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Dietary nutrient profiles of wild wolves: insights for optimal dog nutrition?
q
Guido Bosch
1
*, Esther A. Hagen-Plantinga
2
and Wouter H. Hendriks
1,2
1
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
2
Faculty of Veterinary Medicine, Utrecht University, PO Box 80.151, 3508 TD Utrecht, The Netherlands
(Submitted 22 November 2013 – Final revision received 4 April 2014 – Accepted 6 June 2014 – First published online 21 November 2014)
Abstract
Domestic dogs diverged from grey wolves between 13 000 and 17 000 years ago when food waste from human settlements provided a new
niche. Compared to the carnivorous cat, modern-day dogs differ in several digestive and metabolic traits that appear to be more associated
with omnivorous such as man, pigs and rats. This has led to the classification of dogs as omnivores, but the origin of these ‘omnivorous’
traits has, hitherto, been left unexplained. We discuss the foraging ecology of wild wolves and calculate the nutrient profiles of fifty diets
reported in the literature. Data on the feeding ecology of wolves indicate that wolves are true carnivores consuming a negligible amount of
vegetal matter. Wolves can experience prolonged times of famine during low prey availability while, after a successful hunt, the intake of
foods and nutrients can be excessive. As a result of a ‘feast and famine’ lifestyle, wolves need to cope with a highly variable nutrient intake
requiring an adaptable metabolism, which is still functional in our modern-day dogs. The nutritive characteristics of commercial foods
differ in several aspects from the dog’s closest free-living ancestor in terms of dietary nutrient profile and this may pose physiological
and metabolic challenges. The present study provides new insights into dog nutrition and contributes to the ongoing optimisation of
foods for pet dogs.
Key words: Dogs: Cats: Dietary recommendations: Feeding ecology
The domestic dogs (Canis familiaris) and man share a long
history of co-existence that intensified over time to ‘man’s
best friend’ and a ‘family member’ we keep in many of our
homes today. When man lived as nomadic hunter-gatherers,
encampments likely attracted carnivorous grey wolves
(Canis lupus), the dog’s direct ancestors, to scavenge kills or
opportunistically take wounded animals that escaped the
hunt
(1,2)
. After the transition from the Paleolithic to Neolithic
Era between 13 000 and 17 000 years ago, when man
became sedentary and started agriculture in the Fertile
Crescent of the Near or Middle East, a new food niche
emerged consisting of human-derived vegetal and animal
food waste items
(3)
. Wolves opportunistically took advantage
of this niche, gradually becoming accustomed to human con-
tact and, over generations, with the multiple domestication
and/or interbreeding events with their wild counterparts, the
domesticated dog evolved
(2,4)
. Breeding efforts during the last
3000–4000 years and, in particular, over the past two centuries
have resulted in the remarkable morphological and beha-
vioural diversity of dogs we know today
(2,3)
. The majority of
the morphological diversity among dog breeds has a simple
genetic basis dominated by less than four quantitative trait
loci
(5)
. Although most modern-day dogs no longer look like
wolves, they can still interbreed and produce fertile off-
spring
(6)
making dogs a subspecies of wolves. Considering
the relatively short time span in which domestication occurred
and the close genetic relationship, the dog’s genome would
still predominantly be the product of the environmental selec-
tive pressures imposed upon its ancestor, the wolf. Recent
evidence shows that three genes (AMY2B,MGAM and SGLT1)
involved in starch digestion and glucose uptake were the
target of selection during domestication
(7)
. The AMY2B copy
number expansion is, however, not fixed across all dog
breeds. The Saluki, an ancient breed originating from the
Fertile Crescent, showed twenty-nine copies. Ancient breeds
such as the Dingo and Siberian Husky show no or limited the
expansion (three to four copies), which suggests that these
breeds arose alongside hunter-gatherers rather than agricul-
turists
(8)
. These recent studies also show that other metabolic
traits observed in dogs, like capacity to synthesise sufficient
*Corresponding author: G. Bosch, email guido.bosch@wur.nl
q
This article was published as part of the WALTHAM International Nutritional Sciences Symposium Proceedings 2013.
This paper was published as part of a supplement to British Journal of Nutrition, publication of which was supported by an unrestricted educational grant
from Mars Incorporated. The papers included in this supplement were invited by the Guest Editor and have undergone the standard journal formal review
process. They may be cited.
Abbreviations: BW, body weight; ME, metabolisable energy; NFE, N-free extract.
British Journal of Nutrition (2015), 113, S40–S54 doi:10.1017/S0007114514002311
qThe Authors 2014
British Journal of Nutrition
amounts of essential nutrients such as niacin, taurine and
arginine, were unaffected by domestication. Dogs typically
differ in these traits from carnivorous cats (Felis catus) and,
in this respect, resemble omnivorous man, pigs and rats.
Similar to the ‘metabolic idiosyncrasies’ of cats, their carnivor-
ous nature is also reflected in recent studies focusing on the
macronutrient selection by adult cats
(9,10)
. Cats choose a pro-
tein –fat –carbohydrate profile consisting of 52:36:12 % by
energy, which closely matches with the macronutrient profile
of free-roaming cats being 52:46:2 % by energy
(11)
.
The scientific confirmation of the absence of identical or
similar specialised metabolic pathways in dogs has led many
scientists to question the once-firm carnivorous classification
of our domesticated dogs. This ‘omnivorous dog dogma’ has
developed over the past 40 years and has found its way
into authoritative scientific reference books
(12,13)
, nutritional
concepts in pet nutrition and as a general view. The apparent
contradiction between the dogs’ lack of carnivorous traits
similar to cats and their ancestral carnivorous ecology has,
hitherto, been left unexplained. Here, we present an expla-
nation for the origin of the lack of similar ‘idiosyncratic’
metabolic adaptations of dogs compared to cats by taking into
account the foraging ecology and nutrient intake of modern
wolves. A literature review of studies reporting data on diet
compositions based on stomach contents and scat analyses
was used to calculate the nutrient intake of modern wolves.
Dietary and nutrient profiles consumed by wolves
An overview of twenty-six studies reporting fifty diet compo-
sitions of wolves in their natural habitat and based on 31 276
wolf scat and stomach analyses is shown in Table 1. The var-
ious diet compositions reported in the literature show that
wolves in their natural habitat consume a diet predominantly
composed of ungulates but supplemented with smaller mam-
mals such as beavers, hares and rodents (Table 2). In Europe,
the major dietary items consumed were wild boar, moose, roe
deer and red deer. Beavers (Castor fiber) were overall a less
common prey animal but contributed 12·6 % of total percen-
tage of weight in one study conducted in the summer in
Latvia
(14)
. Various other non-ungulate species were consumed
by wolves in Europe but contributed overall little (,7·8 %) to
the total biomass consumed. Other types of animals consumed
were birds, reptiles, insects and fish. In North-America, wolves
preyed predominantly on moose, white-tailed deer and
beaver (Castor canadensis). Diets also contained various
medium-size and small prey animals, with the snowshoe
hare (Lepus americanus) being the most common but their
contribution to the total amount of biomass consumed was
low (#2·5 %). Darimont et al.
(15)
found that considerable
amounts of mustelidae were consumed by wolves in Western
Canada. Other types of animals consumed were birds, insects,
intertidal organisms and fish.
Plant material was identified in scats in several studies, but
the contribution of plant material to the total biomass con-
sumed was not always calculated. For example, Fritts &
Mech
(16)
did not include grass in the food analyses calculation
as it was not considered a food item, although it could
have been ingested intentionally by wolves. For example,
Jedrzejewski et al.
(17)
detected grasses and sedges in 32·6 %
of all faecal samples. Most often, the grass was present in
well-ordered bundles, and in some cases (n5), it occupied
more than 50 % and up to 100 % of the scat by relative
volume
(17)
. It has been hypothesised that consumed grass
may act as a scouring agent against intestinal parasites such
as roundworms and tapeworms (see Peterson
(18)
). Those
studies that did include plant material in their food analyses
reported values between 0·1 and 3 % of the total percentage
of weight. Identifiable fruit items found in scats included
blueberries (Vaccinium spp.)
(16,19 – 21)
, strawberries (Fragaria
spp.)
(16)
and raspberries (Rubus spp.)
(19,22)
, other berries
(Juniperus communis and Vitis vinifera)
(23)
, nuts (Juglans
regia,Corylus avellana,Fagus sylvatica and Castanea
sativa)
(23)
and other fruits (Rosa spp., Malus spp., Pyrus
spp., Prunus spp., Rubus spp. and Sorbus spp.)
(22,23)
. Corn
(Zea mays) was also detected in scats by Wagner et al.
(22)
.
The fruit items contain some energy in the form of carbo-
hydrates (see online supplementary Table S4) but are,
compared to the other dietary items, considerably lower in
most other nutrients making their contribution to the overall
nutrient intake of wolves negligible. Furthermore, it has
been suggested that fruit items are primarily consumed by
pups
(16,21)
. The consumption of fruit items may underlay the
tasting capacity of dogs that cats lack. Dogs have Type D
units of taste receptors that respond to a small number of
‘fruity-sweet’ compounds
(24)
. Consumption of vegetable
matter is also observed in other carnivores such as polar
bears (Ursus maritimus)
(25,26)
and crocodilians
(27)
. Contrary to
popular belief, wolves do not consume the (partly fermented)
vegetable matter in the rumen of ungulates
(18,19,28 – 33)
. During
removal, however, the rumen can be punctured and its con-
tents spilled
(29)
of which some can be consumed along with
other body tissues
(30)
. Furthermore, the rumen lining and the
intestinal wall can be consumed
(29,30)
. Based on these studies
reporting data on the foraging ecology, wolves can be con-
sidered true carnivores in their nature with vegetal matter
being a minor to negligible component of their overall diet.
