The feeding of rhinoceros in captivityM. CLAUSS & J.-M. HATTDivision of Zoo Animals and Exotic Pets, Vetsuisse Faculty, University of Zurich,Winterthurerstrasse 260, 8057 Zurich, SwitzerlandE-mail: [email protected]
Rhinoceros are large herbivores that are adapted forgaining energy from the fermentation of fibrousplant material. In this paper we address issues ofoversupplementation of energy (leading to obesity)and minerals (particularly iron in Black rhinocerosDiceros bicornis), outline a diet design that relies onforage as the staple component with a reduction inuse of pelleted compound feeds and give suggestionsfor supplement provision. Acquisition of adequateroughage is probably the most important step in thefeeding management of large herbivores and shouldbe regarded and organized accordingly. Ration cal-culation must be an integral part of diet design toavoid the imbalances that are currently observed,especially in relation to mineral provision. The useof grain or grain products in pelleted compoundfeeds is largely discouraged.
Key-words: Asian rhinoceros, Black rhinoceros,browse, hay, nutrition, obesity, pelleted compoundfeed, protein, White rhinoceros
Rhinoceros nutrition has been reviewedby Dierenfeld (1995, 1996, 1999) and inthis article we aim to expand on thosereviews, without duplicating the informa-tion. Four rhinoceros species are main-tained in captivity: the White rhinocerosCeratotherium simum, Asian rhinocerosRhinoceros unicornis, Black rhinocerosDiceros bicornis and Sumatran rhinocerosDicerorhinus sumatrensis. At time ofwriting, few facilities maintain Sumatranrhinoceros outside their native countryand, therefore, the feeding ofD. sumatrensis is not addressed specifi-cally in this review, although the speciescan be expected to have similar nutritionalrequirements to the Black rhinoceros.
Rhinoceros species can be classified asstrict browsers (Black rhinoceros), andstrict (White rhinoceros) or less strict(Asian rhinoceros) grazers (Laurie et al.,
1982; Clauss, Castell et al., in press a).The Asian rhinoceros is often termed a‘mixed feeder’, owing to observations ofbrowse and fruit ingestion in the wild (e.g.Owen-Smith, 1988). From an ecologicalpoint of view, this is correct; however,from a husbandry point of view classifi-cation as a mixed feeder may erroneouslyencourage the provision of an increasedproportion of concentrates or fruits. Inthe wild, the diet of Asian rhinoceros con-sists of 70–89% grasses. Dinerstein &Wemmer (1988) report a maximum intakeof 5·1 kg of Trewia nudiflora fruit per dayduring the monsoon season, with a drymatter (DM) content of c. 16%. Thisresults in a DM intake from fruit pulp of�820 g and, assuming a total daily DMintake of 1·5% of body mass in a 2 tonneAsian rhinoceros, T. nudiflora fruitswould thus account for �3% of the totaldaily DM intake. This finding and the factthat wild fruits do not resemble commer-cial fruits usually provided for animals inzoos (Oftedal & Allen, 1996), emphasizethat offering fruits to Asian rhinoceros incaptivity cannot be justified by chanceobservations of their natural diet. Thenatural diet of any rhinoceros species ischaracterized by a high-fibre and low-to-moderate protein content (Table 1). Theprotein content of forage for Black rhino-ceros (strict browsers) is generally higherthan that of the grazing species. It shouldbe noted that this increase in protein isnot accompanied by a reduction in fibrecontent. It is generally recognized thatcrude protein measurements in browse donot reflect available protein, as some part
198 ELEPHANTS AND RHINOCEROS
species cp cf source
White rhinocerosCeratotherium simum 5 36 Kiefer et al. (2003)
Asian rhinocerosRhinoceros unicornis 5 40 Duke & Atchley (1986); data for staple diet
item, grass Sacchareum spontaneum
Black rhinocerosDiceros bicornis 6–18 30–45 Castell (2005); collated data
Table 1. Crude protein (CP) and crude fibre (CF) content of natural forages of free-ranging rhinoceros species.Values in % dry matter.
of the nitrogen in browse may stem from,or may be bound to, plant secondarycompounds (Oftedal, 1991). Therefore,high measurements of crude protein in thenatural diet of browsing species need notnecessarily translate into higher proteinrequirements as compared to grazers.
The anatomy of the digestive system inrhinoceros species roughly resembles thatof horses: rhinoceros are monogastricanimals with a hindgut-fermentationchamber (Stevens & Hume, 1995). Micro-bial fermentation of plant fibre in thehindgut provides the main energy sourcefor rhinoceros.
The digestive strategy of grazing rhino-ceros is characterized by a slow ingestapassage and, hence, a high digestive effi-ciency that is comparable to that ofdomestic horses (Kiefer 2002, Clauss,Polster et al., 2005a). In contrast, Blackrhinoceros seem to have a comparativelyfaster ingesta passage and a lower diges-tive efficiency (Clauss, Froeschle et al.,2005; Clauss, Castell et al., in press a).Dry-matter intake in an adult rhinocerosranges 1–2·5% of body mass in zoo studies(Dierenfeld, 1999; Dierenfeld et al., 2000).
It appears reasonable to use the dietaryrequirement data from horses, in parti-cular for minerals and some vitamins, asfeeding recommendations for rhinoceros.However, using the standards recom-mended for horses to evaluate the nutrientstatus of rhinoceros from blood samples
may not be appropriate for all targetnutrients (Clauss et al., 2002; Dierenfeldet al., 2005).
