Unusual mortality incidents in tit species (family Paridae) associated with the novel bacterium Suttonella ornithocola

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The Veterinary Record, February 11, 2006
Unusual mortality
incidents in tit species
(family Paridae)
associated with the
novel bacterium
Suttonella ornithocola
J. K. Kirkwood, S. K. Macgregor,
H. Malnick, G. Foster
BETWEEN March and June 1996, 11 unusual mortality inci-
dents apparently involving only species of tits (family Paridae)
in gardens in England and Wales were reported to one of the
authors (J. K. K.) by members of the public. In eight of these
incidents blue tits (Parus caeruleus) only were seen to be
involved, and one case (case 5) involved only long-tailed tits
(Aegithalos caudatus). The other two incidents also involved
blue tits; in one case (case 3) a coal tit (Parus ater) and a long-
tailed tit were also found dead, and in another case (case 6),
a great tit (Parus major) was also reported to be showing signs
of illness (Table 1). Apart from a report in one of these cases
(case 8) that two bullfinches (Pyrrhula pyrrhula) appeared
unwell, no deaths or signs of disease were reported in other
species.
In 1993, J. K. K. had started, on a hobby basis, to investi-
gate unusual mortality incidents in garden birds. Members of
the public who contacted the Royal Society for the Protection
of Birds or the British Trust for Ornithology about deaths in
garden birds were referred so that details of the incidents
could be collected by telephone. People were encouraged to
send carcases, if available, for postmortem examinations,
which were undertaken, when time permitted, in the evenings
and at weekends.
By 1996, this pastime had grown to the extent that dur-
ing that year, 105 reports were received. The cluster of 11 inci-
dents reported in this short communication thus represented
approximately 10 per cent of the total for 1996.
It is important to emphasise that this report gives no
indication of the frequency of disease outbreaks in garden
birds. It is likely that only a very small proportion of inci-
dents were observed and that a still smaller proportion were
reported, as this incident investigation scheme had not been
advertised and was not well known. Information was col-
lected on the species and numbers affected, signs observed,
location, habitat type, when the incident had occurred and
Veterinary Record (2006)
158, 203-205
J. K. Kirkwood, BVSc
,
PhD, FIBiol, MRCVS,
S. K. Macgregor, HTEC,
MSc, CSci, FIBMS,
Institute of Zoology,
Regent’s Park, London
NW1 4RY
H. Malnick, PhD, CSci,
FIBMS,
Laboratory of Healthcare
Associated Infections,
Health Protection Agency,
Centre for Infections,
61 Colindale Avenue,
London NW9 5HT
G. Foster, CSci, FIBMS,
SAC Veterinary Services,
Drummondhill,
Strathkerrick Road,
Inverness IV2 4JZ
Dr Kirkwood’s present
address is Universities
Federation for Animal
Welfare, The Old School,
Brewhouse Hill,
Wheathampstead,
Hertfordshire AL4 8AN
whether the birds were fed and, if so, what foods were pro-
vided.
In the 11 incidents described here the clinical signs
reported consistently included fluffed-up plumage and
lethargy, described variously as an apparent lack of awareness,
a lack of concern about approaching human beings, in some
cases sitting on the ground and in other cases appearing semi-
conscious and disorientated. In two of the incidents, birds had
been seen to be caught easily by cats. In one case, the affected
birds were reported to be gaping, as if trying to swallow, and
to have white material ‘like fungus at the corners of the beaks’.
In another incident, sick birds were observed to stay by a pond
from which they were drinking, and appeared to be very
thirsty.
A total of 21 carcases from nine of these incidents were
submitted for postmortem examination: 19 blue tits (13 male,
one female and five not examined), one female coal tit and
one male long-tailed tit. The birds’body condition varied and,
while a few had some observable fat reserves, they tended to
be thin. The blue tit carcases weighed 5 to 9 g (normal weight
for males 11 g) and the long-tailed tit weighed 3 g (normal
weight for males 5 to 6 g) (Perrins 1979). The coal tit was not
weighed but was judged to be thin. The authors note that it
is curious that there was such a skewed sex ratio – 14 of the
16 birds examined were male – but there is no evidence to
suggest that this was relevant. Few remarkable postmortem
findings were observed. Congestion of the lungs was noted in
the carcases from cases 2, 4, 5 and 9. One blue tit (case 9) had
localised whitish thickening of the skin at the back of its neck.
