Neurologic dysfunction in a ball python (python regius) color morph, and Implications for welfare

Abstract

There is widespread and growing public and professional awareness of genetic disorders associated with artificial breeding, and its implications on the health and welfare of companion animals. Despite increased captive breeding and popularity of atypical color/pattern variants, little research has been conducted, to date, into genetic variants of reptiles, relative to common domestic (e.g., dogs, cats). This work aims to raise awareness among the animal welfare science community of the potential for welfare problems in inbred reptiles, and to stimulate further research in this field. A survey of expert opinion was used to establish a description of a heritable disorder, the “wobble syndrome”, associated with a widely propagated phenotype, the “spider” morph of the ball python (Python regius), a common “pet” snake species. This information was used to provide an assessment of animal welfare impacts of the “wobble syndrome” condition.

Full text

TOPICS IN MEDICINE AND SURGERY
NEUROLOGICAL DYSFUNCTION IN A BALL PYTHON
(PYTHON REGIUS) COLOUR MORPH AND
IMPLICATIONS FOR WELFARE
Mark P. Rose, BSc, MSc, CBiol, MSB, and David L. Williams, MA, VetMD, PhD, CertVOphthal,
CertWEL, FHEA, FSB, FRCVS
Abstract
There is widespread and growing public and professional awareness of genetic disorders associated with
artificial breeding selection, and their implications on the health and welfare of companion animals.
Despite increased captive breeding and the popularity of atypical colour/pattern variants, little research
has been conducted, to date, into genetic variants of reptiles relative to common domestic animals (e.g.,
dogs and cats). This article aims to raise awareness in the animal welfare science community of the
potential for welfare problems in genetic variant reptiles and to stimulate further research in this field. A
survey of expert opinion was used to establish a description of a heritable disorder, the “wobble
syndrome,”associated with a widely propagated phenotype, the “spider”morph of the ball python
(Python regius), a common “pet”snake species. This information was used to provide an assessment of
animal welfare effects of the wobble syndrome condition. Copyright 2014 Elsevier Inc. All rights reserved.
Key words: animal welfare; artificial selection; ball python; captive reptiles; genetic mutation; heritable
disorders
Genetic disorders in captive-bred animals are acknowledged as a leading welfare concern
among animal welfare and veterinary professionals.
1,2
Growing public awareness,
facilitated by mainstream media,
3,4
has promoted advances in animal genetic disease
identification, reduction and remediation.
5,6
The need for continued and enhanced
public education has been emphasised to promote informed choices when purchasing
companion animals.
4
To date, there has been a focus towards disorders
in pedigree dogs and cats with little consideration
of the health and welfare consequences of
selectively breeding captive wild animals,
including reptiles. However, in the United
Kingdom (UK) there are now comparable, if not
collectively greater, numbers of captive reptiles
than dogs (Clark B: A report looking at the reptile
keeping hobby, those who want it banned and
why? University of Kent, BSc Thesis,
unpublished).
7
There are 8 million reptiles kept as
pets across 1.1 million UK households,
8
with a
further 13.6 million across 4.7 million American
(US) households.
9
A significant driver of growth in
the captive-bred reptile industry is the
development of novel colour/pattern strains, or
“morphs,”through artificial breeding selection of
gene mutations. This is a lucrative business, where
naturally occuring “base morphs”are combined to
produce “designer morphs,”reaching values in
excess of US $20,000.
10
Despite the numbers of reptile species
maintained in captivity and the growth in
selection for novel phenotypes, a literature review
reveals scant reference to health and wefare in this
context. However, the web-based hobbyist media
Ó2014 Elsevier Inc. All rights reserved.
1557-5063/14/2101-$30.00
http://dx.doi.org/10.1053/j.jepm.2014.06.002
From enims, Burcot Farm, East Stratton, Hampshire, UK; and Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
Address correspondence to: Mark P. Rose, enims, Burcot Farm, East Stratton, Hampshire SO21 3DZ, UK. E-mail: mark.rose@enims.co.uk.
234 Journal of Exotic Pet Medicine 23 (2014), pp 234–239