DIET FORMULATION: QUANTITY ANDCOMPOSITIONEnergy provision should be the first areaof concern when evaluating captive-feeding regimes for rhinoceros. Atkinsonet al. (2004) collated evidence that Asianrhinoceros in captivity may be substan-tially heavier than their free-ranging coun-terparts. Dierenfeld et al. (2000) warnedthat Sumatran rhinoceros could becomeobese if offered food ad libitum, andreported that the removal of the pelletedcompound feed from the diet and a limiton the amount of hay offered couldresolve the problem. Apart from inappro-priate flooring (Von Houwald & Flach,1998), obesity is considered a major con-tributor to foot problems in Asian rhino-ceros (Atkinson et al., 2004) and it is alsosuspected that the condition contributesto foot problems in Black rhinoceros(Boever, 1976). Uterine tumours (leiomy-omas) are frequently reported in Asianrhinoceros (collated in Clauss, Polsteret al., 2005b), and similar problems inhumans and elephants give rise to the sus-picion that obesity may be a contributingfactor (see also Hatt & Clauss, thisvolume). General considerations onenergy requirements and utilization effi-ciency (explained in Clauss, Polster et al.,
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 199
2005b) lead to the conclusion that themaintenance requirements of hindgut fer-menters should be c. 0·6 MJ digestibleenergy per kg0·75 metabolic body mass.Digestible-energy intakes in excess of thisfigure have been measured in Asian,White and Black rhinoceros in captivityon conventional zoo diets of hay, pelletedcompound feeds and produce, and even inAsian rhinoceros on ad libitum hay-onlydiets (Kiefer, 2002; Castell, 2005; Clauss,Polster et al., 2005b). The roughage por-tion of the diet should possibly berestricted (see also Hatt & Clauss, thisvolume). A scoring system for body con-dition, using the prominence of bonystructures, such as the spine, hip bones orshoulder blades, has been developed forBlack rhinoceros (Reuter & Adcock,1998). Such systems should also bedeveloped for the other rhinoceros speciesand they should be used regularly, inaddition to frequent weighing, to assessthe nutritional status of the animals(Plates 1a,b, 2a,b and 3a,b). For largeanimals, such as rhinoceros, built-in scalesshould be readily available, at least innewly constructed facilities. In theauthors’ experience, it seems that the twograzing and more ‘lethargic’ rhinocerosspecies are more prone to obesity in cap-tivity than the ‘nervous’ Black rhinoceros(see Plates); however, a systematic investi-gation of this suggestion is pending.
DIET COMPOSITION: HAYHay should account for the major pro-portion of any diet for rhinoceros in cap-tivity. The importance of the hygienicquality of the hay has been emphasized bycases resembling a ‘farmer’s lung’ condi-tion reported in Asian rhinoceros at thezoo in Basle (Ruedi, 1984). The tendencyfor Black rhinoceros to develop fungalpneumonia is likely to be secondary to adisturbance of immune functions (Miller,2003); however, using hay of impeccablehygienic status should help to reduce therisk. Constant monitoring of hay quality,
and the disposal of unhygienic batches,must be an integral part of rhinoceroshusbandry. Processing hay through amechanical shaker prior to feeding cansignificantly reduce dust inhalation byboth the animals and keepers.
For the grazing species, grass hay is theappropriate roughage. Even Black rhino-ceros can be offered grass hay alone,without the problem of low food intakethat is often observed in other browsingherbivores, such as tapirs Tapirus spp orgiraffes Giraffa spp (cf. Foose, 1982;M. Clauss, pers. obs). However, if theprotein content of the grass hay is notbeing monitored by laboratory analyses,the addition of a legume hay to the grass-hay portion of the diet (e.g. 20% of thegrass hay offered) is recommended inorder to ensure adequate protein levels,even in grazing species. For the browsingrhinoceros, a 1:1 mixture of grass hay andlucerne hay Medicago sativa (also calledalfalfa hay) has been recommended(Dierenfeld, 1995) in order to mimic thenutrient composition of the natural diet.In contrast, the exclusive use of lucernehay for Black rhinoceros is discouraged(Dierenfeld, 1999), although publishedevidence is missing so far. When available,freshly cut grass can also be offered but,as for horses, the grass should not be cuttoo short as it may cause constipation ofthe hindgut. Hays of particularly high-fibre content are believed to be responsiblefor the rarely observed cases of obstipa-tion (severe and obstinate constipation)(Dierenfeld, 1999), most probably a resultof animals used to more palatableroughage going off their feed for a periodof time. Therefore, the hay (mix) offeredshould not only be of the highest hygienicquality but also of a nutritional qualitythat guarantees a constant intake byrhinoceros.
A problem not investigated so far is theincidence of excessive tooth wear inbrowsing species as a result of the use ofgrass hay (Clauss & Dierenfeld, in press).Grass contains abrasive components
200 ELEPHANTS AND RHINOCEROS
Plate 1a. Free-ranging White rhinoceros Ceratotherium simum and 1b. a White rhinoceros in captivity;Plate 2a. free-ranging Asian rhinoceros Rhinoceros unicornis and 2b. an Asian rhinoceros in captivity; Plate3a. free-ranging Black rhinoceros Diceros bicornis and 3b. a Black rhinoceros in captivity. Note the differencesin body condition, in particular with respect to the spinal process above the pelvis. The White rhinoceros(Plate 1a,b) and the Asian rhinoceros (Plate 2a,b) (both grazing species) are particularly prone to obesity incaptivity. This appears to be a lesser problem in Black rhinoceros (Plate 3a,b). Plate 1a. Mark Atkinson. Plate 1b.The Wilds, Cumberland, OH, USA. Plates 2a and 2b. Nick Lindsay, ZSL, UK. Plates 3a and 3b. White OakConservation Center, Yulee, FL, USA.
