Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris

Abstract

Although many herbivores and omnivores have been shown to balance their intake of macronutrients when faced with nutritionally variable foods, study of this ability has been relatively neglected in carnivores, largely on the assumption that prey are less variable in nutrient composition than the foods of herbivores and omnivores and such mechanisms therefore unnecessary. We performed diet selection studies in 5 breeds of adult dog (Canis lupus familiaris) to determine whether these domesticated carnivores regulate macronutrient intake. Using nutritional geometry, we show that the macronutrient content of the diet was regulated to a protein:fat:carbohydrate ratio of approximately 30%:63%:7% by energy, a value that was remarkably similar across breeds. These values, which the analysis suggests are dietary target values, are based on intakes of dogs with prior experience of the respective experimental food combinations. On initial exposure to the diets (i.e., when naive), the same dogs self-selected a diet that was marginally but significantly lower in fat, suggesting that learning played a role in macronutrient regulation. In contrast with the tight regulation of macronutrient ratios, the total amount of food and energy eaten was far higher than expected based on calculated maintenance energy requirements. We interpret these results in relation to the evolutionary history of domestic dogs and compare them to equivalent studies on domestic cats.

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Original Article
Geometric analysis of macronutrient selection
in breeds of the domestic dog, Canis lupus
familiaris
Adrian K.Hewson-Hughes,a Victoria L.Hewson-Hughes,a AlisonColyer,a Andrew T.Miller,a Scott
J.McGrane,a Simon R.Hall,a Richard F.Butterwick,a Stephen J.Simpson,b and DavidRaubenheimerc
aWALTHAM® Centre for Pet Nutrition, Freeby Lane, Waltham-on-the-Wolds, Melton Mowbray,
Leicestershire LE14 4RT, UK,bSchool of Biological Sciences and the Charles Perkins Centre, University
of Sydney, New South Wales, Australia, and cInstitute of Natural Sciences, Massey University, Auckland,
New Zealand
Although many herbivores and omnivores have been shown to balance their intake of macronutrients when faced with nutri-
tionally variable foods, study of this ability has been relatively neglected in carnivores, largely on the assumption that prey are
less variable in nutrient composition than the foods of herbivores and omnivores and such mechanisms therefore unnecessary.
We performed diet selection studies in 5 breeds of adult dog (Canis lupus familiaris) to determine whether these domesticated
carnivores regulate macronutrient intake. Using nutritional geometry, we show that the macronutrient content of the diet was
regulated to a protein:fat:carbohydrate ratio of approximately 30%:63%:7% by energy, a value that was remarkably similar across
breeds. These values, which the analysis suggests are dietary target values, are based on intakes of dogs with prior experience of
the respective experimental food combinations. On initial exposure to the diets (i.e., when naive), the same dogs self-selected a
diet that was marginally but signicantly lower in fat, suggesting that learning played a role in macronutrient regulation. In con-
trast with the tight regulation of macronutrient ratios, the total amount of food and energy eaten was far higher than expected
based on calculated maintenance energy requirements. We interpret these results in relation to the evolutionary history of
domestic dogs and compare them to equivalent studies on domestic cats. Key words: Canis lupus, carnivore nutrition, domesti-
cation, domestic dog, geometric framework, macronutrient regulation, predation, right-angled mixture triangles. [Behav Ecol]
INTRODUCTION
In the study of animal foraging, there has long been a focus
on single nutritional currencies, most notably energy (in
optimal foraging theory, sometimes with nutrients or second-
ary compounds included as linear constraints) or nitrogen (in
nutritional ecology) (Raubenheimer etal. 2009). Over recent
years, however, the application of an alternative approach,
geometric analysis, has demonstrated that the balance of
energetic macronutrients exerts a powerful, and often domi-
nant, effect on the nutrition-related behavior, physiology, and
performance of animals (Simpson and Raubenheimer 2012).
This is reected, inter alia, in the divergent macronutri-
ent regulatory responses among feeding guilds, with dietary
breadth, and in association with development mode and the
possession of nutrition-related symbionts (see Discussion).
A fundamental, but little-researched, area in the evolution
of nutritional regulatory strategies concerns the impacts of
domestication and the associated selection pressures on the
preferred dietary macronutrient proles of animals. In a
recent study of domestic cats, Hewson-Hughes et al. (2011)
used nutritional geometry to demonstrate that cats actively
selected a diet with a protein:fat:carbohydrate energy bal-
ance of 52:36:12, and interpreted this to reect their largely
unchanged status as an obligate predator. That the selected
macronutrient balance in that study was not an artifact of the
captive history of the cats, or of the experimental conditions,
but rather provides insights into the evolutionary history of
these felids, is suggested by 2 facts. First, not only did the cats
select a specic macronutrient balance but they also altered
the proportions of different experimental food combina-
tions eaten to maintain the target nutrient balance. Second,
Plantinga etal. (2011) have subsequently demonstrated that
a very similar macronutrient prole is selected by feral cats in
thewild.
From an evolutionary viewpoint, among the most
fascinating instances of domestication is the dog. Domestic
dogs, the only large carnivore ever to be domesticated,
were derived from wolves (Canis lupus), probably in several
independent events (Vilà etal. 1997; vonHoldt etal. 2010).
Unlike other domesticated animals, which originated in
agrarian societies 10 000 years B.P. or less, the initial stages
of dog domestication took place among hunter-gatherers
at least 15 000 (Driscoll et al. 2009; Wayne and vonHoldt
2012) and possibly in excess of 100 000years ago (Vilà etal.
1997). In the early stage, this was most likely more a case
of spontaneous coevolution between wild wolf populations
and humans, but with the transition to agriculture there
Address correspondence to A.K. Hewson-Hughes. E-mail: adrian.
hewson-hughes@effem.com.
Received 18 April 2012; revised 31 August 2012; accepted 14
September 2012.
Behavioral Ecology
doi:10.1093/beheco/ars168
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was increasingly intense selection for smaller, more docile
dogs (Wayne and vonHoldt 2012). Over the last 200years,
intensication of articial selection has resulted in a
proliferation of breeds, with the consequence that dogs are
now the most phenotypically diverse of all animal species.
They range in size from 1 kg (Chihuahua) to 100 kg (Mastiff),
display more variation in skeletal and cranial proportions
than the entire carnivore order, and show behavioral
and physiological attributes that are comparably diverse
(Wayne and Ostrander 2007; Wayne and vonHoldt 2012).
This diversity is all the more interesting because it exists
contemporaneously with the ancestral species, from which
it was derived in what is from an evolutionary perspective a
very short time period.
