Journal of Arid Environments 206 (2022) 104841

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Journal of Arid Environments

journal homepage: www.elsevier.com/locate/jaridenv

Constraints and incidence of camel calf morbidity and mortality in Borana

rangeland, Southern Ethiopia
Bantayehu Muluneh a, Desie Shiferaw b, Dereje Teshome a, Jafar Al-Khaza’leh d,
Bekele Megersa c, *
a
Yabelo Pastoral and Dryland Agriculture Research Center, Oromia Agricultural Research Institute, P. O. Box, 085, Yabelo, Ethiopia
b
Faculty of Veterinary Medicine, Hawassa University, PO Box 05, Hawassa, Ethiopia
c
College of Veterinary Medicine and Agriculture, Addis Ababa University, PO Box 34, Bishoftu, Ethiopia
d
Faculty of Agricultural Technology, Al-Balqa’ Applied University, P.O. Box 19117, Al-Salt, Jordan

A R T I C L E I N F O A B S T R A C T

Keywords: A longitudinal study was conducted to determine the incidence of mortality and morbidity rates of camel calves
Camel calf (birth to 180 day) and associated risk factors. Results showed that diseases, parasite infections, feed shortage,
Constraints inadequate veterinary services and recurrent drought were the major constraints. Out of 205 calves, 185 had
Morbidity
manifested 256 disease symptoms and 34 of them were died. Thus, a calf had 74.7% and 16.4% likelihood of
Mortality
Survival analysis
developing a disease and dying during the cohort period. The incidence of diarrhea, pneumonia, camel pox and
Borana septicemia were 59, 51, 38 and 17 cases per 100 calves-six-months at risk, respectively. The risk of diarrhea
(hazard ratio = 1.15) and pneumonia (HR = 1.48) were higher during the wet season and in calves kept on
communal grazing than others. The hazard of camel pox incidence was higher during dry periods and in calves
fed limited amount of colostrum. The mortality rate was found to be lower among calves above three months
(HR = 0.31), calves with normal delivery (HR = 0.32) and those kept at homestead (HR = 0.45) compared to
others. The hazards of mortality were 6.80 and 3.02 times higher during the dry season than wet period and in
calves that consumed less colostrum than their counterparts.

1. Introduction population growth. Adequate supply of young stocks certainly ensures

In Ethiopia, camels are kept under extensive pastoral managements
in arid and semi-arid areas of the country; such as in Somali, Afar,
Karayu and Borana areas (Keskes et al., 2013). Borana pastoralists, who
are traditionally cattle keepers, have started camel production recently
(Megersa et al., 2008; Mirkena et al., 2018) in response to changing
climate, rangeland ecology and socio-cultural conditions (Megersa et al.,
2014). The Gabras who have been rearing camels for centuries are more
experienced and endowed with better indigenous knowledge in camel
husbandry compared to the Boranas (Megersa et al., 2008). All com­
munities in the Borana area are keeping camels owning to the ability of
camels to tolerate droughts or prolonged dry period related feed and
water shortages, and supply the households with milk even during the
dry periods (Megersa et al., 2014).
As in any other livestock farming, camel calves are the underpinning
replacement stock for a sustainable camel herd establishment and
the growth and optimum productivity of a herd. However, rearing camel
calves under a traditional pastoral system in Africa has been reported to
suffer from several challenges that result in high calf losses (Kaufmann,
2000; Megersa et al., 2014). Several factors including vast arrays of
infectious diseases, constraints related to feed and nutrition, calf man­
agement and environmental conditions are among the determinants
(causes) of high death losses in camel calves (Kaufmann, 2000; Isako
et al., 2020).
High camel calf mortality is generally a critical challenge in pastoral
camel production systems (Kaufmann, 2000) and seasonal calving also
poses heavy challenges on calf health care and management while camel
keepers often cannot access veterinary services. A study from Kenya has
illustrated a high camel heifer loss (45.5%) and subsequent impacts on
replacement stock (Shibia et al., 2013). Higher calf mortalities, even
when compared to other livestock species sharing the same eco-zones, is
very costly given the low reproductive performances of camels (long

* Corresponding author.
E-mail addresses: bantuzed2@gmail.com (B. Muluneh), mereba480@gmail.com (D. Shiferaw), derejeteshe@gmail.com (D. Teshome), jkhaza@bau.edu.jo (J. Al-
Khaza’leh), bekelebati@gmail.com (B. Megersa).

