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Zoo Biology 29 : 687704 (2010)

RESEARCH ARTICLE

Carnivorous Mammals: NutrientDigestibility and Energy Evaluation

Marcus Clauss,1

Helen Kleffner,2

and Ellen Kienzle2

1Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, Universityof Zurich, Zurich, Switzerland2Chair of Animal Nutrition and Dietetics, Ludwigs-Maximilians-University Munich,Munich, Germany

Estimating the energy content is the first step in diet formulation, as it determinesthe amount of food eaten and hence the concentration of nutrients required tomeet the animals requirements. Additionally, being able to estimate the energycontent of a diet empirically known to maintain body condition in an animal willfacilitate an estimation of maintenance energy requirements. We collated data on

nutrient composition of diets fed to captive wild canids, felids, hyenids, mustelids,pinnipeds, and ursids and the digestibility coefficients from the literature (45species, 74 publications) to test whether differences in protein and fat digestibilitycould be detected between species groups, and whether approaches suggested forthe estimation of dietary metabolizable energy (ME) content in domesticcarnivores (NRC [2006] Nutrient requirements of dogs and cats. Washington,DC: National Academy Press.) can be applied to wild carnivores as well.Regressions of digestible protein or fat content vs. the crude protein (CP) or fatcontent indicated no relevant differences in the digestive physiology between thecarnivore groups. For diets based on raw meat, fish, or whole prey, applying thecalculation of ME using Atwater factors (16.7 kJ/g CP; 16.7 kJ/g nitrogen-freeextracts; 37.7 kJ/g crude fat) provided estimates that compared well toexperimental results. This study suggests that ME estimation in such diets isfeasible without additional digestion trials. For comparative nutrition research,the study implicates that highly digestible diets typically fed in zoos offer littlepotential to elucidate differences between species or carnivore groups, butresearch on diets with higher proportions of difficult-to-digest components (fiber,connective tissues) is lacking. Zoo Biol 29:687704, 2010. r 2010 Wiley-Liss, Inc.

Published online 13 January 2010 in Wiley Online Library (wileyonlinelibrary.com).

DOI 10.1002/zoo.20302

Received 20 February 2009; Revised 3 September 2009; Accepted 23 November 2009

Correspondence to: Marcus Clauss, Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty,

University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland. E-mail: [email protected]

2010 Wiley-Liss, Inc.


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Keywords: canid; felid; hyenid; mustelid; pinniped; ursid; nutrition; digestion

INTRODUCTION

Animals eat grams, not percentages. The estimation of the amount of a

particular diet required by an animal, based either on personal experience or by an

estimation of the diets energy content, is important for various reasons.

First and foremost, energy estimation and the subsequent calculation of the

amount of diet required is the first step in ration design. In further steps, based on

the (silently or explicitly) assumed amount of diet, and the absolute nutrient

requirements, the percentages of the nutrients are calculated that need to be in that

diet so that the animals requirements are met. To meet a certain absolute nutrient

requirement, a high-energy foodof which less is fed to maintain body massneeds

to contain higher percentages of nutrients than a low-energy foodof which the

animal will have to eat more to maintain body mass. In veterinary practice, exclusivefocus on the percentages of nutrients, and disregard of the absolute amount of food

actually ingested, can lead to dietetic problems. A typical example is that when

feeding lower amounts of food to obese animals to facilitate weight reduction, the

protein content of the diet needs to be increased in order to prevent protein

deficiency and loss of lean body mass. As concerns about obesity have arisen in

many zoo species [Schwitzer and Kaumanns, 2001; Clauss and Hatt, 2006; Hatt and

Clauss, 2006; Cocks, 2007; Videan et al., 2007], an approach to estimate energy

provision via foodsimilar to the estimations used in domestic carnivores [NRC

Council, 2006]would be useful in facilitating control calculations of energy intake.

On the other hand, in zoological practice, food allowance for captive carnivoresis based mainly on experience and a trial-and-error-approach, using the animals

body condition as a gauge. No change in body condition indicates energy intake at

maintenance level [Robbins, 1993]. If the energy content of a currently fed diet could

be estimated with sufficient accuracy, it would therefore allow an estimation of the

animals maintenance energy requirement [e.g. Schwarm et al., 2006]. Finally, in

budgeting the costs of feeds, it is necessary to compare feeds not on a wet weight

basis, but rather on either a dry weight basis [Watkins, 1985] or ideally on an energy

basis; the latter is only possible if adequate methods for the estimation of energy exist.

