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Received: 29 June 2017 | Revised: 20 December 2017 | Accepted: 25 December 2017

DOI: 10.1111/joss.12311

ORIGINAL ARTICLE

A new method to assess the influence of odor on food selection


in dogs

tel | C. Baron | M. Thomsen | L. Callejon | F. Pe


C. Pe ron

Diana Pet Food, Elven, France


Abstract
Correspondence Previous research provides evidence that odor is a key driver in food selection in dogs. Dogs’ flavor
cile Pe
Ce tel, Diana Pet Food, ZA du preferences are generally assessed through paired comparison tests based on food intake. Methods for
Gohelis, Elven 56250, France.
evaluating odor preference in canines are lacking. In this study, the paired comparison test was modi-
Email: cpetel@diana-petfood.com
fied by replacing standard bowls with false-bottom bowls (FBBs). Made of two compartments
separated by a drilled, stainless-steel plate, FBBs enable odorant compounds to be placed under the
food that is presented to the dogs. Several paired comparison trials were conducted on a trained canine
panel with FBBs containing various odorant substances under the kibbles. Results showed that dogs
were able to perceive the hidden substances and to distinguish between the bowls accordingly. These
results demonstrate that the false-bottom bowl paired comparison method could be helpful in evaluat-
ing the role of odor in dogs’ food preferences, thus, also as a way of assessing food odor performance.

Practical applications
The false-bottom bowl method is an adaptation of the paired comparison test that enables the
influence of odor on dog behavior to be isolated from that stimulated by vision, taste or textural
parameters. The odor impact of a hidden substance is tested under pet meal conditions. This new
method could be useful in pet food industry to measure the odor potential of a new ingredient, or
to understand the key food selection drivers for dogs and cats. In addition, as the olfactory stimu-
lus is not eaten by the animal, the influence of odor in non-food products for dogs, such as pet
care and pet medicines, could also be evaluated using this method.

1 | INTRODUCTION Dog food preferences evaluation is generally based on overall con-


sumption of the product, making the impact of smell difficult to assess on
Food choice is complex and is influenced by many internal and external its own. Indeed, the classic study procedure used in dogs and cats is the
factors, such as emotional and physiological states of the dog, food two-bowl paired comparison test (Aldrich & Koppel, 2015; Rashotte,
characteristics, etc. (Di Lorenzo & Youngentob, 2003). Among internal ron, & Larose, 2015) even if multiple com-
Foster, & Austin, 1984; Tobie, Pe
drivers, all sensory perceptions can influence food intake decision parison test are also possible (Hewson-Hughes et al., 2013; Li, Smith,
(Kitchell, 1978). Perception may vary according to species, breeds, and Aldrich, & Koppel, 2017). During the classical test, a panel of individuals is
individuals (Laska, 2017). In human sensory perception, it is known that simultaneously offered two bowls containing different products with the
taste perception can be modified by other sensorial modalities, such as same predetermined quantity. The animals are given free access to the
vision or smell (Arvisenet, Guichard, & Ballester, 2016; Charles et al., food for a limited time period (commonly 15–30 min), or until the quantity
2013; Lim, Fujimaru, & Linscott, 2014; Yin, Hewson, Linforth, Taylor, & equivalent of one bowl has been completely consumed (Aldrich & Koppel,
Fisk, 2017). Moreover, the combination of sensory inputs and their 2015). The criteria recorded are the first choice (first food product eaten)
temporal and spatial concurrence, have an impact on odor/taste inte- and the intake ratio (Food A/[Food A 1 Food B]). Even though the first
gration (Small & Prescott, 2005). It is not unreasonable to expect similar choice can provide information on the attractiveness of the product, it is
mechanisms in other animal species, such as in dogs. still impossible to derive any underlying motivations that might lead to food
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V
C 2018 The Authors. Journal of Sensory Studies Published by Wiley Periodicals, Inc.