https://doi.org/10.1016/j.jaridenv.2022.104841
Received 29 September 2021; Received in revised form 31 May 2022; Accepted 25 July 2022
Available online 14 August 2022
0140-1963/© 2022 Published by Elsevier Ltd.
B. Muluneh et al.
calving intervals and gestation period of camels, and prolonged age at
first calving).
Camel calf morbidity and mortality have been reported to be the
most important hindrances to pastoral camel production, with mortality
figures as high as 20.4% (Zeleke and Bekele, 2000), 15–20% (Megersa
et al., 2008), and 45% (Getahun and Kassa, 2002) from Ethiopia. Studies
in Kenya also reported camel calf mortality to be 20% (Wilson, 1986)
and 22–32% (Kaufmann, 2003) with female calve mortality ranging
from 20 to 30%. Such high camel calf mortality ultimately lowers herd
productivity and population growth.
Nevertheless the health problems of camels and their calves and
associated risk factors were not adequately investigated. Most of the
studies were based on short period cross-sectional surveys that do not
provide a sufficient picture of the disease dynamics in time and space.
Therefore, this longitudinal study was conducted to estimate the inci­
dence of camel calf mortality and morbidity rates, and associated risk
factors in Borana rangeland, southern Ethiopia.
2. Methodology
2.1. Study area
The study was conducted in Yabelo and Gomole districts of Borana
zone (Fig. 1). Geographically, the area is located between 4 and 6◦ N
latitude, and 36 and 42◦ E longitude with altitude ranging from 1000 to
1700 m above sea level. Borana rangeland is characterized by a semi-
arid and arid climate. Camel herds are kept by Borana (cattle breeder)
and Gabra (traditional camel keeper) communities of the study areas.
2.2. Study design and sampling procedures
A longitudinal study design was used to determine the incidence of
camel calf morbidity and mortality and potential risk factors from July
2019 to May 2020. Additionally, questionnaire survey was administered
to camel owners (respondents) at the beginning of the study period
following a pretest in July. The target populations were suckling camel
calves (Camelus dromedaries) aged between birth to 6 months of age, and
those reared under extensive pastoral production systems. The two
districts: Yabelo and Gomole were purposively selected taking into ac­
count the camel population and distributions of the two major camel
rearing ethnic groups. Borana herders traditionally keep cattle and
predominately reside in Yabelo whereas Gabras are traditional camel
herders in Gomole district and some parts of Yabelo. A total of six pas­
toral associations (PAs), the lowest administrative unit locally known as
Ganda, namely Dida-Yabelo, Dharito and Haro-Bake (from Yabelo),
Fig. 1. Map of Ethiopia and Borana zone showing the study areas.
2
Journal of Arid Environments 206 (2022) 104841
Buya, Surupa Badeya and Bake (from Gomole district) were randomly
selected. From each PA, seven villages (pastoral encampments with
10–20 households) having camel herds with at least five or more
breeding females were selected purposively considering accessibility to
the villages and herds throughout the survey period. The minimum
number of breeding females per herd was determined for herd eligibility
in order to increase the probability of having at least one new born calf
during the study period.
2.3. Sample size determination
The number of respondents (camel herders) for face to face interview
was estimated using central limit theorem (n = 0.25/(SE2)) described by
Arsham (2002) taking the standard error (SE) of 0.05 with 95% confi­
dence level plus 10% contingency for refusal or incomplete data. From
the herders that fulfilled criteria in each PA, 112 herders were purpo­
sively sampled and distributed by two ethnic groups. Subsequently,
about half of the herds (a total of 51 herds) were considered feasible for
the longitudinal study (monthly visit) based on willingness of herders to
participate in the longitudinal study and accessibility of herds
throughout the study period. The final study herds were then stratified
by the two camel herding communities i.e. Borana (n = 27) and Gabra
(n = 24) herders.
The sample size of calves required for the cohort study was calcu­
lated using the formula described by Thrusfield (2005). For this purpose,
95% confidence level, a prevalence of 18.1% from previous study report
(Megersa, 2014) and 5% desired precision were used as follow.
1.962 P(1 − P)
n=
d2
where n = required sample size, d = desired absolute precision, P =
expected prevalence (18.1%). Based on this the desired sample size was
found to be 228 calves. However, the actual number of eligible calves
available in the study herds during cohort period was 205 calves, which
were monitored over the six months cohort period.
2.4. Data collection
2.4.1. Questionnaire survey
During the first visit to the selected villages and herds, semi-
structured questionnaire was administered by a face to face interview
to camel herders. The questionnaire was focused on collecting herd-level
data such as management and husbandry practices, production objec­
tives, constraints, health care, perception and restriction of colostrum
intake, time and method of colostrum feeding, frequency of colostrum
B. Muluneh et al. Journal of Arid Environments 206 (2022) 104841