Here we describe a series of experimental studies in which
we explored the patterns of dietary protein, fat, and carbo-
hydrate selection in 5 diverse breeds of domestic dogs, the
papillon (PAP), miniature schnauzer (MS), cocker spaniel
(COS), Labrador retriever (LR), and St Bernard (SB). Our
aims were to determine whether the patterns of macronutri-
ent selection in these breeds were as diverse as other pheno-
typic traits, to compare these to comparable experiments on
domestic cats (Hewson-Hughes et al. 2011), and relate the
results to the composition of prey in the wild.
METHODS
Animals, housing, and welfare
Diet selection studies were performed in adult dogs (C.lupus
familiaris) of both sexes (neutered and entire) representing 5
breeds of dog from toy to giant (PAP, MS, COS, LR, and SB)
at the WALTHAM Centre for Pet Nutrition (WCPN), Melton
Mowbray, UK. Throughout each study, dogs were pair-housed
in purpose-built, environmentally enriched facilities with con-
stant access to an outdoor area where they could interact with
other dogs. Extensive socialization with people and on-lead
walking were provided each day. Food was offered to individ-
ually housed dogs in two 1-h periods per day (08:00–09:00 h
and 14:00–15:00 h) and drinking water was available at all
times. Given the potential for weight gain in these studies due
to the provision of foods in excess of energy requirements,
a limit of 15% above individual dogs’ ideal bodyweight was
set by the WCPN Ethical Review Committee as the maximum
amount of weight a dog could gain before being removed
from the study and dogs that did gain weight underwent a
weight management phase after completing the study to
return them to their ideal bodyweight.
Diets and general protocols
We performed 3 experiments, which differed in the diet for-
mat (wet vs. dry) and the combination of foods (differing in
macronutrient balance) offered to the dogs. We used com-
mercial dog foods that were either dry (kibbles) or wet (cans/
pouches), which differ not only in water content and texture
but also macronutrient proles, most notably a higher carbo-
hydrate level in dry foods. The rst aim of our experiments
was to assess and compare the dietary balance selected by the
different breeds of dog fed either dry or wet foods with vari-
able macronutrient levels (with foods available in excess of
calculated maintenance energy requirements [MERs]). The
second aim was to evaluate whether naivety to the experimen-
tal foods affected the macronutrient balance selected.
All experiments comprised 3 phases (the durations of
which are given below). The rst was a naive self-selection
(NSS) phase, in which the dogs were exposed to all of the
experimental foods simultaneously. The aim of this phase was
to measure nutrient self-selection by the dogs when naive to
the experimental foods. In the second, monadic “learning”
phase, the dogs were exposed to each of the foods on suc-
cessive days. This phase provided the dogs with further expe-
rience of the foods before they were once again allowed to
self-select a diet in the experienced self-selection (ESS) phase.
We considered the ESS phase of the experiments to provide
the best measure of the macronutrient balance preferred by
the dogs, because in this phase they could freely compose a
diet from nutritionally complementary foods of which they
had prior experience. To evaluate the impact of this, we com-
pared macronutrient selection in Phase 1 (NSS) and Phase 3
(ESS).
Experiment 1: dry foods—variable protein, carbohydrate,
andfat
Three dry-format foods (high fat, pFc; high carbohydrate,
pfC; and high protein, Pfc) were manufactured using stan-
dard processing (extrusion) procedures at Mars Petcare,
Verden, Germany. These foods were formulated based on
Mars Inc. commercial recipes with the inclusion level of poul-
try meal, maize gluten, ground rice, wheat our, and beef tal-
low altered to achieve differences in the macronutrient:energy
ratios of the foods (Table S1, SupplementaryData).
The following protocol was carried out in 5 breeds of dog,
details of which are shown in Table S2 (Supplementary Data).
Of the 51 dogs that started the experiment, 16 were removed
as a result of reaching the weight gain limit set by the Ethical
Review committee. Prior to the experiment, dogs were fed
standard commercially available dry diets (Pedigree® com-
plete adult small dog [PAP], Pedigree® Advance adult mini
[MS and COS], and Pedigree® complete adult [LR and SB])
at 200% of their estimated MER (calculated as 460 kJ kg−0.75
[110 kcal kg−0.75]) for at least 1 week to accustom them to
being offered excess food during the experiment. This calcu-
lation for MER falls between the National Research Council
(NRC) recommended energy requirements of 544 kJ kg−0.75
(130 kcal kg−0.75) and 377 kJ kg−0.75 (90 kcal kg−0.75) for active
and inactive dogs, respectively (NRC 2006).
Phase 1:NSS
For 7days, dogs were given foods pFc, pfC, and Pfc simultane-
ously in 3 separate bowls from which to self-select a diet. Each
food was offered at 50% of each dog’s calculated MER at both
the morning (08:00–09:00 h) and afternoon meal (14:00–
15:00 h; i.e., 100% MER of each food was offered in total each
day and 300% MER offered in total each day). To avoid posi-
tional bias the location of each food was rotated daily.
Phase 2: monadic “learning”phase
Dogs were cycled through eight, 3-day periods in which they
were conned to a different food (pFc, pfC, or Pfc) on each
of the 3 days. Each food was offered at 100% of each dog’s
calculated MER at both the morning (08:00–09:00 h) and
afternoon meal (14:00–15:00 h; i.e., 200% MER offered in
total each day). This phase served as a conditioning phase in
which the dogs gained experience of the nutritional prole
of each of the foods separately.
Phase 3:ESS
In this phase, the regimen of Phase 1 was repeated on the
now experienced dogs. However, it was noticed that some
dogs were consuming all of one or more of the foods, and
so to ensure that the composition of the diet self-selected by
the dogs was not constrained by availability of the foods, this
phase was extended by 4 days during which each food was
offered at 100% of each dog’s calculated MER at both the
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morning (08:00–09:00 h) and afternoon meal (14:00–15:00 h;
i.e., 200% MER of each food offered in total each day and
600% MER offered in total each day). Only the data collected
during this 4-day extension were used in the statistical analy-
sis of this experiment (because on reviewing the data it was
apparent that some dogs also depleted one or more foods
during the NSS phase).
Experiment 2: wet foods—variable protein, carbohydrate,
andfat
It appeared from analysis of Experiment 1 that dogs were
selecting a diet composition toward the highest possible fat
intake and lowest possible carbohydrate intake. However, due
to the macronutrient proles of the foods provided in that
experiment, they were unable to compose a diet with less
than 22% of energy from carbohydrate or more than 54%
of energy from fat. We hypothesized that providing foods
with lower carbohydrate and higher fat content would allow
dogs to demonstrate their target intake for protein, fat, and
carbohydrate free from the constraints on fat and carbohy-
drate intake imposed by the foods offered in the dry food
experiment.
