than domestic dogs (Clark 2012; EUARK
2012; Jones 2012). Estimates are variable
and often lacking substantiation, though
EUARK (2012) suggest eight million
reptiles are kept as pets across 1.1 million
UK households, whilst Chang and
Jacobson (2010) suggest that several
million boid (family Boidae and
Pythonidae) snakes alone are kept as pets
or breeding stock in the United States.
A significant proportion of the captive
bred reptile industry is based upon the
development of novel colour/pattern
strains, or ‘morphs’, through artificial
breeding selection. This is a lucrative
business; at the time of writing a leading
UK reptile dealer’s website advertises
wild phenotype royal pythons Python
regius at £39.95, with prices for genetic
48
27
9
8
3
1
1
Number of Conditions
121
27
12
11
3
1
1
variants of the same species reaching
£10,995.00 (CPR 2013). The value of the
reptile sector of the UK pet industry was
valued at £200 million in 2012, with the
annual number of reptiles and amphibians
being captive bred in the UK cited at
250,000 and increasing (EUARK 2012).
Despite the numbers now maintained in
captivity and the growth in captive
breeding for development of novel
phenotypes, a review of the veterinary and
animal welfare science literature reveals
scant reference to reptile health and wefare
in this context. Conversely, a cursory
glance over web-based hobbyist media is
sufficient to identify numerous anecdotal
reports of potential welfare issues linked
to genetic manipulation.
Artificial selection during captive reptile
breeding established during the 1980s and
1990s, following the discovery of wild
snakes with atypical colouration and
patterning. A March 1981 article in the
National Geographic, featuring a picture
of an albino Burmese python from
Thailand, captured the interest of breeders
in the West, who saw the market potential
for these novelty snakes (Collis and Fenili
2011). Colour and pattern morphs arise
from mutations in genes coding for the
type, number and spatial distribution of
chromatophores. In the royal python, these
include the melanophores (containing
black/dark brown pigment), xanthophores
(containing
yellow
pigment)
and
iridiophores (which reflect and refract
2
light). Morphs carrying a single mutation
are known in the industry as ‘base
morphs’, which may be crossbred to
combine multiple mutations, producing
what are termed ‘designer morphs’
(Jepson 2013).
Snakes are diploid organisms. The genetic
bases of the different royal python morphs
include: (i) dominant mutations (a single
inherited defective allele will trigger the
observable trait); (ii) recessive mutations
(only homozygous individuals will display
the observable trait, which will otherwise
be masked by the wild phenotype); (iii)
incomplete-dominant mutations (alleles
combine to produce an intermediary
phenotype); and (iv) line-bred mutations
(consistent artificial selection upon natural
variation to exaggerate a desired trait)
(Jepson 2013).
The need for caution when introducing
artificial selection to the captive breeding
of wild animals was highlighted a decade
ago in the Companion Animal Welfare
Council’s (CAWC) report on the welfare
of non-domestic animals kept for
companionship. Recommendation 7 of the
CAWC (2003) report states that,
“selection for specific traits (e.g. colour,
size, unusual plumage characteristics etc)
should be undertaken only with careful
regard to the possibility of overt or covert
adverse welfare consequences”. The
report goes on to recommend that research
be conducted into the welfare of breeds or
strains where there is reason to believe
that this may have been impacted during
the artifical selection for desired traits.
The herpetocultural community has yet to
address these recommendations. Extensive
research is needed to establish the extent
to which genetic diseases and disorders are
already present in captive-bred reptiles, to
determine their causes, consider the
implications for animal welfare and
identify means of their reduction.
The work presented here aims to:
1. Raise awareness of the potential for
genetic welfare problems in reptiles
among the animal welfare science
community.
2. Establish a description of a heritable
disorder in a captive bred reptile
species, consider its impact to animal
welfare and identify means of its
reduction.
3. Recommend suitable avenues of
further
study
to
increase
understanding in this field.
Materials and Methods
This work focuses on a single genetic
disorder associated with a single, widely
propagated phenotype of the royal python.