includes numerous anecdotal reports of potential
welfare issues linked to genetic manipulation. In
their report on the welfare of nondomestic
companion animals, the Companion Animal
Welfare Council recommended that, “selection for
specifictraits…should be undertaken only with careful
regard to the possibility of overt or covert adverse
welfare consequences.”
1
The report further
recommends research into breeds where there is
reason to believe that welfare may have been
affected during selection for desired traits.
This article aims to (i) raise awareness of the
potential for genetic disease in reptiles among the
veterinary and welfare science communities, and
(ii) establish a description of a heritable disorder
in a captive-bred reptile species and consider its
effect on animal welfare.
MATERIALS AND METHODS __________________
This study focuses on a single genetic disorder
associated with a widely propagated phenotype of
the ball python (Python regius)(Fig. 1). This species
has gained widespread popularity among pet
owners, hobbyists and commercial breeders. The
spider morph (Fig. 2) is a dominant gene trait
characterised by a pattern alteration where the
distribution of dorsal melanophores is altered,
forming a web-like mesh.
10
The genetic dominance
of the trait means that the morph can be readily
outcrossed to introduce spider patterning into
designer morphs (Fig. 3). The spider morph is
linked to a neurological disorder, the “wobble
syndrome.”Examples of the condition may be
observed in open-access, online videos, for
example, http://www.youtube.com/watch?
v=ZP9NWBHqdvU,http://www.youtube.com/
watch?v=zA4lBpoPIWY and http://www.youtube.
com/watch?v=NVQmiywlaJk.
An online survey of expert opinion targeting
hobbyist and commercial breeders was used to
establish a description of the clinical signs of the
“wobble syndrome”condition, and breeder
perceptions on prevalence, cause and possible welfare
effects. A second survey presented these findings to
animal welfare scientists and veterinary professionals,
targeting members of the Animal Welfare Science,
Ethics and Law Veterinary Association. Each survey
employed an e-questionnaire. The group of animal
welfare specialists was asked to give their perception
of the welfare effect, if any, of the wobble condition
on affected snakes. Quantitative methods of statistical
analysis were not employedowingtothelowsample
sizes achieved; rather qualitative analysis was
employed.
FIGURE 1. Typical wild-type colour/pattern of the ball
python.
FIGURE 2. Ball python with the spider colour/pattern
mutation or “morph.”
FIGURE 3. A“designer morph”ball python expressing
the spider morph in combination with the
pastel morph.
Rose and Williams/Journal of Exotic Pet Medicine 23 (2014), pp 234–239 235

RESULTS ______________________________________
Breeder Group
A total of 100 breeders were contacted, with
13 responses received. All respondents were
aware of the spider wobble condition. Of them,
8 respondents commented on the clinical signs
associated with the syndrome, describing side-to-
side head tremors (5), incoordination (4), erratic
corkscrewing of the head and neck (4), inhibited
righting reflex (3), torticollis (2), poor muscle tone
(1), and loose grip with the tail (1).
The clinical signs are more pronounced or
appear only during states of arousal (e.g., feeding),
with a widely acknowledged scale in the severity of
clinical signs between affected individual animals.
Breeders disagreed on the proportion of spider
morphs that present with the condition, to some
degree, at some point during their lives (Fig. 4).
However, there was a general consensus that a low
proportion of these snakes were severely affected
(Fig. 5).
Breeders generally reported a minimal effect
on quality of life in most snake cases in which
clinical signs of wobble syndrome were
detected, with typical statements including
“Most I see lead a comparable life to a normal ball
python except the obvious differences in grace of
motion”and “Even severely affected adults eat great,
breed and will lay good eggs.”Feeding response is
frequently stated as good (6 responses; 46%),
although owing to poor motor skills, strike
accuracy is often poor (4 responses; 30%).
Euthanasia of 2 individuals was reported, with
poor feeding cited as the primary reason for the
decisions, though it is unclear whether “poor
feeding”was related to physical ability or
willingness to feed unassisted. Fecundity was
also reported unaffected, excepting 1 report of
severely affected individuals experiencing
difficulty with the physical act of copulation.
There is no evidence to suggest an effect of the
wobble condition on longevity. One respondent
reported that a spider-spider morph mating
results in a higher incidence of egg failures,
suggesting that the gene mutation may be lethal
when homozygous.
The wobble condition appears to be linked to
the gene mutation causing the spider pattern, but
breeders disagreed on the potential for
disassociation of the condition from the morph
(Fig. 6). Spider offspring that lack the pattern
mutation do not express wobble symptoms.
Further, unaffected hatchlings may be born to
severely affected females and affected offspring
born to adults that have never displayed
observable clinical signs.
Welfare Scientist Group
Respondents (n¼28) typically perceived a
moderate to high welfare effect associated with the
clinical signs of the wobble condition (Table),
based on the feelings of frustration and stress that,
intuitively in their opinion, might be
associated with impaired ability to perform
species-appropriate behaviours (e.g., feeding).
The question of ethical defensibility of
continued propagation of the spider morph, in
light of the available evidence, evoked a mixed
response (Fig. 7). Further research was called for, to
address (i) the effect, if any, of the mutation on
longevity relative to that of the wild phenotype; (ii)
the underlying pathology, including any latent
physiological manifestations that may accompany
the neurological symptoms of the condition; and,
(iii) an extensive dataset of standardised clinical
assessments, gathered by a nonbiased exotic
FIGURE 4. Breeder-reported prevalence of the wobble condi-
tion in spider morph ball pythons (n¼13).
FIGURE 5. Breeder-reported proportion of spider morph ball
pythons severely affected by the wobble condition (n¼12).
236 Rose and Williams/Journal of Exotic Pet Medicine 23 (2014), pp 234–239