Wet food formulations provided an opportunity to
explore lower dietary carbohydrate concentrations because,
unlike dry foods, they do not require starch as a bind-
ing agent. Three commercially available wet foods (i.e.,
processed in cans or aluminum foil trays) providing dif-
fering macronutrient energy ratio proles (Chappie® orig-
inal = pfC; Cesar® chunks in loaf = Pfc; Pedigree® puppy
original=pFc) were used in this experiment (see Table S3,
Supplementary Data). Forty-two dogs representing 4 dif-
ferent breeds started this experiment and 5 were removed
before data were collected (Table S2, Supplementary Data).
Of the dogs that took part in the dry food experiment, 3
PAPs, 2 MSs, 2 COSs, and 3 LRs also took part in this wet
food experiment. Prior to the study, dogs were fed a stan-
dard commercially available canned food (Pal® chunks in
jelly) at 200% of their MER (460 kJ kg−0.75) for at least 1
week to accustom them to being offered excess food during
the study.
Phase 1:NSS
For 7days, dogs were given foods pFc, Pfc, and pfC simultane-
ously in 3 separate bowls from which to self-select a diet. Each
food was offered at 100% of each dog’s calculated MER at
both the morning (08:00–09:00 h) and afternoon meal (14:00–
15:00 h; i.e., 200% MER of each diet was offered in total each
day). If the full allocation of any food was eaten at 1 meal the
amount of that food was increased (in 15% steps) at subsequent
meals to guarantee that some of all foods was left uneaten. This
ensured that the balance of macronutrient intake selected was
not constrained by availability of the foods. To avoid positional
bias, the position of each food was rotated daily.
Phase 2: monadic “learning”phase
Dogs were cycled through eight, 3-day periods in which they
were conned to a different food (pFc, pfC, or Pfc) on each
of the 3days. In order to limit potential for weight gain each
food was offered at 100% of MER (i.e., 50% MER at the
morning meal and 50% MER at the afternoon meal) for the
rst six 3-day cycles and increased to 200% MER (100% each
at morning and afternoon meal) for the nal 2 cycles.
Phase 3:ESS
This was the same as the naive phase with each food initially
offered at 200% of MER and increased if necessary for any
dog that ate the full allocation of any food offered.
Experiment 3: wet foods—xed protein
The results of the above Experiments 1 and 2 suggested
that protein was relatively invariant in the diets selected by
the dogs at close to 30% of total energy, whereas the bal-
ance of fat:carbohydrate varied more widely with experi-
mental circumstances. We performed a third experiment
in which protein was xed at 30% and the foods differed
in their fat:carbohydrate ratio (foods X, Y, and Z, Table S3,
Supplementary Data). Because in this design the foods var-
ied only in 2 dimensions, the NSS, monadic learning, and
experienced simultaneous self-selection phases of the experi-
ment each involved only 2 foods. The food pairings repre-
sented all pairwise combinations of high, medium, and low
fat:carbohydrate foods. This experiment also provided an
opportunity to demonstrate that the macronutrient intake
selected using commercially available wet diets described
above was not driven by differences in “palatability” between
the diets. Foods were prepared fresh each day by mix-
ing (using an electric food mixer) appropriate amounts of
drained skinless chicken breast (steam sterilized in cans at
Mars Petcare, Verden, Germany), lard (Tesco, UK; melted in
a microwave), and pregelatinized wheat our plus vitamins
and minerals. The nutritional composition of the diets was
formulated to meet recommendations for adult dogs (NRC
2006).
Twenty-six MSs (Table S2, Supplementary Data) were used
in 3 studies with n = 12 per study (10 dogs were used in 2
studies) with each study offering a choice between a pair of
foods (X vs. Z, Y vs. Z, and X vs. Y) using the methodology
described above with the following modications.
Phase 1:NSS
Each food was offered at 150% of each dog’s MER equally
divided into two 1-h meals per day (10:00–11:00 h and 14:00–
15:00 h; i.e., 600% MER offered in total each day).
Phase 2: monadic “learning”
Each food was offered at 100% of MER (i.e., 50% MER at the
morning meal and 50% MER at the afternoon meal) for the
rst six 2-day cycles and increased to 200% MER (100% each
at morning and afternoon meal) for the nal 2 cycles.
Phase 3:ESS
This was the same as the naive phase with each food offered
at 150% of MER equally divided into two 1-h meals per day
(i.e., 600% MER offered in total each day).
Statistical analyses
For all studies, the percentages of total energy from protein,
fat, and carbohydrate were analyzed by mixed-model analyses
to take into account the repeated measures for individual dogs
within a phase. The carbohydrate data were log10 transformed
prior to analyses due to positively skewed distributions;
subsequently means and 95% condence intervals (CIs) have
been back transformed for illustration in gures. Statistical
analyses were carried out using GenStat® v13.1 software (VSN
International Limited, Hemel Hempstead, UK). An overall
signicance level of 5% was adopted for all analyses.
Wet and dry foods—variable protein, carbohydrate, andfat
For the ESS wet and dry models, dog was dened as a random
effect and breed as a xed effect to investigate if there were
differences in the macronutrient balance selected between
breeds. For the NSS vs. ESS models (wet foods only), phase
nested in dog was dened as the random effect and breed,
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phase, and their interaction were dened as xed effects to
investigate if there were differences in the macronutrient bal-
ance selected between breeds and if this changed with experi-
ence. Estimates of the target intakes (kJ) for protein, fat, and
carbohydrate as well as total energy intake of dogs during the
ESS of the wet food experiments were determined by mixed-
model analysis with dog as a random effect and breed as a
xed effect. Data were log10 transformed prior to analysis due
to increasing variance of residuals with increasing energy con-
sumed. Means and 95% CIs were back transformed to kJ d−1
for presentation in tables.
Wet foods—xed protein
For the ESS analysis, diet pair nested in dog was dened as
the random effect and diet pair was dened as a xed effect
to investigate if there were differences in the balance of car-
bohydrate and fat selected (protein was xed) between diet
pairs. For the NSS vs. ESS models, phase nested in diet pair
nested in dog were dened as the random effects and diet
pair, phase and their interaction were dened as xed effects
to investigate if the balance of fat and carbohydrate selected
within diet pairs changed with experience.
For both analyses, the variability between diet pairs was
found to differ signicantly and this variability was modeled
by allowing the residual error to change with diet pair.
RESULTS
Experiments 1 and 2: wet and dry foods—variable protein,
fat, and carbohydrate
Figure 1 shows the proportional protein, fat, and carbohy-
drate compositions of the experimental foods used in the dry
and wet diet experiments, together with the nutrient intakes
of each dog breed associated with the phases of the 2 variable
protein environments. Arst thing to note from the gure is
the composition of the experimental foods (lled squares for
wet foods and hollow squares for dry foods). For each experi-
ment, the triangle formed by joining the points representing
the foods denes the accessible area for a dog provided with
ad libitum access to that food combination. The plot shows
that dogs fed the wet and dry food combinations could theo-
retically compose diets with similar maximum carbohydrate
concentration (i.e., >50% energy from carbohydrate), but
those fed the wet foods could achieve an intake with lower
proportional carbohydrate content than those fed dry foods.