feeding, weaning age, history of calf morbidity and mortality in the herd
number of illness or death occurred during observation period
and other variables. Additionally, calf-level data such as the sex, age of IR =
total calf days at risk
calf, time and season of birth, delivery status of the calf (normal, or
dystocia or assisted birth), time of colostrum intake, and the parity of the The numerator is the total number of illness or dead calves, whereas
dam were collected. Herders were also probed to provide detail repro­ the denominator is the number of calf-days at risk for the given disease
ductive history profiles of 120 selected breeding female as well as fates or death occurrence. Number of calf days at risk was calculated by
of each pregnancy and calves borne alive using recall methods. adding the number of days at risk of obtaining a new case in each calf
from birth up to end of the study (Martin et al., 1987). For this purpose,
2.4.2. Longitudinal study of calves (cohort study) total calf days at risk were converted to calf months at risk, as the age of
A total of 205 calves born from July to November were enrolled and calf is defined up to six month and both time scales were reported where
followed monthly until the calves completed the six months cohort necessary. Furthermore, to simplify result comparisons with other
period or lost to follow-up. At the start, new born calves (that aged birth findings incidence rate (true rate: TR) was also converted to incidence
to 15 days using recalls on disease events) were included in the study. risk ratio (IR) or cumulate incidence rate (CIR) as probability of devel­
Other calves were enrolled progressively as they were born within the oping disease or dying over a time (i.e. one month) using the formula:
selected herds during the study period. During the cohort period, calves IR ​ = 1 − etrue ​ rate
were regularly monitored every month to collect data on occurrence of For survival analysis, Kaplan–Meier survivor or failure functions was
morbidity and mortality and their causes. When calf loss occurred dur­ to estimate hazard function of observed hazard differences for various
ing the study period, date and reason of loss was documented. In this factors. To assess the associations between potential risk factors and
study, morbidity was defined as any illness with recognizable symptoms survival up to 180 days of age, multilevel mixed effect parametric sur­
showed by calves which may ultimately results in death or recovery vival model was applied fitting PAs as random variable with Weibull
during the course of follow up; whereas, mortality was defined as any distribution. Association of risk factors disease events such as diarrhea,
observed death of calves above the age of 24 h, irrespective of the cause. pneumonia and pox were analyzed with multivariable Cox’s propor­
Thus, a calf was considered to be at risk of acquiring a disease that tional hazard model. Firstly, the association of individual risk factor
occurred for the first time, and a calf recovered from a disease is also at with an outcome variable was screened by univariable analysis of Cox
risk of being affected by another illness. Likewise, any calf present alive proportional hazard model. Then variables with p < 0.05 in the uni­
in the cohort was considered to be at risk of dying of any disease or variable analysis were modeled using multivariable Cox-proportional
health problem. hazard model.
During the study period, the calves were observed for clinical
symptoms by performing physical examinations for the presence of any 3. Results
disease conditions. Additionally, data on cleanliness of calves, house
conditions, feeding and watering practices, and treatments and drug 3.1. Demographic characteristics of the respondents and calf management
used were collected. Whenever any health problem encountered, the practices
affected calf was examined clinically; appropriate samples were
collected for further analysis. The respondents (herders) had average age of 49.79 ± 17.3 years
and most of them (91%) were without formal education (Table 1).
2.4.3. Fecal sample collection and examination Nearly half of herders (46.4%) allowed the calf to start full suckling just
Fecal samples were collected directly from the rectum of camel after birth, while others (53.6%) restricted the amount of colostrum
calves for the examination of gastrointestinal parasite eggs and proto­ intake by a newborn calf through limiting suckling time (58%), allowing
zoal parasites. A total of 254 fecal samples collected during the dry (n = half teat suckling (28.3%) and partial milking before letting the calf to
95) and wet periods (n = 159) were examined using floatation and suckle (13.3%). Herders mostly associated colostrum restriction with
modified McMaster eggs counting techniques for detection of parasites fear of fatal scouring and gastrointestinal tract disorders (GIT). Calf
eggs and protozoal oocysts as described by Soulsby (1982). All parasites weaning is among the commonly known breeding practice in the study
eggs and coccidia oocysts were counted and the counts were multiplied sites. Among the respondents, 42.0% and 40.2% of them practice
by 50 to obtain the total number of eggs or oocysts per gram of feces. weaning at age of one year and above one year, respectively. The
remaining households (17.9%) reported to wean at any time when
2.5. Data management and statistical analysis
Table 1
Data obtained from the study were analyzed using Stata Version 14.2 Demographic characteristics and calf management practice of respondents.
(StataCorp, College Station, Texas). Data from questionnaire survey Variables Levels/Units Parameters Borana (N Gabra (N
were presented as frequency distributions by bar chart or Tables. Rank = 56) = 56)
data were normalized by converting ranks into standardized values (0, Age of respondent Year mean ± sd 52.13 ± 47.5 ±
1), with values close to 0 and 1 indicating that a variable was ranked 17.7 16.8
least and highest, respectively (Megersa et al., 2014). Family size Number mean ± sd 7.91 ± 2.7 7.6 ± 3.1
Sex Female frequency 2 (3.6) 0
( ) Male frequency 54 (96.4) 56 (100)
(rank − rankmin )
Normalized ​ Rank ​ = ​ 1 − Education Illiterate frequency 54 (98.2) 48 (85.7)
(rankmax − rankmin )
grade 1–4 frequency 2(3.6) 6 (10.7)
grade 5–8 frequency 0 2 (3.6)
where rank is the position of a variable in the order of ranking, and Restrict colostrum yes frequency 29 (51.8) 31 (55.3)
rankmin and rankmax are the lowest and highest positions in the ranking. intake no frequency 27 (48.2) 25 (44.6)
As animals enrolled in this prospective study were at different times Age at weaning one year frequency 22 (39.3) 23 (41.0)
above one year frequency 24 (42.9) 23 (41.0)
and followed for different periods of time and hence incidence density
pregnancy frequency 10 (17.9) 10 (17.9)
(true rate) was used in describing disease occurrences. The speed at Importance of Strength frequency 32 (57.1) 50 (89.2)
which an event occurs per unit time at risk (true rate) was calculated to colostrum Nutritional frequency 4 (7.14) 1 (1.8)
define the risk of morbidity, mortality and other specific disease con­ fast growth frequency 18 (32.1) 2 (3.6)
ditions. Therefore, the incidence rates (IR) or cause specific rates were Disease frequency 2 (3.6) 4 (7.1)
prevention
estimated by the following formula.