Few differences in the digestive efficiency between carnivore species have been

described; the one difference for which evidence has been accumulated is a lowerdigestive efficiency for fat in cats as compared to dogs [Taylor et al., 1995; NRC, 2006].

To investigate differences in crude nutrient digestibility and to test whether the

metabolizable energy (ME) content of the diets of captive carnivores can be reliably

estimated by equations routinely used for dogs and cats, we collated data from the

literature, performed comparisons between taxonomic groups, and compared the energy

content measured experimentally to estimations using the approach of the NRC [2006].

MATERIALS AND METHODS

A literature review was performed using common search engines such as

Google Scholar, Pubmed, Zoological Records, and electronic repositories of the

proceedings of the conferences of American Association of Zoo Veterinarians;

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additionally, a large set of zoo-related literature, including conference proceedings,

was screened manually. In total, 74 publications were used that provided data for 45

species (Table 1).

From the literature sources, data on species, body mass, intake, nutrient

composition of foods (crude protein (CP), ether extracts (EE), crude fiber (CF), totaldietary fiber (Prosky) (TDF), nitrogen-free extracts (NfE), gross energy (GE)), and

the apparent digestibility (aD) of dry matter (DM), organic matter (OM), and

nutrients were extracted; whenever possible, data from individual animals rather

than group averages were used. When NfE was not given but data on CP, EE, CF,

and crude ash (CA) were available, NfE was calculated as 100-CP-EE-CF-CA.

To test for physiological differences between carnivore groups, the Lucas test

was applied [cf. Robbins, 1993, p 293]. The principle behind this way of data

presentation is that the aD of a nutrient, for which a constant endogenous loss and a

constant true digestibility is assumed, increases with increasing dietary content of

that nutrient in an asymptotic fashion that approaches the true digestibility at high

nutrient contents (Fig. 1A). Therefore, if nutrient content is plotted against thedigestible nutrient content in the diet (calculated via the nutrient content and the aD

of that nutrient; DM basis), a linear relationship is evident (Fig. 1B). The slope of this

linear relationship represents the true digestibility of the nutrient, and the

(negative) intercept represents the endogenous losses (per unit ingested DM)

[Robbins, 1993]. Note that measurements of NfE cannot be recommended from a

scientific point of view because the chemical identity of the components that make up

this fraction is unclear, due to the undefined fraction of components retained in the

conventional CF analysis [Van Soest, 1994, p 142144]. Additionally, NfE measured

in the feces consists mainly of the metabolic components and not of dietary NfE [Van

Soest, 1994]; therefore, applying the concept of aD to NfE is questionable. However,because NfE is still an integral part of the energy estimation equations in use for

domestic carnivores [NRC, 2006], it is included in this investigation.

In order to test for a general negative influence of dietary fiber on digestibility,

fiber content (e.g. TDF) was plotted against aD of DM or OM [Karasov and

Martnez del Rio, 2007]. In order to test whether an estimation of ME content is

possible in wild carnivores, recommended procedures for ME estimation in food for

domestic dogs and cats from the NRC [2006] were followed and compared to

experimentally determined data. This comparison can either be done on the basis of

digestible energy (DE), using the unmodified experimental data and the transformed

estimated data (addition of the presumed urinary losses), or on the basis of ME,using the unmodified estimated data and the transformed experimental data

(subtracting, in dogs, 5.2 MJ/kg digestible CP from DE). Because energy

requirements and contents for dogs and cats are usually expressed on an ME basis,

the second approach was used.

For unprocessed foods, such as whole prey or raw meat or homecooked

meat (with cooking temperatures not exceeding 1001C, i.e. excluding the use of

pressure cookers), the NRC [2006] recommends the use of Atwater factors for the

estimation of ME (16.7 kJ/g CP; 16.7 kJ/g NfE; 37.7 kJ/g EE in dogs; and 35.6 kJ/g

EE in cats). Commercial foods based on raw meat, such as typical commercial North

American carnivore diets, and also fish, were included in this category. In the case of

several bear diets, a proxy for NfE was calculated using TDF rather than CF values,

which were not analyzed in the respective studies. The resulting NfE values were 0%;

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TABLE

1.