(silica), which do not occur in lucerne.Grazing species are adapted to this bytheir hypsodont (high-crowned) dentition,but in browsing species with lower toothcrowns, the chronic ingestion and chewingof grass material could, in theory, lead toearly severe tooth wear. Excessive toothwear has been observed in one old and
one middle-aged Black rhinoceros kept ona grass-hay-based diet (M. Clauss et al.,pers. obs). Systematic evaluations arelacking so far. However, these reflectionsmight support the concept that diets forBlack rhinoceros contain not only grasshay but also lucerne hay and especiallybrowse as the staple items.
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 201
In our experience, achieving a regularsupply of fresh grass, and especiallylucerne hay of acceptable quality, is some-times a problem for European zoos andshould probably be regarded as the majorlimiting factor for the optimization of thehusbandry of large herbivores. The pro-vision of high-quality hay is essential andpersonnel responsible for purchasing theseproducts should be experienced in evalu-ating hay quality, and should be able todiscuss the production and harvestingmethods with farmers. The logical solu-tion to the dilemma of limited availabilityof forage is to either contract farmers orcultivate land owned by the zoo. Poten-tially several zoos could collaborate tocontract a farmer if it is more economicalto purchase a high tonnage. Such co-operation should be a long-term commit-ment with a mutual learning process thatwould eventually result in the productionof forage of the highest quality, as speci-fied by zoos and within the limitations ofthe land being cultivated. Silage could beproduced for winter and browse could befarmed (e.g. Hoellerl et al., 2005). Thehygiene problems associated with storagecould partially be reduced by using freshforage (grass, lucerne) during the growingseason.
Supplementation It is recommended thatthe portion of pelleted compound feeds(or other forms of concentrates) in the dietshould not exceed one-third of the overallcalorific value (Dierenfeld, 1999) but itshould be emphasized that this is amaximum recommendation; it should bepossible to deliver sufficient amounts ofenergy and protein while providing a sub-stantially lower proportion of pelletedcompound feeds or concentrates in thediet. In spite of uniform recommendationsfor the proportion of pelleted compoundfeeds to be offered in the diets of all rhino-ceros species (Lintzenich & Ward, 1997;Dierenfeld, 1999), in practice there seemsto be a tendency to provide Black rhino-ceros (strict browsers) with a diet that has
a higher proportion of concentrate thanthe grazing species (Clauss, Castell et al.,in press a). There is no scientific basis forthis practice and high levels of mineralizedpelleted compound feeds may contributeto health problems in Black rhinoceros. Ingeneral, a high proportion of pelletedcompound feeds and a correspondinglylower proportion of hays and/or browse,are probably contributory factors to thedental calculus often observed in thisspecies (Walter et al., 1992; Miller, 2003;Hatt et al., 2004), which may lead to par-odontosis (chronic inflammation of thegums) and oral abscesses.
Pelleted compound feed may be used tobalance mineral, vitamin and, in somecases, protein requirements; it should onlybe used to satisfy energy needs when ade-quate roughage is not available. There isno scientific rationale for the inclusion ofgrain products in pelleted compound feedsfor strict herbivores. Because the additionof grain ingredients to pelleted compoundfeeds will also influence their fatty-acidcomposition unfavourably, the develop-ment of a herbivore pelleted compoundfeed (to be used sparingly) based onlucerne meal, with a high concentration ofvitamins and minerals, is recommendedfor rhinoceros as well as other strictly her-bivorous species. The levels of the aminoacid tyrosine in the ingredients of a com-pound feed should be evaluated and,based on this, a supplementation of theformula could be considered becausehigher levels of tyrosine have beenreported in the red-blood cells of rhino-ceros and equids than in other mammals,and Black rhinoceros in captivity havesignificantly lower tyrosine levels thantheir free-ranging conspecifics. There isspeculation that tyrosine might act as animportant antioxidant in the red-bloodcells of these species (Weber et al., 2004).An investigation into potentially bene-ficial effects of tyrosine supplementationin the diet of rhinoceros is warranted.
202 ELEPHANTS AND RHINOCEROS
SELECTED MICRONUTRIENTS AND NON-ROUGHAGE FOOD ITEMSMineral deficiencies have rarely beenreported in rhinoceros in captivity and formost micronutrients the dietary concen-trations as recommended for horsesshould also be adequate for rhinoceros(Dierenfeld, 1999). Some zoo diets offeredto Asian rhinoceros have been found tobe deficient (when compared to the rec-ommendations for horses) in several nutri-ents, such as phosphorus, copper or zinc(Clauss, Polster et al., 2005b). In contrast,owing to the higher proportion of pelletedcompound feeds in diets offered to Blackrhinoceros, zoo diets analysed by Castell(2005) offered to this species invariablysupplied an excess of all the mineralsinvestigated (iron in particular), with thenotable exception of copper, which waslow in several cases. Here, some observa-tions on selected minerals are presented.
Available data on the mineral composi-tion of natural diet items of Black andWhite rhinoceros, compared to values ingrass, lucerne and browse used in tem-perate-zone zoos, are collated in Table 2.From the table, a general necessity tosupplement certain minerals to roughage-based diets becomes evident. Generally,the mineral and vitamin content of a dietneeds to be monitored by ration calcula-tion, in order to avoid deficiencies orexcesses.
Sodium (Na) Compared to horses,Black rhinoceros have been found to havehigher endogenous faecal sodium losses(Clauss, Castell et al., in press b). For thisspecies, as for other rhinoceros speciesand herbivores in general, salt licks shouldbe available ad libitum.