The small size of these birds presents challenges to gross post-
mortem examination, and many of the carcases were decom-
posed to some extent when they were received. No histological
examinations were undertaken.
Samples of intestine and lung from blue tits from cases 2
and 4 and of lung from the long-tailed tit from case 5 were
sent to the avian virology department of the Veterinary
Laboratories Agency (
VLA) – Weybridge for virus isolation.
No viruses were isolated.
Samples of lung, liver and intestine were taken for bacte-
riological screening from eight carcases from seven incidents:
blue tits at cases 1, 2, 4, 6 (two carcases) and 9; from the coal
tit at case 3; and from the long-tailed tit at case 5 (see Table 1
for details of these cases). A variety of non-pathogenic com-
mensal bacteria and common postmortem invaders was iso-
lated, but only one organism of suspected pathogenic
significance was found (Table 2). Attention was drawn to this
organism because of its unusual characteristics, its presence
in samples from several birds in significant numbers, and
because its beta-haemolytic and capnophilic properties were
suggestive of possible pathogenecity. The bacterium was a
Gram-negative rod to coccobacillus, which grew well in car-
bon dioxide but poorly in aerobic and anaerobic conditions
Case Date of incident Species involved Number dead (number ill) Location
1 22 to 27/3/96 Blue tit (Parus caeruleus) 7 Staffordshire
2 10/3/96 Blue tit 1 Cheshire
3 1 to 9/4/96 Blue tit, coal tit (Parus ater) and
long-tailed tit (Aegithalos caudatus) 4 (1) Buckinghamshire
4 10 to 12/4/96 Blue tit 1 (5) Buckinghamshire
5 9 to 11/4/96 Long-tailed tit 1 (1) Hertfordshire
6 8 to 15/4/96 Blue tit and great tit (Parus major) 3 (20) Kent
7 14 to 17/4/96 Blue tit 10 (10) Rutland
8 15 to 19/4/96 Blue tit 1 (>2)* Hertfordshire
9 3 to 5/5/96 Blue tit 1 (n)
†
Herefordshire
10 22/4/96 Blue tit 2 (2) Norfolk
11 24/4 to 14/5/96 Blue tit 3 (?) Gwynedd
* In addition to blue tits, two bullfinches (Pyrrhula pyrrhula) were also reported to show signs of illness
†
Reported as ‘quite a number’
TABLE 1: Unusual mortality incidents in Paridae in gardens in England and Wales, March to May 1996
Short Communications
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The Veterinary Record, February 11, 2006
Short Communications
on Columbia sheep blood agar (CSBA) plates. Colonies cul-
tured in an atmosphere containing carbon dioxide (3·5 to 9
per cent) at 37°C for 48 hours on
CSBA were found to be flat,
butyrous, entire, opaque and beta-haemolytic, oxidase and
catalase positive, and were phylogenetically atypical when
coupled with routine biochemical testing (
API 20NE;
bioMérieux) using standard methodology (Barrow and
Feltham 1993). This organism was subsequently defined, by
RNA gene sequencing studies, to be a novel species within the
genus Suttonella of the family Cardiobacteriaceae, which has
been named Suttonella ornithocola (Foster and others 2005).
Although the lung was the only site from which S ornithocola
was recovered in these birds, it is not known whether the
organism may have infected the other tissues cultured, as they
were not inoculated in a carbon dioxide-enriched atmos-
phere.