Literaturesourcesusedinthisstudy

Carnivor

e

group

Spec

ies

Sources

Domestic

dogs

List

ofsourcesavailableonrequest

Domestic

cats

List

ofsourcesavailableonrequest

Canids

Alopexlagopus,Canislatrans

,Chrysocyon

brac

hyurus,

Lycaeonpictus,

Pseudalope

xculpaeus,

Urocyoncinereoargenteus,Vulpesvulpes

Harrisetal.,1951;LitvaitisandMau

tz,1976,1980;Hamor,1983;Rouvinenetal.,

19

91;SzymeczkoandSkrede,199

1;BallandGolightly,1992;Barbozaetal.,

19

94;AhlstromandSkrede,1995,1998;Dahlmanetal.,2002;Ahlstrometal.,

20

03;Silvaetal.,2005;Childs-SanfordandAngel,2006

Felids

Acinonyxjubatus,Caracalcaracal,Felisconcolor,

F.margarita,

F.pardalis,F

.viverrina,F.

temminckii,

Leptailurusserval,

Lynxlynx,

L.ru

fus,Neo

felis

nebulosa,

Pantheraleo,P.onca,

P.pardus,

P.

tigris,

Prionailurus

bengalensis,U

nciauncia

Golleyetal.,1965;Morrisetal.,1974;WittmeyerMills,1980;Barbie

rsetal.,1982;

HackenburgerandAtkinson,1983;Hamor,1983;Wynne,1989;Allenetal.,

19

95;Crisseyetal.,1997;Edward

setal.,2001;Bechertetal.,2002;Armato

et

al.,2003;Altmanetal.,2005;V

esteretal.,2008

Hyenids

Crocutacrocuta,Protelescris

tatus

Ham

or,1983

Mustelid

sEnhydralutris,

Lontracanade

nsis,

Martespennati,

Mustelanigripes,

M.nivalis,M.putorius,

M.vison,

Taxideataxus

Sinclairetal.,1962;Allenetal.,1964;RobertsandKirk,1964;Morr

isetal.,1974;

M

oors,1977;Davisonetal.,1978

;Austrengetal.,1979;Skrede,

1979;Glem-

Hansen,1980;Harlow,1981;Chw

alibogetal.,1982;Costa,1982

;Rouvinen,

19

90;SzymeczkoandSkrede,1990;RouvinenandKiiskinen,1991

excl.high-ash

diets;Borsting,1992;Engbergetal.,1993;AhlstromandSkrede,

1995,1998;

Borstingetal.,1995;Hellingaetal.,1997;Mertinetal.,1999;Polonen,2000;

Tausonetal.,2001;Feketeetal.,

2005;Whiteetal.,2007

Pinniped

sEumetopiasjubatus,Halichoerusgrypus,

Monac

hussc

hauinslandi,O

dobenusrosmarus,

Phoca

groenlan

dica,

P.

hispida,P.vitulina

Keiv

eretal.,1983a;Ronaldetal.,1

984a;Fisheretal.,1992a;Martenssonetal.,

19

94;Lawsonetal.,1997a,b;Goodman-Loweetal.,1999a;RosenandTrites,

20

00;Rosenetal.,2000;Trumble

etal.,2003;TrumbleandCastellini,2005

Ursids

Tremarctosornatus,Ursusam

ericanus,

U.arctos,

U.maritimus

Patton,1975;BunnellandHamilton

,1983;Best,1985a;BrodyandPelton,1987;

PritchardandRobbins,1990;Swe

nsonetal.,1999;Goldmanetal.,2001;Rode

et

al.,2001;Felicettietal.,2003;Jansenetal.,2003

aGrossenergycontentofdietsfedwerecalculatedusingcrudenutrients.

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they were not used in the comparisons of NfE digestibility but only in thecomparisons of experimental and estimated ME content. The GE measurements

made by bomb calorimetry reported in several studies (on pinnipeds and polar bears,

indicated in Table 1) differed distinctively from GE values calculated on the basis of

the crude nutrients; in these cases, the calculated GE data were used to derive the

experimental DE and ME.

For processed diets, such as complete dog and cat food, which are usually

pelleted, extruded, or canned, the approach using Atwater factors is not

recommended [NRC, 2006]. The energy content of such diets should instead be

estimated by an approach that estimates energy digestibility via the fiber (CF or

TDF) content. However, in our data set, studies that used such processed foods in

wild carnivores did not report digestibility values for energy; therefore, this approach

could not be tested for processed foods.