Calcium (Ca) and phosphorus(P) Browse material has a drasticallyhigher calcium to phosphorus ratio thangrass, a fact that is reflected in the differ-ence in calcium levels in forage in the nat-ural diets of Black and White rhinoceros(Table 2). Given the high calcium content
in browse, the feeding of lucerne hayshould not be discouraged on account ofits higher calcium content (compared tograss hay). A diet based on any hay (grassor lucerne) or browse, supplemented witha pelleted compound feed on the basis oflucerne meal, does not require any addi-tional calcium source. For example,Kiefer (2002) reports a case of a feedingregime for White rhinoceros in captivitywhere the calcium levels were alreadyhigher than those found in the diet of free-ranging conspecifics, but the animals incaptivity still received a calcium supple-ment. The mineral mix integrated in thepelleted compound feed based on lucernemeal should also not contain an addi-tional calcium source. This is particularlyrelevant insofar as calcium is usually sup-plied by adding lime, which is often richin iron. The omission of an additional cal-cium source might, therefore, be a signifi-cant contribution to the reduction of ironin the pelleted compound feed and theoverall diet (see below). Roughage-baseddiets are particularly prone to phospho-rous deficiency. Hypophosphataemia (lowlevels of phosphorus in the blood) hasbeen observed in Black rhinoceros withhaemolytic crises, so a deficiency of thismineral in the diet should be avoided.Anecdotal success in cases of haemolyticcrises or necrolytic dermatitis (skin dis-ease) in Black rhinoceros in which,amongst other treatments, phosphoroussupplementation was administered, rec-ommend this practice in such cases.Whether particular phosphorous supple-mentation should be regarded as a med-ical treatment in diseased animals only orrecommended in regular diets remains tobe investigated.
Copper (Cu) Dierenfeld et al., (2000),Clauss, Polster et al., (2005b) and Castell(2005) all reported some diets for rhino-ceros to be deficient in copper. Further tothese findings, Dierenfeld et al. (2005)observed low copper levels in the livertissue of browsing rhinoceros and recom-
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 203
mineral
forage
temperate
maintenance
recommendation
forhorses4
blackrhinoceros1
whiterhinoceros2
browse
3lucerne3
grass
3
g/kg
DM
Ca
17·6
2·4
15·6
214·
82·
4(7
·0–4
2·7;
n�25
)(1
·8–3
·7;
n�6)
(9·3
–23·
8;n�
12)
(2·1
–9·7
;n�
14)
P1·
21·
02·
73·
02·
71·
7(0
·4–2
·0;
n�25
)(1
·0–1
·1;
n�6)
(1·6
–4·7
;n�
12)
(2·0
–3·1
;n�
14)
Mg
2·7
0·8
3·4
2·8
1·5
0·9
(1·2
–6·5
;n�
18)
(0·6
–1·1
;n�
6)(2
·0–6
·9;
n�12
)(0
·6–2
·7;
n�13
)
Na
0·14
0·3
0·09
1·10
0·05
1·0
(0·0
1–0·
94;
n�18
)(0
·2–0
·4;
n�6)
(0·0
1–0·
31;
n�10
)(0
·02–
0·08
;n�
5)
K8·
78·
514
·922
21·6
3·0–
6·0
(2·8
–17·
7;n�
18)
(7·0
–10·
8;n�
6)(7
·3–3
1·8;
n�11
)(1
6·0–
27·0
;n�
14)
mg/
kgD
MF
e82
177
120
180
129
40–7
0(1
2–21
5;n�
28)
(91–
220;
n�6)
(64–
191;
n�12
)(4
6–39
1;n�
10)
Mn
6092
4074
40(1
–269
;n�
28)
(14–
248;
n�12
)(3
7–14
7;n�
9)
Cu
54
1111
610
(1–1
2;n�
28)
(3–6
;n�
6)(7
–20;
n�12
)(4
–9;
n�6)
Zn
1423
5324
1940
(3–6
7;n�
28)
(16–
35;
n�6)
(13–
121;
n�12
)(1
5–23
;n�
5)
Tab
le2.
Min
eral
cont
ent
(mea
n,w
ith
rang
ean
dnu
mbe
rof
sam
ples
inpa
rent
hese
s)of
the
diet
offr
ee-r
angi
ngB
lack
rhin
ocer
osan
dW
hite
rhin
ocer
osas
com
pare
dto
tem
pera
tebr
owse
,gr
ass,
luce
rne,
and
reco
mm
enda
tion
sfo
rm
aint
enan
cere
quir
emen
tsin
dom
esti
cho
rses
:1 .
Joub
ert
&E
loff
(197
1),
Ghe
brem
eske
let
al.
(199
1),
Die
renf
eld
etal
.(1
995)
;2 .
Kie
fer
(200
2);
3 .D
LG
(196
0);
4 .N
atio
nal
Res
earc
hC
ounc
il(1
989)
,M
eyer
&C
oene
n(2
002)
;D
M.
dry
mat
ter.
204 ELEPHANTS AND RHINOCEROS
mended further research into coppermetabolism in these species. To date, aclinical case of copper deficiency in arhinoceros has, however, not beenreported to our knowledge.
Zinc (Zn) Zinc deficiency may lead tothe development of skin and foot lesions,so the supply of zinc should be accordingto recommendations.
Iron (Fe) Oversupplementation withiron is of particular concern in browsingrhinoceros, which have contracted severaluncommon diseases (Miller, 2003) thathave been hypothetically linked to theexcessive iron stores observed in speci-mens in captivity, in contrast to free-ranging conspecifics (reviewed by Paglia &Dennis, 1999; Paglia et al., 2001; Dieren-feld et al., 2005). Dierenfeld et al. (2005)interpreted data on circulation and tissue-mineral levels were analysed, and the con-clusion is that dietaryoversupplementation is unlikely to be thesole cause of this phenomenon but a parti-cularly effective absorption mechanism(or a lack of a functional negative feed-back) is a likely contributory factor.Nevertheless, dietary oversupplementa-tion should strictly be avoided. The rec-ommendation for horses of 100 mg iron/kg DM will probably be met by the haymixes described (Castell, 2005). Anymanufactured pelleted compound feed,including the one based on lucerne meal,is likely to increase this concentration(Clauss, Hummel et al., 2005). Green mealfrom grass is particularly prone to highiron levels. Care should be taken that themineral premix ingredient of a pelletedcompound feed does not increase the ironcontent any further.
