1. RESEARCH ARTICLE
Effect of Concentrates Restriction on Feed
Consumption, Diet Digestibility, and Nitrogen
Utilization in Captive Asian Elephants
(Elephas Maximus)
A. Das,1
* M.L. Smith,2
M. Saini,1
Shrikant Katole,1
S.S. Kullu,1
B.K. Gupta,3
A.K. Sharma,1
and D. Swarup4
1
Centre for Wildlife Conservation, Management and Disease Surveillance, Indian Veterinary Research Institute,
Izatnagar, Uttar Pradesh, India
2
Assam State Zoo and Botanical Garden, Guwahati, Assam, India
3
Central Zoo Authority, New Delhi, India
4
CIRG, Mathura, UP, India
In order to study the effect of concentrates restriction on feed consumption, diet digestibility, and utilization of nitrogen in
captive Asian elephants (Elephas maximus), two feeding trials were conducted on three juveniles, four sub-adults, and three
adults. During trial I, the conventional zoo diets of juveniles, sub-adults, and adult contained 22, 17, and 16% of concentrates
on dry matter (DM) basis, respectively. During trial II, the amount of concentrate was reduced by 50%. A digestion trial of five
days collection period was conducted during each period. The animals ate more roughages when concentrates were restricted.
Intake of DM (g/kg BW0.75
/day) was highest in sub-adults, followed by juveniles and adults. Apparent digestibility of crude
protein (CP), neutral detergent soluble (NDS), and supply of digestible energy (DE) was highest in juveniles, followed by sub-
adults and adults. Based upon the estimated metabolic fecal nitrogen (MFN) and calculated endogenous urinary nitrogen
(EUN) and dermal losses, minimum dietary CP required to meet maintenance requirement was estimated to be 6.12, 6.05, and
5.97% in juveniles, sub-adults, and adults, respectively. Restriction of concentrates resulted in decreased (P < 0.05)
digestibility of DM and GE, but the diet still supplied adequate amounts of DE and CP to fulfill estimated requirements of
energy and protein during the period of experimentation. Thus, the concentrates portion of the diets of captive Asian elephants
should be fed in a restricted way so as to reduce the intake of excessive calories and the potential risk of obesity.
Zoo Biol. 9999:1–11, 2014. © 2014 Wiley Periodicals, Inc.
Keywords: Asiatic elephants; intake; metabolic fecal nitrogen; protein utilization; energy restriction
INTRODUCTION
The Asian elephant (Elephas maximus) is categorized
as an endangered species by IUCN. It is also protected from
international trade by listing it in Appendix I of Convention
on International Trade in Endangered Species of Wild Fauna
and Flora [CITES, 2012]. In free range, Asian elephants are
generalist feeders and consume grasses, tree leaves, twigs,
shrubs, fruits, and roots of many different species [Steinheim
et al., 2005; Pradhan and Wegge, 2007; Joshi, 2009]. Their
feeding behaviour is influenced by season and availability of
food items. During wet season when the quality of grasses is
good, they are predominantly grazers. However, during the
Conflicts of interest: None.
Ã
Correspondence to: A. Das, Centre for Wildlife, IVRI, Izatnagar
243122, UP, India.
Email: drasitdas@rediffmail.com
Received 22 November 2013; Revised 27 October 2014; Accepted 17
November 2014
DOI: 10.1002/zoo.21194
Published online XX Month Year in Wiley Online Library
(wileyonlinelibrary.com).
© 2014 Wiley Periodicals, Inc.
Zoo Biology 9999 : 1–11 (2014)

2. dry season when the quality of grasses is inferior, they prefer
browsing to grazing [Sukumar, 2006; Pradhan et al., 2008].
In recent times, considerable attention has been paid on ex-
situ and in-situ conservation of Asian elephants. Proper
nutrition is fundamental not only for successful breeding, but
also for better health and welfare [Dierenfeld, 2006; Hatt and
Clauss, 2006; Veasey, 2006; Hermes et al., 2008]. However,
only limited information on feeding and nutrition of captive
Asian elephants is available. According to these, mean
retention time (MRT) of digesta is much lower in Asian
elephants as compared to other hindgut fermenting mega-
herbivores [Loehlein et al., 2003; Clauss et al., 2003b]. As
the digesta is retained for shorter period, they attain
comparatively lower digestibility of dry matter (DM) than
horses and rhinoceros [Hackenberger and Atkinson, 1982;
Clauss et al., 2003a; Das et al., 2014]. They eat for 16–20 h/d
and dry matter intake (DMI) may vary from 1.03% to 1.64%
of BW [Hackenberger and Atkinson, 1982; Foose, 1982;
Clauss et al., 2003a; Das et al., 2014]. They are hindgut
fermenters and the volatile fatty acids (VFA) produced in the
hindgut may meet 100% of their energy requirement [Jenson,
1986]. The amount and profile of VFA produced in the
hindgut of elephants were found to be similar to those of
horse [Clauss et al., 2003a].
The Nutrition Advisory Group (NAG) of Association
of Zoo and Aquariums (AZA) recommends that a diet
containing 8–10% CP, 0.3% Ca, 0.24% P, 50 ppm Fe,
10 ppm Cu, and 40 ppm Zn would be adequate for
maintenance of adult elephants [Ullrey, 1997]. Digestible
energy (DE) requirements of horse [Meyer and Coenen,
2002] and Indian rhinoceros have been estimated to be
143 kcal/kgBW0.75
/d [Clauss et al., 2005b], and are expected
to be similar in Asian elephants. In principle, roughage based
diet with little or no supplement should be adequate to meet
requirements for adult maintenance. Feeding restricted
amount of concentrates was beneficial to Indian rhinoceros
[Clauss et al., 2005b], tapir [Clauss et al., 2009b], and captive
Asian elephants [Ange et al., 2001] because it improved
faecal score, and decreased the threats of obesity and foot
lesions. However, a more cautious approach would be
required while formulating rations for growing animals
because nutrient requirements for juveniles and sub-adults
are considerably higher than those of adult Asian elephants
[Ullrey, 1997]. Free ranging elephants enjoy freedom of
selection of food items [Sivaganeshan, 1991] and they may
select forages supplying nutrients according to their require-
ments. In addition, Asian elephants also raid on crops, such
as peanut, wheat, millet, and black gram [Sukumar, 1989].
To compensate for a potential inadequacy of the roughage
offered some amounts of supplements may be added in the
diets of growing elephants. However, feeding of diets
containing higher proportion of concentrates may supply
excess of calories [Clauss et al., 2003a]. This coupled with
increased DMI may result in inappropriately fast growth
rates, which have been linked to skeletal deformities in
horses [Donabédian et al., 2006]. Feeding of the concentrates
portion of the diets in a restricted way would be particularly
beneficial to overcome such problems. However, indis-
criminate restriction of concentrates may result in inadequate
supply of energy and protein in the diets of growing
elephants. Thus, it is necessary to balance the ration
according to the need of a specific age group. Hence, this
experiment was conducted to study the effect of restriction of
concentrates on feed consumption, diet digestibility, and
nitrogen utilization in different age-groups of captive Asian
elephants.
MATERIALS AND METHODS
Experimental Site
This study was conducted in Assam State Zoological
Park, Guwahati, India situated at 26°11’N 91°44’E. During
1st to 30th January, 2009, the minimum and maximum
average temperature during the period of experimentation
was 9.8°C and 23.6°C, respectively. During that period the
site received 11.4 mm of rainfall.