Conversely, dogs on the dry foods could achieve an intake
with higher proportional protein content than those on the
wet foods, but the 2 diet formats allowed similar minimal pro-
tein concentrations. Both the minimal and maximal attain-
able fat concentrations were higher on wet than dry foods.
The area of overlap between the triangles shows the range
of protein:fat:carbohydrate dietary concentrations that was
accessible both to dogs on the wet and the dry foods. The rela-
tionship between the accessible region in diet space and the
intakes selected by the dogs in the ESS phase of the experi-
ment provides information about the macronutrient balance
of the targetdiet.
Target macronutrient balance—ESS
Statistical comparison of macronutrient intake in dogs in the
wet and dry experiments is not appropriate because these
experiments were done separately. There are nonetheless
some interesting contrasts apparent from visual comparison
of the scatter of the intake points self-selected by experienced
dogs in the 2 experiments (Figure1). First, intakes of all of
the dogs in the dry food experiment fell within the region
of overlap between the 2 diet triangles, which was equally
accessible to the dogs on both diet formats. However, dogs in
the wet diet treatment did not select this region, suggesting
that the composition selected by dogs on the dry foods was
not a true macronutrient target but a constrained outcome
imposed by the composition of the dryfoods.
Rather, dogs in the wet diet treatments composed a diet
that had similar protein concentration to those in the dry diet
treatment (all dogs fell within the band spanning 25–35%
total energy as protein), but was considerably lower in car-
bohydrate and higher in fat than dogs in the dry diet treat-
ments. This pattern, taken together with the fact that dogs
in the dry diet treatment selected intake points that were
close to the minimum carbohydrate concentration available
to them, suggests that the dry diets are appreciably higher in
carbohydrate than the target diet composition. Indeed, even
dogs on wet foods appear to have minimized the propor-
tional carbohydrate content of their diet. Overall, these data
suggest that the preferred diet composition of the dogs has
low carbohydrate:fat balance, with between 25% and 35% of
energy contributed by protein.
Figure1
The proportional carbohydrate, fat, and protein compositions of
the experimental foods used in the dry (hollow squares) and wet
diet (lled squares) experiments, together with the nutrient intakes
of dogs fed these foods (circles). In these plots, known as right-
angled mixture triangles (Raubenheimer 2011), 2 components of a
3-component mixture are represented in the normal way as x and y
axes (in this case carbohydrate and fat, respectively), and the third
component (in this case protein) varies inversely with the distance
from the origin. Thus, 2 mixtures that have the same balance of
fat:carbohydrate will fall on a line projecting from the origin, and
the mixture with the higher protein content will be closer to the
origin than the mixture with lower protein. The gray- and black-
lined triangles show the areas that are accessible to dogs with access
to the dry and wet foods, respectively. Red solid circles show intake
points selected in the ESS phase and green hollow circles show mean
intakes selected in the NSS phase (wet foods only) by the various
breeds of dog. The dotted diagonals show the highest (closest to the
origin) and lowest % protein energy potentially achievable by the
dogs in the experiment. Dashed diagonals dene the band of actual
protein intakes of dogs during the experienced self-selecting phase.
Dog breeds are not distinguished in the plot.
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Although it appears that dogs were unable to achieve their
target macronutrient composition from the choice of dry
foods offered to them, the selected balance of percentage
energy intake from protein, fat, and carbohydrate was not sig-
nicantly different between the 5 breeds (fat: F(4,32.3)= 1.27,
P = 0.303; protein: F(4,32.4) = 1.22, P = 0.323; carbohydrate:
F(4,32.3) = 1.38, P = 0.261), suggesting that mechanisms for
active regulation of macronutrient intake may be similar
across these breeds. Total energy intake obviously increased
in relation to the size of each breed of dog, with all breeds
apart from PAP consuming >100% of their calculated MER
(Table1) and over the course of the experiment body mass
increased on average by 0.8% in PAP, 5.4% in MS, 11.1% in
COS, 13.1% in LAB, and 4.6% in SB (for those dogs that
completed the experiment).
The choice of wet foods removed the constraints on fat
and carbohydrate intake and the estimated target intakes
(kJ d−1) for protein, fat, and carbohydrate for each breed
are shown in Table2. Similar to the situation seen in the dry
food experiments, PAP consumed close to their calculated
MER, whereas the other breeds all consumed >200% of
their calculated MER (Table 2) and over the course of the
experiment body mass changed on average by −1.2% in
PAP, +9.3% in MS, +8.4% in COS, and +11% in LAB (for
dogs that completed the experiment). When the intake data
were expressed as percentage of energy intake from protein,
fat, and carbohydrate, there were small but statistically
signicant differences in the proportions of protein and
fat (but not carbohydrate) selected by the 4 breeds (fat:
F(3,27.7) =10.51, P< 0.001; protein: F(3,27.9) = 6.5, P = 0.002;
carbohydrate: F(3,27.9)= 1.57, P = 0.22). Figure 2 shows that
this was principally due to PAP and COS composing a diet
with a higher percentage of energy from protein and lower
percentage of energy from fat than LAB and MS. The biggest
difference observed was for percentage energy from fat
between PAP and MS (8.8%, 95% CI 4.8–12.7). The average
macronutrient energy composition of the diet self-selected by
all dogs during the ESS phase of the wet food experiment was
ca. 29% protein (95% CI 27.3, 30.9), 63% fat (62.0, 64.6) and
7% carbohydrate (6.4,7.9).
NSS vs.ESS
A comparison of Phase 1 (NSS) and Phase 3 (ESS) of the
experiments enabled us to assess the effects of experi-
ence gained in Phases 1 and 2 (monadic phase) on the
nutrient selection by the dogs. In the dry food experiment
(Experiment 1), however, dogs in Phase 1 frequently depleted
1 or more of the experimental foods, even though each was
provided at 100% of estimated MER. Consequently, the com-
position of the selected diet partly reected an unanticipated
constraint due to the experimental design and could thus not
be interpreted to indicate the ad libitum selected macronu-
trient balance. The patterns of food depletion did, however,
provide information about the nutritional regulatory priori-
ties of the dogs. Figure 3 shows that the majority of deple-
tions involved the pFc food, which supports the conclusion
reached from our analysis of the ESS phase (above), that the
target diet has a higher fat:carbohydrate ratio than was avail-
able to dogs on the dry food treatments.