For the calculation of the nutrient profiles, the data on
the dietary items were combined with data on the nutrient
composition of each dietary item (see online supplementary
material). Similar approaches as used here have been applied
for the evaluation of nutrient profiles of the diet of free-
ranging cats
(11)
, badgers
(34)
, kiwi birds (Apteryx mantelli)
(35)
,
and that of the hunter-gatherers or Palaeolithic diet of
human subjects
(36 – 40)
. The mean dietary DM content was
38·6 % with crude protein contributing the largest part to the
DM content (mean 67·2 % of DM) followed by EE (24·9 %
of DM) and then ash (6·4 % of DM) (Fig. 1). The dietary con-
tent of N-free extract (NFE) was the lowest and contributed
1·4 % to DM. The mean energy content was 2085 kJ/100 g
DM and ranged from 2004 to 2244 kJ/100 g DM. The mean
Ca content was 1·30 g/100 g DM and varied between 0·83
and 2·04 g/100 g DM. The ratio between Ca and P varied
between 0·83 and 1·30 and was on average 1·05. Mean values
for Na and K contents were 0·28 and 0·99 g/100 g DM, respec-
tively, and showed little variation. Mean dietary contents of
Nutrient intake in wild wolves S41
British Journal of Nutrition
Table 1. Overview of the considered studies presenting diet compositions expressed as percentage of weight for inclusion in the calculations to determine the nutrient composition of wild wolf diets
Study
No. Reference Details Period Material Samples (n) Reason for exclusion
1 Andersone & Ozolins
ˇ
(14)
Summer, Latvia April–September Stomachs, scats 246
Winter, Latvia October–March Stomachs, scats 163
2 Ansorge et al.
(81)
Germany Year Scats 192
3 Ballard et al.
(82)
Alaska, USA May–June Scats 5559
4 Barja
(83)
Spain Year Scats 593 HLF .5%
5 Capitani et al.
(84)
A. Susa Valley, Italy Year Scats 194 HLF .5%
B. Pratomagno, Italy Year Scats 355
C. Cecina Valley, Italy Year Scats 118 HLF .5%
6 Ciucci et al.
(85)
Italy Year Scats 217 HLF .5%
7 Ciucci et al.
(86)
Italy Year Scats 200 HLF .5%
8 Chavez & Gese
(87)
A. Minnesota, USA, 1997 Summer–Autumn Scats 199 HLF .5%
B. Minnesota, USA, 1998 Summer–Autumn Scats 101 HLF .5%
C. Minnesota, USA, 1999 Summer– Autumn Scats 232 HLF .5%
9 Cuesta et al.
(88)
A. Area I, Spain Year Stomachs 92 n,94, HLF .5%
B. Area II, Spain Year Stomachs 44 n,94, HLF .5%
C. Area III, Spain Year Stomachs 65 n,94, HLF .5%
D. Area IV, Spain Year Stomachs 12 n,94, HLF .5%
E. Area V, Spain Year Stomachs 13 n,94, HLF .5%
10 Darimont et al.
(15)
British Columbia, Canada June– August Scats 595
11 Forbes & Theberge
(89)
A. Area A, Ontario, Canada Summer Scats 371*
B. Area B, Ontario, Canada Summer Scats 186*
C. Area C, Ontario, Canada Summer Scats 823*
D. Area A, Ontario, Canada Winter Scats 208*
E. Area B, Ontario, Canada Winter Scats 461*
F. Area C, Ontario, Canada Winter Scats 767*
12 Fritts & Mech
(16)
A. Minnesota, USA April–September Scats 670 HLF .5%
B. Minnesota, USA October–March Scats 174
13 Fuller & Keith
(90)
Alberta, Canada May–September Scats 1524
14 Fuller
(19)
Summer, Minnesota, USA April–October Scats NS†
Winter, Minnesota, USA November–March Scats NS†
15 Gade-Jørgensen & Stagegaard
(20)
Summer, Finland May – September Scats 156 HLF .5%
Winter, Finland October–April Scats 104
16 Jedrzejewski et al.
(91)
Summer, Poland May– September Scats 45 n,94
Winter, Poland October–April Scats 99
17 Jedrzejewski et al.
(17)
Summer, Poland May– September Scats 67 n,94
Winter, Poland October–April Scats 344
18 Jedrzejewski et al.
(92)
Poland Year Scats 328
19 Jethva & Jhala
(93)
India Year Scats 1246 HLF .5%
20 Kojola et al.
(94)
A. Area I, Finland Year Scats 167
B. Area II, Finland Year Scats 117
C. Area III, Finland Year Scats 159
21 Lanszki et al.
(95)
Hungary Year Scats 81 n,94
22 Liu & Jiang
(96)
Qinghai, China Year Scats 119 HLF .5%
23 Mattioli et al.
(97)
Italy Year Scats 240 HLF .5%
24 Mattioli et al.
(98)
A. Area ISA, Italy Year Scats 1862
B. Area SAF, Italy Year Scats .113
C. Area VS, Italy Year Scats .97 HLF .5%
D. Area PM, Italy Year Scats .203
E. Area VT, Italy Year Scats .174 HLF .5%
25 Meriggi et al.
(23)
A. Area A, Italy Year Scats 292 HLF .5%
G. Bosch et al.S42
British Journal of Nutrition
Table 1. Continued
Study
No. Reference Details Period Material Samples (n) Reason for exclusion
B. Area B, Italy Year Scats 71 n,94, HLF .5%
C. Area C, Italy Year Scats 156
26 Messier & Cre
ˆte
(99)
A. Area H, Que
´bec, Canada May–November Scats 220
B. Area M, Que
´bec, Canada May–November Scats 408
27 Milanesi et al.
(100)
Italy Year Scats 103 HLF .5%
28 Nowak et al.
(101)
A. Bydgoscz Forest, Poland Year Scats 81 n,94
B. Wałcz Forest, Poland Year Scats 112
C. Rzepin Forest, Poland Year Scats 126
D. Lower Silesia Forest, Poland Year Scats 124
E. Other areas, Poland Year Scats 31 n,94
29 Olsson et al.
(102)
Sweden–Norway Year Scats 684
30 Peterson et al.
(103)
Alaska, USA May–October Scats 592
31 Peterson & Page
(104)
Michigan, USA May– August Scats 2648
32 Pezzo et al.
(105)
Italy Year Stomachs 38 n,94
33 Potvin et al.
(31)
Summer, Que
´bec, Canada May–September Scats 737
Winter, Que
´bec, Canada December–April Scats 429
34 Reed et al.
(106)
Arizona and New Mexico, USA Year Scats 251 HLF .5%
35 Reig & Jedrzejewski
(107)
Poland December– May Scats 15 n,94
36 Sidorovich et al.
(108)
A. Belarus, 1990–1992 Year Scats 447
B. Belarus, 1994–1996 Year Scats 363 HLF .5%
C. Belarus, 1999–2000 Year Scats 375 HLF .5%
37 S
´mietana & Klimek
(109)
Poland Year Scats 221 HLF .5%
38 Thurber & Peterson
(110)
Michigan, USA June– August Scats 3637
39 Tremblay et al.
(21)
A. Malaie pack, Que
´bec, Canada, 1996 May – October Scats 505
B. Grands-Jardin pack, Que
´bec, Canada, 1996 May – October Scats 118
C. Malaie pack, Que
´bec, Canada, 1997 May– October Scats 866
D. Grands-Jardin pack, Que
´bec, Canada, 1997 May–October Scats 132
40 Vos
(111)
Portugal April – October Scats 87 n,94
41 Wagner et al.
(22)
A. Germany, 2001/2002 Year Scats 100*
B. Germany, 2002/2003 Year Scats 61* n,94
C. Germany, 2003/2004 Year Scats 202*
D. Germany, 2004/2005 Year Scats 322*
E. Germany, 2005/2006 Year Scats 239*
F. Germany, 2006/2007 Year Scats 337*
G. Germany, 2007/2008 Year Scats 232*
H. Germany, 2008/2009 Year Scats 397*
HLF, human-linked foods; A– H, study details with regard to area and/or year.
* Number of scats is not specified in the original manuscript; number of scats after personal communication with authors (i.e. G Forbes and C Wagner).
† Number of scats is not specified in the original manuscript. Considering the large number of total scats (n2386), it was assumed to be larger than ninety-four for both seasons.
Nutrient intake in wild wolves S43
British Journal of Nutrition
Table 2. Data of dietary profiles of wild wolves found in the literature (% of weight)
Study no.
Dietary item...
