Diseases of red deer introduced to Patagonia and implications for native ungulates

Abstract

The red deer (Cervus elaphus) invasion in Patagonia has been continuing for nearly a century, with occurrence in all habitats between 34�S and 55�S. Their distribution, movement patterns and locally high densities raise concerns over their potential epidemiological role in maintaining disease reservoirs or transmitting diseases such as foot-and-mouth disease or tuberculosis, with potential severe health and economical impacts at the interface of humans, livestock or native wildlife. Among adult females collected by rifle and radio-collared deer that died naturally, no ectoparasites were found (n = 73). Fasciola hepatica was encountered in three surveys at prevalences ranging from 9% to 50% (n = 108). Taenia ovis krabbei
was identified, and Cysticerus tenuicollis was found at a prevalence of 8% (n = 12). Ostertagia sp., Bunostomum sp. and Dictyocaulus sp. had a prevalence of 75%, 25% and 13% (n = 9), respectively. Several gastrointestinal parasites reported at low prevalence in endangered Patagonian huemul (Hippocamelus bisulcus) are common in livestock and considered commensals in domestic ruminants. Sympatry of huemul with livestock is commonplace, whereas with red deer it occurs in <2% of known populations, in which case there were 1.2 red deer, but 25.2 livestock per huemul, making livestock the
determining epidemiological factor regarding disease transmission or reservoir. As red deer have been coexisting with livestock for >100 years in Argentina, both red deer and livestock play epidemiological roles for shared diseases. Research, conservation and management efforts should be directed towards livestock herd health programs or restriction of free livestock movements, particularly if diseases are shown to have an impact on recruitment of endangered natives. Livestock are routinely researched and inspected at slaughter and thus provide a proxy for diseases afflicting co-existing ungulates. Testing for antibodies to foot-and-mouth disease viral antigen was negative (n = 41). A tentative diagnosis of mycobacterial infection was based on typical visceral lesions. Antler damage occurred on 73% of shed antlers, with 36% having major breaks of tines and main beams, possibly indicating mineral imbalances. One male had both antlers, including pedicles with portions of frontal, parietal and occipital bones, broken off the skull, causing his death. The prevalence of 0.9% of campylognathia (n = 776) indicates that the disease is unlikely to be inheritable, because the founding stock of 20 animals would have had a prevalence of at least 5%. Among deer, handedness of scoliosis related significantly to the hemisphere
where specimens originated (P < 0.001, n = 131). Coriolis forces are known to affect early stages of development, such as the innervation pattern of the mammalian vestibular system, or the plane of bilateral symmetry. It is, therefore, conceivable that the networks processing these environmental cues, or the mechanisms responsible for compensation, are malfunctioning and thus result in a preponderance of facial scoliosis in accordance to the earth’s rotation.

Full text

Diseases of red deer introduced to Patagonia
and implications for native ungulates
Werner T. Flueck
A,B,C,D,E
and Jo Anne M. Smith-Flueck
D
A
National Council of Scientific and Technological Research (CONICET), Rivadavia 1917,
1033 Buenos Aires, Argentina.
B
Swiss Tropical and Public Health Institute, University of Basel, Socinstrasse 57, 4051 Basel,
Switzerland.
C
Fundación Bariloche, C.C. 592, 8400 Bariloche, Argentina.
D
Institute of Natural Resources Analysis (IARN) –Patagonia, Universidad Atlántida Argentina,
C. C. 592, 8400 Bariloche, Argentina.
E
Corresponding author. Email: wtf@deerlab.org
Abstract. The red deer (Cervus elaphus) invasion in Patagonia has been continuing for nearly a century, with occurrence in
all habitats between 34S and 55S. Their distribution, movement patterns and locally high densities raise concerns over their
potential epidemiological role in maintaining disease reservoirs or transmitting diseases such as foot-and-mouth disease or
tuberculosis, with potential severe health and economical impacts at the interface of humans, livestock or native wildlife.
Among adult females collected by rifle and radio-collared deer that died naturally, no ectoparasites were found (n= 73).
Fasciola hepatica was encountered in three surveys at prevalences ranging from 9% to 50% (n= 108). Taenia ovis krabbei
was identified, and Cysticerus tenuicollis was found at a prevalence of 8% (n= 12). Ostertagia sp., Bunostomum sp. and
Dictyocaulus sp. had a prevalence of 75%, 25% and 13% (n= 9), respectively. Several gastrointestinal parasites reported at
low prevalence in endangered Patagonian huemul (Hippocamelus bisulcus) are common in livestock and considered
commensals in domestic ruminants. Sympatry of huemul with livestock is commonplace, whereas with red deer it occurs in
<2% of known populations, in which case there were 1.2 red deer, but 25.2 livestock per huemul, making livestock the
determining epidemiological factor regarding disease transmission or reservoir. As red deer have been coexisting with
livestock for >100 years in Argentina, both red deer and livestock play epidemiological roles for shared diseases. Research,
conservation and management efforts should be directed towards livestock herd health programs or restriction of free
livestock movements, particularly if diseases are shown to have an impact on recruitment of endangered natives. Livestock
are routinely researched and inspected at slaughter and thus provide a proxy for diseases afflicting co-existing ungulates.