Animals and Design of the Experiment
Arivazhagan and Sukumar [2008] classified Asian
elephants into four age groups namely calf (0–1 year),
juvenile (1–5 years), sub-adult (6–15 years), and adult (>15
years). Accordingly, 10 captive Asian elephants available at
Assam State Zoo were distributed into three groups:
juveniles (n ¼ 3, 2 M, 1 F; 1.6–3 years of age); sub-adults
(n ¼ 4, 3 M, 1 F; 8.6–9.6 years of age); and adults (n ¼ 3, 1 M,
2 F; 17–40 years of age). Two feeding trials of 10 day
adaptation and 5 day collection period were conducted on
each of the animals. During trial I, a diet containing higher
amount of concentrates (HC) was fed. The HC diet of
juvenile, sub-adult, and adult contained 22, 17, and 16% of
concentrates on DM basis, respectively. During trial II, the
animals were fed restricted amount of concentrates (RC) and
the RC diet of juvenile, sub-adult, and adult contained 11,
8.5, and 8% of concentrates on DM basis, respectively.
Management and feeding
All the elephants were apparently healthy. The female
elephants used in this study were neither lactating nor
pregnant. All the animals were dewormed with albandazole
(Cadila Pharmaceuticals Private limited, India) at 7.5 mg/kg
BW, one month prior to the beginning of the trial. Proper
managemental and sanitary guidelines as suggested by the
Central Zoo Authority were followed during the course of
experimentation [CZA, 2000]. Ample clean and fresh
drinking water was available to the animals at all times.
During the course of experimentation, all the animals
were housed in their open air enclosures with facilities for
individual feeding and collection of feces. The feces of
individual animal were collected separately and no animal
could eat another animals feeds. A concentrate mixture was
2 Das et al.
Zoo Biology

3. prepared by mixing boiled paddy (Oryza sativa), soaked
mung bean (Vigna radiata), and soaked gram (Cicer
arietinum) at 20:40:40 and was fed to all the animals.
Different ingredients of concentrate mixture of an individual
elephants were weighed, to which 50–100 g of common salt
and 20–50 g of mineral mixture (Agrimin, Virbac India) (Ca,
25.5%; P, 12.75%; Cu, 1200 ppm; Fe, 1500 ppm; Mn, 1500;
Zn, 9600 ppm; vitamin A, 7,00,000 IU; vitamin D3, 70,000
IU; vitamin E 250 ppm, niacin 1000 ppm) was added, mixed
thoroughly and made into balls of size appropriate for an
individual elephants. The amount of common salt and
mineral mixture varied according to the body weight of the
elephants. During trial I, the conventional zoo diets of
juveniles, sub-adults, and adult contained 22, 17, and 16% of
concentrates on dry matter (DM) basis, respectively. During
trial II, the amount of concentrate was reduced by 50%.
Besides, all the juveniles received banana (Musa paradi-
siaca) fruits at 1.7 kg per animal and the sub-adult and adult
elephants were offered measured amounts of cut branches of
Ficus bengalensis during both the periods. All animals also
received measured amounts of local grasses (a mixture of
Cynodon dactylon, Eleusine indica, Phragmite karka,
Cyperous rotundus, and other unidentifiable leaf blades
and vegetative parts), carrots (Daucus carota), sugarcane
(Saccharum officinarum) and banana leaves. In addition,
during both trial periods, banana stem and dal grass
(Hymenachne amplexicaulis) were fed at 20% in excess of
previous day’s intake i.e., ad libitum. All the animals were
fed according to the timeline listed in Table 1. Table 2
summarizes the DM, CP, NDF, and GE content of items
eaten by Asian elephants during the experimental periods.
The concentrate mixture contained more CP, GE, and less
NDF than other feed ingredients. Among the roughage
components, local grasses and tree leaves contained more
DM and CP than banana stems and dal grass. The BS and DG
were offered ad lib so that the animals could consume feed to
their maximum inherent potential.
Estimation of Intake and Digestibility
It is mention worthy that the only restricted item during
the trail II was the concentrates. However, other feed items
were also offered in measured amounts during both the trials.
All orts, and feces voided were collected in full, measured,
and sampled for estimation of intake and digestibility of
nutrients. Body measurements were taken on day 1, 2, 29,
and 30 of each trial to calculate body weight. Body weight
was calculated from the measurement of heart girth
according to Hile et al. [1997] using the following formula:
Body weight (kg) ¼ 18.0 Â Heart girth (cm) –3336
Analytical Techniques
Samples of feed, orts, and feces were dried in a hot-air
oven (Yorko Hot Air Oven, Yorko Scientific Industries, New
Delhi, India) at 100°C for 16 h to determine the DM content.
At the end of trial, each individual’s orts and feces were
pooled across the five day trial period. Each individual’s data
were pooled and then averaged over the number of replicates
within an age-class. Sub-samples of feed, feces, and orts
were dried in a hot-air oven at 50C for 4 d, ground to pass
through a 1 mm screen in a grinding mill (Retsch-Allee,
Haan, Germany) and stored at room temperature in air-tight
plastic containers (Tarsons Products, New Delhi, India) for
later analysis. The milled samples of feed, orts and feces and
were analyzed for crude protein (CP) according to the
method of AOAC [2005] and neutral detergent fiber (NDF)
according to the method of Van Soest et al. [1991]. Residual
ash was subtracted from NDF. Neutral detergent soluble
(NDS) was calculated by subtracting NDF from DM.
Residues of fecal samples after NDF determination were
analyzed for nitrogen (N). The fraction of N that was soluble
in NDS was calculated by subtracting N content of the NDF
residues from the total N content of the sample. Analysis of
gross energy (GE) content of feed and fecal samples was
done in a Ballistic Bomb Calorimeter (Model CBB 330,
Gallenkemp, London, UK) using benzoic acid as standard.
Calculation and Statistical Analysis
Metabolic fecal nitrogen (MFN) loss was estimated as
the fraction of fecal N which was soluble in neutral detergent
solution (NDS). True protein digestibility (TPD) was
estimated by making correction for the MFN losses from
total faecal N losses. Endogenous urinary nitrogen (EUN)
was assumed to be 140 mg/kgBW0.75
/d [Smuts, 1935].
Dermal losses of N was assumed to be 35 mg N/kg BW0.75
[Meyer, 1984]. Minimum CP requirement was calculated as
per the model of Robbins [1993].
TABLE 1. Timeline of feeding different feed items to the captive Asian elephants at Assam State Zoo, Guwahati, India
Time Feed items
9:00 Full quota of concentrates, banana (Musa paradisiaca) fruit, sugarcane (Saccharum officinarum) and carrots (Daucus carota).
9:30 Full quota of banana leaves.
10:0020% of the total quota of banana stems.
12:0020% of the total quota of banana stems.
15:00Total quota of local grasses (a mixture of Cynodon dactylon, Eleusine indica, Phragmite karka, Cyperous rotundus and other
unidentifiable leaf blades and vegetative parts) þ total quota of tree leaves (cut branches of Ficus bengalensis) þ 20% of the total
quota of banana stems þ 40% of the total quota of Dal grass (Hymenachne amplexicaulis).
18:0040% of the total quota of banana stems þ 60% of the total quota of Dal grass.
Restriction of Dietary Concentrates in Asian Elephants 3
Zoo Biology

4. CP % in diet ¼ {[(EUN þ dermal loss) þ MFN (DMI)
* 6.25]/DMI/TPD} * 100.
Where, EUN, endogenous urinary nitrogen; MFN,
metabolic fecal nitrogen; TPD, true protein digestibility (%);
DMI, dry matter intake (actual dry matter intake observed
during this experiment was used in this calculation).
Data obtained were analyzed using using Students “t”
test according to Snedecor and Cochran [1989] by using
SPSS software package, version 13 (SPSS, Chicago, IL,
USA) and differences were considered as statistically
significant at P < 0.05.