123510 11 12 13 14 15
SW B ABCD E F B SWW
Mammals
Ungulates
Black-tailed deer 22 22264·6 2222 2 2 2 2222
Caribou 22 210·4 2 22222 2 2 2 2222
European bison 22 222 22222 2 2 2 2222
Fallow deer 22 22þ*22222 2 2 2 2222
Livestock 2·3 4·4 220·3 22222 2 22·8 222þ
Moose þ†þ‡281·1 0 0 82·1 57·6 64 87·3 64·6 71·7 20·7 89·3 2296·0
Mouflon 225·0 2þ§22222 2 2 2 2222
Mountain goats 22 22þ§9·12222 2 2 2 2222
Red deer þ†þ‡56·72þ*22222 2 2 2 2222
Roe deer þ†þ‡21·62þ*22222 2 2 2 2222
White-tailed deer 22 2 22 24·7 27·3 24·8 4·3 22·5 13·5 75·3 290·0 98·0 2
Wild boars 19·3 32·1 16·0 280·8 22222 2 2 2 2222
Unknown 0·3 22þ2 22222 2 2 2 2222
Non-ungulates
Beavers 12·6 3·1 23·6 22·1 13·2 15·1 11·1 8·9 13·6 7·6 29·0 7·5 2þ
Bears 22 2225·8 222 2 2 2 0·4 2þþ2
Cats 22 222 22222 2 2 2 2222
Dogs þ2 222 22222 2 2 2 222 þ
Hares or rabbits 0·1 20·8 2·5 22þþþ2·3 1·3 0·0 0·5 1·6 2·5 2·0 1·0
Insectivorakþ2 222 22222 2 2 2 2222
Lynx{22 222222222222þþ2
Medium-size** 0·2 1·3 222 22222 2 2 2 þþþ2
Mustelidae†† þ22228·0 22222222þþþ
Rodents‡‡ 2·0 1·1 þ2·2 20·7 222 2 2 2 2 þþþþ
Squirrels§§ 22 20·1 222222222þþþ2
Birds 0·2 2þþ2þ222 2 2 2 0·0 þ222
Reptiles þ2 222 22222 2 2 2 2222
Fish 22 þ22 þ222 2 2 2 2 þ222
Intertidal organisms 22 222 þ2222 2 2 2 2222
Insects þ22þ222222222222þ
Vegetation 0·2 0·1 2þ2þ22 –22222þþ2
Other 22 224·5 þþþþþ þ þ0·3 þ222
Total 99·4 98·9 100·1 99·9 100 99·9 100 100 99·9 102·8 102 92·8 100 99·9 100 100 97·0
G. Bosch et al.S44
British Journal of Nutrition
Table 2. Continued
Study no.
16 17 18 20 24 25 26 28 29 30
Dietary item...
WW ABCABDCABBCD
Mammals
Ungulates
Black-tailed deer 2 2 222 22222 2 2 2 2222
Caribou 22221·3 25·6 17·3 2222 2 2 2 2222
European bison 21·8 222 22222 2 2 2 2222
Fallow deer 22222222218·9 2227·0 2·0 22
Livestock 21·2 0·4 22 24·4 0·7 2·6 2·0 22222þ2
Moose 221·1 76·2 69·2 80·6 222 267·0 86·0 22264·0 97·2
Mouflon 2222222224·9 2 2 2 2222
Mountain goatskk 2 2 2 22 22222 2 2 2 2222
Red deer 31·5 277·2 22 22222·5 2224·9 26·7 17·8 22
Roe deer 2·9 3·9 1·8 22 219·1 18·8 10·8 14·3 2242·9 33·1 57·6 26·2 2
White-tailed deer 2 2 222 22222 þþ2 2222
Wild boars 7·8 12·7 9·7 22 258·7 70·1 79·2 49·6 2216·2 26·8 19·6 22
Unknown 56·8 69·0 8·6 22 22222 2 2 5·1 3·2 0·9 22
Non-ungulates 2
Beavers 2 2 222 2222221·0 8·0 5·1 0·3 0·1 þ1·0
Bears 2 2 2 22 22222 2 2 2 2222
Cats 2 2 222 22222 2 2 þ2222
Dogs 2 2 222 22222 2 21·6 0·8 222
Hares or rabbits 0·2 0·1 222 222221·0 þ3·2 1·9 1·8 þ1·8
Insectivorak20·2 222 22222 2 2 þ2222
Lynx{2 2 222 22222 2 2 2 2222
Medium-size** 0·6 0·3 1·3 22 2222þþþ1·0 0·2 27·8 þ
Mustelidae†† 2 2 222 22222 2 2 2 20·2 22
Rodents‡‡ þ0·1 222 22222·2 þ þ þ þþþþ
Squirrels§§ þ2 222 22222 5·0 2·0 þ2222
Birds þþ222 22222 2 2 þþ2þþ
Reptiles þþ2 22 22222 2 2 2 2222
Fish 2 2 222 22222 2 2 2 222þ
Intertidal organisms 2 2 222 22222 2 2 2 2222
Insects þ2 222 22220·0 222222þ
Vegetation 0·1 0·1 222 22220·0 2·0 3·0 þþþ2þ
Other 2222·5 5·2 2·1 4·7 3·0 5·3 2·8 4·0 1·0 2 2222
Total 99·9 100·5 100·1 100 100 100 86·9 92·6 97·9 97·2 100 100 100 100 100 98 100
Nutrient intake in wild wolves S45
British Journal of Nutrition
Table 2. Continued
Study no.
31 33 36 38 39 41
Dietary item...
SWA ABCDAC D E FGH
Mammals
Ungulates
Black-tailed deer 22 222 22222 2 2 2 222
Caribou 22 2220·6 1·1 1·7 17·9 2222222
European bison 22 222 22222 2 2 2 222
Fallow deer 22 222 22220·0 0·0 0·3 0·0 1·1 2·3 3·5
Livestock 22 23·7 222220·0 0·0 0·0 0·5 1·1 0·2 0·1
Moose 82·9 44·5 16·0 32·5 88·5 96·3 65·2 95·9 67·9 2222222
Mouflon 22 222 22228·6 0·0 0·3 0·0 0·7 1·4 0·0
Mountain goatskk 22 222 22222 2 2 2 222
Red deer 22 222 222234·9 19·6 28·0 19·4 25·1 23·2 26·4
Roe deer 22 23·6 2222236·0 40·2 48·7 63·8 53·7 53·0 50·8
White-tailed deer 213·5 80·5 22 22222 2 2 2 222
Wild boars 22 252·3 2222219·2 36·1 19·4 11·1 12·6 17·1 15·2
Unknown 22 222 22222 2 2 2 222
Non-ungulates
Beavers 16·6 36·5 2·0 3·3 10·8 1·5 33·2 1·9 13·3 0·0 0·0 0·0 0·0 0·0 0·0 0·0
Bears 22 2221·5 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·0
Cats 22 2þ222220·0 0·0 0·0 0·0 0·2 0·0 0·0
Dogs 22 20·3 222222222222
Hares or rabbits 0·4 222·2 0·8 0·2 0·0 0·1 0·0 1·3 3·8 3·4 4·3 4·9 2·5 4·0
Insectivorak22 222 22220·0 0·0 0·0 0·1 0·0 0·0 0·0
Lynx{22 2220·0 0·2 222222222
Medium-size** 22 20·9 2þ0·0 0·3 0·0 0·0 0·1 0·0 0·1 0·1 0·0 0·0
Mustelidae†† 22 222 22220·0 0·0 0·0 0·0 þ0·0 0·0
Rodents‡‡ 22 2þ222220·0 0·2 0·0 0·6 0·2 0·1 0·1
Squirrels§§ 22 222 220·0 0·2 2222222
Birds 22 20·9 222220·0 þþþþþþ
Reptiles 22 222 22222 2 2 2 222
Fish 22 222 22220·0 þ0·0 0·0 þ0·0 0·0
Intertidal organisms 22 222 22222 2 2 2 222
Insects 22 222 22222 2 2 2 222
Vegetation 22 20·3 2þ2þ20·0 0·0 0·0 0·1 0·3 0·1 þ
Other 25·5 1·5 22 22222 2 2 2 222
Total 99·9 100 100 100 100·1 100·1 99·7 99·9 99·3 100·0 100·0 100·1 100·0 100·0 99·9 100·1
S, summer diet; W, winter diet; A– H, study details with regard to area and/or year (see Table 1); 2, food item was not mentioned; þ, food item was present but not clearly quantified.
* Comprise together 14·2 % of total biomass consumed; for further calculations, percentage of weight (PW) was equally divided across these species.
† Comprise together 62·2 % of total biomass consumed; for further calculations, PW was equally divided across these species.
‡ Comprise together 56·8 % of total biomass consumed; for further calculations, PW was equally divided across these species.
§ Comprise together 0·2 % of total biomass consumed; for further calculations, PW was equally divided across these species.
kAlso including shrews (Sorex araneus) and hedgehogs (Erinaceus spp.).
{Includes bobcats (Lynx rufus) and Canadian lynx (Lynx canadensis).
** Including foxes (Vulpes spp.), porcupines (Erethizon dorsatum), raccoons (Procyon lotor), raccoon dogs (Nyctereutes procyonoides) and striped skunks (Mephitis mephitis).
†† Including badgers (Meles meles and Taxidea taxus), ermines (Mustela erminea), ferrets (Mustela putorius), martens (Martes spp.), minks (Mustela lutreola and Neovison vison), otters (Lutra lutra and Lontra canadensis) and
weasels (Mustela nivalis).
‡‡ Including various species of the rodent family Cricetidae, e.g. microtins or voles (Microtus spp. and Myodes spp.), mice (Apodemus spp.) and muskrat (Ondatra zibethicus).