Testing for antibodies to foot-and-mouth disease viral antigen was negative (n= 41). A tentative diagnosis of mycobacterial
infection was based on typical visceral lesions. Antler damage occurred on 73% of shed antlers, with 36% having major
breaks of tines and main beams, possibly indicating mineral imbalances. One male had both antlers, including pedicles with
portions of frontal, parietal and occipital bones, broken off the skull, causing his death. The prevalence of 0.9% of
campylognathia (n= 776) indicates that the disease is unlikely to be inheritable, because the founding stock of 20 animals
would have had a prevalence of at least 5%. Among deer, handedness of scoliosis related significantly to the hemisphere
where specimens originated (P<0.001, n= 131). Coriolis forces are known to affect early stages of development, such as the
innervation pattern of the mammalian vestibular system, or the plane of bilateral symmetry. It is, therefore, conceivable that
the networks processing these environmental cues, or the mechanisms responsible for compensation, are malfunctioning and
thus result in a preponderance of facial scoliosis in accordance to the earth’s rotation.
Received 12 December 2011, accepted 22 February 2012, published online 11 July 2012
Introduction
Argentina has a long tradition of animal introductions, beginning
with livestock that reached millions of feral cattle, horses and
goats shortly after Spanish settled in the 16th century (Torrejon
2001; Flueck and Smith-Flueck 2012a). Exotic wildlife were
introduced later and included red deer (Cervus elaphus), which
are considered to be one of the world’s 14 worst mammalian
invasive species (IUCN, www.issg.org, accessed April 2012).
The expansion of red deer in the southern cone of South America
began less than a century ago, and has yet to reach a state of
equilibrium (Flueck and Smith-Flueck 1993; Flueck et al.2003).
Feral red deer have established themselves in all mayor
habitats of Patagonia and are currently established in most
forested habitat types encountered between ~34S and 55S,
including semi-captive deer in southern Tierra del Fuego
(Flueck and Smith-Flueck 2012b). The area occupied in 2003
was estimated at >51 000 km
2
, consisting of 29% forest habitat,
57% Patagonian steppe habitat, and 14% of non-forested habitat
CSIRO PUBLISHING
Animal Production Science, 2012, 52, 766–773
http://dx.doi.org/10.1071/AN11342
Journal compilation CSIRO 2012 www.publish.csiro.au/journals/an

such as wet meadows and riparian habitat, brush or grasslands of
anthropogenic origin, and high-altitude vegetation above the tree
line (Flueck et al.2003). In Chile, they were estimated to occupy
~7700 km
2
(also see review in Flueck and Smith-Flueck 2012b).
The distribution of red deer had the following environmental
characteristics: it covers the latitudes between 37420S and
54550S (non-contiguous), longitudes between 73360W and
69500W (non-contiguous) and altitudes from sea level to
>2450 m (Flueck et al.2003). Within the present distribution,
feral red deer may number >100 000 animals at an average
density of ~2 deer/km
2
. This appears to be a conservative
estimate, considering that favourable ecotonal habitats have
revealed densities of ~100 deer/km
2
, whereas in steppe areas
they reached 40–50 deer/km
2
(Flueck et al.1995; J. Amaya, pers.
comm.). After liberation, red deer initially formed resident
populations, but decades later also have established migratory
segments, with individuals traveling 25 km, and with cases of
dispersal reaching as far as 40 km (Flueck 2005). In the study area
reported here, red deer are commonly sympatric with cattle,
horses, sheep, goats and wild species such as fallow deer
(Dama dama), European boar (Sus scrofa), guanaco (Lama
guanicoe), and in one area also with a remnant population of
endangered Patagonian huemul deer (Hippocamelus bisulcus).
The distribution, movement behaviour and uncontrolled
national and transnational shipments of red deer (Flueck and
Smith-Flueck 2006; Flueck 2010a) raise concerns over their
potential epidemiological role for various diseases such as
foot-and-mouth disease (FMD), brucellosis and tuberculosis
(Flueck and Smith-Flueck 1993,2006; Flueck et al.2003;
Flueck 2005). Here, we report for the first time on various
diseases encountered in red deer in Patagonia and evaluate
their potential to have an impact on native ungulates.
Materials and methods
The study area is centred in the ecotone between Andean forests
and Patagonian grasslands (40580S, 71120W), Argentina. The
topography is primarily mountainous, with most features
formed by glacial and volcanic processes. The study sites are
between 900-m and 1800-m elevation and represent grasslands,
or ecotones between forests and grasslands (details in Flueck
and Smith-Flueck 2011a). We evaluated females older than
1 year, shot and collected randomly between 1991 and 2009,
and radio-collared deer that died naturally between 2001 and
2009. All individuals were necropsied in the field (Mitchell et al.
1976; Wobeser and Spraker 1980). The focus of deer collections
varied, relating either to issues of reproduction, development,
seasonal body condition, population dynamics, genetics or
gross pathology. The examination for the presence of distinct
disease entities was thus not equally intense in every collection,
and prevalence is indicated only where an adequate number
of individuals had been examined for that purpose (Jones et al.
1997; Samuel et al.2001; Williams and Barker 2001). The
presence of FMD was evaluated by the federal agency
SENASA, via detection of antibodies to viral infection-
associated antigen. Additionally, in 1994–1995 we collected
entire female deer, which were examined exhaustively in the
pathology laboratory of the National Institute for Agricultural
Technology, INTA. All visceral parasite species reported here
were detected during necropsy. Regarding mycobacterial
infection, Ziehl-Neelsen staining was used to detect acid-fast
organisms. Deer were collected in the following four study sites:
Site A (41000S, 71170W), Site B (40590S, 71110W), Site C
(40570S, 71110W) and Site D (40290S, 70590W). Considering
possible nutritional deficiencies, the damage and frequency of
breakage on antlers collected between 2006 and 2009 were
analysed. Damage on antlers was classified as broken tips of
tines, tines completely broken off and breakage of the main beam.
