Juvenile Mortality in Captive Lesser Kudu (Tragelaphus imberbis) at Basle Zoo

and its Relation to Nutrition and Husbandry

Author(s): Dorothea BesselmannDr. med. vet., Daniela SchaubDr. med. vet., Christian WenkerDr. med.
vet., Jürg VöllmDr. med. vet., Nadia RobertDr. med. vet., Claude SchellingP.D., Dr. med. vet., Hanspeter
SteinmetzM.Sc., Dr. med. vet., and Marcus ClaussM.Sc., Dr. med. vet., Dipl. E.C.V.C.N.
Source: Journal of Zoo and Wildlife Medicine, 39(1):86-91.
Published By: American Association of Zoo Veterinarians
DOI: http://dx.doi.org/10.1638/2007-0004.1
URL: http://www.bioone.org/doi/full/10.1638/2007-0004.1

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 Journal of Zoo and Wildlife Medicine 39(1): 86–91, 2008
Copyright 2008 by American Association of Zoo Veterinarians

JUVENILE MORTALITY IN CAPTIVE LESSER KUDU

(TRAGELAPHUS IMBERBIS) AT BASLE ZOO AND ITS RELATION
TO NUTRITION AND HUSBANDRY

Dorothea Besselmann, Dr. med. vet., Daniela Schaub, Dr. med. vet., Christian Wenker, Dr. med. vet.,
Jürg Völlm, Dr. med. vet., Nadia Robert, Dr. med. vet., Claude Schelling, P.D., Dr. med. vet.,
Hanspeter Steinmetz, M.Sc., Dr. med. vet., and Marcus Clauss, M.Sc., Dr. med. vet., Dipl. E.C.V.C.N.

Abstract: Since 1956, when the Basle Zoo (Switzerland) initiated the breeding of lesser kudu (Tragelaphus im-
berbis), 43% of the lesser kudu juveniles died before reaching an age of 6 mo. In this study, the objective was to
obtain the pathological findings, nutritional history, and family tree information in order to evaluate the influence of
husbandry on juvenile mortality in these animals. The main cause of death was white muscle disease (WMD), diagnosed
in 14 cases (26%) of the deceased juveniles. Although enclosure size had remained constant and animal accessibility
to the public was constantly high, both herd size and juvenile mortality had increased from 1956–2004. The diet
consumed by the whole group in 2004 had deficient levels of vitamin E and selenium. The increasing linear trend of
the mortality rate since the 1960s was significant, and there was a significant correlation between herd size and overall
juvenile mortality. In contrast, there was no correlation between herd size and the occurrence of juvenile mortality
associated specifically with WMD. Other investigated factors (sex, inbreeding, and season) had no significant effect
on overall mortality up to 6 mo of age or on mortality associated with WMD. These results characterize both a dietary
and a husbandry problem, and are supported by a lack of similar juvenile mortality in another facility where the diet
was supplemented with vitamin E, animal numbers were kept low, and the enclosure structure offered more retreat
options for the animals.
Key words: Lesser kudu, Tragelaphus imberbis, white muscle disease, vitamin E, diet, herd size, inbreeding.