§§ Also including marmots (Marmota spp.).
kk Also including chamois (Rupicapra spp.).
G. Bosch et al.S46
British Journal of Nutrition
Cu, Zn and Fe were 0·66, 10·8 and 27·3 mg/100 g DM, respect-
ively. Dietary Mg varied between 76 and 109 mg/100 g DM
with a mean value of 91 mg/100 g DM.
As the nutrient digestibility of most dietary items has not
been described in the literature yet, it was not possible to
take nutrient bioavailability into account. Considering the
digestibility of the macronutrients, proteins are expected to
vary most with the more digestible proteins being present in
soft tissues (e.g. liver and large muscles) and poorly digestible
proteins in bone and hide. The latter are consumed in the later
stages of prey consumption
(32)
or during scavenging
(30)
.With
the organs and muscles contributing to the majority of the
edible proportion of ungulate prey, most proteins may be
considered to be well digestible and amino acids to be avail-
able for metabolism. Bone is one of the major nutrient sources
of Ca and, to a lesser extent, P and Mg, whereas other body
tissues provide more than 95 % of Na, K, Cu, Zn and Fe. For
these nutrients, bioavailability is dependent not only on the
dietary source but also on the nutritional status of the
animal. When nutrient supply is limiting or excessive, absorp-
tion is up- or down-regulated by homeostatic mechanisms
(41)
.
In general, the bioavailability of micronutrients and trace
elements in soft animal tissues such as muscle and liver is
higher than in vegetal sources
(42)
. Altogether, the nutrient pro-
files described provide the hitherto best estimates available for
wild wolves but with the limitation that the bioavailability of
these nutrients remains to be determined.
The selected protein–fat– carbohydrate profile of wolves in
the present study (54:45:1 % by energy) is different from that
in dogs, i.e. 30:63:7 % by energy
(10)
. Furthermore, profiles
were similar between the five dog breeds studied (i.e. papil-
lon, miniature schnauzer, cocker spaniel, Labrador retriever
and St Bernard), indicating that the rapid divergence among
dog breeds over the past 200 years was not substantially
reflected in the macronutrient priorities among the modern-
day breeds of dogs
(10)
. Hewson-Hughes et al.
(10)
attributed
the lipid selection of dogs to the early domestication period
when dogs became ‘adapted’ to a human-associated diet.
During this period, such a diet would have consisted of
human-derived vegetal and animal food waste items
(3)
.
Furthermore, commensal species such as rodents may have
been a food source for early dogs, as it is (a small) part of
many diets for wolves (see Table 2). It is beyond the scope
of the present study to consider possible waste items from
human settlements, but it would be unlikely that hunter-
gatherers disposed such lipid-rich food items when famines
and seasonal food shortages were common in those agricul-
tural societies
(43,44)
as the intake of energy from lipids would
have been vital for survival. The preference of dogs for
lipid-rich diets may thus be a trait that has evolved during
the evolution of its ancestor the wolf rather than during
early dog domestication.
Fluctuating food availability
Wolves are carnivores that cope with distinct periods of feast
and famine, which is different from the ecology of wildcats.
These profound fluctuations in food availability have resulted
80(a)
(b)
(c)
2400
2300
2200
2100
2000
190 0
1800
1700
1600
1·4
1·3
1·2
1·1
1·0
Ratio
0·9
0·7
140
120
100
80
60
40
20
0
0·8
70
Content (g/100 g or g/100 g DM)
Content (kJ/100 g DM)
Content (g/100 g DM)Content (g/100 g DM)
Content (g/100 g DM)
60
50
40
30
20
10
0
3·5
3·0
2·5
2·0
1·5
1·0
0·5
0·0
14
12
10
8
6
4
2
0
DM
Ca
Cu Zn Fe Mg
PNaK
Ca/P
CP EE NFE Ash Energy
Fig. 1. Calculated macronutrient (a), micronutrient (b) and trace mineral (c)
composition of the natural diet (n43) of wild wolves. The upper and lower
hinges represent the 75th and 25th percentiles of the dataset. The band
within the box represents the median. The whiskers extend to the 5 % and
95 % CI. For (a), the calculated means are: DM, 38·6 (SEM 0·1) g/100 g;
crude protein (CP), 67·2 (SEM 0·3) g/100 g DM; ethereal extract (EE), 24·9
(SEM 0·3) g/100 g DM; nitrogen-free extract (NFE), 1·4 (SEM 0·0) g/100 g
DM; ash, 6·4 (SEM 0·1) g/100 g DM; and energy, 2085 (SEM 8) kJ/100 g DM.
For (b), the calculated means are: calcium, 1·30 (SEM 0·04) g/100 g DM;
phosphorus, 1·23 (SEM 0·02) g/100 g DM; sodium, 0·28 (SEM 0·00) g/100 g
DM; potassium, 0·99 (SEM 0·01) g/100 g DM; and calcium/phosphorus, 1·05
(SEM 0·02) g/100 g DM. For (c) the calculated means are: copper, 0·66
(SEM 0·01) mg/100 g DM; zinc, 10 ·8 (SEM 0·13) mg/100 g DM; iron, 27·3 (SEM
0·3) mg/100 g DM; and magnesium, 91 (SEM 1) mg/100 g DM.
Nutrient intake in wild wolves S47
British Journal of Nutrition
in different coping strategies by wolves. As indicated earlier,
wolves hunt in packs on large ungulates and opportunistically
scavenge a varied but essentially animal-based diet. During
periods of abundant prey availability, wolves ingest large
amounts of highly nutritious animal tissues, with a feast
meal weight of up to 22 % of their body weight (BW), and
a preferential consumption of internal organs such as
liver
(30)
. During prolonged periods of low prey availability,
a pack of wolves may go days without catching large prey
during which time they consume smaller prey and some left-
overs of old prey
(33)
. Wolves have been observed to sca-
venge on bone and hide for even up to 10 weeks
(30)
.
Wolves also consume prey parts they cached for later con-
sumption
(45 – 47)
. When food is available, wolves can quickly
recover again from weight loss during fasting. Captive
(sedentary) wolves fasted for 10 d lost 7 –8 % of their BW,
which was replenished after 2 d of consuming white-tailed
deer meat with amounts between 15 and 19 % of their BW
per d
(48)
. Also dogs can resist prolonged periods of
famine. An adult Scotch collie named ‘Oscar’ has the longest
fast on record; after an astonishing 117 d and weighing only
37 % of its initial BW, the fast was stopped
(49)
. In contrast,
wildcats (Felis silvestris), the domestic cat’s ancestor
(50)
, are
predominantly solitary and hunt individually catching a var-
iety of mainly small mammals and birds weighing only
approximately 1 % of their BW
(51)
. Wildcats, therefore,
require multiple small prey items per d and thrive in habitats
abundant in prey year-round.
During times of low food availability, dogs have been
shown to very effectively utilise body fat resources for
energy purposes. de Bruijne & van den Brom
(52)
found that
peripheral utilisation of ketone bodies in fasting dogs was
very efficient. It was estimated that the contribution of
ketone bodies to the daily energy requirement of dogs
increased from 7 % in the overnight-fasted state to 13 % after
10 d of starvation. Also, the capacity to decrease metabolic
losses and to endogenously synthesise essential nutrients
for ongoing metabolic processes will be vital for survival
and, as such, has been conserved throughout evolution.
Wolves efficiently conserve body proteins by down-regulating
enzymes involved in amino acid catabolism to cope with
famine
(53)
. Such protein sparing capacity is also observed
in other carnivores that face prolonged periods of famine
such as polar bears (U. maritimus)
(54)
, Antarctic fur seal
(Arctocephalus gazella) pups
(55)
and chicks of king penguins
(Aptenodytes patagonica)
(56)
. Cats, on the contrary, are less
capable of conserving protein as they maintain high activities
of amino acid catabolising enzymes for gluconeogenesis
(57)
.
This difference becomes apparent when fed a diet without
protein; adult dogs produce half as much urinary urea as
cats (116 v. 243 mg/kg
0.75
per d)
(58)
. The feline feeding eco-
logy with regular nutrient intake relaxed selection pressures
for conserving certain metabolic pathways, which is reflected
by low enzymatic synthesis capacity of cats for a number of
nutrients (e.g. niacin, taurine, arginine and arachidonic
acid)
(57)
. It can be hypothesised that other large carnivores
with a feast-or-famine lifestyle such as polar bears, cougars
(Puma concolor), lions (Panthera leo) or pinnipeds also
have capacities to synthesise essential nutrients such as
arginine and niacin or may have developed other metabolic
strategies that are key for their survival.
As mentioned earlier, the strong preference for lipids shown
by dogs
(10)
could also be linked to the feeding ecology of
wolves. Preferential lipid intake by wolves at times of prey
abundance increases adipose tissue that serves as an energy
store for periods of low prey abundance. The importance of
lipid intake may also be reflected in the preservation of
post-carnassial molars in wolves (and dogs) during evolution.
These molars are used to crush large bones
(59)
and provide
access to the lipid-rich marrow (see online supplementary
Table S3). The extent of seasonal fasting in nature may also
explain why mink (Mustela vison), which preys on small ani-
mals such as wildcats and encounter periods of famine
(60)
,
selects an intermediate diet containing 35 % protein and 50 %
lipid by energy
(61)
. This latter observation, however, requires
further study as it may merely reflect the selection for macro-
nutrients as in their normal diet fed over generations
(61)
.