Cases of campylognathia (facial scoliosis) were recorded from
specimens in our collection (n= 522) and those from hunters
(n= 254), and handedness according to hemisphere was analysed
using binomial probability tests.
Results
Ectoparasites were not present on gross examination (Site A,
n= 21; Site C, n= 9; Site D, n= 43. Flueck et al.1993; Smith-
Flueck and Flueck 1998). Fasciola hepatica was encountered
regularly among deer; at Site A, the prevalence in the population
was 50% (n= 20) (Flueck et al.1993,1995; W. T. Flueck,
J. M. Smith-Flueck, F. V. Olaechea, unpubl. data), whereas at
Site D, it was 9% (n= 43) (Smith-Flueck and Flueck 1998).
Additional deer examined between 1998 and 2009 at Site A
exhibited a prevalence of 13% (n= 45). Taenia ovis krabbei was
identified on the basis of hook characters, size, appearance and
anatomical location of a cysticercus. A sylvatic cycle involving
red deer appears to have been established (Flueck and Jones
2006). On several occasions, we found taenid larval stages
attached to liver, omentum and peritoneum, with the typical
gross appearance of Cysticercus tenuicollis, which were
deposited and identified by the state agency INTA. At Site A,
their prevalence was 8% (n= 12) (Flueck et al.1993). Ostertagia
sp. was found at a prevalence of 75%, with two individuals
carrying 800 and 900 adult parasites, respectively; Bunostomum
sp. was found at a prevalence of 25%; and Dictyocaulus sp.
occurred at 13% prevalence (n= 9, Flueck et al.1995;
W. T. Flueck, J. M. Smith-Flueck, F. V. Olaechea, unpubl.
data). FMD was tested for by SENASA in deer from Site B
(n= 41) in 1994–1995, to allow export of the tissue as part of a
genetic study (Flueck and Smith-Flueck 2011a); all samples
were negative. Among an additional 393 specimens collected
for reproductive and physical-condition studies, the only notable
pathological finding was a suspected case of mycobacterial
infection from Site D. We submitted fresh tissue from this
specimen to INTA, but no cultivation was done. Histological
sections were negative for acid-fast organisms; however, a large
quantity of macrophages with acidophilic material in the
cytoplasm was present. There were substantial multifocal, well
demarcated adhesions between the visceral and parietal pleura;
congregated, well demarcated and firm granulomatous
mediastinal lymph nodes; firm nodules of 5–10-mm thickness
practically covering the entire parietal pleura; and additional
lesions in the intestinal tract, including well demarcated
multifocal and firm nodules of 2–5-mm diameter associated
with rumenal lymph tissue, and focal protrusive aggregations
of up to 25-mm diameter of well demarcated small firm nodules
(1–2 mm) in liver (Fig. 1). The 9-year-old female was lactating, of
average build and without other lesions.
Diseases in red deer introduced to Patagonia Animal Production Science 767

Broken antlers
Damage was found on 73% of shed antlers (n= 132). Antlers with
broken tips had on average two broken tips, and 36% of antlers
had major breaks of tines and main beam (Fig. 2). Breakages
consisted of two main beams only; 10 tines only; three main
beams and tips; one main beam, tines and tip; 32 tines and tips;
and 50 tips only. An extreme case was a male that died during
the rut from fracturing the skull, with antlers remaining solely
attached to skin. Not only were two tines and seven tips broken
off, but both pedicles with portions of frontal, much of the parietal
and craniodorsal portion of occipital bones were broken out
such that the animal lost most of the upper brain case (Fig. 2).
Additionally, deer and cattle have been observed eating bone or
antlers. One ranch reported in 2009 on three free-ranging
domestic cows that continued to deteriorate, and when
eventually captured for checking, all had bones stuck sideways
in the mouth preventing them from foraging.
Campylognathia (facial scoliosis) or bent-nose
Campylognathia affecting principally the maxilla, premaxilla,
nasal bone and cranial portion of the mandible were found
in two female and five male red deer individuals (n= 776).
Case 1 was a female ~4 years old, in good condition, average
size, reproductively active, and there were no indications of
anatomical aberrations in the postcranial skeleton or other
gross pathological changes (Fig. 3). Case 2 was a female
yearling in good condition, and without indications of
anatomical aberrations in the postcranial skeleton or other
pathological changes. Although the body size was slightly
larger than average, the head length was shorter than average
due to the aberrant growth. The other five cases stemmed from
males harvested by hunters, with ages between ~4–14 years
(Flueck and Smith-Flueck 2011b). Of a total of 131 reported
cases of campylognathia in cervids (MacNally 1989,1992a,
1992b; Horsefield 1993; Prior 1993; Suttie and McMahon
1993; Suttie and Pearce 1994; Campbell 1995; Banwell 1999;
the present study), only 12% defy the expected directional
asymmetry according to the Coriolis effect (Suttie and
McMahon 1993); however, the correlation is significant
(P<0.001).
Discussion
The general absence of ectoparasites on gross examination
refers foremost to groups such as ticks, fleas and lice.
Similarly, wild ruminants such as guanaco living in cold
Patagonia are commonly devoid of ectoparasites (Karesh et al.