RESULTS
Feed Consumption and Nutrient Intake
Intake of banana stems was higher when restricted
amount of concentrates were fed. Restricting the amount of
concentrates did not result in significant change in overall
DMI because the reduced concentrate intake was met with
increased roughage intake (Table 3). The relative DMI (g/kg
BW 0.75
/d) (rDMI) was highest in sub-adults, followed by
juveniles and adults. Intake (g/kg BW0.75
/day) of CP and DE
was highest in juveniles, followed by sub-adults and adults
(Table 4). Digestibility of NDF was lower in juveniles,
followed by sub-adults and adults. In spite of this, overall
digestibility of DM and GE was significantly higher in
juveniles in comparison to sub-adults and adults. Reducing
the concentrates of conventional zoo diet by 50% resulted in
decreased (P < 0.05) digestibility of NDS, DM, and GE
(Table 4).
Intake and Utilization of N
Intake and apparent digestibility of N was highest in
sub-adults, followed by juveniles and adults (Table 5). Based
upon the endogenous losses, the minimum N requirement
was calculated to be 824.8, 775.2, and 587.5 mg/kgBW0.75
/d
in juveniles, sub-adults and adults, respectively (Table 5).
The minimum dietary CP required to fulfill this requirement
was calculated to be 6.12, 6.05, and 5.97% in the three
respective groups (Table 5). Total endogenous losses of N
per unit metabolic body mass were higher in juveniles,
followed by sub-adults, and adults. In spite of this, the
content of dietary CP required to fulfill maintenance
requirement was similar among the different age-group of
elephants largely because true protein digestibility was
higher in younger animals and they consumed more DMI.
Reducing 50% of the concentrates of the conventional zoo
diet of captive Asian elephants resulted in decreased
(P < 0.001) intake and apparent digestibility of N. However,
the restricted diets of juveniles, sub-adults, and adult Asian
elephants were able to meet their respective estimated
requirements including those for growth in juveniles and
sub-adults.
DISCUSSION
Feed Consumption, Diet Digestibility, and Energy
Utilization
The relative DMI (per unit metabolic body mass) was
higher in younger elephants. This was expected because in
addition to maintenance, juveniles and sub-adults require
nutrients to support growth [Ullrey, 1997]. According to
Loehlein et al. [2003], DMI in juvenile elephants could be as
high as 2% of BW. However, in adults it ranges from 1.03%
to 1.81% of BW and rarely exceeds 1.5% of BW [Clauss
et al., 2003a; Das et al., 2014]. The study of Aiken et al.
[1989] had shown that DMI in young and adult horses was
2.5 and 2.0% of BW, respectively. Higher DMI in younger
TABLE 2. Chemical composition of feed and forages consumed by different age-group of captive Asian elephants (Elephas
maximus) fed two different levels of concentrates
Feed and forages Nutrient content of the consumed diet
Measures BS DG TL BF LG CA BL SC CON Juveniles Sub-adults Adults
Trial 1 (High concentrates)
DM (%) 6.82 18.1 30.3 22.4 20.1 7.70 17.8 22.5 45.1 — — —
On % DM basis
CP (%) 5.02 8.83 14.3 6.01 10.4 6.82 18.5 3.42 28.5 14.3 Æ 0.46 13.03 Æ 0.14 13.01 Æ 0.13
NDF (%) 58.6 66.3 70.1 16.0 68.7 13.8 65.9 65.3 23.1 48.2 Æ 1.08 55.8 Æ 0.11 56.4 Æ 0.45
GE (kcal/kg DM) 3940 3640 3940 4125 3800 4120 3870 3970 4230 3950 Æ 22.0 3933 Æ 5.5 3958 Æ 10.0
Trial 2 (Restricted concentrate)
DM (%) 6.60 18.6 31.3 21.2 20.5 8.91 18.0 21.6 45.5 — — —
On % DM basis
CP (%) 5.71 8.72 13.1 6.20 10.3 7.01 17.9 3.52 28.6 11.5 Æ 0.03 11.0 Æ 0.03 11.3 Æ 0.16
NDF (%) 48.0 66.2 69.5 15.0 68.5 13.3 63.6 64.6 23.2 50.5 Æ 0.04 58.5 Æ 0.13 59.5 Æ 1.16
GE (kcal/kg DM) 3915 3600 3980 4020 3800 4000 3840 3910 4210 3843 Æ 28.3 3885 Æ 2.3 3927 Æ 13.4
BS, banana stem; DG, Dal grass; TL, tree leaves (cut branches of Ficus bengalensis); BF, banana fruit; LG, local grass (a mixture of
Cynodon dactylon, Eleusine indica, Phragmite karka, Cyperous rotundus, and other unidentifiable leaf blades and vegetative parts); CA,
carrot; BL, banana leaves; SC, sugarcane; CON, concentrates. kcal, kilocalorie; %, percentage; kg, kilogram; DM, dry matter; CP, crude
protein; NDF, neutral detergent fiber; GE, Gross energy.
4 Das et al.
Zoo Biology

5. horses than adult horses was also reported by Cymbaluk
[1990]. However, Earing [2011] pointed out that diets of the
younger horses contained less fiber than those of adult horses
and most of these variations could be due to nature of diets,
not due to age per se. In this study, the NDF content of the
diet of juveniles was lower than that of sub-adults and adults.
Thus, lower DMI in adults could partially be attributed to the
more fibrous nature of the diet. However, higher DMI in
juveniles was consistent on both restricted and conventional
zoo diet. Further, NDF content of sub-adult and adult diet
was similar, but rDMI was always higher in sub-adult as
compared to adult elephants. The results of this experiment
potentially demonstrate that higher DMI in juveniles and
sub-adult may not be solely due to lower fiber contents of
their diets but could also be due to their increased demands
for nutrients as compared to adult elephants.
Restricting the amount of concentrates did not result in
any significant change in DMI. When the concentrates of
conventional zoo diets were reduced by 50%, juveniles
increased the DMI from banana stem, whereas, the sub-adults
and adults increased the consumption of both banana stem and
tree leaves. As a result, DMI was not adversely affected by
restriction of concentrates in the diet during the period of
experimentation.Studies conductedearlierhaveindicatedthat
replacing the concentrate from a basal diet containing 20–30%
of concentrates decreased DMI in hindgut fermenting mega-
herbivores [Clauss et al., 2003a; Clauss et al., 2005b]. Such
differences in response could be due to the fact that in earlier
studies, concentrates were fully replaced, whereas, in this
experiment replacement was restricted to 50% only. The
results of the present experiment potentially demonstrate that
restricting the concentrates of conventional zoo diets by 50%
has no adverse impact on DMI in any age group of elephants
including the juveniles during the short period of
experimentation.