CASE REPORT muscle disease (WMD). Rüedi et al.14 examined the

Lesser kudu are found browsing in dry forests
and brush in northeastern Africa.1,12 They are con-
sidered to be difficult animals in captive situations
and therefore are rarely kept in zoos. The problem
of successfully raising lesser kudu at Basle Zoo
(Switzerland) was discussed in two previous re-
ports.11,14 Lang11 observed that juvenile mortality
decreased after installation of a heatable nest box;
low environmental temperature was identified as
one of the main factors influencing juvenile mor-
tality. Rüedi et al.14 previously reported that low
vitamin E levels in three juvenile animals resulted
in their deaths, which were associated with white
From the Division of Zoo Animals and Exotic Pets,
Vetsuisse Faculty, University of Zurich, Winterthurerstras-
se 260, CH-8057, Zurich, Switzerland (Besselmann,
Schaub, Steinmetz, Clauss); the Zoological Garden Basle,
Binningerstrasse 40, CH-4054, Basle, Switzerland (Wen-
ker, Völlm); the Centre for Fish and Wild Animal Health,
Institute for Animal Pathology, Vetsuisse Faculty, Univer-
sity of Berne, Länggass-Strasse 122, CH-3012, Berne,
Switzerland (Robert); and Clinical Laboratory, Vetsuisse-
Faculty, University of Zurich, 噦 ETH Zurich, Tannen-
strasse 1, 8092 Zurich, Switzerland (Schelling). Corre-
spondence should be directed to Dr. Clauss (mclauss@
vetclinics.uzh.ch).
86
vitamin E content of plasma and liver samples of
healthy and diseased animals as well as the diet
offered to the kudu and recommended the inclusion
of wheat germ to increase dietary vitamin E levels.
Nevertheless, a generally high loss of juveniles
as well as cases of WMD seem to have persisted
over the years. The aim of this study was to assess
juvenile mortality, the incidence of WMD, and po-
tential contributing causes to this scenario by eval-
uating the necropsy reports since 1956, the family
trees of the animals affected, and the diets con-
sumed by lesser kudu at the Basle Zoo.
Basle Zoo
At the Basle Zoo, lesser kudu were kept on a
400-m2 outdoor enclosure. In addition, they had ac-
cess to the outdoor giraffe enclosure, which was
situated next to the kudu enclosure and separated
from it by a semipermeable gate. The indoor en-
closure consisted of four single boxes (4 m ⫻ 9 m),
which usually were combined but could be sepa-
rated. The whole group was kept together at all
times. There was one single box that was not vis-
ible to visitors where, after birth, mother and off-
spring were separated from the group for 2 days.
In winter, the lesser kudu were kept indoors and the
 BESSELMANN ET AL.—MORTALITY IN CAPTIVE LESSER KUDU
Figure 1. Number of juvenile deaths in lesser kudu (Tragelaphus imberbis) attributed to white muscle disease
between 1975 and 2004.
visitors could approach the animals at close dis-
tances (⬍1 m).
Necropsy reports for 54 juvenile (younger than
6 mo of age) lesser kudus that died between 1956
and 2005 at the Basle Zoo were evaluated for the
cause of death and the occurrence of specific dis-
eases. The 54 juveniles that died had an average
lifespan of 45 days. The most frequent diagnoses
at necropsy were WMD (14); enteritis (8); renal
alterations (7); and starvation (7). Other causes of
death were pneumonia (4) and necrobacillosis (2).
The occurrence of WMD did not change notably
over the years (Fig. 1). In particular, there was no
notable change after the 1980 report of Rüedi et
al.14 It is interesting to note that in the few years
after that study, no mortality associated with WMD
was reported. This observation may be the result of
a short-lived awareness of the problem after it was
investigated.
WMD in 14 juveniles had been classified as se-
vere in eight and medium-grade in six cases. His-
topathological investigation revealed typical lesions
limited to skeletal muscle fibers in five cases, heart
muscle fibers in one case, and combined alterations
in eight cases. Histologically, lesions were charac-
terized by multifocal hypercontraction and hyaline
degeneration and mineralization of disseminated or
grouped myofibers, associated with varying mac-
87
rophage infiltration and proliferation of satellite
cells. The lesions were compatible with the changes