It has been speculated that, with regardto excessive iron absorption, browsingrhinoceros should benefit from the addi-tion of tannins to their diet (e.g. Paglia &Dennis, 1999). Tannins are natural che-lators of metal ions, which reduce theavailability of dietary iron, and occur in
the forage of free-ranging browsing rhino-ceros but rarely in the grass or lucernehays offered as staple diet items in zoos(Wright, 1998). To date, there is no quan-titative proof of the effect of tannin sup-plementation on rhinoceros in captivitybut assessing the results of studies onother species (reviewed by Clauss, 2003),it is probable that an increased dietarytannin content will reduce iron absorptionin rhinoceros. However, in studies withhumans it has been shown that the tanninsource must be consumed in synchronywith the iron source, in order for thetannin to have an effect (e.g. Disler et al.,1975). Tannins can only be added tomanufactured feed components (e.g. inthe form of tea leaves or as red-grapepomace) and as these feeds will alwaysrepresent the minor proportion of the dietof rhinoceros in captivity, this goal isunlikely to be met. Nevertheless, the inclu-sion of a tannin source that does not initself increase iron content should be con-sidered when composing a pelleted com-pound feed for browsing rhinoceros.However, this should not be an excuse fornot attempting to reduce the iron levels inthe diet in rhinoceros. In most zoos, itappears unlikely that excessive ironabsorption in Black rhinoceros can beavoided completely, therefore veterinarymonitoring of iron status, including inter-vention in the form of regular phlebotomy(controlled bleeding, as carried out inhumans with iron-storage disease) ifnecessary, should be an integral part ofthe husbandry routine for Black rhino-ceros (Paglia, 2004).
Vitamin E Circulating vitamin E levelsof both free-ranging and captive rhino-ceros are generally very low (Dierenfeldet al., 1988; Clauss et al., 2002). Since1991 vitamin E supplementation of rhino-ceros has increased and, on average,higher circulating vitamin E levels havebeen detected (Clauss et al., 2002). How-ever, no significant effect of this increaseon the occurrence of uncommon diseases
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 205
in Black rhinoceros has been reported. Itappears unlikely that supplementationwith specially designed, water-solublevitamin E forms is necessary, and dietarylevels of 150–200 IU/kg DM should beadequate (Dierenfeld, 1999).
Fatty acids Serum fatty acids measuredin Black rhinoceros in captivity (com-pared with values from wild counterparts)were at elevated levels for n-6 (linoleicacid) and lowered levels for n-3 (linolenicacid) (Clauss, Dierenfeld et al., 2005), apattern consistent with the relative con-centrations of these nutrients in zoo dietsversus wild dietary plant material; thesource of n-6 in zoo diets are the grainswidely used to formulate compound feedsroutinely offered to balance roughage,because these are naturally high in n-6(Grant et al., 2002). Clauss, Dierenfeldet al. (2005) found a significant correla-tion between the proportion of grainproducts in the diet of Black rhinoceros incaptivity and the proportion of n-6 fattyacids in their serum and red blood cells.These n-6 fatty acids are pro-inflamma-tory, whereas the n-3 fatty acids are anti-inflammatory. Thus it is not only thequantities that are significant but also thebalance between the two. It has beenhypothesized that the occurrence of fatty-acid imbalances in zoo diets that usegrain-based compound feeds contributetowards a number of uncommon skin-dis-ease phenomena observed in Black rhino-ceros (Grant et al., 2002). The n-3 fattyacids can be supplemented by feedingfresh forage, such as freshly cut grass andbrowse, by increasing the proportion ofgrass or lucerne hay in the overall diet, byusing pelleted feed compounds based onlucerne meal rather than grain or soyproducts, or by including linseed productsor linseed oil in the pelleted compoundfeed (Grum et al., 2005).
Several commercially available pelletedcompound feeds exist for rhinoceros andtheir use should be judged according to
the considerations reported here. Thedevelopment of a commercially availablepelleted compound feed with no grainingredients is awaited. If a commercialpelleted compound feed is used, it is rec-ommended that it has a high-fibre content[crude fibre 20% or ADF (acid-detergentfibre) 25% of DM]. In parallel to obser-vations in horses (reviewed in Clauss &Kiefer, 2003), Goltenboth (1995) specu-lated that an increased supplementationwith energy-dense feeds, such as grain-based products, could lead to laminitis(founders, inflammation of the hoof-hornproducing stratum of the hoof) and con-tribute to foot problems in rhinocerosspecies.
There is no nutritional or financialrationale for offering fruits or vegetablesto rhinoceros (Oftedal & Allen, 1996). Ifa fruit component of the natural diet is tobe mimicked for pedagogic or emotionalreasons, then commercially availablegreen leafy vegetables best resemble ‘wildfruits’ in their nutritional composition.Onions, brassicas and rape should beavoided, as they have all been linked withhaemolytic anaemia in other species(Dierenfeld, 1999).
In order to avoid ingestion of sand,which can cause colic in these species(Miller, 2003), rhinoceros should not befed on sandy ground.