Linear regression was performed using SPSS 16.0 (SPSS Inc., Chicago, IL),

and 95% confidence intervals (CI) were calculated for the individual factors of the

respective equations.

RESULTS

Protein digestion is similar for domestic dogs and cats (Fig. 2A). The regression

lines of the domestic animals (variables given in Table 2) are used as comparison forthe wild animal groups. Canids (Fig. 2B), felids and hyenids (Fig. 2C), mustelids

(Fig. 2D), pinnipeds (Fig. 2E), and ursids (Fig. 2F) all show a similar pattern as the

domestic animals. Accordingly, the respective regression equations are similar, and

95% CI for factors are generally overlapping (Table 2). Coefficients for the

regression slope mostly vary between 0.80 and 0.98, indicating a high true protein

digestibility. Exotic felids are the notable exception; in this group, the available data

result in a regression with a slope significantly higher than 1.0 (Table 2). This would

indicate that the true protein digestibility is 4100%a physical impossibility.

These data include results from a study on tigers fed muscle meat only

[Hackenburger and Atkinson, 1983] in which very high apparent protein digestibility

coefficients were measured, and one very low digestibility measured in one individual

sand cat [Crissey et al., 1997]. If these values were excluded, the true protein

Fig. 1. Different ways to present data on nutrient content and aD, using protein in studieswith bears as example (sources see Table 1). (A) The aD of a nutrient (for which a constanttrue digestibility and constant endogenous losses can be assumed) increases with the dietarycontent of that nutrient. (B) The digestible nutrient content of the diet increases linearly withthe nutrient content (Lucas principle).


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digestibility was 96%, and the CI showed overlap with that of other groups

(Table 2). Among all animal groups, there was a high correlation between the

calculated parameters a and b in Table 2 (R50.985, Po0.0001; using the values

for cats without outliers), indicating that differences between groups were not of asystematic nature (e.g. a higher true digestibility at similar endogenous losses, or

higher endogenous losses at similar digestive efficiency), but due to a stochastic effect

of data scatter around a common regression line.

Fat digestion differs between domestic dogs and cats (Fig. 3A); this is the

reason why for cats, a slightly lower factor of 35.6 kJ/g EE rather than 37.7 kJ/g EE

and is used in the estimation of ME from fat (see Methods). When compared to the

regression lines of the domestic animals (variables given in Table 3), canids (Fig. 3B),

felids and hyenids (Fig. 3C), mustelids (Fig. 3D), pinnipeds (Fig. 3E), and ursids

(Fig. 3F) all resemble the pattern in domestic dogs rather than that of domestic cats.

Accordingly, the respective regression equations are similar, and 95% CI for factors

are generally overlapping (Table 3). Coefficients for the regression slope mostly vary

between 0.90 and 1.00, indicating a high true fat digestibility. Among all animal

Fig. 2. Relationship between dietary CP and digestible CP contents in (A) domestic dogs andcats, (B) wild canids, (C) wild felids and hyenids, (D) mustelids, (E) pinnipeds, and (F) bears.For sources see Table 1. Regression equations in Table 2.

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TABL

E

2.

Regressionequationsfor

digestiblecrudeprotein(%

drymatter)5

a

dietarycrudeprotein(%

drymatter)1b.

a

reflectsthetrue

digestibilityandb

theendogenouslosses(ingramper100gingesteddrymatter)

n

a

95%CI

P

b

95%CI

P

R2

Cat

190

0.900

0.866;0.934

1.805

3.237;0.338

0.016

0.936

Dog

401

0.947

0.933;0.961

3.139

3.623;2.655

0.977

Canid

59

0.978

0.940;1.015

4.837

6.155;3.519

0.979

Felid(Felidsa)

70(57)

1.126

(0.960)

1.060;1.192

(0.864;1.056)

()

11.943

(3.807)

16.233;7.653

(8.131;0.518)

(n.s.)

0.906

(0.879)

Hyenid

8

0.777

0.442;1.111

0

.001

4.316

11.295;19.927

n.s.

0.843

Muste

lid

146

0.980

0.953;1.008

5.580

6.654;4.507

0.972

Pinnip

ed

27

0.856

0.690;1.002

2.134

7.684;11.935

n.s.