3
B. Muluneh et al.
pregnancy is observed. Most of the herders believed that colostrum
feeding makes the calves strong and vigorous (73.2%) while others re­
ported its role as providing good nutrition (4.5%), fast growth (17.4%)
and disease prevention (5.4%)
3.2. History profile of breeding female pregnancies and fates of live born
calves
The reproductive history profiles of 120 breeding camels were pro­
bed, and plotted to assess the relationship of reproductive disorders
(abortion and stillbirth) and calf death with parity (Fig. 2.). Out of the
total 533 pregnancies, 43 abortions, 63 stillbirths (19.9% non-viable
pregnancies) and 427 live births were recorded. Reproductive disor­
ders and death of calves were found to be inconsistent when plotted
across parity. Accordingly, the highest proportion of abortion was
observed at late parity (parity 9: 22.2%) and the lowest was at mid
parity (parity 4: 0%). The proportion of calf mortality was also peaked at
late parity (parity 8: 25%). In the contrary, the proportion of stillbirth
was higher at early parity (parities 2 & 3).
Out of the 427 camel calves born alive, 18.7% of them were
considered as lost due to deaths (n = 53), or theft and predation (n = 27)
while beneficial off-take (e.g. emergency slaughtering and gift out)
accounted for 18.5% (n = 79) of the calves. Eventually, about 62.8% of
the calves were reported to reach age at maturity of four years and
mainly kept in herds for production purposes.
3.3. Priority constraints and diseases affecting camels and their calves
Various production constraints ranked by herders were shown by
Fig. 3. Prevailing diseases (rank scale of 0.94), feed shortage (0.81),
inadequate veterinary services (0.69), recurrent drought (0.50) and
market constraints (0.50) were ranked to be the most important con­
straints for camel production in the area.
Camel herders of the study area also prioritized several factors that
have roles in causing calf mortality (Fig. 4.). According to respondents,
disease was ranked (rank scale = 0.97) as the top cause of camel calf
mortality followed by drought related malnutrition (0.77), predator
(0.54), and accident losses (0.34).
As illustrated by Fig. 5., camel herders also ranked the most impor­
tant diseases that cause calf morbidity and mortality in the study area.
The commonly observed causes of calf morbidity were pneumonia,
camel pox, diarrhea, swollen lymph nodes, neck paralysis, contagious
skin necrosis, contagious ecthyma and manage mite infection. Among
the reported diseases camel pox, septicemia, swollen lymph nodes, neck
paralysis, chronic wasting disease and calf diarrhea were ranked to be
the major causes of mortality.
Fig. 2. Proportion of reproductive disorders (abortion & stillbirth) and death of
calves across parity.
4
Journal of Arid Environments 206 (2022) 104841
3.4. Gastrointestinal tract parasites of camel calves
In addition to other health issues, parasitic infections have been the
most widespread health problems in the study areas (Table 2). Results of
McMaster egg counts showed that 62.2% (95% CI = 48.1–64.9%) of the
calves had nematode and cestode eggs while few calves had coccidia
infections (7.1%). Average count of eggs per gram of feces was found to
be 304.2 and 340.5 during wet and dry periods, respectively.
3.5. Longitudinal cohort study
A total of 205 camel calves were enrolled and followed monthly for
six months. Female and male calves contributed 112 (54.63%) and 93
(45.37%) of the entries over the observation period, respectively. The
distribution of the study cohort was displayed in Table 3. A total of 35
calves have left the study before the termination of the cohort period
mainly due to deaths (34 calves) and gift out (one calf). Withdrawals
accounted for 17.1% of the total cohort, of which 19 (9.26%) and 16
(7.8%) were female and male calves, respectively. Relatively more
number of deaths were observed in October (n = 7) and November (n =
5), which peaked in December (n = 10). But no mortality case was
recorded in May and July.
Fig. 6. shows median age of morbidity by diseases/syndromes. As
evident from the figure, diarrhea had smallest median age of morbidity
of 18 days (interquartile range: 7–68 days) followed by septicemia with
a median of 37 days (IQR: 7–98). These two diseases also exhibited
longer age ranges, so that they were more frequently occurred in early
ages, while still affecting older age groups. The median age of pneu­
monia cases was 77 days (IQR: 59–100 days). Camel pox had the largest
median age of mortality (145 days) and shorter age range (IQR: 116–160
days) as the disease occurred as an outbreak.
The cumulative hazards of different diseases or symptoms also reflect
the aforementioned conditions (Fig. 7.). Diarrhea had steeply increased
during the first three weeks of early life and revealed a slight change
thereafter. The cumulative hazard for pneumonia showed a noticeable
increasing trend between 30 and 90 days, while that of pox increased
after 90 days of the cohort period.
Table 4 shows summary of incidence rate of different diseases and
crude mortality in camel calves of the study area. Most of the monitored
calves (185 out of 205) had manifested one or more disease symptoms (i.
e. 256 symptoms were recorded), during the 187 calf-6 months-at risk,
making the incidence risk of 74.7%. The incidence of diarrhea, pneu­
monia, camel pox and septicemic infections were 59, 51, 38 and 17 cases
per 100 calves-six-months at risk, respectively. Thus, diarrhea was the
leading cause of morbidity (risk ratio of 44.5%), followed by pneumonia
(39.7%), camel pox (31.4%) and septicemia (15.8%). A total 34 calves
died of different causes during the 1137 calf–months at risk. Accord­
ingly, the crude mortality rate was found to be 18 death cases per 100
calf-six-months at risk or 16.4% incidence risk of mortality during the
entire cohort period.
In this study, the major causes of camel calf mortality were pneu­
monia (23.5%), septicemic infections (17.6%), camel pox (14.7%) and
calf diarrhea (11.8%). Diseases locally called Kanicha (swollen gland)
and Elgof (wasting disease) also caused deaths of three calves each. The
remaining mortalities (n = 5) were due to sudden death, bloat and
starvation.
3.5.1. Association of risk factors with camel calf morbidity and mortality
Initially 29 independent variables were recruited in univariable
analysis using Cox’s proportional hazards model. Those variables
showed significant associations with mortality were further subjected to
mixed-effect multivariable analysis. Accordingly, age of calf, colostrum
feeding, calf delivering status, season, pre-weaning management and
household level livestock species diversity were significantly associated
with mortality (Table 5).
Holding the effect of other variables constant, the crude mortality
B. Muluneh et al. Journal of Arid Environments 206 (2022) 104841

