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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]
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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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