usually described in nutritional myopathies in do-
mestic livestock.18
There were four additional animals that showed
only mild signs of WMD at necropsy and therefore
were assigned to a main ‘‘cause of death’’ group
other than WMD. In animals affected with enteritis,
bacteriologic culture revealed Escherichia coli in
three cases and Clostridium perfringens in three
cases. There was also a severe infestation of C. per-
fringens in animals with primary diagnoses other
than enteritis. Overall, 11 animals (20%) were di-
agnosed with C. perfringens at necropsy. All par-
asitologic examinations (n ⫽ 8) were negative.
In the spring of 2004, all diet items offered to
the whole group of lesser kudus, as well as the
remaining uneaten food, were weighed for 3 con-
secutive days in order to assess the diet. Intake re-
cording on an individual level was not deemed fea-
sible for this survey, because it would have caused
undue stress for the respective animals. The diet
ingested daily by nine animals (one adult male, six
adult females [including two that were lactating],
and two juveniles) in the spring of 2004 consisted
of 8.53 kg lucerne hay (Medicago sativa); 1.96 kg
of a pelleted compound feed (crude protein 15.3%,
crude fiber 18.0%, vitamin E 400 mg/kg, selenium
88 JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 2. Correlation between the number of births per year and the total cases of mortality in lesser kudu
(Tragelaphus imberbis) younger than 6 mo.
0.5 mg/kg); 2.29 kg carrots; 1.63 kg beet roots;
0.58 kg fennel; 0.49 kg sugar beets; and 0.13 kg
chicory. The proportion of roughage to nonrough-
age food components, on an as-fed basis, was 55:
45. The results were entered into Zootrition soft-
ware V2.5 (St. Louis Zoo, St. Louis, Missouri
63110 USA), which contained customized infor-
mation on the composition of the diet items used
at the Basle Zoo, and compared this information
with the recommendations for another browsing ru-
minant, the okapi (Okapia johnstoni). Calculated
crude protein levels of this diet were 95% of the
recommendations for okapi maintenance, whereas
vitamin E levels were 52% and selenium levels
were 60% of the recommendations. During the
growing season, the animals also received freshly
cut grass.
Historically, inbreeding, as judged from the fam-
ily trees compiled from the lesser kudu register of
the Basle Zoo, often occurred in the herd. Daugh-
ters bred with their fathers in 32 cases, mothers
with sons in 11 cases, and a sister with a brother
in one case. Thus, 44 of 133 animals are a product
of direct inbreeding. The breeding male who sired
offspring from 1985–1994 was diagnosed at autop-
sy with severe WMD.
The number of animals per year, based on births
and losses, were compiled from the lesser kudu reg-
ister of the Basle Zoo. During the initial decade,
the herd of lesser kudu consisted of two to six an-
imals but increased steadily up to 11 animals in
2004. Statisical analyses of birth and mortality data
were performed using Statistika娂 5.0 (Stat-Soft威,
Tulsa, Oklahoma 74115 USA). Logistic regressions
were used (PROC LOGISTIC from SAS, Release
8.01, SAS Institute Inc., Cary, North Carolina 2002
USA) to investigate if the overall mortality up to 6
mo of age and mortality due to WMD were affected
by sex, inbreeding, season of birth, and decade of
birth. Additionally, correlations between herd size
(measured as number of births per year) and mor-
talities were evaluated. The results of the logistic
regression analyses revealed a significant effect of
the decade of birth on the mortality rate up to 6 mo
of age. The linear trend of the mortality rate since
the 1960s is as follows: 1959–1969, 13% (n ⫽ 31);
1970–1979, 21% (n ⫽ 19); 1980–1989, 28% (n ⫽
18); 1990–1999, 55% (n ⫽ 47); 2000–2005, 75%
(n ⫽ 20) and was determined to be significant (P
⬍ 0.001). All other investigated factors such as sex,
inbreeding, and season had no significant effect on
either mortality up to 6 mo of age or mortality as-
sociated with WMD. As for WMD, the decade of
birth did not have a significant effect. There was a
significant correlation between the herd size, as
characterized by the number of births per year, and
the occurrence of juvenile mortality (r2 ⫽ 0.48, P