Comparison of nutrient selection in the NSS and ESS
phases of the wet foods experiment suggested that when fed
wet foods, naive dogs selected a region in nutrient space that
was close to the target region (Figure 1). Closer inspection,
however, revealed that on average (i.e., over all 4 breeds)
there was a small but statistically signicant decrease in the
percentage of energy intake from protein (F(1,28.7) = 8.27,
P= 0.008) and increase in percentage of energy intake from
fat (F(1,29.1) = 12.17, P = 0.002) in the ESS phase compared
with the NSS phase, whereas carbohydrate intake did not dif-
fer (F(1,29.3) =0.59, P = 0.449) (Figure 4). The breed effect
seen in the ESS analysis reported above was also seen in the
NSS phase, but the phase by breed interaction was not sig-
nicant, indicating that the differences seen between breeds
were consistent between NSS andESS.
Experiment 3: wet foods—xed protein
The diet compositions and selected intakes of dogs in NSS
and ESS phases of the wet foods, variable protein experiment,
are shown in Figure 5. Unlike Experiments 1 and 2, where
choices involved 3 foods and the dogs could thus move freely
within a triangle (Figure1), the dogs in this experiment had
2-way choices and were thus conned to move along the line
joining the composition points for the 2 foods in their respec-
tive diet pairings (X + Y, Y + Z, and X +Z).
Table1
Mean daily energy intake (kJ d−1) and percentage of maintenance
energy requirement (%MER) consumed in 5 breeds of dog during
ESS phase of the dry food experiments
Breed Energy intake (kJ d−1) %MERa
PAP 1010 (872–1149) 96 (87–105)
MS 3427 (3033–3821) 146 (129–163)
COS 4616 (4086–5147) 164 (148–180)
LAB 9979 (8941–11 019) 168 (150–187)
SB 11 705 (10 253–13 157) 109 (95–124)
Values shown are means with 95% CIs in parentheses. PAP, papillon;
MS, miniature schnauzer; COS, cocker spaniel; LAB, Labrador
retriever; SB, St Bernard.
aMER based on the calculation 460 kJ kg−0.75.
Table2
Mean daily macronutrient and energy intake (kJ d−1) and percentage of maintenance energy requirement (%MER) consumed in 4 breeds of dog
during ESS phase of the wet foods with variable protein, fat, and carbohydrate experiments
Breed
Macronutrient energy intake (kJ d−1)
Total energy intake (kJ d−1) %MERa
Protein Fat Carbohydrate
PAP 365 (281–475) 652 (476–894) 79 (52–121) 1114 (841–1477) 108 (99–117)
MS 1087 (920–1283) 2973 (2436–3628) 336 (257–439) 4403 (3684–5262) 208 (197–220)
COS 2254 (1919–2648) 4392 (3622–5327) 435 (335–564) 7172 (6034–8525) 266 (247–285)
LAB 3101 (2541–3785) 7900 (6222–10 032) 933 (676–1287) 12 029 (9713–14 897) 226 (208–244)
Values shown are means with 95% CIs in parentheses. PAP, papillon; MS, miniature schnauzer; COS, cocker spaniel; LAB, Labrador retriever.
aMER based on the calculation 460 kJ kg−0.75.
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Target macronutrient balance—ESS
Figure5 shows that in the ESS phase the dogs in the Y + Z and
X + Z treatments selected a diet that was tightly convergent
(mean % energy intake from fat: Y + Z=61.2 [95% CI 59.7,
62.8]; X + Z = 60.8 [58.7, 63.0], P = 0.759. Mean % energy
from carbohydrate: Y + Z = 7.9 [6.8, 9.2]; Z + X = 6.3 [5.2,
7.7], P = 0.063). This point corresponds very closely to the
selected intake point by dogs in the 3-way choice of wet foods
(Figure1), providing further support that this represents the
selected target balance of dogs in our experiment. The macro-
nutrient balance selected in Y + Z and X + Z pairings was sig-
nicantly different from the macronutrient balance selected
in the X + Y food pairing (mean % energy intake from fat: X
+ Y= 50.8 [49.2, 52.4]; Y + Z=61.2 [59.7, 62.8], P <0.001; X
+ Z = 60.8 [58.7, 63.0], P < 0.001. Mean % energy from car-
bohydrate: X + Y = 20.1 [18.0, 22.4]; Y + Z = 7.9 [6.8, 9.2],
P< 0.001; Z + X=6.3 [5.2, 7.7], P <0.001). This reects that
dogs in the X + Y treatment could not move closer to the tar-
get point than the point representing the composition of food
Y, and their intake thus represents a constrained compromise.
NSS vs.ESS
Mixed-model analysis revealed a signicant phase effect
(P<0.001) and a signicant phase by diet–pair interaction
(P< 0.001) indicating that differences in fat and carbohy-
drate energy intake seen between phases were not consis-
tent between the different diet pairings. Thus, in pairing
Figure2
Mean macronutrient: energy composition (with 95% CI) of the diet composed from a choice of 3 wet foods with variable protein, fat, and
carbohydrate content in the experienced self-selecting phase by 4 breeds of dogs (Experiment 2). COS, cocker spaniel; LAB, Labrador
retriever; MS, miniature schnauzer; PAP, papillon. Letters a–e indicate homogenous breed groupings within a macronutrient at the 5% level
(i.e., those macronutrients with the same letter are not signicantly different between breeds).
Figure3
Frequencies at which various individual foods and 2- and 3-way combinations of foods were depleted in the NSS phase of the dry foods
experiment (Experiment 1).
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Y + Z (the 2 foods that were closest together and encom-
passed the target) the intakes for both self-selection phases
of the experiment were superimposed (Figure 5, green
circles) and there was no signicant difference in the %
energy intake from fat (and hence carbohydrate, because
protein density was held constant in the foods and there-
fore changes in the proportion of fat energy in the food
were offset by carbohydrate energy) between NSS and ESS
(Figure6). In contrast, the largest difference in % energy
intake from fat between NSS and ESS phases (5.5%, 95% CI
2.9, 8.1; Figure5, red circles) was seen in food pairing X +
Z (the 2 foods furthest apart; P< 0.001; Figure6), whereas
the difference in % fat energy intake between ESS and NSS
for pairing X + Y, which did not encompass the target, was
intermediate between the other diet pairings (Figure 5,
blue circles; Figure6).
Figure4
Effect of experience on the proportional macronutrient content of the self-selected diet of 4 breeds of dog in the 3-choice wet food
experiment (Experiment 2). The plot shows the mean differences (with 95% CI) in percentage energy intake from fat, protein, and
carbohydrate (CHO) between the experienced and NSS phases. Apositive value thus indicates that experience resulted in an increase in
proportional intake of that macronutrient.