J Sens Stud. 2018;33:e12311.


https://doi.org/10.1111/joss.12311 wileyonlinelibrary.com/journal/joss | 1 of 7

2 of 7 | PETEL ET AL.

selection, such as visual discrimination, difference in odor intensity, odor


recognition (from previous experience), individual odor preference, etc.
Despite these limitations, currently available literature indicates that
odor is a key driver in dogs’ food choice (Bradshaw, 1991, 2006; Horo-
witz, Hecht, & Dedrick, 2013; Houpt, Davis, & Hintz, 1982; Houpt, Hintz,
& Shepherd, 1978). For instance, dogs first trained to discriminate foods
from different meat sources are no longer able to do so once rendered
anosmic (Houpt et al., 1982). Less invasive approaches have been devel- FIGURE 1 Schematic representation of the false-bottom bowl
used to study the impact of odors in dogs’ food selection
oped to investigate the impact of odor on food preference. A recent
study measured the odor preference by using dogs’ exploration behavior
variations could influence their feeding pattern, and that the dogs would
toward two types of food that differed in palatability. In this two-step
not need to actually taste the product to confirm their first choice.
method, dogs could first see and smell the foods, but were not able to
This method could be helpful for pet food manufacturers to under-
reach them physically. In the second phase, dogs were allowed to con-
stand the reaction of dogs to new products and ingredients, and to
sume the products in a restrictive-intake consumption test (Thompson,
help in developing new appealing aromas for dog foods. It could also
Riemer, Ellis, & Burman, 2016). The authors observed that the proportion
provide further scientific insight into how dogs select their food.
of time spent by the dogs exploring both products in the first step was cor-
related to the consumption ratio observed during the second step. This
result emphasizes the impact of odor (and perhaps vision) on dogs’ food 2 | MATERIALS AND METHODS
choice. The main advantage of this technique is the ease of evaluating the
impact of odor on food selection. Nevertheless, several limitations have 2.1 | Subjects
been identified, including the delay between the exploration phase and A total of 36 kennel dogs from Diana Pet Food panels (Panelis, Elven,
the consumption period, the necessity for the product to be easily France) were involved in the study.
extracted from the device used for the study, and the possibility that vision Diana Pet Food’s dogs enter the panels following weaning. They
could well be involved in food selection in dogs. Furthermore, this method are housed in pairs with permanent outdoor access (pen size: 6 m2
may be limited to the comparison of finished products. indoors and 6 m2 outdoors for each pair of dogs), with a daily, 5-hr
In another study conducted in 2017, Hall et al. used an olfactome- period of exercise in outdoor enclosures in groups (average park size:
ter previously employed for discrimination tasks (Hall, Collada, Smith, & 260 m2 for 4–6 dogs). The dogs are isolated twice a day (morning and
Wynne, 2016) to evaluate food odor preference in dogs. After a train- afternoon) for 30 min during feeding time. The dogs are fed with nutri-
ing phase, dogs took part in several trials sessions, during which they tionally balanced, high premium, pet food products and the ration dis-
were asked to explore odors presented on both olfactometer ports
tributed is adjusted for each individual.
before selecting the one that they preferred. The authors did not
The group selected for the study was made up of 17 males (4 neu-
observe any significant preferences between the odors tested in the
tered, 13 entire) and 19 neutered females. The dogs age ranged from
dogs. Nevertheless, they found that dogs preferred to smell a food
0.5 to 7 years old (average 5 2.5 years old 6 0.24 years SE), and com-
odor rather than clean air. In the described study design, the only sen-
prised different sizes (average weight 5 17.7 6 1.9 kg SE, ranging from
sorial parameter evaluated was the odor, which enables a wider range
3 to 44 kg), and different breeds (19 different breeds).
of products to be compared using this method, as it is not carried out
under pet meal conditions (the dogs do not eat the odor). However, the
small sample size, the discrepancy between the odor presented and the
2.2 | False-bottom bowls apparatus
treat delivered, and the time required for the training and data acquisi- The newly developed method to assess food odor impact on dog’s
tion, are some limitations of the study. Other limitations could also preferences—The false-bottom bowls method (FBBs method)—derives
include be the difficulty of the task, or suitability of the test for dogs. from the paired comparison procedure (Tobie et al., 2015). In this new
ron, Cambou, Callejon, and Wynne (2017) study
While the Hall, Pe method, bowls traditionally used to compare food were modified by
was carried out to study food odor perception by dogs and to potentially adding a drilled, stainless-steel separation plate at the bottom of each
assess the impact of odor on dogs’ food choice, it was not carried out bowl, dividing them in two compartments (cf. Figures 1 and 2). These
under actual meal conditions. The results are an initial indication and do FBBs were designed to receive enough food in the superior compart-
not provide in-depth insights into food preference parameters in dogs. ment to cover the higher dogs’ energetic needs for one meal, and to
This study initially had different aims: (a) to develop a simple measure- allow positioning odorant compounds under the food.
ment device, close to meal conditions, with no training period required,
in order to assess odor impact on food choice in dogs; (b) to evaluate
2.3 | Products
odor detection and discrimination in dogs; (c) to evaluate if a product/
ingredient has odor potential; (d) to assess the effect of odor on dogs’ Four substances with different palatability levels were tested: tap-
food selection. Initial hypotheses were made based on the assumption water from Elven, France (Water); a simple ingredient diluted at 1.5%
that dogs could detect odor variations in a meal context, that these in tap-water (SI); and two commercial meat-based palatants from SPF,