This species has gained widespread
popularity among companion animal or
“pet” owners, as well as hobbyist and
commercial breeders. The disorder is
known in the hobby as ‘wobble
syndrome’, and is associated with a
genetic variant known as the ‘Spider’
morph. The Spider morph is a dominant
gene trait characterised by a pattern
alteration, where the dorsal melanophores
are reduced in area, forming a web-like
mesh. This may be accompanied by a
retreat toward the dorsal surface of the
ventral xanthophores, leaving white flanks
(Jepson 2013). The Spider morph is
deliberately selected for due to its high
commercial value, resulting from its
striking pattern. The trait’s genetic
dominance means that the morph can be
readily outcrossed to introduce the Spider
patterning into designer morphs.
The means of data capture for this
investigation was online survey of expert
opinion. In the first instance, hobbyist and
commercial breeders were targeted in
order to establish a description of the
nature and severity of clinical signs of the
wobble condition, as well as breeder
perceptions on prevalence, cause and
impacts of the disorder. One hundred
breeders from the United Kingdom,
mainland Europe, the United States and
Australia were identified via internet
search using relevant keywords.
A second survey targeted animal welfare
scientists and veterinary professionals.
Here, the findings of the breeder survey
were presented to members of the Animal
Welfare Science, Ethics and Law
3
Veterinary Association, who were then
asked to comment on their perception of
the intensity and duration of the welfare
impact, if any, of the wobble condition on
affected royal pythons.
Delivery of the breeder and AWSELVA
questionnaires were facilitated by Google
Documents
and
Survey
Monkey®
respectively. In each case, an option to
anonymise responses was included.
Responses were omitted from analysis
where they were incomplete or
inconsistent. Due to the low sample sizes
achieved, quantitative methods of
statistical analysis were not employed.
Results
Breeder Questionnaire
Survey uptake was poor, with 13 of the
100 breeders contacted partaking in the
survey. Four further breeders returned
contact via email to enquire about the
research aims of the investigation. A
standardised response was provided,
which in each case failed to elicit uptake
of the survey. The number of royal
pythons under the care of each respondent
was reported to range from 9-2000, with a
mean of 322. Eight respondents selfidentified at hobby breeders, three as
commercial breeders, with the remaining
two not specifying. Every respondent was
aware of the Spider wobble condition.
When asked to describe the signs and
symptoms of the condition, respondents
widely reported:
- Mild torticollis (abnormal/asymmetrical
head and neck positioning);
- Side-side tremors of head and neck;
- Erratic looping or corkscrewing of head
and neck;
- Poor directional skills / incoordination /
loss of motor function; and
- Symptoms appearing particularly or only
during states of arousal, such as when
feeding or seemingly stressed/nervous.
Other signs and symptoms cited included:
- Poor, tense or wiry muscle tone;
- Loose grip with tail;
- Inability to right when placed in dorsal
recumbency; and
- Likened to Parkinson's disease in
humans.
There was a widely acknowledged scale in
the severity of symptoms between
individual animals, with age (although
reports were contradictory), with degree of
arousal and according to combination with
other morphs. There was disagreement
among breeders over the proportion of
Spider morphs which present the condition
to some degree at some point in their lives
(Figure 2), however there was consensus
that a low proportion are severely affected
Figure 3).
The wobble condition is generally
reported by breeders to have little impact
on quality of life in the majority of cases,
with statements such as, “Most I see lead a
comparable life to a normal ball python
except the obvious differences in grace of
motion”, and “I have not found that it
affects them in any meaningful adverse
way. Even severely affected adults eat
great, breed and will lay good eggs.”
Feeding response is widely cited to be
normal, although due to poor motor skills
strike accuracy is often poor. Two
independent reports were received of
animals euthanised due to the condition,
with poor feeding cited as the primary
reason, though it is unclear as to whether
this was related to the physical ability or
the willingness to feed unassisted.
Fertility and fecundity are also generally
said to be unaffected, with one report of
severely affected individuals having
difficulty with the physical act of
copulation (presumed to be the result of
the characteristic incoordination). A single
report was received that there is no
homozygous form of the Spider genotype,
as any Spider-Spider pairing will result in
a high incidence of egg failures and
severely defected hatchlings. Whilst it was
noted that there is no evidence to date that
the condition reduces longevity in
captivity, the Spider morph was
discovered too recently for a true
assessment.
4
7
Number of reports
6
5
4
3
2
1
0
1-33%
34-66%
67-99%
100%
Proportion of spider morph royal pythons affected by
the wobble condition to a greater or lesser degree
Figure 1 Breeder reported prevalence of the wobble syndrome in Spider
morph royal pythons.