Fig. 3. Ranked constraints of camel calf production in the study area (n = 112).

Fig. 4. Ranked causes of camel calf mortality in study area (n = 112).

Fig. 5. Prioritized diseases that cause morbidity and mortality of camel calves (n = 112).

Table 2
Parasitic infection of camel calves (n = 254) distributed by sex, season and districts.
Factors Helminthes eggs Coccidia Oocyst

Samples positive % Mean EPG Sample positive %

Sex Male 112 90 80.3 318.7 112 7 6.3

Female 142 68 47.5 333.5 143 11 7.7
Seasons wet 95 50 52.6 304.2 95 7 7.4
Dry 159 108 68 340.5 159 11 6.9
District Yabelo 121 77 63.6 502.5 121 10 8.3
Gomole 133 81 60.9 487.4 133 8 6
Total 254 62.2 326.9 254 18 7.1

5
B. Muluneh et al. Journal of Arid Environments 206 (2022) 104841

Table 3 rate was significantly lower among calves above three months (HR =
Number of calves (cohort) monitored and reasons of withdrawals from the 0.31; p = 0.002), calves with normal delivery (HR = 0.32, p < 0.004)
longitudinal cohort. and kept at homestead (HR = 0.45; p = 0.037) compared to others. The
Monthly visits number of entry Number of withdrawals total hazards of mortality were 6.80 and 3.02 times higher during the dry
(births) cohort
death gift total
out
Table 4
July 52 0 0 0 52
August 46 2 0 2 96
Incidence of different diseases (symptoms) and crude mortality in camel calves
September 44 2 0 2 138 in Borana.
October 27 7 0 7 158 Health Number Calf Calf calf 6 Incidence (over
November 36 5 0 5 189 Problems of cases days at months months six months)
December NI 10 0 10 179 risk at risk at risk
January NI 2 0 2 177 True Risk
February NI 2 0 2 175 rate ratio
March NI 3 0 3 172 (%)
April NI 1 1 2 170 Diarrhea 79 24061 802 134 0.59 44.6
May NI 0 0 0 170 Respiratory 77 27363 912 152 0.51 39.7
Overall 205 34 1 35 170 infections
NI = Not included as those calves borne from December to May were not part of Camel pox 66 31516 1050 175 0.38 31.4
Septicemic 23 24034 801 134 0.17 15.8
the cohort.
conditions
Miscellaneous 11 25927 864 144 0.08 7.4
casesa
Crude 256 33558 1119 187 1.37 74.7
morbidityb
Crude 34 34122 1137 190 0.18 16.4
mortality
a
Miscellaneous cases include conditions like swollen gland, chronic wasting,
starvation and bloat.
b
Crude morbidity was estimated from number of disease cases, but not from
the number of affected calves.

Table 5
Mixed-effect multivariable Cox regression analysis of factors associated with
mortality rate.
Variables levelsa HR P-value

Age ≥3m vs.<3m 0.31 0.002

Colostrum feeding Limited vs. Full 3.02 0.005
Calf delivery status Normal vs. assisted 0.32 0.004
Seasons Dry vs. wet 6.80 0.000
calf management KH vs. KGH 0.45 0.037
Fig. 6. Median age of calf morbidity by diseases. Animal spp diversity ≥4 spp vs. < 4 spp 1.39 0.517

HR: Hazard ratio (comparable to relative risk). KGH=Kept with grazing herd
and KH=Kept at homestead.
a
Levels written to the right side were references.

Fig. 7. Cumulative hazards of diarrhea, pneumonia, pox and septicemia.