Juveniles were not able to digest NDF quite as
efficiently as sub-adult and adult elephants. Studies
conducted earlier indicated that the mean retention time
(MRT) of digesta was 21.6 and 32.1 h in elephants of 4 and
38 years, respectively [Loehlein et al., 2003]. As MRT is
TABLE 3. Consumption of different feed items (kg/d) in different age groups of captive Asian elephants (Elephas maximus) fed two
different levels of concentrates
Parameter Age-group
Dietary treatments
P-valueHC RC
Banana stem Juveniles 1.11x
Æ 0.38 2.45y
Æ 0.34 0.049
Sub-adults 8.05x
Æ 0.25 9.04y
Æ 0.14 0.014
Adults 13.1x
Æ 0.09 14.4y
Æ 0.79 0.050
Dal grass Juveniles 3.53 Æ 1.12 3.44 Æ 0.50 0.941
Sub-adults 9.69 Æ 0.66 9.19 Æ 0.14 0.489
Adults 7.99 Æ 1.30 8.36 Æ 0.19 0.790
Tree leaves Juveniles 0.00 0.00 —
Sub-adults 4.80 Æ 0.55 5.7 Æ 0.09 0.145
Adults 10.3 Æ 0.37 11.3 Æ 0.61 0.227
Banana fruits Juveniles 1.70 Æ 0.06 1.71 Æ 0.23 0.969
Sub-adults 0 0 —
Adults 0 0 —
Banana leaves Juveniles 1.57 Æ 0.11 1.24 Æ 0.17 0.266
Sub-adults 0.34 Æ 0.14 0.57 Æ 0.11 0.155
Adults 0.30 Æ 0.08 0.20 Æ 0.09 0.079
Local grasses Juveniles 1.57 Æ 0.11 1.24 Æ 0.17 0.184
Sub-adults 1.41 Æ 0.25 2.04 Æ 0.33 0.081
Adults 2.04 Æ 0.03 2.21 Æ 0.08 0.637
Carrots Juveniles 0.05 Æ 0.00 0.05 Æ 0.00 0.374
Sub-adults 0.09 Æ 0.00 0.09 Æ 0.00 1.000
Adults 0.11 Æ 0.00 0.11 Æ 0.01 1.000
Sugarcanes Juveniles 0.28 Æ 0.05 0.20 Æ 0.00 0.210
Sub-adults 0.78 Æ 0.09 0.76 Æ 0.03 0.806
Adults 0.48 Æ 0.03 0.40 Æ 0.03 0.119
Concentrates Juveniles 2.78y
Æ 0.41 1.42x
Æ 0.20 0.041
Sub-adults 5.11y
Æ 0.02 2.51x
Æ 0.04 0.001
Adults 6.48y
Æ 0.08 3.1x
Æ 0.17 0.001
Total DMI Juveniles 12.6 Æ 1.68 11.8 Æ 1.62 0.751
Sub-adults 30.4 Æ 0.28 29.9 Æ 0.46 0.387
Adults 41.0 Æ 1.73 40.2 Æ 1.91 0.784
Æ SEM, standard error of mean; DMI, average daily dry matter intake. Conventional zoo diet (HC) of juveniles, sub-adults and adults
contained 22, 17, and 16% of concentrates, respectively. The restricted diet (RC) contained 50% of the concentrate of the HC. x
xMeans
(Æ SEM) in the same row with different letters are significantly different (P < 0.05). y
yMeans (Æ SEM) in the same row with different
letters are significantly different (P < 0.05).
Restriction of Dietary Concentrates in Asian Elephants 5
Zoo Biology

6. positively correlated with digestibility of fiber [Hacken-
berger, 1987], digestibility of NDF was lower in juveniles,
followed by sub-adults and adults. A similar within species
trend in digestibility of acid detergent fiber was also observed
in Asian elephants fed hay based rations [Clauss et al.,
2003a]. In this experiment, NDF digestibility ranged from
23.0 to 35.9 (mean 32.3 Æ 0.77) %. Two studies conducted
earlier have reported that the digestibility of NDF was 20%
[Reichard et al., 1982] and 31% [Ullrey et al., 1979] in Asian
elephants fed hay based diets, similar to the range observed
in this study. On the other hand, digestibility of NDF ranged
from 29 to 64 (mean 46.3 Æ 1.81) % in horses [Cymbaluk,
1990] and 36.0 to 50.1 (mean 44.3 Æ 1.07) % in Indian
rhinoceros [Clauss et al., 2005a]. This inter-species
comparison demonstrates that the digestibility of fiber is
consistently lower in Asian elephants as compared to other
hindgut fermenters. It has been demonstrated that the larger
body size does not automatically confer digestive advantage
[Clauss et al., 2007; Clauss et al., 2009a; Steuer et al., 2014].
Clauss et al. [2007] suggested that a generalization of an
allometric relationship between body mass and mean
retention time (and hence digestibility) among different
species could be misleading. Hence, morpho-physiological
adaptation of digestive tract of the individual species should
also be considered [Clauss et al., 2007].
The proportion of concentrates in the diet of juveniles
was higher than that of sub-adults and adults. The cell
content of forages contain significant proportion of NSP
which are resistant to enzymatic digestion [Van Soest et al.,
1991]. On the other hand, cell contents of grains and fruits
mostly comprise of starch, protein, and lipid which are
efficiently digested by pancreatic enzymes of horses [De
Fombelle et al., 2004]. Pagan et al. [1998] had reported that
digestibility of non-structural carbohydrates in horse was
TABLE 4. Nutrient intake, diet digestibility, and energy utilization in different age groups of captive Asian elephants (Elephas
maximus) fed two different levels of concentrates
Parameter Age-group
Dietary treatments
P-valueHC RC
Nutrient intake (g/kg BW0.75
/d)
DMI Juveniles 102.6 Æ 2.86 99.7 Æ 2.80 0.637
Sub-adults 106 Æ 2.81 106 Æ 0.28 0.858
Adults 80.9 Æ 0.75 82.5 Æ 0.61 0.241
CP Juveniles 15.4y
Æ 0.58 11.5x
Æ 0.35 0.004
Sub-adults 14.1y
Æ 0.20 11.7x
Æ 0.35 <0.001
Adults 10.9y
Æ 0.15 9.1x
Æ 0.18 <0.001
NDF Juveniles 53.1 Æ 2.90 50.4 Æ 1.42 0.208
Sub-adults 62.8 Æ 1.62 61.9 Æ 1.55 0.778
Adults 48.3 Æ 0.54 48.2 Æ 0.40 0.994
DE (kcal/kg BW0.75
/d) Juveniles 228.4y
Æ 5.04 204.2x
Æ 5.52 0.032
Sub-adults 194.5y
Æ 6.76 175.0x
Æ 3.92 0.047
Adults 147.1y
Æ 1.72 134.6x
Æ 0.08 0.002
Digestibility of nutrients (%)
DM Juveniles 53.3 Æ 0.53 52.5 Æ 0.46 0.337
Sub-adults 42.7y
Æ 0.64 40.3x
Æ 0.72 0.045
Adults 41.2y
Æ 0.15 38.3x
Æ 0.23 <0.001
CP Juveniles 58.6y
Æ 1.25 45.9x
Æ 1.68 0.014
Sub-adults 50.6y
Æ 0.57 45.2x
Æ 0.90 0.002
Adults 49.1y
Æ 0.52 42.9x
Æ 1.58 0.021
NDF Juveniles 22.4 Æ 2.01 23.9 Æ 1.33 0.324
Sub-adults 27.4 Æ 0.37 29.3 Æ 0.71 0.550
Adults 31.9 Æ 1.04 34.2 Æ 0.68 0.198
GE Juveniles 53.7 Æ 0.63 53.3 Æ 0.45 0.658
Sub-adults 45.8y
Æ 0.55 42.6x
Æ 0.49 0.005
Adults 44.3y
Æ 0.44 41.6x
Æ 0.29 0.008
NDS Juveniles 83.6 Æ 1.43 80.5 Æ 1.28 0.173
Sub-adults 60.7y
Æ 2.61 55.4x
Æ 1.8 0.169
Adults 50.0y
Æ 1.9 44.1x
Æ 1.1 0.893
Average Body weight (kg) Juveniles 576 Æ 94.3 584 Æ 94.5 0.957
Sub-adults 1852 Æ 46.1 1860 Æ 45.7 0.906
Adults 3840 Æ 206.4 3841 Æ 207.1 0.995
Æ SEM, standard error of mean; kcal, kilocalorie; g, gram; kg, kilogram; BW, body weight; d, day; DMI, dry matter intake; CP, crude
protein; NDF, neutral detergent fiber; DE, Digestible energy; NDS, neutral detergent solubles. Conventional zoo diet (HC) of juveniles,
sub-adults and adults contained 22, 17, and 16% of concentrates, respectively. The restricted diet (RC) contained 50% of the concentrate of
the HC. x
xMeans (Æ SEM) in the same row with different letters are significantly different (P < 0.05). y
yMeans (Æ SEM) in the same row
with different letters are significantly different (P < 0.05).