0.818

Ursid

46

0.969

0.930;1.008

4.158

5.626;2.690

0.983

Allwild

356

0.987

0.967;1.007

5.256

6.085;4.426

0.965

Po0.001;n.s.5notsignificant.

aFelidsre-analyzedafterexclusionofoneoutlierwithexceptionallylowdigestiveefficiencyfromCriss

eyetal.[1997]andtheextremelyhighprotein

digestibilitydatafromHackenburger

andAtkinson[1983].Datagivenincludingtherespective95%

CI,statisticalsignificance,andtheoverall

correlationcoefficient.


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Fig. 3. Relationship between dietary EE (crude fat) and digestible EEs contents in (A)domestic dogs and cats, (B) wild canids, (C) wild felids and hyenids, (D) mustelids, (E)pinnipeds, and (F) bears. For sources see Table 1. Regression equations in Table 3.

TABLE 3. Regression equations for digestible crude fat/ether extracts (% dry matter)5 adietary crude fat (% dry matter)1b. a reflects the true digestibility and b the endogenous losses(in gram per 100 g ingested dry matter)

n a 95% CI P b 95% CI P R2

Cat 159 0.900 0.870; 0.930 0.129 0.895; 0.638 n.s. 0.957Dog 392 0.965 0.957; 0.973 0.461 0.649; 0.273 0.993Canid 42 0.981 0.952; 1.010 0.850 1.537; 0.164 0.016 0.991Felid 42 1.002 0.967; 1.037 1.257 2.443; 0.071 0.038 0.988Hyenid 8 1.004 0.956; 1.053 1.160 2.892; 0.573 n.s. 0.998Mustelid 82 0.907 0.846; 0.969 0.250 1.550; 1.050 n.s. 0.915Pinniped 23 0.945 0.914; 0.975 0.547 1.625; 0.530 n.s. 0.995Ursid 11 0.995 0.974; 1.016 0.815 1.628; 0.002 0.050 0.999All wild 208 0.984 0.965; 1.002 1.248 1.769; 0.728 0.981

Po0.001; n.s.5not significant. Data given including the respective 95% CI, statisticalsignificance, and the overall correlation coefficient.

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groups, there was a high correlation between the calculated parameters a and b in

Table 3 (R50.934, P5 0.001), again indicating that differences between groups

were not of a systematic nature, but due to a stochastic effect of data scatter around

a common regression line.

The plots of NfE and digestible NfE content for domestic dogs and cats yield aless uniform pattern than those for protein and fat (Fig. 4A). The data show a high

degree of scatter, mostly due to low apparent NfE digestibility coefficients on

processed diets. Because of an accumulation of low digestibility coefficients in the

lower NfE range in dogs, the slope of the regression line is significantly higher in

dogs than in cats (Table 4). The patterns observed in wild carnivores resemble that of

domestic ones where data are available (Fig. 4BE). Wild canids are a notable

exception with particularly low aD coefficients measured on high-NfE diets in one

study [Dahlman et al., 2002], which leads to a lower slope of regression than in other

carnivore groups (Table 4). The diet used in that study was based on fish meal,

cooked wheat starch, and wheat bran as a fiber source. Among all animal groups,

Fig. 4. Relationship between dietary NfE and apparently digestible NfE contents in (A)domestic dogs and cats, (B) wild canids, (C) wild felids, (D) mustelids, and (E) bears. Forsources see Table 1. Regression equations in Table 3.


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there was a high correlation between the calculated parameters a and b in Table 4

(R50.977, P5 0.004, excluding felids as an outlier with a too small data base),

again indicating that differences between groups were not of a systematic nature, but

due to a stochastic effect of data scatter around a common regression line.

Data for dietary fiber in trials with wild carnivores were hardly published,

making a comparison between groups, let alone species, unfeasible. Dietary TDF

contents were given for some ursid and felid diets. The data indicate no relevantdeviation from regression equations for domestic dogs and cats (Fig. 5).