6
B. Muluneh et al. Journal of Arid Environments 206 (2022) 104841

season than wet periods and in calves that consumed a limited amount of 2014). Such a high parasitic burden has been already observed to hinder
colostrum than those without restriction. the weaning and growth performance of camel calves (Mohammed et al.
Analysis of potential risk factors with the incidence of calf diarrhea 2013), and call for seasonal deworming.
showed significant association of seasons and calf management in the Our finding regarding the outcomes of 533 pregnancies revealed that
multivariable Cox proportional model. Holding the effect of other var­ only 62.8% of the calves survive to age at maturity of four years, sug­
iables constant, the incidence of diarrhea was significantly higher during gesting substantial losses of young stocks before they reach reproductive
the wet period (HR = 1.15; p = 0.001). Lower incidence of diarrhea was age. Under pastoral management conditions such as in Borana, camel
observed in calves kept at homestead (HR = 0.29, p = 0.046) compared calves rearing, and ensuring their growth and survival to reproductive
to those kept at communal grazing with camel herd (Table 5). Restricted age is so challenging given the wide prevalence of constraining factors
colostrum intake was significantly associated with increased incidence including infectious diseases, parasitic burden, feed shortage and inad­
of diarrhea in the univariable analysis, but no difference was observed in equate veterinary services. Additionally, recurrent drought and restric­
the multivariable model. tion of herd mobility are also emerging constraining factors. Other
Three of the variables; assisted delivery, dry season, and pre-weaning studies also reported infectious diseases, feed and water shortage as
calf management were also significantly associated with the incidence of major challenges camel calf production in pastoral areas (Kaufmann,
pneumonia. Thus, the risk of pneumonia was higher among calves 2000; Kassa et al., 2015; Isako et al., 2020). These studies concluded that
delivered without assistance (HR = 0.43, p = 0.045) and those kept at feed shortage and associated malnutrition during the dry periods
homestead (HR = 0.41, p = 0.039) compared to the other groups. The contributed to up 27.8% (Kassa et al., 2015) of the camel calf deaths in
hazard of pneumonia occurrence was higher during the wet season (HR Ethiopia and to 22% of the calf losses in Kenya (Kaufmann, 2000). Ex­
= 1.48, p = 0.043) than dry periods. Likewise, the hazard of camel pox istence of high competition between people and calves for milk,
incidence was higher among calves fed limited amount colostrum and in particularly during the dry period, certainly worsens malnutrition
calves older than three months compared to their counterparts (Table 6). related mortality (Schwartz et al., 1983). Other emerging socio-political
factors (e.g. crop farming, administrative boundaries and, and enforce­
4. Discussion ments of local rules) may weaken key herd management strategies such
as herd mobility, and further exacerbate the dry period feed and water
The present study revealed that the morbidity and mortality of camel shortages. Thus, ensuring consumption of sufficient milk during the first
calves are important problems of camel production. Camel diseases are three months of age before calves are able to graze and provide addi­
among the major constraints to camel production in general and calf tional supplementary feeds in dry period are also very crucial for the
production and survival to reproductive ages in particular. The observed wellbeing and survival calves.
major causes of camel calf morbidity and mortality (pneumonia, camel The magnitude of camel calf mortality may vary with season, age of
pox, diarrhea, septicemic infections, contagious skin necrosis) in this study calves, environmental conditions and management risk factors.
study were also reported from different parts of Ethiopia (Megersa, Mortality figures of 18.1%–20% from Borana (Megersa et al., 2008;
2014; Keskes et al. 2013; Tefera and Abebe, 2012) as well as from Megersa, 2014) and 20.4% from Afar (Zeleke and Bekele, 2000) have
neighboring countries (Gilbert, 2012; Kuria et al., 2011). GIT parasite been reported from camel herds in Ethiopia. Mortality can be as high as
infections were also a widespread health problems in the study areas 45% (Getahun and Kassa, 2002) and 27% (Kaufmann 2005) in pastoral
with 62.2% (95% CI = 48.1–64.9%) of the study calves harboring herds with poor health care and management practices. Camels are slow
various helminthic parasites. Higher parasitic prevalence of 70% reproducing animals, i.e. late age at maturity, prolonged gestation and
(Megersa, 2014) and 83.3% (Mohammed et al., 2013) has been reported calving interval, thus such a high death losses (above 10%) are costly as
from camel calves in Ethiopia, whereas a lower prevalence (47%) was it leads to stringent shortage of replacement stock that hinder herd
also recorded from Afar region of Ethiopia (Gebru et al., 2017). Parasitic growth. A study by Shibia et al. (2013) also reported high losses of fe­
prevalence in calves may differ with various factors i.e. can be lower in male calves (45.5%) before reaching reproductive age.
arid environment and during dry season, and increase with age of calves In this study, camel calf diarrhea was the primary cause of calf
as they start foraging with herds (Mohammed et al., 2013; Megersa, morbidity with incidence risk of 44.6%, followed by pneumonia, camel
pox and septicemic infections similar to a study finding from northern
Kenya (Kaufmann, 2000). Our empirical data are congruent with the
Table 6 important calf diseases ranked by camel keepers and as well as with
Potential risk factors associated with the incidence of calf diarrhea, pneumonia previous study findings that identified diarrhea, respiratory infections
and pox occurrence in multivariable Cox’s proportional hazards model. and septicemia as most important health problems of camel calves
Variables Levels** Univariable Multivariable (Megersa 2014; Rirash et al., 2017). With regard to mortality, pneu­
monia was the most frequently observed cause of calf death, followed by
HR P- HR P-
value value septicemia, pox and diarrhea. In agreement with our findings, other
studies have also reported similar causes of calf mortality elsewhere
Diarrhea
Colostrum feeding limited vs. full 1.9 0.022 0.72 0.605
from pastoral herds (Kaufmann, 2000; Megersa, 2014; Ahmed and
Seasons wet vs. dry 4.5 0.000 1.15 0.001 Hegde, 2007). Farah et al. (2007) observed diarrhea as a major cause of
Calf management KH vs. KGH 0.53 0.024 0.29 0.046 death (73%) in Somalia whereas Mahmoud et al. (2012) reported high
Animal spp >4 Spp vs. ≤ 4 Spp 0.64 0.053 1.14 0.777 morbidity (80%) and mortality (12.7%) caused by pox in camel calves in
diversity
Egypt.
Sex male vs. female 1.57 0.043 1.2 0.735
Pneumonia As evident from the median age of morbidity and cumulative
Calf delivery status normal vs. assisted 0.55 0.043 0.43 0.045 morbidity curves of different diseases, the incidence of diarrhea and
Seasons wet vs. dry 3.39 0.000 1.48 0.043 septicemia were higher during the first few weeks of early life so that
Calf management KH vs. KGH 0.36 0.001 0.41 0.039 they might have caused most of the early mortalities. Pneumonia cases
Pox
Age group ≥3month 1.27 0.054 3.51 0.001
were more incident between 30 and 90 days, and can be responsible for
vs.<3month most of the deaths encountered during this period. Camel pox affected
Colostrum feeding limited vs. full 2.16 0.002 2.22 0.002 mainly calves above 90 days of age, so that accountable for deaths
Seasons wet vs. dry 0.55 0.033 0.61 0.093 recorded in older age groups. This could be partly because of the effects
*KGH=Kept with grazing herd and KH=Kept at Homestead, **levels placed to of passive immunity that might have protected the younger calves.
the right of Vs are references. Camel pox has been characterized by strong maternal passive immune