Macronutrient profiling of other carnivorous species varying
in lifestyle might provide insight if profiles can be linked to
the extent of seasonal fasting in nature.
At times of feast, when large ungulates are killed, wolves in
general rapidly open the body cavity and consume the
internal organs such as the heart, lungs, liver, spleen and
kidneys
(30)
. The liver of an ungulate would provide stored
vitamin A and potentially glycogen. Dogs transport vitamin A
as retinyl esters in the blood and clear blood retinyl through
the kidney
(62)
, which makes them more resistant to hyper-
vitaminosis A and can be considered as functional for
wolves. Although it is unclear what proportion of the glycogen
stores remains after the chase and catch of the prey, intestinal
amylase and hepatic glucokinase activities as present in
domestic dogs would be functional for glycogen utilisation.
Furthermore, liver contains glycogen that, like starch from
plants, can be digested and utilised by the use of intestinal
amylase and hepatic glucokinase. The higher activities of
these enzymes in dogs than in cats
(63,64)
may be consistent
with a diet periodically high in liver and muscle tissue rather
than a diet high in plant starch.
Dogs share numerous typical carnivorous characteristics
with cats (see Fig. 2). For example, both species lack salivary
amylase, have a short and simple gastrointestinal tract, con-
jugate bile acids with taurine and are unable to synthesise
vitamin D
(12)
. The metabolic adaptations, such as protein
sparing and endogenous niacin synthesis capacity, facilitating
survival during times of low dietary nutrient availability
are similar to those observed in omnivores, and this may be
a key factor to explain differences in digestive physiology
and metabolism between today’s domestic dogs and cats.
Omnivores, such as pigs and rats, may not experience similar
periods of famine like wolves but more specifically encounter
fluctuations in amounts and types of vegetal and animal matter
in their diets (e.g. due to season). The omnivorous pig and
rat, consuming lower and fluctuating amounts of protein
due to seasonal changes in availability of vegetal and animal
matter, can reduce urea excretion even further to 70 and
60 mg/kg
0·7 5
per d
(58)
, respectively. It can be speculated that
G. Bosch et al.S48
British Journal of Nutrition
the array of metabolic traits shaped by a feast-or-famine
lifestyle enabled carnivorous wolves to metabolically thrive
on relatively lower-nutritious human food wastes. These
wolves were likely already capable of utilising the starch
from plants. Glycogen stored in muscles and in particular
liver from prey is, after consumption by carnivores, processed
similarly using pancreatic amylase, small intestinal GLUT and
hepatic glucokinase. Those dogs with genetic mutations in
the AMY2B,MGAM and SGLT1 genes were more fit to this
new niche opened up by man
(7)
. Furthermore, this niche
Table 3. Approximated dietary nutrient profiles reported in the literature of wild wolves, profiles
as affected by a wolf’s ranking and during scavenging, and minimal and recommended allowance (RA)
nutrient composition for dogs in growth and at maintenance
National Research Council
(12)
Growth Maintenance Commercial
(66)
Item Unit Wolf* Minimum RA Minimum RA Dry Moist
ME kJ/100 g DM 2085 1745 1849
CP g/MJ ME 32·2 10·8 13·5 4·8 6·0 16·1 17·4
EE g/MJ ME 11·9 5·1 3·3 9·3 12·0
NFE g/MJ ME 0·7 25·8 20·0
Ca g/MJ ME 0·62 0·48 0·72 0·12 0·24 0·76 0·65
P g/MJ ME 0·59 0·60 0·18 0·58 0·50
Na g/MJ ME 0·13 0·13 0·02 0·05 0·24 0·29
K g/MJ ME 0·48 0·26 0·24 0·40 0·48
Cu mg/MJ ME 0·32 0·65 0·36 NA NA
Zn mg/MJ ME 5·2 2·4 6·0 3·6 NA NA
Fe mg/MJ ME 13·1 4·3 5·3 1·8 NA NA
Mg mg/MJ ME 43·4 10·8 23·9 10·8 35·9 68·8 54·1
ME, metabolisable energy; CP, crude protein; EE, ethereal extract; NFE, N-free extract; NA, not available.
* Average dietary profiles reported in the literature (n50, see Table 2).
Traits similar to cats Traits functional for famine Traits functional for feast
Carnassials for
shearing
Jaws fixed
for cutting
Vitamin A transported
in blood as retinyl
esthers
Bile acids conjugated
with taurine only
Short and simple
intestinal tract
Urinary
clearance of
retinyl esthers
Traits affected by domestication
Canines and
incisors for
holding
Taste sensors
for amino acids
and nucleotides
No salivary
amylase
Increased glucokinase
activity for glucose use
Stomach
extension for
large meals
Slower catabolism
of amino acids for
conserving body N
Flat premolars
and molars for
crushing
Synthesis of arginine,
taurine, niacin and
arachidonic acid
Efficient peripheral use
of ketone bodies Increased capacity for
glycogen/starch digestion
and for glucose uptake
Stomach pH
approximately 2
Fig. 2. Omnivorous dog traits revisited. Dogs are classified as omnivores based on traits that are different from carnivorous cats. The authors hypothesise that
these ‘omnivorous’ traits, highlighted in white boxes, reflect the typical feast-or-famine lifestyle of the carnivorous dog’s ancestor, the wolf. Traits outlined in green
and blue are functional for periods of feast and famine, respectively. Dogs share numerous traits with cats, shown in orange. Capacities of traits shown in grey
are the target during domestication
(7)
.
Nutrient intake in wild wolves S49
British Journal of Nutrition
favoured wolves smaller in body size, which required less
energy, and those more tolerant to human proximity
(65)
.
Comparison with dog nutrition
The wolf’s natural dietary nutrient profile differs in several
aspects from the nutrient guidelines and in nutritive charac-
teristics of commercial foods. Table 3 provides the average
dietary nutrient profile for wild wolves (based on n50 diets)
reported in the present study (in units/MJ metabolisable
energy (ME)) compared to the minimum nutrient requirement
of growing dogs and of dogs at maintenance as provided
by the National Research Council
(12)
. The physiological
minimum nutrient requirement have been accurately deter-
mined for several nutrients and can be considered to represent
the limit of the adaptation capacity of domestic dogs in
relation to dietary nutrient concentrations
(11)
. Contents of
crude protein, Ca, Zn, Fe and Mg in the average wolf diet
are well above the set minimum nutrient requirement for
these nutrients, although the bioavailability of these nutrients
is unknown.
The recommended allowance set by National Research
Council
(12)
for dietary Ca for growth and Cu for growth and
maintenance is higher than that found in the average diet of
wolves (Table 3). Furthermore, the average Ca content of
the wolf’s diet is lower than that found in commercial dry
foods, and the wolf’s dietary Na and Mg contents are lower
than the average for commercial dry and moist dog foods. It
should be noted, however, that due to higher energy require-
ments, the actual daily nutrient intake of wolves is higher than
that of the average sedentary pet dog living in a temperate
environment. The daily energy requirement of adult wolves
(35 kg BW) has been estimated to be 25 025 kJ ME
(29)
or
1739 kJ/kg
0·7 5
BW, which is 3·2 times higher than the daily
energy requirements for the maintenance of adult dogs
(544 kJ/kg
0·7 5
BW)
(12)
. Thus, the actual daily intake of micro-
nutrients and trace elements included in the profile would
be higher in wild wolves than in pet dogs fed foods with
nutrient contents close to the recommended allowance
values and fed the average commercial foods reported in
Table 3. Little information is available about how nutrient
requirements vary with energy expenditure in dogs
(12)
, but it
is reasonable to assume that the increase in energy require-
ments for physical activity and thermoregulation does not
result in an equal increase in reported micronutrients and
trace elements. Hence, the wolf’s metabolism may be accus-
tomed to high dietary availability of these nutrients.
The nutritive characteristics of commercial foods may differ
in several aspects from the wolf’s natural dietary nutrient
profile, and this may pose physiological and metabolic chal-
lenges that dogs need to cope with. The average nutrient
composition of commercial high-quality dry extruded (n93)
and moist canned (n39) dog foods
(66)
is presented in
Table 3. The average dietary NFE content of dogs fed dry
and moist commercial foods is substantially higher (25·8 and
20·0 g/MJ ME, respectively) than the dietary NFE content of
wolves (0·7 g/MJ ME). The NFE content in dog foods mainly
originates from the starch of cereal grains. These starches
are cooked during processing and are, therefore, generally
well digested by dogs, with ileal apparent digestibility reach-
ing values of above 99 % for starches in dry extruded
diets
(67)
. For wolves, the NFE intake would be conditionally
high and in the form of glycogen, i.e. when a liver of a
large prey, containing approximately 10·5 g/MJ ME in a
white-tailed deer
(68)
(see also later texts), is consumed. To
the authors’ knowledge, the glycaemic index of glycogen is
unknown, but wolves are not likely to be exposed to a daily
glycaemic load that pet dogs fed commercial dry and wet
foods may experience. Although the dog has been shown to
have an increased digestive and absorptive capacity to cope
with starch-containing foods compared to wolves, the impact
of a consistent high amount of absorbed glucose on the dog’s
health and longevity remains to be determined.