BROWSEBlack rhinoceros should be provided withfresh browse, such as branches of shrubsor trees, with foliage in the vegetationperiod or without foliage during winter-time, on a regular basis. In our experience,willow Salix spp, beech Fagus spp, hazelCorylus spp, ash Fraxinus, birch Betulaspp, oak Quercus spp, poplar Populus spp,apple Malus spp, cherry and prune Prunusspp, pear Pyrus spp and wild rose Rosaspp, have been fed to Black rhinoceros,mostly in combination, without problems.It should be stated that Dierenfeld (1999)explicitly warns against the use of mapleAcer spp and oak, as these have been
206 ELEPHANTS AND RHINOCEROS
reported to lead to haemolysis in otheranimal species. Dierenfeld (1999) alsogives a list of other browse species thatcan be fed to Black rhinoceros. Before anew browse item is fed, enquiries shouldbe made about any potentially toxiceffects of that browse species. In general,a variety of browse species should beoffered simultaneously. For winterfeeding, browse can be preserved by sil-aging (Hatt & Clauss, 2001; Nijboer et al.,2003) and bare branches can be offered,which will also provide a source of behav-ioural enrichment. With the increasingaddition of browse to the diet of Blackrhinoceros in captivity, their digestive effi-ciency decreases to values reported forboma-held or free-ranging animals(Clauss, Castell et al., in press a). AsAsian rhinoceros are not as high on thepriority list of animals that should receivebrowse in a zoological institution, and ifbrowse supply is limited, they could beoffered uneaten branches from otherexhibits in the zoo if there is no concernabout disease transmission.
ENRICHMENTTo our knowledge, the only behavioural-enrichment study in rhinoceros associatedwith feeding is on the influence of fooddispersal on the behaviour of 1.5 (�.�)White rhinoceros in a group exhibit(Schmidt & Sachser, 1996). When hay wasoffered in only one pile for all the animalsthere were more agonistic encounters thanwhen hay was provided in several heaps,one for each animal. Stress-hormonelevels, as measured in the saliva, were ele-vated during clumped feeding and ago-nistic behaviour continued to be observedlong after the hay was consumed. Salivarystress-hormone levels of a single bull in anadjacent enclosure also increased duringthe clumped-feeding period. These resultsunderline the importance of providing anappropriate number of feeding places foranimals that are maintained in socialgroups.
For large herbivores, such as rhino-ceros, the best behavioural-enrichmentmeasure is probably to offer a diet that isbulky with a low-energy density, namelya hay-based diet containing few concen-trates and with the possible addition ofbrowse.
CONCLUSIONSEnergy and protein should be provided toall rhinoceros species in captivity in theform of roughage: best fresh or silage, ordry (hays). For White and Asian rhino-ceros, grass material is most appropriate,with a potential small addition of lucerneto increase protein levels. For Blackrhinoceros, the 1:1 mixture of grass andlucerne has been recommended, plus asmuch browse material as possible.
Commercial fruits, vegetables, cerealsand grain products should not be fed,except for medication or training pur-poses, although even in these cases, greenleafy vegetables are to be preferred.
Minerals and vitamins should be bal-anced by the provision of small amountsof pelleted compound feeds based onlucerne meal. Deficiencies and excessesshould be avoided. In the Black rhino-ceros in particular, care should be takento avoid an excess of iron, often intro-duced to the diet via pelleted compoundfeeds and mineral supplements.
Rhinoceros are prone to obesity andfood should be given restrictively, basedon either the results of regular weighingor regular assessment of the body-condi-tion score. Changes to the amount ofroughage offered should be accompaniedby corresponding changes to the amountof pelleted compound feeds offered.
ACKNOWLEDGEMENTS
We thank Nick Lindsay (Zoological Society ofLondon), Mark Atkinson, Dave Clawson (Inter-national Rhino Foundation) and the White OakConservation Center for the provision of photo-graphic material. M.C. thanks Jurgen Hummel forcontinuous discussions about the nutrition ofbrowsing animals.
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 207