Figure5
Right-angled mixture triangle showing proportional protein, fat, and carbohydrate intakes of miniature schnauzers fed wet format diets
with variable fat:carbohydrate balance and protein content xed at ~30% of energy (Experiment 3). Solid squares show the composition
of the 3 foods: X=low fat:carbohydrate; Y=intermediate fat:carbohydrate; Z=high fat:carbohydrate. Colors represent different diet
pairings (blue=X + Y; green=Y + Z; red=X + Z), and symbols distinguish different phases in the experiment (hollow circles=NSS; lled
circles=ESS). The diagonal lines show the minimum and maximum selected proportional protein intakes from the variable protein, fat, and
carbohydrate wet and dry experiments, as in Figure1.
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DISCUSSION
Evolutionary perspectives
We have investigated the selection by domestic dogs of the
macronutrient balance as well as metabolizable energy con-
tent of their diet. Diet selection in animals has long been eval-
uated in relation to energy intake, but research over the past
2 decades has demonstrated a critical role for macronutrient
balance (Raubenheimer et al. 2009). This work, involving a
wide range of animals, has linked macronutrient balance to
many aspects of evolutionary tness, including growth rates
and size (Raubenheimer and Simpson 1997; Simpson et al.
2004), obesity (Simpson and Raubenheimer 2005; Warbrick-
Smith et al. 2006), fecundity (Lee et al. 2008), longevity
(Piper et al. 2011), disease resistance (Cotter et al. 2010),
sexual advertisement (Maklakov etal. 2008), and risk of pre-
dation (Hawlena and Schmitz 2010).
Such results underpin a strong expectation that animals
would have evolved by natural selection an ability to balance
their macronutrient intake through selecting appropriate
foods and combining them in the required proportions. It
has long been expected that herbivores and omnivores would
possess such mechanisms, based on the premise that these
animals generally feed on nutritionally imbalanced and vari-
able foods (Westoby 1978). Carnivores, in contrast, are widely
assumed to feed on nutritionally balanced and relatively
invariant foods, and therefore not to require the mechanisms
for regulating the balance of macronutrient intake (Westoby
1978). However, several recent experiments involving both
invertebrate and vertebrate predators have demonstrated that
they do, indeed, regulate their intake of foods to balance the
gain of macronutrients, and that failure to do so can result
in tness penalties (Mayntz etal. 2005, 2009; Raubenheimer
et al. 2007; Wilder and Rypstra 2008; Hewson-Hughes et al.
2011; Jensen et al. 2011, 2012). We therefore expected that
the same would be true of domesticdogs.
Dogs are interesting with regard to the evolution of nutri-
tional strategies because of their peculiar evolutionary
history (Akey etal. 2010). Derived from Eurasian gray wolves,
domestication began over 14 000 years ago, and much more
recently dogs have undergone an intense period of articial
selection generating phenomenal phenotypic divergence
among the more than 400 breeds (Akey et al. 2010). There
are therefore at least 3 clearly identiable periods in the evo-
lutionary history of extant domestic dogs, each characterized
by different environmental and selective circumstances: pre-
domesticated wolf ancestry, early domestication, and rapid
articially selected diversication. Successive periods of dif-
ferent selection pressures can each leave a distinct imprint
on the nutritional regulatory responses of a species. Different
aspects of the nutritional biology of humans, for example,
can be traced to our catarrhine primate ancestry (Milton
2000), our Palaeolithic hunter-gather prehistory (Lindeberg
et al. 2003), and the rapid changes in nutritional ecology
wrought by agriculture (Beja-Pereira etal. 2003; Burger etal.
2007). Although a good deal of more research is needed, our
study provides some interesting pointers as to how the vari-
ous stages of the evolution of domestic dogs might have inu-
enced their pattern of macronutrient selection, the subject to
which we now turn.
Macronutrient selection
Our results showed, as expected, that dogs do indeed
regulate the macronutrient balance of their diet. In all
experimental treatments where it was possible, the diets of
experienced self-selecting dogs converged on an intake with
approximately one-third of energy derived from protein and
a low carbohydrate:fat ratio. These treatments comprised
the wet foods, 3-way diet choice experiment (Experiment
2; Figure 1), and 2 of the treatments (Y + Z and X + Z) in
the wet foods, xed protein 2-way diet choice experiment
(Experiment 3; Figure 5). Substantially different diet com-
positions were selected only by the dogs in the dry foods
experiment (Experiment 1), and in the X + Y pairing of
the xed protein experiment (Experiment 3), both of
Figure6
Effects of experience on the proportional fat content of the selected diet of miniature schnauzers fed different food pairings (see Figure5;
Experiment 3). The plot shows the mean (with 95% CI) of the difference in proportional fat intake in the selected diet of dogs between the
experienced and NSS phases. Apositive value thus indicates that experience resulted in an increase in proportional fat intake. Because in this
experiment the proportion of protein in the diets was xed, changes in proportional fat intake are exactly offset by changes in carbohydrate
content and for this reason carbohydrate is not presented.
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which were constrained by available foods from reaching
the point of convergence. Dogs in the dry food experiment
also selected a diet with between 25% and 35% protein, but
with a fat:carbohydrate ratio that was close to the maximum
possible given the available diet choice. When the protein
content was xed at 30% in wet foods, the dogs with diet
pairing X + Y similarly selected a diet with a fat:carbohydrate
ratio close to the maximum possible given their diet pairing.
Taken together, these results suggest that the target diet of
dogs in our study consists of approximately 30% of energy
from protein, 63% of energy from fat, and 7% of energy
from carbohydrate.
Two previous studies have investigated macronutrient
intake in domestic dogs. Romsos and Ferguson (1983)
offered 2-year-old female beagles ad libitum access to 1
of 2 pairings of 3 foods differing in protein content. The
foods contained metabolizable nutrient energy proportions
of 20:38:42 (protein:fat:carbohydrate) (food 1), 25:55:20
(food 2), and 46:27:27 (food 3). Dogs were offered a choice
between foods 1 and 3, or foods 2 and 3.In both cases dogs
selected 30% of energy as protein, which is consistent with
the results of our study, although it is not possible to discern
the roles of fat and carbohydrate from the experimental
designs used. In a more recent study, Tôrres et al. (2003)
conned beagles to 1 of 5 choices between 2 isocaloric foods
differing in protein content (0% vs. 25%, 9% vs. 32%, 18%
vs. 32%, 18% vs. 48%, or 25% vs. 48%). Again in agreement
with our study, the dogs adjusted their food choices to main-
tain dietary protein intake at close to 27% of metabolizable
energy.