Because of the similarity in fat digestion between domestic dogs and wild

carnivores (Fig. 3), only the equations for domestic dogs were used for ME

estimation. There was a close fit between the estimated and the experimentally

determined dietary ME content (Fig. 6) except for diets of low digestibilityin

particular, these consisted of two diets fed to foxes that contained native fruits as the

only or the dominant ingredient and had CF levels of 12.515.2% DM [Silva et al.,

2005], and one diet of pine nuts only that contained TDF at 40% DM fed to bears

[Pritchard and Robbins, 1990]. When these three diets were excluded, the regression

equation for MEestimated was 0.835 MEexperimental14.226 (n5 87, R25 0.883,

Po0.001). If the equation for domestic cats was used for the estimation of ME

(with a lower factor for fat), the estimated ME content showed a similar pattern

TABLE 4. Regression equations for digestible nitrogen-free extracts (NfE, % dry matter)5 adietary NfE (% dry matter)1b. a reflects the true digestibility and b the endogenous losses (ingram per 100 g ingested dry matter)

n a 95% CI P b 95% CI P R2

Cat 92 0.836 0.786; 0.886

1.711

3.528; 0.107 0.065 0.925Dog 167 0.962 0.940; 0.985 3.694 4.614; 2.775 0.977Canid 33 0.578 0.444; 0.711 8.291 2.501; 14.081 0.006 0.715Felid 16 0.188 0.140; 0.235 1.688 1.370; 2.005 0.838Hyenid Mustelid 48 0.822 0.784; 0.860 1.443 2.735; 0.151 0.029 0.976Pinniped Ursid 6 0.777 0.695; 0.860 1.257 1.770; 4.283 n.s. 0.994All wild 102 0.770 0.736; 0.804 0.156 1.039; 1.351 n.s. 0.953

Po0.001; n.s.5not significant. Data given including the respective 95% CI, statisticalsignificance, and the overall correlation coefficient.

Fig. 5. Relationship of TDF and the aD of DM in wild felids and ursids as compared todomestic dogs and cats. For data sources see Table 1.

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when compared against experimental data, but a higher systematic deviation from a

slope of 1 (MEestimated5 0.785 MEexperimental15.213; n5 87, R25 0.881, Po0.001).

DISCUSSION

The results of this literature evaluation suggest that mammalian carnivores of

different taxonomic groups share certain common characteristics in digestive efficiency.

The estimation of the energy content of foods based on approaches used in domestic

carnivores [NRC, 2006] appears also feasible for wild carnivores in general.

Data compilations such as the one of this study depend, in their quality, on theaccuracy of the individual contributions from which the data are gathered. Two

examples of potential problems inherent in such data compilations can be found in

this study. Values for the aD of protein were extremely high in a study on tigers

[Hackenburger and Atkinson, 1983], with values between 97 and 99%. The diet used

was pure muscle meat that was only very moderately mineralized (dusted with

calcium lactate); mineralization usually leads to higher CA levels, which depress the

digestibility of crude nutrients, the very high digestibility coefficients in this study

therefore are plausible. The other examples are the values for the GE content of food

offered to polar bears and pinnipeds; these values, determined by bomb calorimetry

in several studies, were lower than the calculated GE content, which translated intodifferent values for the DE and ME content in these diets. Actually, due to the low

sample volumes used, bomb calorimetry is particularly susceptible to erroneous

measurements, and up to five replicate measurements per sample have been

recommended when using this method [Kienzle et al., 2002].

However, such data deviations show that within the precision of digestibility

measurements, there appears to be no reason to suspect fundamental differences in

the digestive efficiency of the various carnivore groups investigated, within the range

of diets investigated. Actually, the high true digestibility coefficients for protein and

fat indicated by the regression equations (Tables 2 and 3) corroborate similar data

compilations in Robbins [1993]. The fact that many intercepts show non-significant

P-values despite generally high R2 (Tables 24) reflects that for many regressions, the

individual data points are far from 0 due to high contents of the respective nutrients

Fig. 6. Comparison of ME content of diets determined by experiment (DE and correctionfor urinary protein losses) and estimated by calculations based on NRC [2006] recommenda-tions for homemade foods (whole prey and diets based on raw meat and fish) for dogs(using Atwater factors; experimental ME for pinnipeds re-calculated by using calculatedvalues based on crude nutrient composition for GE rather than the published data based onbomb calorimetry).


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in the diets used. Therefore, potential differences or similarities in endogenous losses

are difficult to test in the current data. In order to do so, more challenging diets with

lower contents of the respective nutrients would have to be used.