6 Das et al.
Zoo Biology

7. 74.4% and 97.0% when they were fed forage only and
mixed diets, respectively. The diet of juveniles contained
proportionately more concentrates and less NSP. As
starches are more digestible than NSP, digestibility of
NDS was higher in juveniles. In addition, the diet of
juveniles contained up to 14% of banana, which mostly
comprises (up to 88% of) of soluble sugars that are nearly
completely ($98%) absorbed from the small intestine
[Englyst and Cummings, 1986]. This increase in digest-
ibility of NDS was also reflected in higher digestibility of
DM and GE in juveniles as compared to sub-adults and
adults. The proportion of concentrates was similar in the
diets of sub-adults and adults, yet sub-adults digested more
NDS than adults. It has been demonstrated earlier that foals
selectively retained digesta in the stomach for longer
period than mature horses [Alexander and Benzie, 1951].
The results of this experiment indicate that a similar
mechanism might be operational in younger elephants,
which also allows them to selectively derive more
digestible nutrients from easily digestible food fractions.
Digestibility of NDF was not significantly different
among the groups fed high and restricted amount of
concentrates. Supplementation of small quantities of con-
centrates to basal diets is reported to increase the digestibility
of NDF by supplying protein and other essential nutrients
required for fibrolytic microorganisms [Hussein et al., 2004].
In this present experiment, the restricted diet supplied an
adequate amount of protein for captive Asian elephants
[Ullrey, 1997]. Thus, it would be logical to assume that the
restricted amount of concentrate would supply adequate N
necessary for degradation of fiber by the microbes in the
hindgut of elephants. These findings are in accord with those
of Clauss et al. [2003a] who reported that NDF digestibility
was similar in Asian elephants fed either a hay only diet or a
hay diet supplemented with oat grains. Forages contain more
non-starch polysaccharides (NSP) than concentrates. Thus,
restricting the amount of concentrates increased the
proportion of NSP in the diet. Digestibility of NSP is lower
as compared to starches [Brøkner et al., 2012]. As a result,
replacing 50% of concentrates of the conventional zoo diet
resulted in decreased digestibility of NDS. Consequently,
apparent digestibility of DM and GE was lower in adult and
sub-adult elephants fed restricted amount of concentrates.
Similarly, Clauss et al. [2003a] reported that digestibility of
TABLE 5. Intake and utilization of N in different age groups of captive Asian elephants (Elephas maximus) fed two different levels
of concentrates
Parameter Age-group
Dietary treatments
P-valueHC RC
Intake and utilization of N (mg/kg BW0.75
/d)
Intake Juveniles 2466y
Æ 92.1 1837x
Æ 55.4 0.004
Sub-adults 2249y
Æ 33.5 1870x
Æ 50.3 <0.001
Adults 1750y
Æ 77.5 1463x
Æ 12.6s <0.001
Absorbed Juveniles 1443y
Æ 48.9 919x
Æ 53.0 0.002
Sub-adults 1138y
Æ 15.5 846x
Æ 37.5 <0.001
Adults 860y
Æ 50.3 628x
Æ 19.6 <0.001
MFN losses Juveniles 714.5y
Æ 98.2 585.1x
Æ 25.4 0.039
Sub-adults 627.2y
Æ 19.8 573.2x
Æ 19.3 0.037
Adults 445.6y
Æ 30.2 379.4x
Æ 22.6 0.047
EUN losses Juveniles 140 140 —
Sub-adults 140 140 —
Adults 140 140 —
Dermal losses Juveniles 35.0 35.0 —
Sub-adults 35.0 35.0 —
Adults 35.0 35.0 —
Total endogenous losses Juveniles 889.5y
Æ 98.3 760.1x
Æ 8.90 0.038
Sub-adults 802.1y
Æ 19.82 748.2x
Æ 19.32 0.037
Adults 620.6y
Æ 16.38 554.4x
Æ 22.66 0.048
Minimum dietary Crude protein (%) to fulfill requirements for
Maintenance Juveniles 6.26 Æ 0.43 5.98 Æ 0.13 0.580
Sub-adults 6.26 Æ 0.154 5.84 Æ 0.240 0.190
Adults 6.10 Æ 0.083 5.83 Æ 0.341 0.537
Growth Juveniles 8.84 Æ 0.0.17 9.18 Æ 0.53 0.710
Sub-adults 7.47 Æ 0.27 7.21 Æ 0.18 0.458
Adults — — —
Æ SEM, standard error of mean; N, nitrogen; mg/kg, milligram per kilogram; g/d, gram per day; CP, crude protein; MFN, metabolic faecal
nitrogen; EUN, endogenous urinary nitrogen. Conventional zoo diet (HC) of juveniles, sub-adults and adults contained 22, 17, and 16% of
concentrates, respectively. The restricted diet (RC) contained 50% of the concentrate of the HC. x
xMeans (Æ SEM) in the same row with
different letters are significantly different (P < 0.05). y
yMeans (Æ SEM) in the same row with different letters are significantly different
(P < 0.05).
Restriction of Dietary Concentrates in Asian Elephants 7
Zoo Biology

8. DM and GE was lower in elephants fed hay only diet as
compared to those fed mixed diets containing hay and
pelleted feed. It is apparent that the restriction of concentrates
in the diet would result in decreased digestibility of DM in
adult and sub-adult elephants. A similar trend was also
observed in juveniles. It is acknowledged that the conven-
tional juvenile diet contained 14% banana fruit which was
not replaced. Thus, conventional and restricted diets of
juveniles comprised 36% and 25% of non-fibrous feedstuff,
respectively. Therefore, the magnitude of effective restric-
tion was 31%, not 50% as in case of sub-adult and adult
elephants. This magnitude of restriction was probably not
enough to cause any significant change in the digestibility of
DM and GE in juveniles. In this experiment, the apparent
digestibility of DM ranged from 38.6 to 54.3%. The highest
apparent DM digestibility value of 54.3% was recorded in
juveniles fed on conventional zoo diet which was close to the
value of 53.3% reported in captive Asian elephants fed on
grass hay based diet [Hackenberger and Atkinson, 1982]. It
is, however, emphasized that the apparent digestibility of
DM in adult Asian elephants as observed in this and other
study [Clauss et al., 2003a] was consistently lower than that
observed in horses [Fonnesbeck et al., 1967].
Precise energy requirements for different life stages of
captive Asian elephants are not known. The domestic horse
has been advocated as a model for Asian elephants [Oftedal
et al., 1996; Ullrey, 1997]. Energy requirement for horses
were successfully used to test the ration adequacy of Indian
rhinoceros. Hence, we used energy requirement of horses to
test the diet adequacy. The digestible energy (DE) require-
ment of horses has been estimated to be 143 kcal/kgBW0.75
/d
[Meyer and Coenen, 2002]. It is obvious that an additional
amount of DE would be required to support growth in
juvenile and sub-adult elephants. The average daily weight
gain in wild Asian elephants ranged from 301–410 g/d and
they attained 1725 kg of body weight at an age of 11–15 years
[Sukumar, 1989]. According to NRC [1989], for each kg of
body mass gain, a long yearling horse requires 18.4 Mcal DE
in addition to its maintenance requirement. Assuming that
composition of gain and efficiency of utilization of DE is
similar between horses and Asian elephants, it was calculated
that an elephants growing at 410 g/d would require 7544 kcal
DE in addition to its maintenance requirement. By adding
this value to their respective requirement for maintenance,
total DE requirements were 209 and 170 kcal DE/kgBW0.75
/
d for juvenile and sub-adult elephants, respectively. The
conventional zoo diets of juveniles, sub-adults, and adults
supplied 8, 14, and 3% DE in excess of their respective
requirement. An adverse impact of feeding excessive
calories has earlier been demonstrated in tapir [Clauss
et al., 2009b], Indian rhinoceros [Clauss et al., 2005b], and
adult Asian elephants [Ange et al., 2001]. The results of the
present experiment indicate that DE supply in captive
juvenile and sub-adult elephants fed a conventional zoo diet
were higher than their requirement. The average body weight
of the elephants as observed in this study was higher than that
recorded for wild elephants of similar age [Sukumar, 1989].