7
B. Muluneh et al.
transfer and also transmitting through ticks vectors (OIE, 2018). As a
result, risk of infection would naturally increase when contact with
potentially infected animals and/or vectors increase after maternal an­
tibodies in circulation had dwindled. In general the three major disease
problems, enteric infections (diarrhea), septicemia conditions and res­
piratory infections were found to be responsible for larger proportion of
calf losses (Kaufmann, 2000) and require intensive health care and good
calf management to minimize early mortality.
Observed higher early mortality, among calves below 30 days of age
compared to those in the age group of 30 days and above, is in line with
previous study findings such as by Megersa (2014) in Borana, by Rirash
et al. (2017) in Somali region of Ethiopia, by Farah et al. (2004) from
Somalia and Musa et al. (2000) from Omani camels. Ahmed and Hegde
(2007) also recorded high calf mortality (about 50%) during the first few
weeks following birth, which was eventually reduced to 30%by half
during 90 days after birth. Higher risk of mortality during the early life
of calves implies the need to implement proper camel calf management
practices (such as ensuring sufficient colostrum and milk consumption,
and provide intensive health care) at early age when calves are highly
susceptible to infections. Our finding of the negative effect of restriction
of colostrum consumption on camel calf survival may substantiate the
linkage of early mortalities with poor management practices. Insuffi­
cient and delayed colostrum consumption as well as failure of passive
transfer has been linked to early calf mortality in pastoral herds. Ac­
cording to a study by Kamber et al. (2001), 39% of the studied calves had
below 4 g/L of serum colostrum concentration, which can be considered
as a critical value for other farm animals. Observed higher risk of mor­
tality in calves with restricted colostrum intake compared to others is in
agreement with previous findings (Kamber et al., 2001; Bishr et al.,
2013; Megersa 2014). Restrictions of early colostrum consumption by
most camel keepers (as preventive measures of calf scour) and associ­
ated mortalities have been widely reported (Kaufmann, 2000; Isako
et al., 2020), while good practices on colostrum feeding are not yet well
adopted. Thus, participatory discussions among veterinarians, early
adopters and non-adopter pastoralists would improve their awareness
and good practices on colostrum feeding.
In the present study delivery status was significantly associated with
camel calf mortality and calf pneumonia. Calves that delivered through
assistance were at higher risk of mortality than those normally deliv­
ered, a finding that is similar to another study in Ethiopia (Assen et al.,
2016). Assistance during delivery increases risks of infection and mor­
tality due to delayed and inadequate intake of colostrum, high chance of
contamination during delivery and the immunosuppressive effects of
cortisol hormone released by the stressed calf. Camels generally need
less assistance during delivery, but labor take a bit longer time than
other farm animals.
Mortality was significantly higher during dry season than wet sea­
son, which can be ascribed to the coincidence with shortage of feed and
water, which affect both dam and calf. This finding is consistent with the
research reports by Rirash et al. (2017) in which feed shortage during
dry period was found to be the major cause of calf death. Schwartz et al.
(1983) also reported malnutrition to be the major cause of mortality
during the dry period. Another literature review on calf management
(Isako et al., 2020) also demonstrated competition for milk between
people and calves and feed forages during dry period to be the major
causes of calf mortality in Kenya. This situation points to the need to
provide camel calves with adequate (additional) feed and water during
the dry periods.
Calves kept on communal rangeland with adults were at higher risk
of death compared to that kept at homestead before weaning. This could
be related to the fact that most of the camel calf diseases are contagious,
and can be transmitted directly by contact or by ingestion of contami­
nated feed. Overall, the claves that were allowed to browse with the
herd earlier may have a greater exposure to various disease causing
factors which logically can increase risk of mortality compared to calves
kept near the residence areas. Similarly, calves kept with grazing herds
8
Journal of Arid Environments 206 (2022) 104841
had higher risk of diarrhea compared to those kept at homestead. This
could be ascribed to higher exposure of calves to contaminated envi­
ronment shared by adult animals and increase the opportunity of being
infected due to prolonged exposure to pathogens (Larson et al., 2004).