12
Number of reports
10
8
6
4
2
0
1-33%
34-66%
67-99%
100%
Proportion of spider morph royal pythons severely
affected by the wobble condition
Figure 2 Breeder reported proportion of Spider morph royal pythons
severely affected by the wobble condition.
It was widely stated that the genetic origin
of the wobble condition is linked to the
gene fault coding for the Spider mutation,
i.e. the signs and symptoms of the wobble
are as much integral to the Spider morph
as the characteristic colour and pattern.
Evidence for this is drawn from the
presence of the wobble condition in
designer morphs where the Spider has
been combined with other base morphs.
As a dominant gene trait, the Spider
morph is one of the most outbred in the
industry, as opposed to recessive gene
traits which are often inbred to achieve
fixation. Furthermore, snakes born to a
Spider bloodline which lack the Spider
pattern/pigment expression do not express
the wobble. It was also reported that the
original wild-caught Spider female was
symptomatic for the condition.
When breeders were asked of the potential
for disassociation of the wobble condition
from the Spider morph through selective
breeding, there was inconsistency across
responses. Some believe this is not
possible, with reports made of unaffected
hatchlings born to severely affected
5
females, as well as affected offspring born
to adults who’d never displayed
observable symptoms. Conversely, some
breeders were optimistic, stating that
incidence could be significantly reduced,
though not eradicated, by selective
breeding for unaffected animals. For
example, “All of our holdback breeders
are selectively kept because they exhibit
little to no signs of head wobble, and many
of our hatchlings come out the same way,
with the occasional animal (perhaps 1 in
30-40) that has obvious head wobble
issues. Of our associates, customers, and
friends that breed affected animals freely,
the percentages of affected offspring [are]
much higher, based on my personal
observations.”
minded to categorise the wobble signs and
symptoms (as established by the breeder
questionnaire data), as having a negligible
welfare impact either in intensity or
duration.
Isolated reports were also received that
incidence of the condition may vary
according to combination with other
genetic mutations in designer morphs.
Incidence is said to be reduced in designer
morphs carrying the Butter and Enchi
Pastel mutations, but to increase when the
Spider is combined with the Pastel morph.
Of the respondents that felt the welfare
impact was minimal, rationales were cited
such as, “Although there are cognitive
defects that appear to be present [these]
don’t seem to adversely affect quality of
life too severely,” and, “There seems to
only rarely be a severe welfare issue with
the wobble condition, with the majority
leading a largely ‘normal’ life.”
AWSELVA Questionnaire
Survey uptake among this group was
higher relative to the breeder group.
However, survey completion was poor,
with 31 of the 76 respondents completing
only their personal details.
Prior awareness of the wobble condition
was lower relative to the breeder group, at
24% (Figure 3). Statistical methods were
not employed due to the limited sample
size, however there was an apparent trend
in the respondents’ perceptions of welfare
impact associated with the wobble
condition toward moderate to high
intensity, and moderate to prolonged
duration (Table 2). No respondents were
The ethical defensibility of the continued
propagation of the Spider morph, in light
of the available evidence on the
prevalence, characteristics and genetic
origin of the wobble condition, evoked a
mixed response from the animal welfare
science and veterinary community.
Although none were minded to conclude
that propagation is ethically defensible,
56% of respondents stated that further
research was required before conclusions
could be drawn (Figure 4).
Conversely, some respondents suggested
that the artificial selection for lines
carrying
deleterious
traits
was
fundamentally
indefensible,
with
comments such as, “I am strongly against
breeding of morphs, breeds or lines that
carry undesirable traits,” and “…any
welfare cost cannot be justified by
aesthetic reasons.”
The rationale for assessments of moderate
to high welfare impacts were frequently
centred around the feelings of frustration
and stress that, intuitively, might be
associated with impaired ability to
perform species-appropriate behaviours.
6
24%
Yes
No
76%
Figure 3 Prior awareness of the wobble condition among AWSELVA
members (n=44).
Table 2 Perception of welfare impact (intensity and duration) of the wobble condition among
respondents (n=28).
Perceived Welfare Impact: Intensity
Perceived
Welfare
Impact:
Duration
Negligible
Minimal
Moderate
High
Negligible
0
0
0
0
Short
0
1
1
0
Moderate
0
1
2
2
Prolonged
0
1
11
10
0%
Yes
No
56%
Insufficient
information
44%
Figure 4 Respondent conclusions on whether it is ethically defensible to
continue to propagate the Spider morph royal python (n=43).