Attaining an appropriate body weight is fundamental for
successful breeding, and underweight animals may fail to
breed [Khyne et al., 1997]. On the other hand, fast growing
animals have shorter reproductive life and are prone to
stillbirth [Kurt and Hartl, 1995]. In addition, obesity can lead
to metabolic changes that impair fertility [Mason and
Veasey, 2010].Thus, regular monitoring of body weight
and adjustment of feeding regimes are necessary to ensure
optimum health and reproduction. When 50% of the
concentrates of conventional zoo diet was reduced, DE
intake was À 2, 2.8, and À 5.9% in excess/deficit of respective
requirements of juveniles, sub-adults, and adults, respec-
tively. Apparently, the restricted diets of juveniles and adults
were marginally deficient in energy supply. However, it is of
interest to note that even at this level of feeding, juveniles,
sub-adults, and adults were gaining body mass at 622, 508,
and 84 g/d. It seems that the DE requirement of Asian
elephants could be lower than those of horses. Research
conducted earlier indicated that adult semi-captive Asian
elephants performing 6 h of outdoor activity were able to
maintain body mass when diet supplied 142 kcal DE/
kgBW0.75
/d [Das et al., 2014]. As zoo kept Asian elephants
performed no outdoor activity their DE requirement could be
further less. The results of this short term feeding trial
potentially demonstrate that feeding restricted amount of
concentrates is beneficial not only for adults, but also for
juveniles and sub-adult Asian elephants. However, the
impact of concentrate restriction on energy supply needs to
be ascertained in long term feeding trial involving
more animals.
Intake and Utilization of N
In this experiment, the apparent and true digestibility
of CP was higher in juveniles than sub-adult and adult Asian
elephants. The higher apparent and true digestibility of CP in
juveniles could be due to the fact that their diet contained
higher proportion of non-fibrous components than sub-adults
and adults. While feeding on a conventional zoo diet about,
44, 36, and 35% of the total protein of juvenile, sub-adult,
and adult diet was contributed by non-fibrous components.
Contribution of non-fibrous components to total dietary CP
intake was 30, 22, and 20% in the three respective groups
when they were fed on restricted amount of concentrates.
Only 37% of the N from hay was digested in the stomach and
small intestine of horses [Gibbs et al., 1988], whereas, 72%
of N from soybean meal was digested in the small intestine of
horse [Farley et al., 1995]. Digestion of protein from grains is
considerably higher than that of forage origin [Graham-
Thiers and Bowen, 2011]. As the diet of juvenile contained a
higher proportion of grains and also contained fruits, the
digestibility of protein was higher in juveniles than sub-adult
and adult Asian elephants. On the other hand, the diets of the
sub-adult and adult elephants contained lower proportion of
concentrates. A large proportion of CP was contributed by
8 Das et al.
Zoo Biology

9. grasses, tree fodder, and some other minor food items in the
diets of sub-adults and adults. Protein bound to forage cell
walls are poorly utilized. Furthermore, the diet of sub-adults
and adults also contained tree fodders which are known to
impair protein utilization due to presence of condensed
tannins [Schofield et al., 2001]. All these factors might have
contributed to lower digestibility of CP in sub-adults and
adults as compared to juveniles. However, digestibility of CP
was higher in sub-adults than adults Asian elephants, in spite
of similar proportion of grasses and tree forages. On per kg
metabolic BW basis, sub-adult elephants consumed 29%
more CP than adult elephants. The difference in CP intake
largely explained the observed differences in apparent CP
digestibility between sub-adult and adult Asian elephants.
Similarly, increased CP intake resulted in increased apparent
digestibility of CP in horses [Crozier et al., 1997]. Restriction
of 50% of the concentrate of conventional zoo diet resulted in
decreased CP content of the diet. Generally, apparent
digestibility of CP increases with increased level of CP in
the diet, because MFN losses are dependent on DM intake
[Blaxter and Mitchell, 1948]. As a result, apparent
digestibility of CP was higher in elephants fed conventional
zoo diet as compared to those fed restricted diet.
On per kg metabolic BW basis, MFN losses were
higher in juveniles than those of sub-adult and adult Asian
elephants. In herbivores, MFN (non-NDF bound N) is mostly
of bacterial origin [Clauss et al., 2005a]. It has earlier been
established in 48 species of captive herbivores that feeding of
higher quality feed will enhance the growth of gastro-
intestinal flora [Schwarm et al., 2009]. Increased proportion
of concentrates in the diet of juveniles as compared to those
of sub-adult and adult Asian elephants might have increased
the activity of bacteria in the hind gut resulting in increased
MFN losses. Restriction of 50% of the concentrate of
conventional zoo diet might have decreased the activity of
bacteria resulting in decreased MFN losses. In this experi-
ment MFN losses ranged from 334 to 886 (mean
550 Æ 28.6 mg/ kg BW 075
/d), which was higher than the
value of 323 mg/ kg BW 075
/d reported for Indian rhinoceros
[Clauss et al., 2005a]. However, other studies have indicated
higher MFN losses of 9.1 g/ kg DMI. Considering that a
growing horse weighing 300 kg would consume 4.5 kg of
DM that would translate into MFN losses of 568 mg/kg
BW075
/d in horses [Gibbs et al., 1988]. Review of literature
indicates that the exact determination endogenous/metabolic
losses of N are difficult and to establish a reliable base for
inter-specific comparisons is challenging [Clauss et al.,
2005a; Schwarm et al., 2009]. The results of this experiment
indicate that MFN losses in captive Asian elephants fed
conventional zoo diets are influenced by age, level of intake,
and proportion of concentrates in the diet.
On the basis of estimated MFN and calculated EUN
and dermal losses, total endogenous losses ranged from 748–
1061, 706–837, and 509–653 mg/ kg BW0.75
in juvenile, sub-
adult, and adult, respectively. These estimates indicate that a
diet containing 5.59–6.70, 5.48–6.51, and 5.05–6.20% of CP
would be adequate to fulfill maintenance requirement of CP
in juveniles, sub-adults, and adults Asian elephants fed zoo
diets (Table 5). It is to be noted that even though the
endogenous losses were higher in younger animals than
adults, a diet containing similar amount of dietary CP would
be able to fulfill maintenance requirement because the DMI
was higher in younger animals. However, growing animals
will require much higher protein to sustain growth.