REFERENCESAtkinson, M. W., von Houwald, F., Gairhe, K.P., Gandolf, A. R. & Blumer, E. S. (2004): Veter-inary observations of wild greater one-horned rhino-ceros (Rhinoceros unicornis) in the Royal ChitwanNational Park: implications for captive manage-ment. Proceedings of the Association of AmericanZoo Veterinarians 2004: 130–133.Boever, W. J. (1976): Interdigital corns in a blackrhinoceros. Veterinary Medicine and Small AnimalClinician 71: 827–830.Castell, J. (2005): Untersuchungen zu Futterung undVerdauungsphysiologie am Spitzmaulnashorn(Diceros bicornis). Vet. med. thesis, University ofMunich, Germany.Clauss, M. (2003): Tannins in the nutrition of wildanimals: a review. In Zoo animal nutrition 2: 53–89.Fidgett, A., Clauss, M., Ganslosser, U., Hatt, J.-M.& Nijboer, J. (Eds). Furth: Filander.Clauss, M. & Dierenfeld, E. S. (In press): Thenutrition of browsers. In Zoo and wild animal medi-cine (6th edn). Fowler, M. E. & Miller, R. E. (Eds).Philadelphia, PA: W. B. Saunders.Clauss, M. & Kiefer, B. (2003): Digestive acidosisin captive wild herbivores: implications for hoofhealth. Verhandlungsbericht Erkrankungen der Zoo-tiere 41: 57–70.Clauss, M., Jessup, D. A., Norkus, E. B., Chen, T.C., Holick, M. F., Streich, W. J. & Dierenfeld,E. S. (2002): Fat soluble vitamins in blood and tis-sues of free-ranging and captive rhinoceros. Journalof Wildlife Diseases 38: 402–413.Clauss, M., Dierenfeld, E. S., Bigley, K. E.,Wang, Y., Ghebremeskel, K., Hatt, J.-M., Flach,E. J., Behlert, O., Castell, J. C., Streich, W. J. &Bauer, J. E. (2005): Fatty acid status of free-rangingand captive black rhinoceros. NAG Proceedings 6:54–56.Clauss, M., Froeschle, T., Castell, J., Hatt, J.-M., Ortmann, S., Streich, W. J. & Hummel, J.(2005): Fluid and particle retention times in theblack rhinoceros Diceros bicornis, a large hindgut-fermenting browser. Acta Theriologica 50: 367–376.Clauss, M., Hummel, J., Eloff, P. & Willats, R.(2005): Browse provision for captive herbivores:design and management of a browse plantation(Abstract). European Zoo Nutrition Meeting AbstractBook: 44. Leipzig: Leipzig Zoo.Clauss, M., Polster, C., Kienzle, E., Wiesner, H.,Baumgartner, K., von Houwald, F., Ortmann,S., Streich, W. J. & Dierenfeld, E. S. (2005a):Studies on digestive physiology and feed digestibili-ties in captive Indian rhinoceros (Rhinoceros uni-cornis). Journal of Animal Physiology and AnimalNutrition 89: 229–237.Clauss, M., Polster, C., Kienzle, E., Wiesner, H.,Baumgartner, K., von Houwald, F., Streich, W.J. & Dierenfeld, E. S. (2005b): Energy and mineralnutrition and water intake in the captive Indian
rhinoceros (Rhinoceros unicornis). Zoo Biology 24:1–14.Clauss, M., Castell, J. C., Kienzle, E., Dieren-feld, E. S., Flach, E. J., Behlert, O., Ortmann,S., Streich, W. J., Hummell, J. & Hatt, J.-M. (Inpress a): Digestion coefficients achieved by the blackrhinoceros (Diceros bicornis), a large browsinghindgut fermenting fermenter. Journal of AnimalPhysiology and Animal Nutrition. DOI. 10.1111/j.1439-0396.2006.00606.xClauss, M., Castell, J. C., Kienzle, E., Schramel,P., Dierenfeld, E. S., Flach, E. J., Behlert, O.,Hatt, J.-M., Streich, W. J. & Hummell, J. (Inpress b): Micromineral absorption in the blackrhinoceros (Diceros bicornis) as compared to thedomestic horse. Journal of Nutrition.Dierenfeld, E. S. (1995): Rhinoceros nutrition: anoverview with special reference to browsers. Verhan-dlungsbericht Erkrankungen der Zootiere 37: 7–14.Dierenfeld, E. S. (1996): Nutrition. In AZA Rhino-ceros husbandry resource manual: 52–55. Fouraker,M. & Wagener, T. (Eds). Fort Worth, TX: CockerellPrinting Company.Dierenfeld, E. S. (1999): Rhinoceros feeding andnutrition. In Zoo and wild animal medicine (4th edn):568–571. Fowler, M. E. & Miller, R. E. (Eds). Phil-adelphia, PA: W. B. Saunders.Dierenfeld, E. S., du Toit, R. & Miller, R. E.(1988): Vitamin E in captive and wild black rhino-ceros (Diceros bicornis). Journal of Wildlife Diseases24: 547–550.Dierenfeld, E. S., du Toit, R. & Braselton, W. E.(1995): Nutrient composition of selected browsesconsumed by black rhinoceros in the ZambeziValley, Zimbabwe. Journal of Zoo and Wildlife Med-icine 26: 220–230.Dierenfeld, E. S., Wildman, R. E. C. & Romo, S.(2000): Feed intake, diet utilization, and compositionof browses consumed by the Sumatran rhino (Dicer-orhinus sumatrensis) in a North American zoo. ZooBiology 19: 169–180.Dierenfeld, E. S., Atkinson, S., Craig, A. M.,Walker, K. C., Streich, W. J. & Clauss, M.(2005): Mineral concentrations in serum/plasma andliver tissue of captive and free-ranging rhinocerosspecies. Zoo Biology 24: 51–72.Dinerstein, E. & Wemmer, C. M. (1988): Fruitsrhinoceros eat: dispersal of Trewia nudiflora(Euphorbiaceae) in lowland Nepal. Ecology 69:1768–1774.Disler, P. B., Lynch, S. R., Charlton, R. W., Tor-rance, J. D., Bothwell, T. H., Walker, R. B. &Mayer, F. (1975): The effect of tea on iron absorp-tion. Gut 16: 193–200.DLG (1960): Futterwerttabellen der DLG Mineral-stoffe. Frankfurt: DLG-Verlags-GmbH.Duke, J. A. & Atchley, A. A. (1986): CRC hand-book of proximate analysis tables of higher plants.Boca Raton, FL: CRC Press.