7
Where it was stated that further
information is necessary before the ethical
defensibility of Spider morph propagation
can be fully considered, these could be
broken down into the following fields:
- Data on the affect, if any, of the wobble
Spider morph and/or wobble condition on
longevity relative to wild phenotype royal
pythons.
- Investigation into the underlying
pathology, as well as any latent
physiological
changes
that
may
accompany the wobble condition.
- An extensive dataset of standardised
clinical assessments, gathered by a nonbiased exotic veterinary team, “focusing
on sensory and motor performance,
divergences from normal behaviour
patterns, and general physical and
physiological status.”
Others felt that sufficient information was
already available to conclude a significant
welfare cost associated with the wobble
condition (e.g. “Even from the brief
description provided by this survey it is
easy to see that this condition has a
significant impact on the day to day life
quality
of
affected
individuals.”)
warranting the cessation of breeding from
the Spider morph.
Discussion
The Spider Morph Wobble
Genetic welfare problems brought about
through artificial selection can be broadly
attributed to one of three categories
(CAWC 2006). The first is where the trait
being selected for directly results in stress,
disease or discomfort. Examples of this
are the wide range of dermal, ocular and
respiratory complications exhibited in
brachycephalic dog breeds (Oechtering, et
al.
2010;
Meola
2013)
or
osteochondrodysplasia in Scottish fold
cats (Malik, et al. 1999). A further
category includes issues not linked to
specific traits, either deliberately selected
for or otherwise, but instead brought about
as a side effect of excessive inbreeding,
concentrating deleterious recessive alleles.
An example of this is dental malocclusion
in certain bloodlines in domestic rabbits
(Harcourt-Brown 2002).
The final category includes welfare
problems with no physiological causal link
to the morphological or behavioural trait
targeted through selection, but by a
disease or trait with an intrinsic genetic
association with that which is being
selected. For example, breeders of
canaries with the recessive white mutation
have unwittingly co-selected for animals
with impaired ability to absorb vitamin A
from their diet (Wolf, et al. 2000). The
results presented here show that it is this
category into which the wobble condition
associated with the Spider phenotype of
the royal python fits.
Clinical signs of the wobble condition
have been shown to include head and neck
tremors,
torticollis,
incoordination,
disequilibrium and inhibited righting
reflex, which are indicative of a central
nervous system disorder (Bennett and
Mehler 2005). Symptoms may only
appear, or be exaggerated, during periods
of arousal, such as when feeding. While
prevalence of the condition among Spider
morphs remains unclear, with many
experts stating that all are affected to some
degree, there is consensus that a minority
of individuals are severely impacted in
their ability to perform their full repertoire
of species-appropriate behaviours, relative
to wild-type captive pythons. No data is
available on longevity, with the relatively
recent discovery of the Spider morph.
Captive royal pythons are recorded to have
reached 47.5 years (Funk 2005).
Other disorders presenting similar
neurologic manifestations in reptiles
include nutritional (e.g. hypothiaminosis),
trauma-induced,
metabolic
(e.g.
xanthomatosis), toxic (e.g. insecticide
toxicosis, metronizadole overdose) and
infectious (various parasitic, bacterial and
viral) neuropathies (Lawton 1992; Bennett
and Mehler 2005).
Welfare Consideration
While respondents to the breeder
questionnaire generally agreed that quality
of life was not significantly affected, 89%
(n=28) of respondents from the animal
welfare science and veterinary group
considered the welfare impact to be of
8
moderate to high intensity, based on the
information provided. This conclusion was
predominantly based on perceived
impairment of affected individuals to
perform species-appropriate behaviours.
One respondent went on to state, “'Mild
torticollis' etc would still be quite
uncomfortable, according to my take on
the 'how would that make me feel?'
principle.”
Although
such
anthropomorphism is clearly subject to
limitations, common sense and empathy
can, in some cases, provide insight into an
animal’s welfare state. Human and nonhuman animals exist on an evolutionary
continuum of physiology, from singlecellular organisms to higher vertebrates. It
follows that lower phylogenies, such as
sponges which lack a nervous system, are
incapable of feelings of pain, suffering or
discomfort.