According to INRA [1990], for sustaining 410 g of ADG,
185 g of MADC (maiteres azotees digestibles chevals; which
is close to DCP in meaning) would be required. In other
words, 344 and 387 g of CP would be required for sustain
410 g of ADG in juveniles and sub-adult Asian elephants fed
zoo diets. Adding this requirement to maintenance require-
ment, total CP requirement for juvenile and sub adult would
be 8.3 –10.6 and 7.1 –8.7 g/kg BW0.75
/d, respectively. A diet
containing 8.1–10.1 and 7.3 – 8.2% CP would be able to meet
estimated requirements when DMI ranged from 1.99– 2.38
and 1.51–1.80% of BW, in juveniles and sub-adult,
respectively. The results of the present experiment showed
that a diet containing 12% CP would be adequate to meet
requirement for juvenile Asian elephants fed zoo diets. Thus,
the recommendation of NAG could be safely followed. All
the diets including the restricted ones were able to supply
adequate amount of CP. The conventional zoo diet of
juveniles, sub-adults, and adults contained 14.3, 13.03, and
13.01% CP, which was 19, 8.6, and 63% in excess of
requirement. The restricted diet of juvenile and sub-adult
supplied 96% and 92% of the requirement recommended by
NAG [Ullrey, 1997]. During the period of restricted feeding,
all the growing elephants were gaining body mass at a rate
higher than 301–410 g/d observed in wild elephants
[Sukumar, 1989] and no problem regarding general health
of the animals was observed. Thus, such marginal deficiency
of protein may not cause any adverse impact on nutrition and
health of the animals. Further, our estimates indicate that CP
requirement for sub-adult elephants could be considerably
lower than the 12% recommended by NAG [Ullrey, 1997].
The restricted diet of adults, however, supplied 41% more CP
than requirement. Thus, it would be desirable to restrict the
amount of concentrates in the diet of captive Asian elephants.
CONCLUSIONS
1. The amounts of DE and CP ingested by Asian elephants on
conventional zoo diets indicate that excess energy and
protein intakes do occur.
2. Restriction of 50% of the concentrate of conventional zoo
diet resulted in decreased digestibility of DM, CP, and GE,
but the diet still met estimated requirements of energy and
protein in all age-groups of elephants during the period of
experimentation. Thus, the concentrates portion of the diets
of captive Asian elephants should be fed in a restricted way
so as to reduce the intake of excessive calories and the
potential risk of obesity.
Restriction of Dietary Concentrates in Asian Elephants 9
Zoo Biology

10. 3. Data on true digestibility and endogenous losses of N are
novel and can be useful for formulation of age-specific ration
for captive Asian elephants.
ACKNOWLEDGMENTS
The authors wish to thank the Director, Indian
Veterinary Research Institute for providing necessary
facilities to conduct the present study. Our thanks are also
due to the Member Secretary, Central Zoo Authority of India,
and the Director of Assam State Zoo, Guwahati for providing
all necessary support during the course of the feeding trials.
We specially acknowledge the engaged support provided by
the elephant keepers of Assam State Zoo including Niranjan
Boro, Bipin Deka, Pramod Deka and Romiz Ali. We thank
the anonymous reviewers and Marcus Clauss for their
comments.
REFERENCES
Aiken GE, Potter GD, Conrad BE, Evans JW. 1989. Voluntary intake and
digestion of coastal Bermuda grass hay by yearling and mature horses. Eq
Nutr Physiol Symp 9:262–263.
Alexander F, Benzie D. 1951. A radiological study of the digestive system of
foal. Quarterly J Exp Physiol Cog Med Sci 36:213–217.
Ange K, Crissey SD, Doyle C, Lance K, Hintz H. 2001. A survey of African
(Loxodonta africana) and Asian (Elephas maximus) elephants diets and
measured body dimensions compared to their estimated nutrient require-
ments. N A G 5–14.
AOAC (Association of Official Analytical Chemists). 2005. Official
Methods of Analysis of AOAC International. 18th Ed. Gaithersburg,
MD: AOAC International.
Arivazhagan C, Sukumar R. 2008. Constructing age structures of Asian
elephants populations: a comparison of two field methods of age
estimation. Gajah 29:11–16.
Blaxter KL, Mitchell HH. 1948. The factorization of the protein require-
ments of ruminants and of the protein values of fe eds with particular
reference to the significance of the metabolic fecal nitrogen. J Anim Sci
7:351.
Brøkner C, Bach Knudsen KE, Karaman I, Eybye KL, Tauson AH. 2012.
Chemical and physicochemical characterisation of various horse feed
ingredients. Anim Feed Sci Technol 177:86–97.
CITES. 2012. Appendices I, II and III. cites. org. CITES. Retrieved 13.
February 2012.
Clauss M, Loehlein W, Kienzle E, Wiesner H. 2003. Studies on feed
digestibilities in captive Asian elephants (Elephas maximus). J Anim
Physiol Anim Nutr 87:160–173.
Clauss M, Frey R, Kiefer B, et al. 2003b. The maximum attainable body size
of herbivorous mammals: morphophysiological constraints on foregut,
and adaptations of hindgut fermenters. Oecologia 136:14–27.
Clauss M, Polster C, Kienzle E, et al. 2005a. Studies on digestive physiology
and feed digestibilities in captive Indian rhinoceros (Rhinoceros
unicornis). J Anim Physiol Anim Nutr 89:229–237.
Clauss M, Polster C, Kienzle E, et al. 2005b. Energy and mineral nutrition
and water intake in the captive Indian rhinoceros (Rhinoceros unicornis).
Zoo Biol 24:1–14.
Clauss M, Schwarm A, Ortmann S, et al. 2007. A case of non-scaling in
mammalian physiology? Body size, digestive capacity, food intake, and
ingesta passage in mammalian herbivores. Comp Biochem Physiol Part A
Mol Inte Physiol 148:249–265.
Clauss M, Nunn C, Fritz J, Hummel J. 2009a. Evidence for a tradeoff
between retention time and chewing efficiency in large mammalian
herbivores. Comp Biochem Physiol Part A Mol Inte Physiol 154:376–382.
Clauss M, Wilkins T, Hartley A, Hatt J-M. 2009b. Diet composition, food
intake, body condition, and fecal consistency in captive tapirs (Tapirus
spp.) in UK collections. Zoo Biol 28:279–291.
Crozier JA, Allen VE, Jack NE, Fontenot JP, Cochran MA. 1997.
Digestibility, apparent mineral absorption and voluntary intake by horses
fed alfalfa, tall fescue and Caucasian bluestem. J Anim Sci 75:1651–1658.
Cymbaluk NF. 1990. Cold housing effect on growth and nutrient demands of
young horses. J Anim Sci 68:3152–3162.
CZA (Central Zoo authority). 2000. Zoos- Instrument for Conservation.
New Delhi, India: CZA 1–42.
Das A, Saini M, Katole S, et al. 2014. Effect of feeding different levels of
wheat roti on nutrient utilization and blood metabolite profile in semi-
captive Asian elephants (Elephas maximus). J Anim Physiol Anim Nutr
DOI: 10.1111/jpn.12200.
De Fombelle A, Viego L, Drougal C, Julliand D. 2004. Effect of diet
composition and feeding pattern on the pre-cecal digestibility of starches
from diverse botanical origin measured with the mobile nylon bag
techniques in horses. J Anim Sci 82:3625–3634.
Dierenfeld ES. 2006. Nutrition. In: Fowler ME, Mikota SK, editor., Biology,
medicine, and surgery of elephants. Balckweel Publishing Ltd: Oxford,
UK. p 57–66.
Donabédian M, Fleurance G, Robert C, et al. 2006. Effect of fast vs.
moderate growth rate related to nutrient intake on developmental
orthopaedic disease in the horse. Anim Res 55:471–486.
2011. Earing JE. Comparison of digestive function in young and mature
horses. PhD. Thesis. Lexington: University of Kentucky.
Englyst HN, Cummings JH. 1986. Digestion of the carbohydrates of banana
(Musa paradisiaca sapientum) in the human small intestine. Am J Cl Nutr
44:42–50.
Farley EB, Potter GD, Gibbs PG, Schumacher J, Murray-Gerzik M. 1995.
Digestion of soybean meal protein in the equine small and large intestine at
various levels of intake. J Eq Vet Sci 9:391–397.