The average content of EE of the wolf’s diet was slightly
higher than the average content normally observed in com-
mercial foods. The origin of lipids in both diets, however,
would also be different resulting in a different fatty acid profile
consumed. Dog foods contain lipids from vegetable oil (e.g.
soyabean, sunflower and maize) and/or animal origin (e.g.
pork fat, beef tallow, poultry fat and fish oil). Lipids from
vegetable origin are typically higher in n-6 PUFA than in n-3
PUFA. In addition, with regard to the n-3 PUFA, vegetable
oils are relatively rich in a-linolenic acid (18 : 3n-3) whereas
those from animal origin are typically high in EPA (20 : 5n-3)
and DHA (22 : 6n-3). The PUFA profile lipids derived from ani-
mals vary according to diets fed during rearing. The n-6:n-3
ratios in muscle lipids of cattle and chickens raised in captivity
range between 6:1 and 19:1
(69)
whereas those for wild mule
deer and red deer contain a ratio of approximately 2:1 to
3:1
(70)
, closely matching the ratio of 2:1 of wolf subcutaneous
fat
(71)
. Also, modern aquaculture produces fish that contain
less n-3 PUFA than do their wild counterparts, although the
n-6:n-3 ratio is still very low (1:6 for cultured and 1:11 for wild
salmon (Salmo salar)
(72)
). The vegetable and animal lipid
sources commonly used in dog foods result in higher n-6:n-3
ratio than that of lipids from wild animals. Commercial dog
foods (n12) showed an average n-6:n-3 ratio of 8:1, ranging
from 5:1 to 17:1
(73)
. Furthermore, the average PUFA concen-
tration in the lipid fraction of these dog foods was 24·4 %
(range 18·1 – 43·1 %)
(73)
, which is lower than 31·3 and 28·7 %
PUFA content in muscle lipids of mule deer and red deer,
respectively
(70)
. Considering the involvement of n-3 PUFA
(EPA and DHA) in numerous physiological processes, including
the mediation of inflammatory and immune responses, renal
functioning, cardiovascular health and neurologic develop-
ment
(72,74 – 76)
, the fatty acid profiles of our pet dog foods
deserves careful (re)consideration. The impact of a relative
shortage of n-3 fatty acids in the commercial diet on the func-
tioning immune system of dogs requires further study.
Undigested dietary fractions provide substrates for the
microbiota in the distal small and large intestine and the
type of substrates can be expected to differ between those
of a wolf’s diet and dry and moist dog foods. Whole prey
and, specifically, lower-quality animal tissues (e.g. hide and
bones) provide low digestible or indigestible substances
such as cartilage, collagens and glycosaminoglycans, with
G. Bosch et al.S50
British Journal of Nutrition
specific fermentative characteristics
(77)
other than fibres of
vegetal origin and indigestible proteins in processed foods.
Given the involvement of the intestinal microbial community
in host physiology, immune function and behaviour
(78)
, the
effect of these specific substances on the canine microbial
composition and activity and on canine (intestinal) health
warrants further investigation.
The concept of ‘natural’ foods that may better match the
physiological and metabolic make-up of dogs is comparable
to the paradigm that the Palaeolithic hunter-gatherer diet
would better fit modern man than our current nutrition.
The discordance hypothesis originally described by Eaton &
Konner
(37,79)
states that the human genome evolved to adapt
to conditions that no longer exist, the change from Palaeolithic
to current nutrition occurred too rapidly for adequate genetic
adaptation and the resulting mismatch helps to cause some
common ‘diseases of civilisation’ such as diabetes mellitus,
obesity and dental disease
(80)
. Furthermore, the nutrient
intake of modern-day hunter-gatherers is suggested to rep-
resent a reference standard for modern human nutrition and
a model for defence against these diseases. To what extent
the discordance hypothesis may also apply for dogs and to
what extent the nutrient profile of the wolf’s diet is optimal
for pet dogs are subjects for study. The nutrient profile
described here originates from a wolf population living
under severe physiological and climatic conditions and in
which nutrition is a precondition for species survival and
procreation. In general, our domestic dogs have a much
more sedentary lifestyle, regular meals and a longer lifespan,
which may have a significant effect on nutrient requirements
and handling. Dogs have adapted to a starch-rich diet
(i.e. increased enzymatic capacity to digest starch and increa-
sed glucose uptake capacity) and are able to cope with large
variations in nutrient intake. There are also situations of
reduced adaptation capacity (such as geriatrics and chronic
disease) in which the consumption of a diet that requires an
adaptable metabolism may place the animal under stress.
Nevertheless, the wolves’ feeding ecology and nutrient
intake may provide valuable information to further improve
our understanding of the origin of the dogs’ digestive phy-
siology and metabolism and possibly provide new leads for
optimising individual health and longevity.
Conclusions and implications
Data on the wolf’s feeding ecology show that the progenitors
of our modern-day dogs were adaptive, true carnivores and
not omnivores. During times of feast and famine, wolves
would have had to cope with a variable nutrient intake requir-
ing an adaptable metabolism, which is still functional in our
modern-day dogs. These traits may also allow wolves to
make the transition from carnivory to omnivory during domes-
tication. The nutritive characteristics of commercial foods
differ in several aspects from the dog’s closest free-living pro-
genitor in terms of dietary nutrient profile, and this may pose
physiological and metabolic challenges that dogs need to
cope with. The question remains to what extent the approxi-
mated nutrient profile also optimally supports health and
longevity of domestic dogs with a more sedentary lifestyle
and a longer lifespan in a different environment. The present
study describing the wolf’s dietary nutrient profile may pro-
vide an impetus for further research in this area similar to
research activities in the field of human nutrition
(79)
. Labora-
tory, clinical and epidemiological studies would be required
in which the nutrient profile and other aspects of a wolf’s
diet are translated and evaluated for their contribution to the
health and longevity in today’s pet dogs.
Supplementary material
To view supplementary material for this article, please visit
http://dx.doi.org/10.1017/S0007114514002311
Acknowledgements
This research was funded by Wageningen University and
Utrecht University. All authors contributed fundamentally to
the present manuscript. G. B. contributed to all facets includ-
ing research design, data collection, calculations and writing
the initial manuscript. E. A. H.-P. and W. H. H. contributed
to research design, data interpretation and manuscript prep-
aration. The authors thank David L. Mech for his willingness
to answer the questions relating to the feeding ecology of
wolves. Laura de Vries, Gijs Hulsebosch, Joyce Neroni and
Esther Lichtenberg are thanked for their contributions at the
beginning of this research. There are no conflicts of interest.
References
1. Clutton-Brock J (1995) Origins of the dog: domestication
and early history. In The Domestic Dog: Its Evolution, Beha-
viour and Interactions with People, pp. 7–20 [JA Serpell,
editor]. Cambridge, UK: Cambridge University Press.
2. Driscoll CA, Macdonald DW & O’Brien SJ (2009) From
wild animals to domestic pets, an evolutionary view of
domestication. Proc Natl Acad Sci U S A 106, 9971 – 9978.
3. Driscoll CA & MacDonald DW (2010) Top dogs: wolf
domestication and wealth. J Biol 9, 10.
4. VonHoldt BM, Pollinger JP, Lohmueller KE, et al. (2010)
Genome-wide SNP and haplotype analyses reveal a rich
history underlying dog domestication. Nature 464,
898–902.
5. Boyko AR, Quignon P, Li L, et al. (2010) A simple genetic
architecture underlies morphological variation in dogs.
PLoS Biol 8, e1000451.
6. Vila
`C & Wayne RK (1999) Hybridization between wolves
and dogs. Conserv Biol 13, 195–198.
7. Axelsson E, Ratnakumar A, Arendt ML, et al. (2013) The
genomic signature of dog domestication reveals adaptation
to a starch-rich diet. Nature 495, 360 – 364.
8. Freedman AH, Gronau I, Schweizer RM, et al. (2014)
Genome sequencing highlights the dynamic early history
of dogs. PLoS Genet 10, e1004016.
9. Hewson-Hughes AK, Hewson-Hughes VL, Colyer A, et al.
(2013) Consistent proportional macronutrient intake
selected by adult domestic cats (Felis catus) despite vari-
ations in macronutrient and moisture content of foods
offered. J Comp Physiol B 183, 525–536.
10. Hewson-Hughes AK, Hewson-Hughes VL, Colyer A, et al.
(2013) Geometric analysis of macronutrient selection in
Nutrient intake in wild wolves S51
British Journal of Nutrition
breeds of the domestic dog, Canis lupus familiaris.Behav
Ecol 24, 293–304.
11. Plantinga EA, Bosch G & Hendriks WH (2011) Estimation of
the dietary nutrient profile of free-roaming feral cats: poss-
ible implications for nutrition of domestic cats. Br J Nutr
106, S35–S48.
12. NRC (2006) Nutrient Requirements of Dogs and Cats.
Washington, DC: National Academies Press.
13. Hand MS, Thatcher CD, Remillard RL, et al. (editors) (2010)
Small Animal Clinical Nutrition, 5th ed. Topeka, KS: Mark
Morris Institute.
14. Andersone Z & Ozolins
ˇJ (2004) Food habits of wolves
Canis lupus in Latvia. Acta Theriol 49, 357–367.