1998), although contact with sheep may lead to cross-
contaminations. Infections with F. hepatica and C. tenuicollis,
both cosmopolitan parasites, as well as with the exotic
T. o. krabbei, are considered to have low pathogenic potential
for otherwise healthy cervid hosts. Although it is not possible
to differentiate between T. o. ovis and T. o. krabbei on
morphological grounds with absolute certainty, red deer have
been reported to be refractory to T. o. ovis infection, whereas
other potential intermediate hosts such as cattle, goats, pigs and
sheep have been shown to be refractory to T. o. krabbei. Possible
or known definitive hosts in the study area include native felids
such as Puma concolor,Felis colocolo,F. guigna and canids
such as Dusicyon griseus,D. culpaeus, and domestic dogs. The
adult stage of C. tenuicollis, the tapeworm Taenia hydatigena,
is also found commonly in domestic and wild canids and felids
in the region.
Ostertagia sp., Bunostomum sp. and Dictyocaulus sp. are also
considered of low pathogenic potential to otherwise healthy
cervid hosts, but the latter two can be a concern when deer are
weak for other reasons. These parasites have been noted in
Argentine Patagonia in livestock and wildlife, including red
deer (Flueck and Jones 2006; Suárez et al.2007; the present
study).
In Chile, Ostertagia sp., Capillaria sp., Bunostomum sp.,
C. tenuicollis and Dictyocaulus sp. have all been found at low
levels in free-ranging exotic fallow and red deer, whereas faecal
exams from nine native huemul deer individuals showed only
(a)(c)(b)
Fig. 1. Female red deer. (a) Well demarcated multifocal and firm nodules of ~2–5-mm diameter associated with
rumenal lymph tissue. (b) Multifocal and well demarcated adhesions between visceral and parietal pleura, and firm
nodules of 5–10-mm thickness covering the parietal pleura. (c) Focal protrusive aggregation of 25-mm diameter of
well demarcated, firm nodules (1–2 mm) diameter in liver.
768 Animal Production Science W. T. Flueck and J. M. Smith-Flueck

very low egg or larval output; and in only three animals Moniezia
sp. was confirmed and also considered to be harmless to huemul
(Rioseco et al.1979). Most of these parasites, considered in
general to be non-threatening, are common in livestock and thus
occur in most areas with livestock.
Huemul deer are frequently claimed to be highly susceptible to
diseases such as C. tenuicollis, FMD, coccidiosis, ‘parasites’,or
actinomycosis (Povilitis 1978; Redford and Eisenberg 1992;
Simonetti 1995; Wemmer 1998; Lord 2007). According to
Simonetti (1995), ‘Cysticercus tenuicollis, when transmitted
by livestock is fatal to huemul’. However, the original source
did not consider C. tenuicollis to have caused death, but rather
the deterioration of the female after a premature parturition,
aggravated by tight confinement and low variety of food
(Texera 1974). Furthermore, in other cervids and ungulates,
C. tenuicollis has little significance (Leiby and Dyer 1971).
The frequently mentioned high susceptibility of huemul to
coccidiosis is based on the only existing study on this topic;
however, the original source questioned whether coccidiosis was
the cause of death, because of many additional problems, again
referring to limited space and poor nutrition (Texera 1974).
A sheep arriving later to this pen had coccidia, but when the
huemul died, it showed many other problems besides coccidia.
The presumptive case of mycobacterial infection would be
a concern more for red deer production systems with high
densities of animals. The present case stemmed from a high-
density population of red deer at ~50 deer/km
2
(W. T. Flueck
and J. M. Smith-Flueck, unpubl. data). The disease is widespread
in Argentina, particularly related to dairy production, and
has been recorded in the province of our presumed case (Perez
et al.2002), with a 10% prevalence in one studied Patagonian
province (Torres 2011). As a zoonosis, it requires caution by
people involved with wild deer. Similar lesions (parietal and
pulmonary pleura, rumen, liver) have been described for white-
tailed deer (Odocoileus virginianus) and red deer infected with
Mycobacterium bovis (O’Brien et al.2001; Glawischnig et al.
2006; Martín-Hernando et al.2010).
FMD tests in deer were all negative, even though there had
been a local outbreak in livestock 3 years earlier. Patagonia
is declared free of FMD, although there are occasionally focal
outbreaks, and northern Argentina has regular recurrences
(FBZP 2007). Anecdotal accounts by settlers are cited to
(a)(b)(c)
(e)
(d)
Fig. 2. Antler damage in red deer, including (a) broken tines, (b) broken crowns and (c) broken main beams. Skull
fracture, including (d) bases of antlers as found and (e) dorsal view of cranium, with caudal part of frontals and most
of parietal broken out. Note that the occipital is fractured and has the craniodorsal portion broken out (arrow).
Diseases in red deer introduced to Patagonia Animal Production Science 769

claim that FMD via livestock was responsible for decimating
Patagonian huemul over huge areas 60–70 years ago. In contrast,
recent FMD outbreaks in the UK resulted in experimental studies
of five cervid species that were all susceptible to FMD. On the
basis of natural behaviour of these free-living deer in the UK, they
are considered unlikely to be an important factor in the
maintenance and transmission of virus during an epidemic of
FMD in domestic livestock (Thrusfield and Fletcher 2002;
Fletcher 2004). Earlier concerns about FMD spill-over from
cattle to deer during an outbreak in 2001 in the UK proved to
be unfounded; numerous samples from deer showing lesions
suggestive of FMD proved to be negative (Davies 2002). There
has been no evidence of wild deer being implicated in this
epidemic, despite the fact that the deer population in UK was
10 times greater in 2001 than it was in 1967 (Davies 2002). At
normal densities of cervids, FMD is considered a self-limiting
disease (Morgan et al.2003). The very low densities of huemul
and reactions of other cervids to FMD renders those early
anecdotal accounts by settlers doubtful. Additionally, even if
FMD would reduce the population, after an outbreak is over and
considering the documented annual rate of increase of 21% in
Chile for huemul, a population would have recovered by 300%
in only 6 years. Thus, claims that FMD decimated huemul
populations in the past century are unfounded. Last, a recent
review on FMD among several South American wild animal
species considered susceptible to this disease found no reports of
any previous disease events nor outbreaks in wildlife populations
under field conditions (Pinto 2004).