An interesting nding of our study is the remarkable
consistency in the proportional composition of the target
diet across breeds. In the dry diets experiment, there was
no signicant difference between breeds in proportional
macronutrient composition of the selected diet, whereas
breed explained a small but signicant proportion of the
variance in the 3-choice wet diet experiment. Assuming
that the discrepancy between breeds is robustly associated
with the different food formulations, this would suggest
that when fat is limiting and carbohydrate excessive (i.e.,
dry foods) all breeds prioritize maximizing proportional fat
intake whereas when fat is not limiting (wet food formula-
tions) different breeds are able to express preferences for
their respective macronutrient targets. It is unclear, how-
ever, why LAB and MS should select slightly higher fat and
lower protein than PAP and COS; expanding the study to
a wider range of breeds would provide a more substantial
comparative perspective which could shed light on this
question. In the meantime, however, the overriding conclu-
sion is that the recent rapid divergence among dog breeds is
not substantially reected in their macronutrient priorities
compared with other phenotypic features such as size, color,
and temperament.
In contrast with the similarity between dog breeds, experi-
ments have shown that some more distantly related vertebrate
carnivores select a diet with very different macronutrient bal-
ance than the P:F:C balance of 30:63:7 selected by the dogs in
our study. Using a similar experimental protocol to the pres-
ent study, Hewson-Hughes etal. (2011) found that domestic
cats selected a diet that is substantially higher in protein and
lower in fat (52:36:12). Interestingly, a subsequent meta-anal-
ysis showed that the diets of free-roaming feral cats also com-
prised 52% of energy from protein. On the other hand, the
relative contributions of fat and carbohydrate to the energy
intake of feral cats (46% and 2%, respectively) differed from
the 36%:12% selected under experimental conditions in the
study of Hewson-Hughes etal. (2011), a difference to which
we returnbelow.
Why should cats select a diet with higher proportional
protein and lower proportional fat content than dogs? In
common with all of the extant members of the cat fam-
ily, domestic cats are metabolically reliant on a diet that in
the wild can be satised by eating largely vertebrate prey
(Bradshaw 2006). Because historically very few households
would regularly have had surplus meat or sh, there was up
until recently strong selection pressure on cats to satisfy their
specialized nutrient needs through hunting small vertebrates
(Bradshaw 2006), which typically have a high protein:fat con-
tent. For example, the data on body compositions of several
species of typical prey of domestic cats presented by Eisert
(2011) range from 33% energy from protein (common vole)
to 68% energy from protein (bank vole), with a midpoint of
50.5% which is very similar to 52% selected both by domes-
tic cats in experimental conditions (Hewson-Hughes et al.
2011) and free-roaming feral cats (Plantinga et al. (2011).
Domesticated dogs, in contrast, have not been under the
same constraint and would have relied on a wider range of
human-provided foods during the process of domestication.
Furthermore, being social hunters, the wolf ancestors of
domestic dogs were able to utilize larger prey. Because the
proportional body fat content of mammals increases with
size (Prothero 1995), the fat:protein balance of the diet of
the ancestors of domestic dogs would likely have been higher
compared with the small, solitary-hunting ancestor of domes-
tic cats. Finally, compared with dogs, the domestication of
cats is very recent (possibly <200 years B.P.) and might be
incomplete (Driscoll et al. 2009). This is reected in the
minimal morphological divergence of domestic cats from
their wildcat ancestors (Driscoll etal. 2009) and might also
explain the similarity in the protein content of experimen-
tally selected and wilddiets.
Interestingly, however, Darwin (1868) noted that domes-
tic cats have longer intestines than wildcats, a difference he
attributed to a less carnivorous diet associated with feed-
ing on kitchen scraps. If Darwin is correct on this, then the
intensication of articial selection for divergent morphol-
ogy in cats, initiated in the Victorian era, might also have had
nutritional implications. This could explain why cats in the
experiments of Hewson-Hughes etal. (2011), although select-
ing a similar proportion of protein in the diet as feral cats
in the wild (Plantinga etal. 2011), selected a higher propor-
tion of carbohydrate (12% vs. 2%, respectively). If the 1.7%
average carbohydrate content of the 8 species of small verte-
brate prey listed by Eisert (2011) is representative, then feral
cats would be ecologically constrained from achieving an
intake of 12% carbohydrate even if this did reect an arti-
cially selected dietary preference. But why, if the macronutri-
ent preference of cats has been evolutionarily altered since
Victorian times, has comparable divergence not taken place
among the diverse breeds included in our study? Owing to
the longer history of dog domestication, it is likely that the
pattern of macronutrient selection in domesticated dogs
had already diverged signicantly from their wolf ancestors
by 200years ago when articial selection intensied (Wayne
and vonHoldt 2012), and all of the breeds in our study were
derived from a common ancestor that was already “adapted”
to a human-associateddiet.
Several species of carnivorous shes have also been found
to select a diet high in protein (ca. 55%—Ruohonen et al.
2007). By contrast, an obligate predator, the mink, selects a
diet more similar to that of dogs, consisting of 35% protein
by energy (Mayntz et al. 2009). This is interesting, because
like cats mink feed on small vertebrates and therefore almost
certainly have a natural diet that is higher in protein than
the self-selected preference. It is possible, however, that the
macronutrient preference of the mink in the experiments
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of Mayntz et al. (2009) is not representative of their wild
counterparts, but inuenced by articial selection in cap-
tivity. Suggestively, the standard diet of the experimental
population, which had been in captivity for 75 generations,
contained 32% protein, which is very similar to the 35%
self-selected by these animals. An equivalent example of
tight adaptation in captive-bred animals to the macronutri-
ent composition of the diet has been described by Warbrick-
Smith etal. (2009).
Effects of experience
Experiments on herbivorous (Simpson and White 1990;
Raubenheimer and Tucker 1997) and omnivorous (Gadd and
Raubenheimer 2000) insects have demonstrated that learning
can play an important role in balancing macronutrient gain.
Recently, Hewson-Hughes et al. (2011) showed that adult
domestic cats offered a 3-way choice between foods varying
in the protein, fat, and carbohydrate content selected a diet
higher in protein and lower in carbohydrate following experi-
ence with the diets than when naive. The dogs in the present
experiments similarly selected a different macronutrient bal-
ance when experienced (ESS) than when naive (NSS), both
in the 3-choice wet food study and the 2-choice xed protein
study. In the 3-choice study, experienced dogs selected a sig-
nicantly higher proportion of fat and lower proportion of
protein in ESS than NSS, with no signicant difference in
the proportion of energy from carbohydrate. In the 2-choice
study, dogs similarly selected a higher proportion of energy
from fat in ESS than NSS (Figure 6), but in this case the
proportion of protein was xed and fat thus displaced car-
bohydrate. It seems, therefore, that the main effect of expe-
rience with the experimental foods was to enable the dogs
to increase the proportional contribution of fat to the diet.