PETEL ET AL. | 3 of 7

dog’s ability to detect a variation of intensity of an olfactory stimulus,


(c) to evaluate the odor potential of an ingredient; and (d) to assess the
capacity of dogs to discriminate between different stimuli (Table 2).
The conditions were not equal regarding their anticipated difficulty
level, based on previous, classic palatability tests. Nevertheless, the pre-
sentation order was randomized to take the effect of habituation into
account.

2.5 | Statistical analysis


F I G U R E 2 A dog eating in one of the two false-bowls. Kibbles are All the analyses were carried out using SAS version 9.4 (SAS Institute
placed above the separation and the olfactory stimuli under the INC, Cary, NC). Student paired t tests were used to determine the sta-
separation
tistical significance of intake ratios of the two bowls presented. Chi-
squared tests were performed on the first choices of the dogs between
Elven, France, differing in their composition: P1, a premium palatant
the two bowls presented.
and P2 a super-premium palatant, known to have a superior palatability
Mixed-effect models were performed to compare the ratio of
level than P1 in dogs (Table 1).
products KP1/P2 and KP1/water (in condition versus KP1/P1) and
Each substance was presented as an olfactory stimulus in the infe-
ratios of products KP1/SI and KP1/P1 (in condition versus KP1/water).
rior compartment of the FBBs, under nutritionally balanced dog kibbles
The models included dogs as random effect and the product as fixed
coated with fat and P1 (named KP1). The olfactory stimuli quantity
categorical effect.
used comprised 10% of the food ration placed above. This percentage
Mixed-effect models for each paired comparison test were per-
is a compromise between the minimum quantity required as a percepti-
formed to evaluate the effects of dog size, dog gender and day of test
ble intensity through the kibbles, and the maximum quantity that could
on intake ratio. The model included dog as random effect and the fixed
be placed under the separation plate for the biggest food rations.
categorical effects of dog size, day of test and gender.
All the effects were tested at 5% level.
2.4 | Procedures
The evaluated substances were presented twice in FBBs, under paired
2.6 | Ethical note
comparison conditions, on different days, at different meal times. The
side of the bowl containing the stimuli was changed between tests. Diana Pet Food’s panels’ activity (Panelis) is in compliance with the
The FBBs were removed once the dog had eaten the quantity equiva- rules of the French Ministry of Agriculture. Only palatability tests are
lent to one ration. conducted on site, the animals’ living conditions closely resemble pet
The first bowl selected by the dogs and the quantities of kibbles care that is given in a good home environment, and the animals benefit
eaten in both bowls were recorded and converted into two criteria: first from a varied well-being program with obedience training, agility, exer-
choice and intake ratio between bowls. The intake ratio criterion was pre- cise in enclosures, walks in the fields and forest, etc.
ferred over the total consumption criterion to avoid potential bias related As only behavioral data and noninvasive physiological parameters
to the individuals’ body size and the meal period (morning/afternoon). were followed, no special permission for the use of dogs was required
A total of four trials were conducted sequentially with different by the French Authorities. The research protocol was not subject to
objectives: (a) to assess each dog’s position bias; (b) to assess each the EU Directive 2010/63/EU.