⬍ 0.001; Fig. 2); however, there was no correlation
 BESSELMANN ET AL.—MORTALITY IN CAPTIVE LESSER KUDU
between the number of births per year and the oc-
currence of juvenile mortality associated with
WMD (r2 ⫽ 0.03, P ⫽ 0.39).
Stuttgart Zoo
For comparison, husbandry, nutrition, and juve-
nile mortality data in lesser kudu at a comparable
zoo (Zoological and Botanical Garden Wilhelma,
Stuttgart, Germany) also were obtained for this
study. In contrast to the Basle Zoo, the Stuttgart
Zoo keeps lesser kudu with a juvenile mortality av-
erage of 20%. The outside and inside enclosures
are not accessible to the visitors at the Stuttgart
Zoo. Similar to the Basle Zoo, there is a semiper-
meable fence to the giraffe enclosure, well visible
to visitors. In contrast, the lesser kudu at the Stutt-
gart Zoo are able to withdraw from display at all
times and can return to their hidden outdoor enclo-
sure. There are 10 boxes for the lesser kudu group,
whose size is comparable to that of Basle Zoo. At
the Stuttgart Zoo, the buck is separated at night;
once young males become sexually mature, they
are removed from the group to prevent inbreeding.
Moreover, a breeding male is removed if there are
attempts to breed with his female offspring. After
birth, mother and offspring are separated from the
group for 3 or 4 wk and in the winter, up to 4 mo.
Juveniles obtain a single preventive vitamin E / se-
lenium injection on their first day. In addition, the
food of the whole herd is supplemented with an
oral vitamin E / selenium formulation (Vitamin E /
Selen Liquid RS, Chevita AG, 85276 Pfaffenho-
fen, Germany) that is sprayed over the food three
times a week. In pregnant females, the formulation
is applied daily 1 wk before and after birthing. Ku-
dus have access to branches with leaves ad libitum
throughout the vegetation period. The regular diet
consists of lucerne, grass, pellets, oat flakes, soft
food, potatoes, a variety of breads, and corncobs.
DISCUSSION
Although the problem of low vitamin E and se-
lenium status has been recognized at the Basle Zoo
for a long time,8,14 cases of WMD have occurred
continuously over the years, as documented by pa-
thology reports and serum biochemistry and vita-
min E levels in various animals. In general, vitamin
E deficiency is a well-recognized problem in zoo
animal management.5,6 The lack of cases around the
time of the first investigation into the problem at
Basle Zoo, together with its later reoccurrence, sug-
gests that changes in management must be imple-
mented in a manner that guarantees their persis-
tence over time. Although parenteral application of
vitamin E / selenium achieves increased serum lev-
89
els and potentially a reduction of serum biochem-
istry abnormalities, as documented by Rüedi et
al.,14 applying medication parenterally to animals
with a nervous nature can be stressful and imprac-
tical. The addition of vitamin E / selenium to the
diet is the preferred method of administration as
described by Graffam et al.7 or as reported in prac-
tice at the Stuttgart Zoo. In particular, the supple-
mentation of pregnant and recent lactating females
with vitamin E / selenium is extremely important
and will help to provide sufficient levels of those
nutrients to the offspring via colostrum and milk.
In sheep, serum values of vitamin E and selenium
from the dam are positively correlated with the con-
tent of their colostrum and with the serum values
of lambs after intake of colostrum.9,13
Apart from the fact that the diet as measured for
this study was deficient in both vitamin E and se-
lenium, the feeding of fresh grass during the sum-
mer is also a probable factor that can lead to WMD.
It should be noted that grass grown in the Jura re-
gion of Switzerland is known to be deficient in se-
lenium.10 Therefore, such grass should not be fed
unsupplemented to susceptible species. It has been
suggested that the herd should be provided browse
forage by ensilaging tree foliage. However, unless
nutritional analyses demonstrate a different result,
foliage from locally grown trees also should be
evaluated for selenium content.
The susceptibility to C. perfringens, which also
was detected in some animals affected with WMD,