The prevalence of antler breakage reported here was similar
to that found in C. elaphus in California by Johnson et al.
(2005), who suggested that it was related to copper (Cu) and/
or phosphorus (P) deficiencies (Johnson et al.2007). Moreover,
bone and antler chewing in C. elaphus was suggested in response
to calcium and phosphorus deficiencies in forage plants, and that
such inadequacies were related to antler breakage (Bowyer
1983). There are no reports of Cu deficiency in this Andean
region; however, P is low in part due to volcanic soils (Thomas
et al.1999). Given that the area has been exploited for >100 years
without fertiliser replacement, P concentrations might have
continued to diminish. The harvest of red deer alone represents
an export of ~1.8 kg P/female, whereas removing from the
system the antlers shed by a male that is harvested later at an
average age of 8 years exports about a total of 7.2 kg of P per
animal (Flueck 2009). Removing livestock from the systems
exports additional substantial P, and the estimated overall
export rate for P compares with rates measured in other
extensive production systems which, in contrast, often receive
10–50 kg/ha.year of P as fertiliser to compensate for the losses
from biomass exports.
Campylognathia can result from atrophic rhinitis, although
restricted to suids (Lutz 1988). Factors such as abnormal
fetal position, intra-uterine pressure, mineral deficiencies, or
injuries from physical impacts have been suggested (MacNally
1989,1992a), but all cases in cervids were from apparently
healthy individuals. Arthrogryposis (inherited, viral or from
teratogenic factors) in domestic ruminants is often associated
(a)(b)
(a)(b)
Fig. 3. Campylognathia in red deer affecting principally the maxilla, premaxilla, nasal bone and cranial portion
of the mandible. Above, female with (a) lateral and (b) ventral views of scoliosis; below, male with (a) lateral
and (b) ventral scoliosis.
770 Animal Production Science W. T. Flueck and J. M. Smith-Flueck

with campylognathia (Bähr et al.2003; de la Concha-Bermejillo
2003). Although wild North American cervids are often
seropositive to viral infections causing campylognathia in
livestock (Blackmore and Grimstad 1998), we found no
reference of seropositive deer exhibiting campylognathia.
Furthermore, causative Cache Valley or Potosi viruses have
not been reported for southern Argentina (Camara et al.
1990). A female deer with facial scoliosis to the left was
exported from New Zealand to Canada. There, she produced a
daughter that also exhibited campylognathia but to the right,
thus suggesting genetic (Suttie and Pearce 1994) or epigenetic
inheritance. Nonetheless, there are many confounding variables
possibly involved in deer living together and presenting similar
pathologies. Genetic inheritance as a primary cause seems
unlikely, given that the extensive red deer population in
Patagonia (Flueck et al.2003) resulted from 20 initial
individuals (Franke 1949), and thus the original frequency
would have had to be at least 5% (1 of 20) and is expected to
remain so. Since the 1920s, no instances have been reported
from this population, and the seven cases found represent <1%
of deer revised by us. Thus, the origin of campylognathia in
deer appears to be related to a non-inheritable developmental
disorder. Primary causes are not known and might include
congenital genetic aberrations, teratogenic compounds,
infections and other epigenetic factors affecting developmental
processes. The pronounced difference in developmental
patterns with respect to hemispheres suggests that the
disturbed developmental process may be influenced by
geophysical factors such as the Coriolis force (see Suttie and
McMahon 1993).
Inertial Coriolis forces arise when objects move linearly
within a rotating spatial reference frame such as the earth.
Any body movement not parallel to the earth axis will be
affected by a transient Coriolis force that arises as the
movement begins and decays as the movement ceases. For
instance, humans subjected to artificial Coriolis forces cannot
reach out and hit targets with their finger, until repeated attempts
have corrected the responses of the central nervous system and
motor compensations (Lackner and DiZio 2000). Similarly,
Coriolis forces are constantly acting on arms or legs from limb
movements made during voluntary body rotation; although they
are not perceived, motor compensations for their presence are
made, otherwise the movements would be inaccurate (Lackner
and DiZio 2000). Furthermore, Coriolis forces affect early stages
of development, such as movements of embryos within the
uterus, while the mother herself moves about, causing Coriolis
effects that affect innervation patterns of the mammalian
vestibular system (Bruce et al.2006). Geophysical forces even
have subcellular effects, such as gravity influencing both the
plane of bilateral symmetry and the orientation of microtubules in
the vegetal pole region of the embryos (Kochav and Eyal-Giladi
1971; Fluck et al.1998). These various systems affected by
Coriolis forces all play roles in mammalian ontogeny, yet normal
individuals grow symmetrical within the range of geophysical
forces encountered on the globe. It is, therefore, conceivable that
the networks processing these environmental cues, or the
mechanisms responsible for compensation, are malfunctioning
and thus result in a preponderance of facial scoliosis in accordance
to the earth’s rotation.