15. Darimont CT, Price MHH, Winchester NN, et al. (2004)
Predators in natural fragments: foraging ecology of wolves
in British Columbia’s central and north coast archipelago.
J Biogeogr 31, 1867–1877.
16. Fritts SH & Mech LD (1981) Dynamics, movements, and
feeding ecology of a newly protected wolf population in
Northwestern Minnesota. Wildl Monogr 80, 3– 79.
17. Jedrzejewski W, Jedrzejewska B, Okarma H, et al. (2000)
Prey selection and predation by wolves in Białowiez
˙a
Primeval Forest, Poland. J Mammal 81, 197–212.
18. Peterson RO (1977) Wolf ecology and prey relation-
ships on Isle Royale. PhD Thesis, Purdue University, West
Lafayette, IN.
19. Fuller TK (1989) Population dynamics of wolves in North-
Central Minnesota. Wildl Monogr 105, 1–41.
20. Gade-Jørgensen I & Stagegaard R (2000) Diet composition
of wolves Canis lupus in east-central Finland. Acta Theriol
45, 537–547.
21. Tremblay J-P, Jolicoeur H & Lemieux R (2001) Summer
food habits of gray wolves in the boreal forest of the Lac
Jacques-Cartier highlands, Que
´bec. Alces 37, 1–12.
22. Wagner C, Holzapfel M, Kluth G, et al. (2012) Wolf (Canis
lupus) feeding habits during the first eight years of its
occurrence in Germany. Mamm Biol 77, 196 – 203.
23. Meriggi A, Brangi A, Matteucci C, et al. (1996) The feeding
habits of wolves in relation to large prey availability in
northern Italy. Ecography 19, 287– 295.
24. Bradshaw JW (2006) The evolutionary basis for the feeding
behavior of domestic dogs (Canis familiaris) and cats
(Felis catus). J Nutr 136, S1927–S1931.
25. Derocher AE, Andriashek D & Stirling I (1993) Terrestrial
foraging by polar bears during the ice-free period in
western Hudson Bay. Arctic 46, 251 – 254.
26. Iversen M, Aars J, Haug T, et al. (2013) The diet of polar
bears (Ursus maritimus) from Svalbard, Norway, inferred
from scat analysis. Polar Biol 36, 561–571.
27. Platt SG, Elsey RM, Liu H, et al. (2013) Frugivory and
seed dispersal by crocodilians: an overlooked form of
saurochory? J Zool 291, 87–99.
28. Bump JK, Peterson RO & Vucetich JA (2009) Wolves
modulate soil nutrient heterogeneity and foliar nitrogen
by configuring the distribution of ungulate carcasses.
Ecology 90, 3159–3167.
29. Peterson RO & Ciucci P (2003) The wolf as a carnivore.
In Wolves: Behavior, Ecology, and Conservation, pp. 104– 111
[LD Mech and L Boitani, editors]. Chicago, IL: University
of Chicago Press.
30. Stahler DR, Smith DW & Guernsey DS (2006) Foraging and
feeding ecology of the gray wolf (Canis lupus): lessons
from Yellowstone National Park, Wyoming, USA. J Nutr
136, S1923–S1926.
31. Potvin F, Jolicoeur H & Huot J (1988) Wolf diet and prey
selectivity during two periods for deer in Quebec: decline
versus expansion. Can J Zool 66, 1274–1279.
32. Wilmers CC, Crabtree RL, Smith DW, et al. (2003) Trophic
facilitation by introduced top predators: grey wolf subsidies
to scavengers in Yellowstone National Park. J Anim Ecol 72,
909–916.
33. Mech LD (1970) The Wolf: The Ecology and Behavior of
an Endangered Species. Garden City, NY: The Natural
Histroy Press.
34. Remonti L, Balestrieri A & Prigioni C (2011) Percentage of
protein, lipids, and carbohydrates in the diet of badger
(Meles meles) populations across Europe. Ecol Res 26,
487–495.
35. Potter MA, Hendriks WH, Lentle RG, et al. (2010)
An exploratory analysis of the suitability of diets fed to a
flightless insectivore, the North Island brown kiwi (Apteryx
mantelli), in New Zealand. Zoo Biol 29, 537–550.
36. Eaton SB, Eaton SB III & Konner MJ (1997) Paleolithic nutri-
tion revisited: a twelve-year retrospective on its nature and
implications. Eur J Clin Nutr 51, 207–216.
37. Eaton SB & Konner M (1985) Paleolithic nutrition. A con-
sideration of its nature and current implications. N Engl
J Med 312, 283–289.
38. Kuipers RS, Luxwolda MF, Dijck-Brouwer JDA, et al. (2010)
Estimated macronutrient and fatty acid intakes from an East
African Paleolithic diet. Br J Nutr 104, 1666–1687.
39. Cordain L, Miller JB, Eaton SB, et al. (2000) Plant – animal
subsistence ratios and macronutrient energy estimations in
worldwide hunter-gatherer diets. Am J Clin Nutr 71,
682–692.
40. Eaton SB (2006) The ancestral human diet: what was it and
should it be a paradigm for contemporary nutrition? Proc
Nutr Soc 65,1–6.
41. Fairweather-Tait S, Hurrell RF, Van Dael P, et al. (1996)
Bioavailability of minerals and trace elements. Nutr Res
Rev 9, 295–324.
42. Nohr D & Biesalski HK (2007) ‘Mealthy’ food: meat as a
healthy and valuable source of micronutrients. Animal 1,
309–316.
43. Prentice AM (2001) Fires of life: the struggles of an ancient
metabolism in a modern world. Nutr Bull 26, 13 – 27.
44. Prentice AM, Rayco-Solon P & Moore SE (2005) Insights
from the developing world: thrifty genotypes and thrifty
phenotypes. Proc Nutr Soc 64, 153 – 161.
45. Mech LD and Boitani L (editors) (2003) Wolves: Behavior,
Ecology, and Conservation. Chicago, IL: University of
Chicago Press.
46. Harrington FH (1981) Urine-marking and caching behavior
in the wolf. Behaviour 76, 280–288.
47. Phillips DP, Danilchuk W, Ryon J, et al. (1990) Food-
caching in timber wolves, and the question of rules of
action syntax. Behav Brain Res 38,1–6.
48. Kreeger TJ, DelGiudice GD & Mech LD (1997) Effects of
fasting and refeeding on body composition of captive
gray wolves (Canis lupus). Can J Zool 75, 1549–1552.
49. Howe PE, Mattill HA & Hawk PB (1912) Distribution of
nitrogen during a fast of one hundred and seventeen
days. J Biol Chem 11, 103–127.
50. Driscoll CA, Menotti-Raymond M, Roca AL, et al. (2007) The
Near Eastern origin of cat domestication. Science 317,
519–523.
51. Pearre S & Maass R (1998) Trends in the prey size-based
trophic niches of feral and house cats Felis catus L.
Mammal Rev 28, 125–139.
G. Bosch et al.S52
British Journal of Nutrition
52. de Bruijne JJ & van den Brom WE (1986) The effect of
long-term fasting on ketone body metabolism in the dog.
Comp Biochem Physiol B 83, 391–395.
53. Kreeger TJ (2003) The internal wolf: physiology, patho-
logy, and pharmacology. In Wolves: Behavior, Ecology,
and Conservation, pp. 192–217 [LD Mech and L Boitani,
editors]. Chicago, IL: University of Chicago Press.
54. Derocher AE, Nelson RA, Stirling I, et al. (1990) Effects of
fasting and feeding on serum urea and serum creatinine
levels in polar bears. Mar Mammal Sci 6, 196–203.
55. Arnould JPY, Green JA & Rawlins DR (2001) Fasting meta-
bolism in Antarctic fur seal (Arctocephalus gazella) pups.
Comp Biochem Physiol A 129, 829–841.
56. Cherel Y & Le Maho Y (1985) Five months of fasting in
king penguin chicks: body mass loss and fuel metabolism.
Am J Physiol Regul Integr Comp Physiol 18, R387 – R392.
57. Morris JG (2002) Idiosyncratic nutrient requirements of
cats appear to be diet-induced evolutionary adaptations.
Nutr Res Rev 15, 153–168.
58. Hendriks WH, Moughan PJ & Tarttelin MF (1997) Urinary
excretion of endogenous nitrogen metabolites in adult
domestic cats using a protein-free diet and the regression
technique. J Nutr 127, 623–629.
59. Biknevicius AR & Van Valkenburg B (1996) Design
for killing: craniodental adaptations of predators. In
Carnivore Behavior, Ecology, and Evolution, pp. 393 – 428
[JL Gittleman, editor]. Ithaca, NY: Cornell University Press.
60. Mustonen AM, Puukka M, Pyykonen T, et al. (2005) Adap-
tations to fasting in the American mink (Mustela vison):
nitrogen metabolism. J Comp Physiol B 175, 357 – 363.
61. Mayntz D, Nielsen VH, Sørensen A, et al. (2009) Balancing
of protein and lipid intake by a mammalian carnivore, the
mink, Mustela vison.Anim Behav 77, 349–355.
62. Schweigert FJ, Ryder OA, Rambeck WA, et al. (1990) The
majority of vitamin A is transported as retinyl esters in the
blood of most carnivores. Comp Biochem Physiol A Comp
Physiol 95, 573–578.
63. Kienzle E (1993) Carbohydrate metabolism of the cat. 1.
Activity of amylase in the gastrointestinal tract of the cat.