Likewise, observed higher risk of pneumonia in calves that let to graze
with herd at communal rangeland compared to those kept at homestead
can be attributable to increased interactions and contacts with other
adult camels. The risk of respiratory infections increases with in­
teractions and gathering of camels at watering points or grazing area
(Kebede and Gelaye 2010). Hence pre-weaning calf management
(separate calf herding) is vitally important in reducing disease risks that
can be transmitted from adult animals or from contaminated
environment.
The risk of calf diarrhea was also higher during rainy season than dry
period; similar to previous study findings from Borana area (Megersa,
2014) and Sudan (Ali et al., 2005). Another study also reported a high
incidence of calf diarrhea (21.9%) during early summer coinciding with
the peak of the calving period for camels in Sudan (Agab and Abbas
1999). High prevalence of infections during wet and warm period can be
by favorable environmental conditions that help the maintenance and
multiplication of pathogens. Camels are also seasonal breeders, in which
parturition occurs in the wet season with good feed availability. Simi­
larly, the incidence of pneumonia was significantly higher in wet than
dry season, which is also in line with another study (Megersa (2014).
Agab and Abbas (1999) described housing of camels in unsheltered pens
and dust storms emerging during the first weeks of the rainy season as
predisposing factors for respiratory disease in camels (Abbas et al.,
2002). Unlike diarrhea and pneumonia, pox was found to be more
incident during the dry period compared to the wet season.
5. Conclusion
It is indisputable that camel plays a vital role in ensuring food se­
curity and human wellbeing in the arid environments, and camel calves
are the foundation of camel herds. The study showed that calves suffered
from production constraints and wide range of diseases of which diar­
rhea, respiratory infections, septicemia and camel pox were responsible
for most of the calf mortalities. Calf age, colostrum feeding, delivery
status, seasons and pre-weaning calf management were found to be the
major risk factors for morbidity and mortality in camel calves. Our study
findings suggested that intervention measures on production constraints
and management factors (e.g. ensuring adequate colostrum intake, dry
season feed supplementation, deworming and avoiding pre-weaning
release of calves with herds may reduce the mortality losses.
Authorship contributions
BMu and BM were responsible for the study design, data acquisition
and analysis, drafting and revising the manuscript, and interpretation of
results. DS, DT and JA have participated in the design of the study,
drafting and revising the manuscript. All authors read and approved the
final manuscript.
Funding information
This study was supported by the Oromia Agricultural Research
Institute and Hawassa University, Ethiopia as postgraduate research
fund.
CRediT authorship contribution statement
Bantayehu Muluneh: Funding acquisition, Formal analysis, Writing
– original draft, Writing – review & editing, and were responsible for the
study design, data acquisition and analysis, drafting and revising the
manuscript, and interpretation of results. Desie Shiferaw: Writing –
original draft, Writing – review & editing, have participated in the
B. Muluneh et al.
design of the study, drafting and revising the manuscript. All authors
have sufficiently contributed to the work, read and approved the final
manuscript. Dereje Teshome: Writing – original draft, Writing – review
& editing, and have participated in the design of the study, drafting and
revising the manuscript. All authors have sufficiently contributed to the
work, read and approved the final manuscript. Jafar Al-Khaza’leh:
Writing – original draft, Writing – review & editing, have participated in
the design of the study, drafting and revising the manuscript. All authors
have sufficiently contributed to the work, read and approved the final
manuscript. Bekele Megersa: Funding acquisition, Formal analysis,
Writing – original draft, Writing – review & editing, were responsible for
the study design, data acquisition and analysis, drafting and revising the
manuscript, and interpretation of results, .
Declaration of competing interest
The authors declare that they has no any known competing financial
interests or personal relationships that could have influence on the work
reported in this paper.
Acknowledgments
The authors are grateful to Yabelo Regional Laboratory Analysis. We
acknowledge the pastoralists from our study area for their participation
and cooperation in this study.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.jaridenv.2022.104841.
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