However,
evolutionary
continuities in anatomy, neurology and
biochemistry support a hypothesis of
increasing sentience with increasing
physiological
complexity
(Nuffield
Council on Bioethics 2005). Reptiles are
vertebrates
with
complex
neural
architecture, possessing a cerebral cortex
with two hemispheres and 12 cranial
nerves (Bennett and Mehler 2005). Nerve
endings in the skin are also noted to be
similar in form and function to those
identified in mammals.
It was widely stated by breeder
respondents that fecundity was unaffected
by the wobble condition (excepting one
report of animals experiencing difficulty
with the physical act of copulation) and
implicitly this demonstrated absence of
impact to quality of life. Indeed, a primary
function of the stress response is to
maximise energy availability to vital
functions, therefore non-vital functions
such
as
reproduction
are
often
dramatically inhibited (Denardo 2005).
Superficially, it therefore follows that an
absence of demonstrable impact on
fecundity would indicate absence of stress;
however this is an overly simplistic
interpretation. Although energy-expensive
reproductive
behaviours
such
as
aggression and territory maintenance
(Tokarz 1987) will be inhibited,
copulation is comparatively energyinexpensive and carries a high fitness
value (Denardo and Licht 1993; Denardo
2005). The captive breeding environment,
where supportive behaviours are not
required for successful reproduction, could
therefore effectively mask an induced
stress-response.
Our historical failure to identify signs of
stress potential poor welfare in reptiles
relative to, for example, mammalian
companion animals, is probably best
explained by the alien nature of their
morphology and behaviour (Arena and
Warwick 1995). This may account for the
paucity of published works on genetic
welfare problems in this taxon. However,
if
superficially
mechanistic
and
behaviourally incomplex, reptiles are in
fact collectively capable of sophisticated
communication, problem solving, parental
care and play behaviours (Chapple 2003;
Leal and Powell 2012; Burghardt 2013).
Further research is warranted to improve
our understanding of reptile welfare,
including the effects of artificial breeding
selection. This was highlighted by the
results of the AWSELVA questionnaire,
where 56% of respondents concluded that
insufficient information was available on
the wobble condition to reach a
determination on the ethical defensibility
of continued propagation of the royal
python Spider morph (Figure 4, n=43).
It should be noted that there may be
advantages to animal welfare arising from
the growing interest in and business of
captive breeding. For example, Mader and
Mader-Weidner (2005) note that in the
past it has been more financially viable to
replace an diseased reptile than to seek
veterinary intervention. This is no longer
the case due to more widespread
veterinary expertise in reptile medicine
and the growing commercial value of
reptiles - both factors which have no doubt
increased partially as a result of extensive
captive breeding of these species.
However, it is beyond the scope of this
work to present a comprehensive costbenefit analysis of the captive breeding of
reptiles. Further, any such favorable
factors do not detract from our ethical
9
responsibilty to highlight and address
potential sources of poor welfare where
they are identified.
Recommendations and Research
Opportunities
Paragraph 5.4.1 of the CAWC (2003)
report highlights that the prevention of
husbandry-related diseases is of great
moral importance, but emphasizes the
need
for
a
measured
response.
Disproportionate legislative control may
not promote optimum welfare, has been
unsuccessful in the past, and can have
unforeseen consequences such as increases
in invasive species damaging native
ecology (EUARK 2012).
The strength of the herpetological hobby
and industry is in its community of
enthusiasts,
closely
connected
by
dedicated web-based media. It is selfevident from review of such media that the
vast majority of herpetoculturists care
deeply for the health and welfare of their
companion animals and/or breeding stock,
however further research and effective
dissemination of findings is required of
community leaders. The European Union
Association of Reptile Keepers (EUARK),
International Herpetological Society (IHS)
and Federation of British Herpetologists
(FBH) are therefore called on to promote
research into the welfare consequences of
heritable disorders associated with captive
breeding, and to publish position
statements on the breeding of morphs or
lines carrying known defects or disease.
Progress toward this self-regulation is
already being made. Some breeders
provide online “genetic calculators” used
to determine the statistically probable
outcome of a given morph pairing, with
some specifically highlighting where a
pairing may result in a known defect (see
OWAL Reptiles n.d.).
The work presented here highlights
several avenues of research opportunity
relating to the Spider morph wobble
condition, as well as wider issues relating
to captive breeding for novel morphs.
Isolated reports were received from
breeder respondents of varying intensity of
wobble condition signs according to the
Spider morph’s combination with other
base morphs. Statistical analysis of an
extensive dataset on the intensity of
wobble signs among royal pythons
carrying the Spider morph in combination
with others may therefore yield
opportunities for the reduction in
symptoms of neurologic dysfunction.