J Anim Physiol Anim Nutr 69, 92–101.
64. Washizu T, Tanaka A, Sako T, et al. (1999) Comparison of
the activities of enzymes related to glycolysis and gluco-
neogenesis in the liver of dogs and cats. Res Vet Sci 67,
205–206.
65. Coppinger RP and Coppinger L (editors) (2001) Dogs: A
Startling New Understanding of Canine Origin, Behavior
and Evolution. New York, NY: Scribner.
66. Debraekeleer J (2000) Appendix L: nutrient profiles of
commercial dog and cat foods. In Small Animal Clinical
Nutrition, 4th ed., pp. 1073–1083 [MS Hand, CD Thatcher,
RL Remillard and P Roudebush, editors]. Topeka, KS: Mark
Morris Institute.
67. Murray SM, Flickinger AE, Patil AR, et al. (2001) In vitro
fermentation characteristics of native and processed cereal
grains and potato starch using ileal chyme from dogs.
J Anim Sci 79, 435–444.
68. McCoullough DR & Ullrey DE (1983) Proximate mineral
and gross energy composition of white-tailed deer. J Wildl
Manage 47, 430–441.
69. Rule DC, Broughton KS, Shellito SM, et al. (2002) Compari-
son of muscle fatty acid profiles and cholesterol concen-
trations of bison, beef cattle, elk, and chicken. J Anim Sci
80, 1202–1211.
70. Cordain L, Watkins BA, Florant GL, et al. (2002) Fatty acid
analysis of wild ruminant tissues: evolutionary implications
for reducing diet-related chronic disease. Eur J Clin Nutr
56, 181–191.
71. Ka
¨kela
¨R & Hyva
¨rinen H (1996) Site-specific fatty acid
composition in adipose tissues of several northern aquatic
and terrestrial mammals. Comp Biochem Physiol B 115,
501–514.
72. Simopoulos AP (2002) The importance of the ratio of
omega-6/omega-3 essential fatty acids. Biomed Pharmac-
other 56, 365–379.
73. Ahlstrøm Ø, Krogdahl A, Vhile SG, et al. (2004) Fatty
acid composition in commercial dog foods. J Nutr 134,
S2145–S2147.
74. Bauer JE (2006) Facilitative and functional fats in diets of
cats and dogs. J Am Vet Med Assoc 229, 680–684.
75. Bauer JE (2007) Responses of dogs to dietary omega-3 fatty
acids. J Am Vet Med Assoc 231, 1657–1661.
76. Bosch G, Beerda B, Hendriks WH, et al. (2007) Impact of
nutrition on canine behaviour: current status and possible
mechanisms. Nutr Res Rev 20, 180–194.
77. Depauw S, Bosch G, Hesta M, et al. (2012) Fermentation
of animal components in strict carnivores: a comparative
study with cheetah fecal inoculum. J Anim Sci 90,
2540–2548.
78. Sekirov I, Russell SL, Antunes LC, et al. (2010) Gut micro-
biota in health and disease. Physiol Rev 90, 859 – 904.
79. Konner M & Boyd Eaton S (2010) Paleolithic nutrition:
twenty-five years later. Nutr Clin Pract 25, 594– 602.
80. Eaton SB, Konner M & Shostak M (1988) Stone agers in
the fast lane: chronic degenerative diseases in evolutionary
perspective. Am J Med 84, 739–749.
81. Ansorge H, Kluth G & Hahne S (2006) Feeding ecology of
wolves Canis lupus returning to Germany. Acta Theriol 51,
99–106.
82. Ballard WB, Whitman JS & Gardner CL (1987) Ecology of an
exploited wolf population in South-Central Alaska. Wildl
Monogr 98, 3–54.
83. Barja I (2009) Prey and prey-age preference by the Iberian
wolf Canis lupus signatus in a multiple-prey ecosystem.
Wildl Biol 15, 147–154.
84. Capitani C, Bertelli I, Varuzza P, et al. (2004) A comparative
analysis of wolf (Canis lupus) diet in three different Italian
ecosystems. Mamm Biol 69, 1–10.
85. Ciucci P, Boitani L, Pelliccioni ER, et al. (1996) A compari-
son of scat-analysis methods to assess the diet of the wolf
Canis lupus.Wildl Biol 2, 37–48.
86. Ciucci P, Tosoni E & Boitani L (2004) Assessment of the
point-frame method to quantify wolf Canis lupus diet by
scat analysis. Wildl Biol 10, 149–153.
87. Chavez AS & Gese EM (2005) Food habits of wolves in
relation to livestock depredations in northwestern Minne-
sota. Am Midl Nat 154, 253–263.
88. Cuesta L, Barcena F, Palacios F, et al. (1991) The trophic
ecology of the Iberian wolf (Canis lupus signatus Cabrera,
1907). A new analysis of stomach’s data. Mammalia 55,
239–254.
89. Forbes GJ & Theberge JB (1996) Response by wolves to
prey variation in central Ontario. Can J Zool 74, 1511 – 1520.
90. Fuller TK & Keith LB (1980) Wolf population dynamics and
prey relationships in northeastern Alberta. J Wildl Manage
44, 583–602.
91. Jedrzejewski W, Jedrzejewska B, Okarma H, et al. (1992)
Wolf predation and snow cover as mortality factors in the
ungulate community of the Bialowiez
˙a National Park
Poland. Oecologia 90, 27–36.
92. Jedrzejewski W, Schmidt K, Theuerkauf J, et al. (2002) Kill
rates and predation by wolves on ungulate populations
Nutrient intake in wild wolves S53
British Journal of Nutrition
in Białowiez
˙a primeval forest (Poland). Ecology 83,
1341–1356.
93. Jethva BD & Jhala YV (2004) Foraging ecology, economics
and conservation of Indian wolves in the Bhal region of
Gujarat, Western India. Biol Conserv 116, 351– 357.
94. Kojola I, Huitu O, Toppinen K, et al. (2004) Predation
on European wild forest reindeer (Rangifer tarandus)by
wolves (Canis lupus) in Finland. J Zool 263, 229–235.
95. Lanszki J, Ma
´rkus M, U
´jva
´ry D, et al. (2012) Diet of wolves
Canis lupus returning to Hungary. Acta Theriol 57,
189–193.
96. Liu B & Jiang Z (2003) Diet composition of wolves Canis
lupus in the northeastern Qinghai-Tibet Plateau, China.
Acta Theriol 48, 255–263.
97. Mattioli L, Apollonio M, Mazzarone V, et al. (1995) Wolf
food habits and wild ungulate availability in the Foreste
Casentinesi National Park, Italy. Acta Theriol 40, 387– 402.
98. Mattioli L, Capitani C, Avanzinelli E, et al. (2004) Predation
by wolves (Canis lupus) on roe deer (Capreolus capreolus)
in north-eastern Apennine, Italy. J Zool 264, 249 – 258.
99. Messier F & Cre
ˆte M (1985) Moose-wolf dynamics and the
regulation of moose populations. Oecologia 65, 503 – 512.
100. Milanesi P, Meriggi A & Merli E (2012) Selection of wild
ungulates by wolves Canis lupus (L. 1758) in an area of
the Northern Apennines (North Italy). Ethol Ecol Evol 24,
81–96.
101. Nowak S, Myslajek RW, Klosinska A, et al. (2011) Diet
and prey selection of wolves (Canis lupus) recolonising
Western and Central Poland. Mamm Biol 76, 709– 715.
102. Olsson O, Wirtberg J, Andersson M, et al. (1997)
Wolf Canis lupus predation on moose Alces alces and roe
deer Capreolus capreolus in south-central Scandinavia.
Wildl Biol 3, 13–23.
103. Peterson RO, Woolington JD & Bailey TN (1984) Wolves
of the Kenai Peninsula, Alaska. Wildl Monogr 88, 3 – 52.
104. Peterson RO & Page RE (1988) The rise and fall of Isle
Royal wolves, 1975–1986. J Mammal 69, 89 – 99.
105. Pezzo F, Parigi L & Fico R (2003) Food habits of wolves in
central Italy based on stomach and intestine analyses. Acta
Theriol 48, 265–270.
106. Reed JE, Ballard WB, Gipson PS, et al. (2006) Diets of free-
ranging Mexican gray wolves in Arizona and New Mexico.
Wildl Soc Bull 34, 1127–1133.
107. Reig S & Jedrzejewski W (1988) Winter and early spring
food for some carnivores in the Bialowieza National Park,
Eastern Poland. Acta Theriol 33, 57–65.
108. Sidorovich VE, Tikhomirova LL & Jedrzejewska B (2003)
Wolf Canis lupus numbers, diet and damage to livestock
in relation to hunting and ungulate abundance in northeast-
ern Belarus during 1990 – 2000. Wildl Biol 9, 103 – 111.
109. S
´mietana W & Klimek A (1993) Diet of wolves in the
Bieszczady Mountains, Poland. Acta Theriol 38, 245–251.
110. Thurber JM & Peterson RO (1993) Effects of population
density and pack size on the foraging ecology of gray
wolves. J Mammal 74, 879–889.
111. Vos J (2000) Food habits and livestock depredation of two
Iberian wolf packs (Canis lupus signatus) in the north of
Portugal. J Zool 251, 457–462.
G. Bosch et al.S54
British Journal of Nutrition