Fonnesbeck PV, Lydmann, der Noot GW, Symons LD. 1967. Digestibility
of the proximate nutrients of forage by horses. J Anim Sci 26:1039–1045.
Foose TJ. 1982. Tropic strategies of ruminant versus non-ruminant
ungulates. PhD Dissertation. Chicago: University of Illinois.
Gibbs PG, Potter GD, Schelling GT, Kreider JL, Boyd CL. 1988. Digestion
of hay protein in different segments of the equine digestive tract. J Anim
Sci 66:400–406.
Graham-Thiers PM, Bowen LK. 2011. Effect of protein source on nitrogen
balance and plasma amino acids in exercising horses. J Anim Sci 89:729–
735.
Hackenberger MK, Atkinson JL. 1982. Digestibility studies with captive
Asiatic and African elephants: Proceedings of the AAZPA Regional
Conference. Wheeling. WV: American Association of Zoological Parks
and Aquariums 129–137.
1987. Hackenberger MK. Diet digestibilities and ingesta transit times of
captive Asian and African elephants. MS Thesis. Guelph: University of
Guelph.
Hatt J-M, Clauss M. 2006. Feeding Asian and African elephants Elephas
maximus and Loxodonta africana in captivity. Int Zoo Yb 40:88–95.
Hermes R, Saragusty J, Schaftenaar W, et al. 2008. Obstetrics in elephants.
Theriogenol 70:131–144.
Hile ME, Hintz HF, Erb HN. 1997. Predicting body weight from body
measurements in Asian elephants (Elephas maximus). J Zoo Wildl Med
28:424–427.
Hussein HS, Vogedes LA, Fernandez GCJ, Frankeny RL. 2004. Effects of
cereal grain supplementation on apparent digestibility of nutrients and
concentrations of fermentation end-products in the faeces and serum of
horses consuming alfalfa cubes. J Anim Sci 82:1986.
INRA. 1990. In: Martin-Rosset W, editor., L’alimentation des chevaux.
Versailles: INRA Publications. p 23.
Jenson BB. 1986. Methanogensis in non-ruminant livestock. Environ Monit
Assess 42:99–112.
Joshi R. 2009. Asian elephants’s Elephas maximus behaviour in the Rajaji
National Park, north-west India: eight years with Asian elephants. Nat Sci
7:49–77.
Khyne UM, Kurt F, Thaung N, Aung M. 1997. Fortpflanzung bei
rbeitselefanten in Myanmar. In: Schaller K, Ziegler C, editor., Elefant
und Mensch. Workshop zur Elefantenhaltung in Zoo und Zirkus. p 26–37.
Kurt F, Hartl GB. 1995. Asian elephants (Elephas maximus) in captivity - A
challenge for zoo biological research. In: Ganslosser U, Hodges JK,
Kaumanns W, editor., Research and captive propagation. p 310–326.
Loehlein W, Kienzle E, Wiesner H, Clauss M. 2003. Investigations on the
use of chromium oxide as an inert external marker in captive Asian
elephants (Elephas maximus): passage and recovery rates. In: Fidgett A,
10 Das et al.
Zoo Biology

11. Clauss M, Ganslosser U, Hatt JM, Nijboer J, editor., Zoo Animal Nutrition
2. p 223–232.
Mason GJ, Veasey JS. 2010. What do population level welfare indices
suggest about the well-being of zoo elephants. Zoo Biol 29:256–273.
2002. Meyer H, Coenen M. . Pferdefuetterung. 4th edition. Berlin : Paul
Parey Verlag, p. 44.
Meyer H. 1984. Intestinaler N-stoffwechsel, endogener N-verlust und N-
bedarf ausgewachsener pferde. Übersichten Tierernährung 12:251–271.
1989. NRC (National Research Council). . Nutrient Requirements of
Horses. 5th Rev. Ed. Washington, DC: National Academy Press.
Oftedal OT, Baer DJ, Allen ME. 1996. The feeding and nutrition of
herbivores. In: Kleimann DG, Allen ME, Thompson KV, Lumpkin S,
editor., Wild Mammals in Captivity: Principles and Techniques. Chicago,
IL: University of Chicago Press. p 129–138.
Pagan JD, Harris P, Brewster-Barnes T, Duren SE, Jackson SG. 1998.
Exercise affects digestibility and rate of passage of all-forage and mixed
diets in thoroughbred horses. J Nutr 128:2704S–2707S.
Pradhan NMB, Wegge P. 2007. Dry season habitat selection by a
recolonizing population of Asian elephants (Elephas maximus) in lowland
Nepal. Acta Theriologica 52:205–214.
Pradhan NMB, Wegge P, Moe SR, Shrestha AK. 2008. Feeding ecology of
two endangered sympatric megaherbivores: Asian elephants Elephas
maximus and greater one-horned rhinoceros Rhinoceros unicornis in
lowland Nepal. Wildl Biol 14:147–154.
Reichard TA, Ullrey DE, Robinson PT. 1982. Nutritional implications of
dental problems in elephants: proceedings of the Second Annual Dr Scholl
Nutrition Conference on the Nutrition of Captive Wild Animals. Chicago:
Lincoln Park Zoological Society 63–67.
Robbins CT. 1993. Wildlife feeding and nutrition. 2nd ed. San Diego:
Academic Press p 352.
Schofield P, Mbugua DM, Pell AN. 2001. Analysis of condensed tannins: a
review. Anim Feed Sci Technol 91:21–40.
Schwarm A, Schweigert M, Ortmann S, et al. 2009. No easy solution for the
fractionation of faecal nitrogen in captive wild herbivores: results of a pilot
study. J Anim Physiol Anim Nutr 93:596–605.
1991. Sivaganeshan N. Ecology and Conservation of Asian elephants
(Elephas maximus) with special reference to the habitat utilization in
Mudumalai Wildlife Sanctuary, Tamilnadu, South India. Ph.D. Thesis.
Tiruchirapalli, India: Bharathidasan University.
Smuts DB. 1935. The relation between the basal metabolism and the
endogenous nitrogen metabolism, with particular reference to the
estimation of the maintenance requirement of protein. J Nutr 9:403–433.
Snedecor GW, Cochran WG. 1989. Statistical Methods. Ames: Iowa State
University Press 503.
Steinheim G, Wegge P, Fjellstad JI, Jnawali SR, Weladji RB. 2005. Dry
season diets and habitat use of sympatric Asian elephants (Elephas
maximus) and greater one-horned rhinoceros (Rhinoceros unicornis) in
Nepal. J Zool 265:377–385.
Steuer P, Südekum K-H, Tütken T, et al. 2014. Does body mass convey a digestive
advantage for large herbivores? Funct Ecol doi: 10.1111/1365–2435.12275.
Sukumar R. 1989. The Asian Elephants: Ecology and Management.
Cambridge: Cambridge University Press.
Sukumar R. 2006. A brief review of the status, distribution and biology of
wild Asian elephants. Int Zoo Yb 40:1–8.
Ullrey DE. 1997. Hay quality evaluation. Nutrition Advisory Group
Handbook Fact Sheet 1:1–10.
Ullrey DE, Robinson PT, Whetter PA. 1979. Comparative digestibility
studies with zoo herbivores. Proceedings of the Annual Conference.
Denver: American Association of Zoo Veterinarians 120–121a.
Van Soest PJ, Robertson JB, Lewis BA. 1991. Methods for dietary fiber,
neutral detergent fiber, and nonstarch polysaccharides in relation to animal
nutrition. J Dairy Sci 74:3583–3587.
Veasey J. 2006. Concepts in the care and welfare of captive elephants. Int
Zoo Yb 40:63–69.
Restriction of Dietary Concentrates in Asian Elephants 11
Zoo Biology