Interestingly, the effect of experience in cats and dogs thus
echoes the relative proportions of different macronutrients
in the target diet, with cats learning to increase the propor-
tional protein content of the diet, and dogs the proportional
fat content.
Results of the 2-choice xed protein study suggested that
the role of learning was dependent on diet pairing (Figures
5 and 6). There was no signicant difference in propor-
tional fat intake for dogs given the Y + Z pairing, indicating
that the dogs were able to regulate to the target point even
when rst exposed to the experimental foods (in the NSS
phase). In contrast, when given food pairing X + Z, which
also encompassed the macronutrient target but had widely
discrepant fat:carbohydrate balances, the dogs only reached
the target composition when experienced (in ESS) and
when naive ingested a low fat:carbohydrate diet. Learning
similarly played a role for dogs given the Y + X diet pair-
ing, which comprised foods less dissimilar than the X + Z
pairing but did not encompass the target balance. In this
case, the compositions of the foods precluded the dogs from
achieving the target balance, but they approached the target
balance more closely when experienced. It is interesting to
speculate on why the need for learning should be context
dependent in this way. The common factor in the 2 treat-
ments that did require learning is that both involved food
X, which had a high carbohydrate:fat (38%:33%) balance.
It is plausible that the reason that learning was required on
these 2 diet pairings is that short-term regulatory mecha-
nisms, which enabled inexperienced dogs to reach the
target when given food pairing Y + Z, are ineffectual on
extreme foods with carbohydrate:fat balance as high as food
X because they are beyond the evolutionary experience of
dogs. In such circumstances more general mechanisms,
such as positive associative and aversion learning, might be
required to enable dogs to meet their macronutrient target
(Berthoud and Seeley 2000).
Energyintake
Whereas the evidence is compelling that dogs regulated the
relative proportions of protein, carbohydrate, and fat in the
diet, it was apparent that the total amount of food and energy
eaten was far higher than expected. In fact, as set out in the
Methods, we had to make various adjustments in food pro-
visioning to ensure that our subjects were maintained under
conditions of excess food availability. The daily metabolizable
energy requirement for adult dogs at maintenance (i.e., to
support energy equilibrium) recommended by the NRC is 544
kJ kg−0.75 (130 kcal kg−0.75) although it is recognized that there
is considerable individual variation, even between dogs kept
under the same conditions (NRC 2006). In the present stud-
ies, we used 460 kJ kg−0.75 (110 kcal kg−0.75) as the basis for cal-
culating the “maintenance” amount of food to offer the dogs
and for expressing their subsequent energy intake relative to
their “maintenance” requirement. Our results show that of
the breeds used in these studies, MS, COS, and LAB all con-
sumed well in excess of their calculated energy requirement
during the self-selection phases of both dry (146%, 164%,
and 168% of MER, respectively) and wet (208%, 266%, and
226% of MER, respectively) food experiments. When offered
ad libitum access to 2 different diet pairings, adult beagles
consumed similar amounts of energy (~5100 and 5400 kJ
d−1) in both choice treatments over the course of the 4-week
experiment (Romsos and Ferguson 1983). The authors con-
cluded that dogs regulate both protein (see above) and total
energy intake when offered appropriate food choices. It is
interesting to note that the energy intake at which the bea-
gles “regulated” their intake in both choice treatments was
approximately 208% and 224% of MER (based on 460 kJ
kg−0.75)—similar to the values seen in dogs in the wet choice
experiments in the presentstudy.
These ndings may reect the feeding behavior of the
wild ancestors of domestic dogs, wolves. Wolves may only kill
prey every few days or even less frequently and therefore are
adapted to a feast or famine foraging pattern, facing great
uncertainty in the availability and intake of protein and
energy. Hence, it is not surprising that when wolves do make
a kill they can consume large amounts of food, enabling them
to sustain periods of limited or no food availability. Amini-
mum daily food requirement of 3.25 kg wolf−1 d−1 (5× basal
metabolic rate) has been estimated for a 35 kg wolf (Peterson
and Ciucci 2003) and consumption rates of 5.7 kg wolf−1 d−1
and 10.4 kg wolf−1 d−1 have been estimated for larger wolves
(~45 kg) depending on kill rates (Stahler etal. 2006). It seems
that dogs still have this propensity to ingest a large amount
of food/energy if given the opportunity. However, now that
they are domesticated and have regular access to food with
no need to expend energy obtaining it, it is easy to see how
dogs could become overweight if the amount of food offered
is not controlled.
CONCLUSIONS
Our study has added to the growing list of experiments
demonstrating that carnivores, like herbivores and omni-
vores, are able to combine foods of varying composition
to compose a diet of xed macronutrient balance. The
diet composed by the dogs in our study (P:F:C = 30:63:7)
was lower in protein-derived energy than previous stud-
ies have demonstrated for the domestic cat and predatory
shes, but comparable to farmed mink. Many interesting
Behavioral EcologyPage 10 of 12
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questions remain regarding the origins of the diversity of
nutritional priorities among predators. In domesticated
animals, these questions are complicated but particularly
interesting because of the different timescales involved
(predomestication, early domestication, and recent), and
a considerable amount of work remains to be done before
robust generalizations regarding the inuence of the differ-
ent periods can be drawn. On a shorter timescale, there are
many interesting questions concerning the contributions
of genetically evolved regulatory responses versus the role
of individual experience. The nding in the present study
that macronutrient selection in dogs is inuenced by expe-
rience, combined with our earlier demonstration that the
same is true for cats, demonstrates the need for integrated
studies that span timescales from the evolutionary to the
developmental. Finally, the present study has focused on
macronutrition, based on a large body of data showing that
protein, fat, and carbohydrates exert a powerful inuence
on the nutritional responses of many animals (Simpson and
Raubenheimer 2012). We suggest that nutritional geometry
provides a powerful framework for future studies to inves-
tigate the roles of micronutrients (e.g., minerals) in the
dietary responses of companion animals and their interac-
tions with macronutrients.
SUPPLEMENTARY MATERIAL
Supplementary material can be found at http://www.beheco.
oxfordjournals.org/
FUNDING
This work was funded by the WALTHAM Centre for Pet
Nutrition, part of Mars Petcare. D.R. is part-funded by the
National Research Centre for Growth and Development,
New Zealand. S.J.S. was supported by an Australian Research
Council Laureate Fellowship.
The authors would like to acknowledge the skills and expertise of
many people at the WALTHAM Centre for Pet Nutrition involved
in feeding and caring for the dogs in these experiments. The tech-
nical assistance of Matthew Gilham and Gaëlle Thomas is greatly
appreciated.
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