In conclusion, red deer were found to harbour a few diseases
commonly associated with livestock and wildlife, with the only
exception of T. o. krabbei, which, however, is a parasite of low
pathogenic potential. Having been in Argentina for >100 years
and in coexistence with livestock, both red deer and livestock play
roles in the epidemiology of the various diseases they share.
Regarding huemul deer, whereas livestock are commonly
sympatric with them (probably 100% of huemul populations),
spatial overlap with red deer is exceptionally rare, occurring in
<2% of known populations, and is of recent time (Flueck 2010b).
Even in this latter case, livestock presence is the determining
epidemiological factor for disease spill-over, since in the one
(of two) population, for each huemul, there were 1.2 red deer, but
25.2 livestock (Pastore and Vila 2003). Thus, for most, if not all,
huemul populations, feral and free-ranging livestock plays a
key role for spill-over of infectious and parasitic diseases.
Research, conservation and management efforts should thus
be directed towards finding appropriate solutions, including
livestock herd health programs and restriction of free livestock
movements, particularly where huemul still occur in protected
areas. Livestock, being regularly researched and inspected at
slaughter, provide a good proxy for the parasite community
and other diseases afflicting sympatric red deer. Although
sympatry between red deer and guanaco is common and
substantial, including the formation of mixed groups, and has
been suggested to affect the epidemiology of shared diseases
(Flueck 1996; Flueck et al.2003), we found no other reports
expressing sanitary concerns. Uncontrolled importations of
wild ungulates are of special concern if they involve cervids,
due to transmissible spongiform encephalopathy of cervids. The
appearance of this disease could be disastrous for South America
due to the large variety of endemic and threatened cervids. Last,
mineral disorders, as indicated by the high prevalence of antler
breakage, and in relation to extractive production systems, need to
be further investigated.
Acknowledgements
We thank several landowners for access to their properties to evaluate red
deer, and several students for their field assistance. Most of the research was
conducted in a natural reserve under the jurisdiction of the Argentine
Administración de Parques Nacionales. The study was funded in part by
the Argentine government through FONCYT Pict99, CONICET Grants 87/99
and 327/04, Ministry of Foreign Affairs through NZAID, and Swazi,
New Zealand. We also thank four anonymous reviewers for their many
constructive comments.
References
Bähr C, Kuiper H, Peters M, Scholz H, Distl O (2003) Arthrogryposis
associated with facial scoliosis and torticollis in German Holstein
calves. Deutsche tierärztliche Wochenzeitschrift 111, 403–407.
Banwell DB (1999) Campylognathie. Twisted or bent-nosed deer. Deer 11,
70–73.
Blackmore CG, Grimstad PR (1998) Cache valley and Potosi viruses
(Bunyaviridae) in white-tailed deer (Odocoileus virginianus):
experimental infections and antibody prevalence in natural
populations. The American Journal of Tropical Medicine and Hygiene
59, 704–709.
Bowyer RT (1983) Osteophagia and antler breakage among Roosevelt elk.
California Fish and Game 69,84–88.
Diseases in red deer introduced to Patagonia Animal Production Science 771

Bruce LL, Burke JM, Dobrowolska JA (2006) Effects of hypergravity on
the prenatal development of peripheral vestibulocerebellar afferent
fibers. Advances in Space Research 38, 1041–1051. doi:10.1016/
j.asr.2006.03.002
Camara A, Contigiani MS, Medeot SI (1990) Concomitant activity of Kairi
and Cache Valley bunyaviruses in Argentina. Revista Argentina de
Microbiologia 22,98–101.
Campbell J (1995) Bent-nose deer. Deer 9, 353.
Davies G (2002) The foot and mouth disease (FMD) epidemic in the
United Kingdom 2001. Comparative Immunology, Microbiology
and Infectious Diseases 25, 331–343. doi:10.1016/S0147-9571(02)
00030-9
de la Concha-Bermejillo A (2003) Cache Valley virus is a cause of fetal
malformation and pregnancy loss in sheep. Small Ruminant Research 49,
1–9. doi:10.1016/S0921-4488(03)00050-6
FBZP (2007) ‘Las barreras sanitarias y el desarrollo de la ganadería
Patagónica. Aportes para un debate necesario.’(Fundación Barrera
Zoofitosanitaria Patagónica: Viedma RN, Argentina). Available at
http://www.funbapa.org.ar [verified April 2012]
Fletcher J (2004) Foot and mouth disease in deer. In ‘Proceedings of the First
Deer Branch NZVA/World Deer Veterinary Congress’. (Ed. PR Wilson)
pp. 31–33. (Deer Branch NZVA: Palmerston North, New Zealand)
Fluck RA, Krok KL, Bast BA, Michaud SE, Kim CE (1998) Gravity
influences the position of the dorsoventral axis in medaka fish embryos
(Oryzias talipes). Development, Growth & Differentiation 40, 509–518.
doi:10.1046/j.1440-169X.1998.t01-3-00005.x
Flueck WT (1996) Zwischenartliche Beziehungen zwischen freilebenden
Guanaco (Lama guanicoe) und angesiedeltem Rotwild (Cervus elaphus)
in Argentinien. Zeitschrift fur Jagdwissenschaft 42,12–17. doi:10.1007/
BF02239623
Flueck WT (2005) Spatio-temporal movements among red deer males,
Cervus elaphus, introduced to Patagonia. In ‘XXVIIth congress of the
International Union of Game Biologists’. (Ed. K Pohlmeyer) pp. 330–332.