While some caution is appropriate, it seems very likely that
S ornithocola may have been a factor in these incidents. The
organism was isolated from three species of tit from four
unusual mortality incidents and, although postmortem inves-
tigations were not exhaustive, no other causes of death were
found in these cases. No studies of the pathogenicity of
S ornithocola have been undertaken, but other Cardio-
bacteriaceae are associated with several diseases of human
beings and other animals; Suttonella indologenes, hitherto the
only known species in the genus, has been isolated from
human eye infections and from endocarditis (Foster and oth-
ers 2005).
Relatively little is known about infectious diseases of
garden birds (Kirkwood and Macgregor 1997, Friend and
Franson 1999). However, it has become apparent that salmo-
nellosis and colibacillosis are among the more common
causes of mortality incidents in provisioned garden birds in
the
UK and other countries (Kirkwood and Macgregor 1997,
1998, Foster and others 1998, Pennycott and others 1998,
2002, Daoust and others 2000, Tauni and Osterlund 2000,
Refsum and others 2003). These infections appear predomi-
nantly to affect finches, notably greenfinches (Carduelis chlo-
ris), siskins (Carduelis spinus) and house sparrows (Passer
domesticus), but smaller numbers of death among tits and
other species are often reported in association with outbreaks
of these diseases in finches and sparrows.
One of the unusual features of the cluster of 11 incidents
described here is that they appeared to involve tits almost
exclusively. All the deaths observed were in Paridae, and in
only one incident were other species seen to show signs of
disease (two bullfinches in case 8). For this reason, and
because of their close temporal clustering, it seems possible
that all 11 incidents may have had a common aetiology and,
since no other cause was identified, that S ornithocola may
have played a role in all of them. Although the organism was
isolated from only half the birds from which samples were
taken, it is quite possible that it was present in the others but
not detected because of its fastidious nature, the state of
decomposition of the carcases and the overgrowth of com-
mensal organisms.
The 11 incidents began within a period of little over four
weeks and had a wide geographical distribution, occurring in
10 counties in England and Wales (Table 1). This pattern sug-
gests the relatively sudden and widespread emergence of a
causal factor. The number of birds observed to be involved
in these 11 incidents exceeded 75 (Table 1). In view of the
points made above about the likelihood of cases being
observed and reported, this suggests that there was consid-
erable adult mortality in Paridae nationally at that time. At
the time of year when these incidents occurred, the spring and
early summer, there is, perhaps, the possibility of wide dis-
persal of infectious agents with summer migrants. Such a pat-
tern might also occur through exposure to a risk factor in
food (all the birds in these cases were provisioned).
The authors suggest that S ornithocola, which was dis-
covered through the investigation of these incidents, may
have been a factor in their aetiology. The evidence is cir-
cumstantial but may alert others who may be involved in
investigating further unusual incidents of mortality involv-
ing Paridae.
ACKNOWLEDGEMENTS
The authors are grateful to Mr Dick Gough of the
VLA –
Weybridge, for the virological examinations.
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Species Date of postmortem
Case sampled examination Organisms cultured
1 Blue tit (Parus caeruleus) 29/3/96 Pure isolate of alpha-haemolytic Corynebacterium species
2 Blue tit 12/4/96 Mixed, predominance Suttonella species
3 Coal tit (Parus ater) 16/4/96 Mixed, predominance Suttonella species with non-haemolytic
Staphylococcus species
4 Blue tit 15/4/96 Mixed, predominance alpha-haemolytic Streptococcus species
5 Long-tailed tit (Aegithalos caudatus) 12/4/96 Nearly pure isolate of Suttonella species
6 Blue tit 17/4/96 Pure isolate of non-haemolytic Escherichia coli
9 Blue tit 3/5/96 Mixed, predominance non-haemolytic E coli
TABLE 2: Results of bacteriological culture of lung samples from tit carcases from mortality incidents in spring 1996
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The Veterinary Record, February 11, 2006
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doi: 10.1136/vr.158.6.203
2006 158: 203-205Veterinary Record
J. K. Kirkwood, S. K. Macgregor, H. Malnick, et al.
Suttonella ornithocolabacterium
(family Paridae) associated with the novel
Unusual mortality incidents in tit species
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