A true assessment of impact on quality of
life should be based upon complete
information on the effects of the condition.
Other neuropathies presenting comparable
behavioural symptoms to the wobble are
often found to be accompanied by
physiological clinical signs during
cytology,
biopsy
and
necropsy
investigation (Bennett and Mehler 2005).
For example, inclusion body disease, a
disorder found in Boid snakes thought to
be caused by a retrovirus, is characterised
by
general
signs
of
neurologic
dysfunction.
However,
further
examination reveals intra-cytoplasmic
inclusions present in cells of many
epidermal, epithelial and neuronal tissues
(Schumacher, et al. 1994). Comprehensive
pathological analysis of royal python
Spider morph specimens may therefore
identify
latent
physiological
manifestations of the wobble condition,
which may themselves open further
avenues of investigation.
Where AWSELVA survey respondents
perceived a moderate-high welfare impact
intensity associated with the wobble
condition, the rationale was frequently
reported as likely (though unproven)
frustration associated with impaired ability
to perform species-appropriate behaviours.
Indeed, breeders reported that strike
accuracy in affected pythons was reduced
during feeding. Further study to quantify
any increase in stress experienced during
feeding is therefore warranted, to support
a robust assessment of the welfare
implications of the condition. The
neuroendocrine stress reponse in reptiles
comprises both acute and chronic phases.
The former is regulated by the sympathetic
nervous system and results in rapid
10
secretion of epinephrine from the adrenal
medulla. The chronic phase comprises the
induction of the slower onset but longeracting
hypothalamic-pituatory-adrenal
(HPA) axis. Here, corticotropin-releasing
factor (CRF) is released from the
hypothalamus, which travels via the
hypothalamic-pituitary portal system to
stimulate
the
release
of
adrenocorticotropic hormone (ACTH)
from the anterior pituitary. The ACTH in
turn stimulates the adrenal cortex to
secrete glucocorticoids, predominantly
corticosterone (D. Denardo 2005). Kreger
and Mench (1993) succesfully employed
sampling of plasma corticosterone
following
handling
treatments
to
demonstrate that brief periods of handling
do not cause chronic stress in zoo-housed
royal pythons. It is recommended that the
same methodology be employed to
measure basal and feeding levels of
plasma corticosterone in Spider morph
royal
pythons
presenting
wobble
symptoms, compared to wild phenotype
control subjects.
As previously stated, it is beyond the
scope of this work to discuss the welfare
implications of the wider issue of
maintaining
reptiles
in
captivity,
particularly as companion animals, and
comprehensive reviews are already present
in the literature (see Warwick 1987;
Warwick 1990; Arena and Warwick 2004;
Laidlaw 2005; Clark 2012; ENDCAP
2012; EUARK 2012; McLennan 2012;
Toland, Warwick and Arena 2012).
However it is relevant to highlight an
inter-relationship of the subject matter
with ethical concerns surrounding wild
capture and international transport of
reptiles to supply the exotic pet trade; both
issues
bearing widely-acknowledged
welfare compromises (HSUS 2001, Auliya
2003). It is frequently suggested by
herpetoculturists that captive breeding has
acted to reduce pressure on wild stocks,
thus avoiding the welfare compromises
inherent in capture and transport (Laidlaw
2005). Prior to the advent of widespread
captive breeding, the royal python was
imported from its native sub-Saharan
African countries, notably Benin and Togo
(for example, 48,740 and 28,844
individuals from each country respectively
to the United States in 1997; HSUS 2001).
Such a relationship between captive
breeding and importation is certainly
intuitive, and supported by importation
figures (see Figure 5). However, these
figures refer to total numbers of reptiles
(including but not limited to those subject
to captive artificial breeding selection) and
do not account for variables such as the
economic climate. The author would
postulate that significant numbers of wild
caught royal pythons (and other species)
continue to be imported, specifically
driven by the search for novel,
undiscovered base morphs. In addition,
where importation of wild caught species
to western countries has significantly
decreased, this will also need to account
for the increase in live exports from these
countries if a net reduction in international
trade is to be concluded. Between 2005
and 2011, 60,000 royal pythons were
exported from the United States, the
majority of which were high-priced
morphs (Collis and Fenili 2011). Further
study is therefore warranted into the
precise effects of captive breeding for
genetic morphs on the international trade
in reptiles, and corresponding implications
for animal welfare.