(DSV-Verlag: Hamburg, Germany)
Flueck WT (2009) Biotic translocation of phosphorus: the role of deer in
protected areas. Sustainability 1, 104–119. doi:10.3390/su1020104
Flueck WT (2010a) The slippery slope of exporting invasive species: the case
of Himalayan tahr arriving in South America. Biological Invasions 12,
1467–1475. doi:10.1007/s10530-009-9590-5
Flueck WT (2010b) Exotic deer in southern Latin America: what do we know
about impacts on native deer and on ecosystems? Biological Invasions
12, 1909–1922. doi:10.1007/s10530-009-9618-x
Flueck WT, Jones A (2006) Potential existence of a sylvatic cycle of Taenia
ovis krabbei in Patagonia, Argentina. Veterinary Parasitology 135,
381–383. doi:10.1016/j.vetpar.2005.10.009
Flueck WT, Smith-Flueck JM (1993) Über das in Argentinien angesiedelte
Rotwild (Cervus elaphus, L., 1758): Verbreitung und Tendenzen.
Zeitschrift fur Jagdwissenschaft 39, 153–160. doi:10.1007/BF02242892
Flueck WT, Smith-Flueck JM (2006) Predicaments of endangered
huemul deer, Hippocamelus bisulcus, in Argentina: a review.
European Journal of Wildlife Research 52,69–80. doi:10.1007/
s10344-005-0020-4
Flueck WT, Smith-Flueck JM (2011a) Blood proteins of red deer introduced
to Patagonia: genetic origins and variability. Animal Production Science
51, 359–364.
Flueck WT, Smith-Flueck JM (2011b) Red deer introduced to Patagonia. 2.
Campylognathia or bent-nose disease. Animal Production Science 51,
cxxxxiv–cxxxix. [Short Communication]
Flueck WT, Smith-Flueck JM (2012a) Huemul heresies: beliefs in search of
supporting data. 2. Biological and ecological considerations. Animal
Production Science 52, 694–706. doi:10.1071/AN11345
Flueck WT, Smith-Flueck JM (2012b) A review of introduced cervids in
Chile. Animal Production Science 52, 681–684. doi:10.1071/AN11343
Flueck WT, Smith-Flueck JM, Rüegg KA (1993) El ciervo rojo introducido en
la Patagonia. In ‘XVl Reunión Argentina de Ecología’. p. 279. (Puerto
Madryn: Chubut, Argentina)
Flueck WT, Smith-Flueck JM, Rüegg KA, Bonino N (1995) Datos
preliminares sobre la densidad del ciervo colorado (Cervus elaphus)
introducido en la Patagonia, Argentina. III Congreso Latinoamericano
de Ecología, Merida, Venezuela 24,9.
Flueck WT, Smith-Flueck JM, Naumann CM (2003) The current distribution
ofreddeer (Cervus elaphus) in southern Latin America. EuropeanJournal
of Wildlife Research 49, 112–119.
Franke FR (1949) ‘Mein Inselparadies.’(Verlag A. Francke AG: Bern,
Switzerland)
Glawischnig W, Steineck T, Spergser J (2006) Infections caused
by Mycobacterium avium subspecies avium, hominissuis, and
paratuberculosis in free-ranging red deer (Cervus elaphus hippelaphus)
in Austria, 2001–2004. Journal of Wildlife Diseases 42, 724–731.
Horsefield T (1993) Bent-nosed deer. Deer 9, 77.
Johnson HE, Bleich VC, Krausman PR (2005) Antler breakage in tule
elk, Owens Valley, California. The Journal of Wildlife Management
69, 1747–1752. doi:10.2193/0022-541X(2005)69[1747:ABITEO]2.0.
CO;2
Johnson HE, Bleich VC, Krausman PR (2007) Mineral deficiencies in tule elk,
Owens Valley, California. Journal of Wildlife Diseases 43,61–74.
Jones TC, Hunt RD, King NW (1997) ‘Veterinary pathology.’6th edn.
(Williams & Wilkins: Baltimore MD)
Karesh WB, Uhart MM, Dierenfeld ES, Braselton WE, Torres A, House C,
Puche H, Cook RA (1998) Health evaluation of free-ranging guanaco
(Lama guanicoe). Journal of Zoo and Wildlife Medicine 29, 134–141.
Kochav S, Eyal-Giladi H (1971) Bilateral symmetry in chick embryo
determination by gravity. Science 171, 1027–1029. doi:10.1126/
science.171.3975.1027
Lackner JR, DiZio P (2000) Artificial gravity as a countermeasure in long-
duration space flight. Journal of Neuroscience Research 62, 169–176.
doi:10.1002/1097-4547(20001015)62:2<169::AID-JNR2>3.0.CO;2-B
Leiby PD, Dyer WG (1971) Cyclophyllidean tapeworms of wild carnivores.
In ‘Parasitic diseases of wild mammals’. (Eds JW Davis, RC Anderson)
pp. 174–234. (Iowa State University Press: Ames, IA)
Lord RD (2007) ‘Mammals of South America.’(JHU Press: Baltimore, MD)
Lutz W (1988) Verbiegungen des Gesichtsschädels beim Wildschwein
(Sus scrofa scrofa L.) als mögliche Folge einer Rhinitis atrophicans.
Zeitschrift fur Jagdwissenschaft 34, 125–131. doi:10.1007/BF02241910
MacNally L (1989) Crooked-nose deer. Deer 7, 471–472.
MacNally L (1992a) Bent-nosed phenomenon. Deer 8, 558.