veterinary team, “focusing on sensory and motor
performance, divergences from normal behaviour
patterns, and general physical and physiological status.”
Others stated that sufficient information was
available to conclude a significant welfare
compromise 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.”).
DISCUSSION _________________________________
Clinical signs of the wobble condition are
indicative of a central nervous system disorder.
11
Although prevalence of the condition among
spider morphs remains unclear, with many experts
stating that all are affected, there is consensus that
a minority are severely affected in their ability to
perform species-appropriate behaviours, relative to
wild-type, captive pythons. No data are available
on longevity of these morphs, given the relatively
recent discovery of the spider morph in ball
pythons, a species recorded to reach 47.5 years.
12
Although breeders generally agreed that quality
of life was not significantly affected, 89% (25/28)
of welfare scientists concluded a moderate to high
welfare effect based on the information available.
This disparity may reflect biases inherent in the
respective groups.
One animal welfare respondent stated, “‘Mild
torticollis’would still be quite uncomfortable, according
to the ‘how would that make me feel?’principle.”Such
anthropomorphism is clearly subject to
limitations; however, 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, where sentience
increases with physiological complexity.
13
Our
historical failure to identify signs of potential
welfare compromises in reptiles is probably best
explained by their alien morphology and
behaviour.
14
If superficially mechanistic, reptiles in
fact have complex neural architecture
11
and are
collectively capable of sophisticated
communication, problem solving, parental care
and play behaviours.
15-17
Fecundity was widely
reported as unaffected by the wobble condition,
excepting 1 report of animals experiencing
difficulty with the physical act of copulation, and
FIGURE 6. Breeder conclusions on the potential for
disassociation of the wobble condition from the spider
morph, with a widely implemented programme of
selective breeding (n¼13).
TABLE. Reported perception of welfare effect (intensity and duration) of the wobble condition among the
Welfarist Group (n ¼28)
Perceived Welfare Impact: Intensity
Negligible Minimal Moderate High
Perceived Welfare Impact: Duration
Negligible 0 0 0 0
Short 0 1 1 0
Moderate 0 1 2 2
Prolonged 0 1 11 10
FIGURE 7. Welfarist conclusions on whether it is
ethically defensible to continue to propagate the ball
python spider morph (n¼43).
Rose and Williams/Journal of Exotic Pet Medicine 23 (2014), pp 234–239 237