11
No. of Reptiles Imported
1600000
1400000
1200000
1000000
800000
600000
400000
200000
0
2005
2006
2007
2008
Year
2009
2010
Figure 5: Reptile imports into the United States (adapted from Collis and
Fenili 2011). Note that 2005 data is from January and 2010 data is to May
only, thus artificially exaggerating the declining trend.
Limitations
The results presented here are based on
low sample sizes. Uptake of the breeder
survey was poor at 13%. Breeder contact
details were obtained from company
websites. However, no checks were made
to ensure that breeders remained active.
This may in part account for the poor
survey uptake by this stakeholder group.
However, the emails received from
breeders requesting further information,
who were then disinclined to partake, may
indicate a degree of unwillingness. Survey
completion was poor among the animal
welfare science and veterinary group,
where numerous entries were discounted
due to incompletion or inconsistency.
Although 24% of respondents to the
AWSELVA questionnaire had prior
awareness of the wobble condition, this is
unlikely to be representative of the
veterinary
and
welfare
science
community. Instead, prior awareness of
the subject matter likely engaged the
interest of respondents, encouraging
survey completion and potentially
introducing bias.
Acknowledgements
The author wishes to extend his sincere
gratitude to the Universities Federation for
Animal Welfare (UFAW) for their
generous support, to Dr Fritha Langford of
the University of Edinburgh for her
guidance, and to James Yeates and
Vanessa Ashall of the Animal Welfare
Science, Ethics and Law Veterinary
Association for their kind assistance.
References
APGAW 2009 A healthier future for
pedigree dogs. London: Associate
Parlimentary Group for Animal
Welfare
APGAW 2012 A Healthier Future for
Pedigree Dogs. London: Associate
Parlimentary Group for Animal
Welfare
Arena PC and Warwick C 1995
Miscellaneous factors affecting health
and welfare. In C. Warwick, F. L.
Frye, & J. Murphy, Health and
Welfare of Captive Reptiles pp. 263283. London: Chapman and Hall
Auliya M 2003 Hot trade in cool
creatures: A review of the live reptile
trade in the European Union in the
1990s with a focus on Germany.
Belgium: TRAFFIC Europe
Bennett RA and Mehler SJ 2005
Neurology. In: Mader DR (ed) Reptile
12
Medicine and Surgery pp 239-250. St
Louis, Missouri: Saunders Elsevier
Medicine and Surgery pp. 119-123. St
Louis, Missouri: Saunders Elsevier
Burghardt GM 2013 Environmental
enrichment and cognitive complexity
in reptiles and amphibians: Concepts,
review, and implications for captive
populations.
Applied
Animal
Behaviour Science 147: 286-298
ENDCAP 2012 Wild Pets in the
European Union. Horsham: ENDCAP
CAWC 2006 Breeding and Welfare in
Companion
Animals.
Sidmouth:
Companion Animal Welfare Council
Funk RS 2005 Snakes. In: Mader DR
(ed) Reptile Medicine and Surgery pp.
42-58. St Louis, Missouri: Saunders
Elsevier
CAWC 2003 Report on the Welfare of
Non-Domesticated Animals Kept for
Companionship.
Sidmouth:
Companion Animal Welfare Council
Chang LW and Jacobson ER 2010
Inclusion Body Disease, A Worldwide
Infectious Disease of Boid Snakes: A
Review. Journal of Exotic Pet
Medicine 9: 216-225
Chapple DG 2003 Ecology, lifehistory and behaviour in the Australian
scincid genus Egernia, with comments
on the evolution of complex sociality
in lizards. Herpetological Monographs
17: 145-180
Clark B 2012 A Report Looking at the
Reptile Keeping Hobby, Those Who
Want it Banned and Why? BSc Thesis
(Unpublished)
Collis AH and Fenili RN 2011 The
Modern
US
Reptile
Industry.
Georgetown: Georgetown Economic
Services
CPR 2013 Pricelist: GHI Mojave.