MacNally L (1992b) Bent-nosed roebuck. Deer 8, 538.
Martín-Hernando MP, Torres MJ, Aznar J, Negro JJ, Gandia A, Gortazar C
(2010) Distribution of lesions in red and fallowdeer naturally infected with
Mycobacterium bovis.Journal of Comparative Pathology 142,43–50.
doi:10.1016/j.jcpa.2009.07.003
Mitchell B, McCowan D, Nicholson IA (1976) Annual cycles of body weight
and condition in Scottish red deer, Cervus elaphus. Journal of Zoology
180, 107–127. doi:10.1111/j.1469-7998.1976.tb04667.x
Morgan JT, Fischer J, Hostetler ME (2003) If foot-and-mouth disease
came to Florida: potential impact on white-tailed deer in Florida. WEC
171, Department of Wildlife Ecology and Conservation, University of
Florida.
O’Brien DJ, Fitzgerald SD, Lyon TJ, Butler KL, Fierke JS, Clarke KR,
Schmitt SM, Cooley TM, Berry DE (2001) Tuberculosis lesions in free-
ranging white-tailed deer in Michigan. Journal of Wildlife Diseases 37,
608–613.
Pastore H, Vila A (2003) Situación de la población de huemules en la
jurisdicción de la Seccional Nirihuau, Parque Nacional Nahuel Huapi,
Informe Final 2000–2002. Fundación Vida Silvestre Argentina y Wildlife
Conservation Society, Buenos Aires, Argentina.
772 Animal Production Science W. T. Flueck and J. M. Smith-Flueck

Perez AM, Ward MP, Torres P, Ritacco V (2002) Use of spatial statistics
and monitoring data to identify clustering of bovine tuberculosis in
Argentina. Preventive Veterinary Medicine 56,63–74. doi:10.1016/
S0167-5877(02)00124-1
Pinto AA (2004) Foot-and-mouth disease in tropical wildlife. Annals of the
New York Academy of Sciences 1026,65–72. doi:10.1196/annals.1307.
008
Povilitis A (1978) The Chilean Huemul Project –A case history (1975–1976).
In ‘Threatened deer’. pp. 109–128. (IUCN: Gland, Switzerland)
Prior R (1993) Comment. Deer 8, 684.
Redford KH, Eisenberg JF (1992) ‘Mammals of the Neotropics: The southern
cone. Vol. 2. Chile, Argentina, Uruguay, Paraguay.’(The University of
Chicago Press: Chicago, IL)
Rioseco H, Cubillos V, Diaz L (1979) Patologia en cervidos. Archivos
Medicina Veterinaria Suplemento 1, 108–110.
Samuel WH, Pybus MJ, Kocan AA (2001) ‘Parasitic diseases of wild
mammals.’2nd edn. (Iowa State University Press: Ames, IA)
Simonetti JA (1995) Wildlife conservation outside parks is a disease-
mediated task. Conservation Biology 9, 454–456. doi:10.1046/j.1523-
1739.1995.9020454.x
Smith-Flueck JM, Flueck WT ((1998) ) Demography, health and reproductive
status of introduced red deer in Patagonia, Argentina. Proceedings of the
Wildlife Society Annual Conference 5, 143.
Suárez VH, Olaechea FV, Romero JR, Rossanigo CE (2007) ‘Enfermedades
parasitarias de los ovinos y otros rumiantes menores en el cono sur de
América. Publicación Técnica Nr. 70.’(Ediciones INTA: Anguil,
Argentina)
Suttie JM, McMahon CD (1993) Bent-nosed red deer in New Zealand. Deer
9, 42.
Suttie JM, Pearce JT (1994) Translocation of bent-nosed red deer from the
southern to the northern hemisphere. Deer 9, 297.
Texera WA (1974) Algunos aspectos de la biología del huemul
(Hippocamelus bisulcus) (Mammalia: Artiodactyla, Cervidae) en
cautividad. Anales del Instituto de la Patagonia. Punta Arenas (Chile)
5, 155–188.
Thomas SM, Johnson AH, Frizano J, Vann DR, Zarin DJ, Joshi A (1999)
Phosphorus fractions in montane forest soils of the Cordillera de Piuchue,
Chile: biogeochemical implications. Plant and Soil 211, 139–148.
doi:10.1023/A:1004686213319
Thrusfield M, Fletcher J (2002) Epidemiological concerns posed by deer
during the 2001 British foot and mouth disease outbreak. Deer 12,
169–171.
Torrejon F (2001) Variables geohistoricos en la evolucion del sistema
economico Pehuenche durante el periodo colonial. Revista Universum
16, 219–236. [Chile]
Torres PM (2011) ‘Situacion de la tuberculosis bovina en la republica
Argentina. Programa Control de Tuberculosis.’(SENASA: Buenos
Aires, Argentina). Available at http://www.senasa.gov.ar [verified
April 2012]
Wemmer C (1998) ‘Deer: status survey and conservation action plan.’(IUCN/
SSC Deer Specialist Group: Gland, Switzerland)
Williams ES, Barker IK (2001) ‘Infectious diseases of wild mammals.’
3rd edn. (Iowa State University Press: Ames, IA)
Wobeser GA, Spraker TR (1980) Post-mortem examination. In ‘Wildlife
management techniques manual’. (Ed. SD Schemnitz) pp. 89–98.
(The Wildlife Society: Washington, DC)
Diseases in red deer introduced to Patagonia Animal Production Science 773
www.publish.csiro.au/journals/an