208 ELEPHANTS AND RHINOCEROS
Foose, T. J. (1982): Trophic strategies of ruminantversus nonruminant ungulates. PhD thesis, Universityof Chicago, IL, USA.Ghebremeskel, K., Williams, G., Brett, R. A.,Burek, R. & Harbige, L. S. (1991): Nutrient com-position of plants most favoured by black rhinocerosin the wild. Comparative Biochemistry and Physi-ology A 98: 529–534.Go»eltenboth, R. (1995): Zu einigen Problemen inder Haltung und der Krankheiten der Nashorner inZoologischen Garten. Verhandlungsbericht Erkran-kungen der Zootiere 37: 53–58.Grant, J. B., Brown, D. L. & Dierenfeld, E. S.(2002): Essential fatty acid profiles differ across dietsand browse of black rhinoceros. Journal of WildlifeDiseases 38: 132–142.Grum, C., Hatt, J.-M. & Clauss, M. (2005): Fattyacid status of free-ranging and captive wildlife:literature survey. NAG Proceedings 6: 180–182.Hatt, J.-M. & Clauss, M. (2001): Browse silage inzoo animal nutrition—feeding enrichment ofbrowsers during winter. EAZA News. Special Issueon Zoo Nutrition 2: 8–9.Hatt, J.-M., Wenker, C., Castell, J. & Clauss, M.(2004): Dietary and veterinary management of a lin-gual abscess in a geriatric captive black rhino(Diceros bicornis) with iron storage disease. Pro-ceedings of the Scientific Meeting of the EuropeanAssociation of Zoo and Wildlife Veterinarians 5:339–340.Hoellerl, S., Stimm, B., Hummel, J. & Clauss, M.(2005): Browse provision for captive herbivores:design and management of a browse plantation.Abstracts of the European Zoo Nutrition Meeting 4:31.Joubert, E. & Eloff, F. C. (1971): Notes on theecology and behaviour of the black rhinoceros insouth west Africa. Madoqua 1: 5–53.Kiefer, B. (2002): Qualitat und Verdaulichkeit dervom Breitmaulnashorn (Ceratotherium simumsimum) aufgenommenen Nahrung. Vet. med. thesis,University of Munich, Germany.Kiefer, B., Ganslosser, U., Kretzschmar, P. &Kienzle, E. (2003): Food selection and food qualityin territorial males of a free-ranging population ofwhite rhinoceros (Ceratotherium simum simum) inSouth Africa. In Zoo animal nutrition 2: 199–207.Fidgett, A., Clauss, M., Ganslosser, U., Hatt, J.-M.& Nijboer, J. (Eds). Furth: Filander.Laurie, A. (1982): Behavioural ecology of theGreater one-horned rhinoceros (Rhinoceros uni-cornis). Journal of Zoology 196: 307–341.Lintzenich, B. A. & Ward, A. M. (1997): Hay andpellet ratios: considerations in feeding ungulates.Nutrition Advisory Group Handbook Fact Sheet 006:1–12.Meyer, H. & Coenen, M. (2002): Pferdefutterung.Berlin: Parey.Miller, R. E. (2003): Rhinoceridae (Rhinoceroses).In Zoo and wild animal medicine (5th edn): 559–569.
Fowler, M. E. & Miller, R. E. (Eds). St Louis, MO:W. B. Saunders.National Research Council (1989): Nutrientrequirements of horses (5th edn). Washington, DC:National Academy Press.Nijboer, J., Clauss, M. & Nobel, J. (2003): Browsesilage: the future for browsers in wintertime? EAZANews. Special Issue on Zoo Nutrition 3: 5–7.Oftedal, O. (1991): The nutritional consequences offoraging in primates: the relationship of nutrientintakes to nutrient requirements. PhilosophicalTransactions of the Royal Society of London B 334:161–170.Oftedal, O. T. & Allen, M. E. (1996): Nutritionand dietary evaluation in zoos. In Wild mammals incaptivity: 109–116. Kleiman, D. G., Allen, M. E.,Thompson, K. V. & Lumpkin, S. (Eds). Chicago, IL:The University of Chicago Press.Owen-Smith, N. (1988): Megaherbivores: the influ-ence of very large body size on ecology. Cambridge:Cambridge University Press.Paglia, D. E. (2004): Recommended phlebotomyguidelines for prevention and therapy of captivity-induced iron-storage disease in rhinoceroses, tapirsand other exotic wildlife. Proceedings of the Amer-ican Association of Zoo Veterinarians 2004: 122–127.Paglia, D. E. & Dennis, P. (1999): Role of chroniciron overload in multiple disorders of captive blackrhinoceroses (Diceros bicornis). Proceedings of theAmerican Association of Zoo Veterinarians 1999:163–171.Paglia, D. E., Kenny, D. E., Dierenfeld, E. S. &Tsu, I.-H. (2001): Role of excessive maternal iron inthe pathogenesis of congenital leukoenceophaloma-lacia in captive black rhinoceroses (Dicerosbicornis). American Journal of Veterinary Research62: 343–349.Reuter, H.-O. & Adcock, K. (1998): Standardisedbody condition scoring system for black rhinoceros.Pachyderm 26: 116–121.Ru»edi, D. (1984): The great Indian rhinoceros(Rhinoceros unicornis). In One medicine: 171–190.Ryder, O. A. & Byrd, M. L. (Eds). New York, NY:Springer.Schmidt, C. & Sachser, N. (1996): Auswirkungenunterschiedlicher Futterverteilungen auf Verhaltenund Speichel-Stresshormonkonzentrationen vonBreitmaulnashornern im Allwetterzoo Munster.Aktuelle arbeiten zur artgemassen tierhaltung. KTBLSchrift 376: 188–198.Stevens, C. E. & Hume, I. D. (1995): Comparativephysiology of the vertebrate digestive system. Cam-bridge: Cambridge University Press.Von Houwald, F. & Flach, E. J. (1998): Preva-lence of chronic foot disease in captive greater one-horned rhinoceros (Rhinoceros unicornis).Proceedings of the Scientific Meeting of the EuropeanAssociation of Zoo and Wildlife Veterinarians 2:323–327.Walter, J. H., Kirchhoff, A., Schauer, G. &Goeltenboth, R. (1992): Globulare peridontale
REVIEW: RHINOCEROS FEEDING IN CAPTIVITY 209
Zementdysplasien bei einem Spitzmaulnashorn. Ber-liner Muenchner Tieraerztliche Wochenschrift 105:311–314.Weber, B. W., Paglia, D. E. & Harley, E. H.(2004): Elevated free tyrosine in rhinoceros erythro-cytes. Comparative Biochemistry and Physiology A138: 105–109.Wright, J. B. (1998): A comparison of essential fattyacids, total lipid, and condensed tannin in the diet of
captive black rhinoceroses (Diceros bicornis) in NorthAmerica and in browses native to Zimbabwe, Africa.MSc thesis, Cornell University, Ithaca, NY, USA.
Manuscript submitted 22 April 2005;accepted 13 February 2006; revised28 March 2006