Retrieved October 2013, from Crystal
Palace
Reptiles:
http://www.crystalpalacereptiles.com/i
ndex.php/pricelists/snakes/ballpythons/product/68-ghi-mojave
Denardo DF and Licht P 1993
Effects of corticosterone on social
behavior of male lizards. Hormones
and Behavior 27: 184-199
Denardo D 2005 Stress in Captive
Reptiles. In: Mader DR (ed) Reptile
EUARK
2012
Reptiles
and
Amphibians as Companion Animals:
The Facts. Brussels: European Union
Association of Reptile Keepers
Harcourt-Brown F 2002 Textbook of
Rabbit Medicine. Oxford: Reed
Education and Professional Publishing
HSUS 2001 The Trade in Live
Reptiles: Imports to the United States.
Washington DC: The Humane Society
of the United States
Jepson L 2013 Ball Pythons:
Understanding and caring for your pet.
Llandow: Magnet and Steel
Jones T 2012 Move Over Rover.
Retrieved October 2013, from
Federation of British Herpetologists:
http://www.fbh.org.uk/facts/move_ove
r_rover.html
Kirkwood J 2012 Tackling genetic
problems in pets. The Biologist 59: 11
Kreger MD and Mench JA 1993
Physiological and behavioral effects of
handling and restraint in the ball
python (Python regius) and the bluetongued skink (Tiliqua scincoides).
Applied Animal Behaviour Science 38:
3233-336
Laidlaw R 2005 Scales and Tails: The
Welfare and Trade of Reptiles Kept as
Pets in Canada. Toronto: Zoocheck
Canada
Lawton M 1992 Neurological disease.
In P. H. Benyon, Manual of reptiles.
Gloucestershire: British Small Animal
Veterinary Association
13
Leal M and Powell BJ 2012
Behavioural flexibility and problemsolving in a tropical lizard. Biology
Letters 8: 28-30
Mader DR and Mader-Weidner BS
2005 Understanding the HumanReptile Relationship. In: Mader DR
Reptile Medicine and Surgery pp. 1424. St Louis, Missouri: Saunders
Elsevier
Malik R, Allan GS, Howlett CR,
Thompson DE, James G and
McWhirter
C
1999
Osteochondrodysplasia in Scottish
Fold cats. Autralian Veterinary Journal
77: 85-92
McLennan S 2012 Keeping of exotic
animals: welfare concerns. Federation
of Veterinarians of Europe
Meola SD 2013 Brachycephalic
Airway
Syndrome.
Topics
in
Companion Animal Medicine 28: 9196
Nuffield Council on Bioethics 2005
The ethics of research involving
animals. London: Nuffield Council on
Bioethics
Oechtering GU, Schlüter C and
Lippert JP 2010 Brachycephaly in dog
and cat: a human induced obstruction
of the upper airways. Pneumologie 64:
450-2
http://www.dogadvisorycouncil.com/p
age2/index.php
RSPCA 2013 Pedigree dog breeding
progress report. Retrieved September
2013, from Royal Society for the
Prevention of Cruelty to Animals:
http://www.rspca.org.uk/ImageLocator
/LocateAsset?asset=document&assetId
=1232733600296&mode=stg
Schumacher J, Jacobson ER, Homer
BL and Gaskin JM 1994 Inclusion
body disease in boid snakes. Journal of
Zoo and Wildlife Medicine 25: 511524
Tokarz
R
1987
Effects
of
corticosterone treatment on male
aggressive behavior in a lizard (Anolis
sagrei). Hormones and Behavior 21:
358-370
Toland E, Warwick C and Arena P
2012. Pet Hate. The Biologist 59: 1418
UFAW
2012
Genetic
welfare
problems of companion animals.
(Universities Federation for Animal
Welfare) Retrieved October 2013,
from
http://www.ufaw.org.uk/geneticwelfar
eproblems.php
Warwick C 1987 Effects of captivity
on the ethology and psychology of
reptiles. Herpetoculturist 10-12
OWAL Reptiles n.d. Genetics
Calculator. Retrieved October 2013,
from
http://www.owalreptiles.com/genetics.
php
Warwick C 1990 Reptilian Ethology
in Captivity: Observations of Some
Problems and an Evaluation of their
Aetiology. Applied Animal Behaviour
Science 1-13
PDSA 2011 Animal Welbeing Report.
Telford: People's Dispensary for Sick
Animals
Wolf P, Bertels T, Sallman HP,
Heisler K and Kamphues J 2000
Vitamin a Metabolism in Recessive
White Canaries. Animal Welfare 9:
153-165
Peck H 2010 Background to the
Council. Retrieved September 2013,
from
14