Further determinations of digestibility in captive wild carnivores appear useful

only when aiming at evaluating particular diets that have an unusual nutrientcomposition [e.g. extremely high levels of CA investigated by Rouvinen and

Kiiskinen, 1991] or to test the reliability of energy estimation in wild carnivores on

industrially processed diets (dry or canned food). With respect to comparative

studies, crude nutrient digestibilities on conventional carnivore diets appear unlikely

to yield further promising insights. Only with respect to the fiber content of diets

used is there a lack of data, and future digestibility studies with wild carnivores could

aim to characterize fiber and other more difficult-to-digest components of the foods

used, such as connective tissues, collagen etc.

In theory, differences could exist between different carnivore species in their

adaptation to such difficult-to-digest components. In contrast to herbivores, in which

diet quality decreases with body mass of the species [Owen-Smith, 1988], the converseeffect could be postulated for carnivores. Small carnivore species up to approximately

20 kg of body mass feed on prey that is distinctively smaller than themselves [Carbone

et al., 1999]e.g. domestic cats feed on mice. This small prey is usually consumed

whole, including fur, skin, bones, and connective tissues as well as muscles and

organs. On the contrary, larger carnivores feed on prey within the range of their own

body mass [Carbone et al., 1999], and consequently can afford to selectively feed only

on the more digestible body parts. The largest extant terrestrial carnivore, the polar

bear, preferentially ingests the fat of seals, often ignoring even the still highly (but not

as highly) digestible muscle meat [Stirling and McEwan, 1975]. Actually, larger prey

has been shown to be more digestible than small prey within a carnivores species[Jethva and Jhala, 2004; Ru he et al., 2008]. Therefore, one could hypothesize that

smaller-sized carnivores might be better adapted to less digestible diet components,

potentially via additional microbial fermentative digestion.

Microbial fermentation can and does take place in the large intestine (and the

distal part of the small intestine) of canids and felids [Banta et al., 1979; Kienzle,

1994; Sunvold et al., 1995a,b; Buena et al., 2000; Hesta et al., 2001, 2003; Backus

et al., 2002; Bosch et al., 2008; Janssens et al., 2008; Vester et al., 2008]. Data from

Vester et al. [2008] appear to indicate a higher capability of smaller felids for the

digestion of TDF components (Fig. 7), in accord with the carnivore body size

Fig. 7. Association of body mass and the aD of TDF in felid species of varying body massfrom Vester et al. [2008] (linear regression, R25 0.80, P5 0.042).

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be considered [e.g. differences in the requirement of taurine, vitamins, or

polyunsaturated fatty acids, Morris, 2002]. And although this study is concerned

with digestive physiology rather than behavioral needs, behavioral aspects of the

feeding of captive wild carnivores should not be dismissed [e.g. Law et al., 1997;

McPhee, 2002; Bashaw et al., 2003]. For research in comparative digestivephysiology, the results suggest that tests based on highly digestible diets, such as

raw meat-based diets, offer little potential for interspecific differences, and that more

challenging diets, such as whole (small) prey (e.g. blended to assure a nonselective

intake) or meat diets supplemented with fiber sources, appear more promising.

CONCLUSIONS

1. Literature data suggest that differences in micronutrient requirements and

physical characteristics of the diet notwithstanding, the digestive physiology/

efficiency does not show evident differences between different carnivore groups

(canids, felids, hyenids, mustelids, ursids, pinnipeds) with respect to protein andfat. When comparing species in their capacity to digest crude nutrients for which

endogenous losses must be assumed (e.g. protein and fat), it should be

remembered that the dietary content of these crude nutrients is the most

important determinant of aD.

2. Literature data suggest that an estimation of the energy content of diets for

captive wild carnivores based on whole prey or raw meat can be performed with

sufficient reliability using the approach suggested for homemade diets for

domestic dogs [Atwater factors, NRC, 2006]. The similarity in the influence of

TDF on digestibility between domestic and wild carnivores suggests that until

more data are available, the recommended ME estimation using fiber content[NRC, 2006] can be used. In other words, estimating the energy contents of

carnivore diets for the development of feeding plans for captive carnivores can be

performed reliably using NRC [2006] estimation procedures for domestic

carnivores.

3. For further studies, comparative investigations on the influence of difficult-to-

digest components, such as connective tissue of dietary fiber, appears more likely

to elucidate species differences than the digestibility of crude nutrients.

ACKNOWLEDGMENTS

We thank Barbara Schneider for support in literature acquisition.

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