indicates an increased prevalence of infection or a
weakened immune system. A low level of vitamin
E and/or selenium in the juveniles could have re-
sulted in an insufficient immune defense.17 Stress,
as a result of group size, no hiding opportunities,
and/or an inadequate feeding could have resulted in
an increased bacterial infections. During a study be-
tween 1991 and 1998 involving different stocks
from Niedersachsen (Germany), 125 sheep and 23
goats with a suspicion of vitamin E / selenium de-
ficiency were examined. Twenty percent of these
sheep with vitamin E / selenium deficiency did not
show any muscle or liver alterations but had un-
specific signs such as anemia and hypoproteinae-
mia, partly in combination with endoparasitism, di-
arrhea, and cachexia.2 Hence, it appears that a gen-
erally poor vitamin E status of the Basle Zoo’s less-
er kudus could have made juveniles susceptible to
a variety of other diseases,16 although no measure-
ments on immunological function were performed.
In contrast to our hypothesis that the family tree
may have impacted mortalities, it could not be
demonstrated that the inbreeding that occurred at
the Basle Zoo had a measurable effect on the health
90 JOURNAL OF ZOO AND WILDLIFE MEDICINE
status of neonate animals, as demonstrated in other
species. Therefore, even though inbreeding is un-
desirable and should be prevented, it could not be
associated definitively with the high juvenile mor-
tality of lesser kudus at the Basle Zoo. Rather, other
management factors seem to be of more importance
in impacting mortality. It was noted that both herd
size and juvenile mortality increased over the de-
cades and that there was a significant correlation of
the number of births with the number of juvenile
deaths per year but not with the number of deaths
associated with WMD. These findings suggest that
social stress should be regarded as another factor
that may have some influence on juvenile mortality.
Compared with the Stuttgart Zoo, the lesser kudus
at the Basle Zoo were exposed to more stressful
conditions due to the lack of opportunities to with-
draw from visitors, the continuous presence of the
adult male in the herd, and the high number of an-
imals stocked. The separation of the male at night,
as performed at the Stuttgart Zoo, corresponds to
the natural behavior of the species, because free-
ranging males rarely stay together with the fe-
males.12 Social stress caused by overcrowding leads
to maternal malnutrition, parasitism, disease, and
higher juvenile mortality rates in white-tailed deer
(Odocoilus virginianus).15 In another browsing spe-
cies commonly regarded as nervous, namely the
black rhinoceros (Diceros bicornis), the accessibil-
ity of the enclosure to visitors has been demonstrat-
ed to be correlated directly with increased fecal
stress hormone levels and the occurrence of dis-
ease.3,4 A group size of six adults is recommended
for the lesser kudu,11 but the Basle Zoo group size
has increased continuously since 1991. In addition
to dietary measures addressing vitamin E / seleni-
um supplementation, a general reduction in herd
size seemed warranted and was predicted also to
reduce overall juvenile mortality.
CONCLUSIONS
Due to the results of this study, the herd size at
the Basle Zoo was reduced to six adult animals and
an oral vitamin E / selenium supplement (Vitamin
E-Selen Liquid RS, Chevita, Pfaffenhofen, Ger-
many) was added to the daily ration (calculated
dose per animal and day: alpha tocopherol acetate
1,800 IU, sodium selenite 0.5 ␮g). In addition,
measures that limit visitor access to all parts of the
animals’ enclosures have been installed in the form
of wood covers and plant groups. The efficacy of
these measures will have to be evaluated over the
coming years to determine if these management
changes will reduce the juvenile mortality associ-
ated with the lesser kudu herd.
Acknowledgments: We thank Hoffmann-La
Roche AG of Basle, which determined the vitamin
levels between 1980 and 1996, and Wolfram Riet-
schel for his support in collecting information on
kudu husbandry at the Stuttgart Zoo.
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Received for publication 10 January 2007