herpetoculturists implicitly considered this
demonstrated the absence of effect on quality of
life. This may not be the case, as even in stressful
situations, sexual activity is likely to be maintained
in reptiles where the negative influences of
corticosteroids on sexual endocrine function
seen in many mammals do not seem to be
replicated.
18
Aspects of reptile welfare may have benefited from
the growth of captive breeding. In the past, it has
been more financially viable to replace a diseased
reptile than to seek veterinary intervention.
19
This is
no longer the case owing to greater veterinary
expertise and growing commercial value of reptiles.
However, any such favourable factors do not detract
from our ethical responsibilty to address potential
sources of poor welfare where they are identified. A
true assessment of effect on quality of life should be
based on complete information on the effects of the
condition. Other neuropathies presenting
comparable behavioural symptoms to the wobble
syndrome are often found to be accompanied by
physiological clinical signs during cytology, biopsy
and necropsy investigation.
12,20
Comprehensive
pathological analysis of ball python spider morph
specimens may therefore identify latent physiological
manifestations of the wobble condition, which may
themselves open further avenues of investigation.
Where welfare science respondents perceived a
moderate-high welfare impact intensity associated
with the wobble condition, the rationale was often
stated as likely frustration associated with impaired
ability to perform species-appropriate behaviours,
with strike accuracy in affected pythons reportedly
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 response in affected snakes
could be assessed through the measurement of
plasma corticosterone level. The corticosterone levels
may be employed to identify chronic stress
21
by
measuring basal and feeding stress levels in spider
morph ball pythons presenting with signs of the
wobble syndrome relative to wild phenotype control
subjects.
CONCLUSIONS _______________________________
Although further research is necessary for
improved understanding, there is clear potential
for significant welfare compromises to result from
artificial breeding selection of reptiles. The 2003
Companion Animal Welfare Council report
highlights the ethical importance of prevention of
captivity-related diseases but emphasises the need
for a measured response.
1
Disproportionate
legislative control may not promote optimum
welfare and can have unforeseen consequences.
8
The strength of the herpetocultural industry is in its
community of enthusiasts, closely connected by
web-based media. It is self-evident from a review of
such media that most herpetoculturists care greatly
for the health and welfare of their companion
animals and/or breeding stock. This aspect of the
herpetoculturist community should be supported
and used to fuel further research into the welfare
consequences of heritable disorders in reptile
species, effectively disseminate findings, and
improve self-regulation by community leaders.
ACKNOWLEDGEMENTS
We thank the Universities Federation for Animal
Welfare (UFAW) who funded this work, and
Dr Fritha Langford (University of Edinburgh),
James Yeates and Vanessa Ashall (Animal Welfare
Science, Ethics and Law Veterinary Association) for
their support and assistance.
REFERENCES
1. CAWC. Report on the Welfare of Non-Domesticated
Animals Kept for Companionship. Sidmouth: Companion
Animal Welfare Council, 2003
2. PDSA. Animal Wellbeing Report. Telford: People’s Dis-
pensary for Sick Animals, 2011
3. APGAW. A Healthier Future for Pedigree Dogs. London:
Associate Parliamentary Group for Animal Welfare, 2009
4. APGAW. A Healthier Future for Pedigree Dogs: Update
Report. London: Associate Parliamentary Group for Ani-
mal Welfare, 2012
5. Peck H: Background to the Council. Advisory Council on
the Welfare Issues of Dog Breeding, 2010. (Accessed Sept
2013)
6. RSPCA. Pedigree Dog Breeding Progress Report. Horsham:
Royal Society for the Prevention of Cruelty to Animals,
2013. (Accessed Sept 2013)
7. Jones T: Move Over Rover. Federation of British Herpetol-
ogists, 2012 http://www.fbh.org.uk/facts/move_over_r
over.html. Accessed Oct 2013
8. EUARK: Reptiles and Amphibians as Companion Animals:
The Facts. Brussels, European Union Association of Reptile
Keepers, 2012
9. Collis AH, Fenili RN: The Modern US Reptile Industry.
Georgetown: Georgetown Economic Services, 2011
10. Jepson L: Ball Pythons—Understanding and Caring for
Your Pet. Llandow: Magnet and Steel, 2013
11. Bennett RA, Mehler SJ: Neurology, in Mader DR (ed):
Reptile Medicine and Surgery (ed 1). St. Louis, MO,
Saunders/Elsevier, pp 239-250, 2006
12. Funk RS: Snakes, in Mader DR (ed): Reptile Medicine and
Surgery (ed 1). St. Louis, MO, Saunders/Elsevier, pp
42-58, 2006
13. Nuffield Council on Bioethics. The Ethics of Research Involv-
ing Animals. London: Nuffield Council on Bioethics, 2005
238 Rose and Williams/Journal of Exotic Pet Medicine 23 (2014), pp 234–239

14. Arena PC, Warwick C: Miscellaneous factors affecting
health and welfare, in Warwick C, Frye FL, Murphy J
(eds): Health and Welfare of Captive Reptiles. London,
UK, Chapman and Hall, pp 263-283, 1995
15. Chapple DG: Ecology, life-history and behaviour in the
Australian scincid genus Egernia, with comments on the
evolution of complex sociality in lizards. Herpetol
Monogr 17:145-180, 2003
16. Leal M, Powell BJ: Behavioural flexibility and problem-
solving in a tropical lizard. Biol Lett 8:28-30, 2012
17. Burghardt GM: Environmental enrichment and cognitive
complexity in reptiles and amphibians: concepts, review,
and implications for captive populations. Appl Anim
Behav Sci 147:286-298, 2013
18. Moore IT, Jessop TS: Stress, reproduction, and adrenocort-
ical modulation in amphibians and reptiles. Horm Behav
43:39-47, 2003
19. Mader DR, Mader-Weidner BS: Understanding the
human-reptile relationship, in Mader DR (ed): Reptile
Medicine and Surgery (ed 2). St. Louis, MO, Saunders/
Elsevier, pp 14-24, 2006
20. Schumacher J, Jacobson ER, Homer BL, et al: Inclusion
body disease in boid snakes. J Zoo Wildl Med 25:
511-524, 1994
21. Kreger MD, Mench JA: Physiological and behav-
ioral effects of handling and restraint in the ball
python (Python regius) and the blue-tongued skink (Tiliqua
scincoides). Appl Anim Behav Sci 38:3233-3336, 1993
Rose and Williams/Journal of Exotic Pet Medicine 23 (2014), pp 234–239 239