TA BL E 1 Previous palatability results for standard paired comparison tests: first choice and intake ratio; with “first choice” the first bowl
selected by the dogs and “intake ratio” the ratio of eaten quantities in both bowls (Internal data—36 kennel dogs from Diana Pet Food panels
[Panelis, Elven, France])

Standard paired- First Intake First choice Intake ratio


comparison test Bowl Kibbles choice (%) ratio (%) significance significance
** **
Test 1 A KP1 23 35
B KP2 77 65
** ***
Test 2 A KP1 25 33
B KP2 75 67

Results of Chi-squared test for first choices, and T test for intake ratios: NS: p > .05; *: .05  p < .01; **: .01  p < .001; ***: p  .001.
KP1: Nutritionally balanced kibbles, coated with fat and P1.
KP2: Nutritionally balanced kibbles, coated with fat and P2.
P1, P2: respectively a premium and super-premium commercial meat-based palatant differing in composition and palatability level.

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TA BL E 2 False-bottom bowl trials: food and olfactory stimuli presented

Olfactory
Food above stimuli under Products
Trial n8 Objective Bowl the separation the separation code

1 Assess dog’s position bias A KP1 P1 KP1/P1


B KP1 P1 KP1/P1

2 Assess dog’s ability to detect a variation of intensity of an olfactory stimulus A KP1 Water KP1/Water
B KP1 P1 KP1/P1

3 Evaluate the odor potential of a stimulus A KP1 Water KP1/Water


B KP1 SI KP1/SI

4 Assess the capacity of the dogs to discriminate between stimuli A KP1 P1 KP1/P1
B KP1 P2 KP1/P2

KP1: Nutritionally balanced kibbles, coated with fat and P1.


P1, P2: respectively a premium and super-premium commercial meat-based palatant differing in composition and palatability level.
SI 5 simple ingredient.

3 | RESULTS level, showing that the dogs not only were able to detect the palatants
but also to rank them in accordance with results obtained with stand-
The results of the different trials are presented in Table 3. Results of ard paired comparison tests. The results of the comparison of KP1/P1
Trial 1 demonstrated that the new FBBs method did not lead to posi- with KP1/P2 (Trial 4) reflect the palatant ranking observed from previ-
tion bias. Indeed, there was no significant difference for both first ous standard paired comparison tests (KP2 > KP1—see Table 1).
choice and intake ratio between the two bowls that contained the Additional statistical analysis demonstrated that the dogs con-
same food and olfactory stimulus. In Trial 2, the first choice and intake sumed a significant (p < .001) portion of their kibble ration in the bowl
ratio were significantly higher for the bowl containing P1 as an olfac- KP1/P1 (85%), in the bowl KP1/P2 (60%), and in the bowl KP1/SI
tory stimulus, than for the one containing water (p < .001). The dogs (62%), in Trials 2, 3, and 4, respectively (Table 4). This result indicates
were able to detect the bowl, in which the palatant was placed under different palatability ranking based on odor: water < P1 < P2 and
the kibbles, and they showed a clear preference for that bowl. This was water < SI < P1.
probably due to a higher odor intensity effect, In Trial 3, there was no Finally, there were no significant effects of dog gender, dog size,
significant difference in the dogs’ first choice between the bowl con- or meal time on trial result (p > .1) (Table 5). According to these results,
taining the odorant ingredient and the bowl containing water, but they no effect can be attributed to external parameters.
ingested significantly more kibbles from the bowl containing the odor-
ant ingredient (p < .001). Finally, in Trial 4, the dogs showed a signifi- 4 | DISCUSSION
cant preference for the bowl containing P2, over the bowl containing
P1, for both first choice and intake ratio. The preference for the bowl The results of the trials provide evidence that the FBBs method fulfilled
containing P2 was consistent with the palatant superior palatability the aims of the study. Easy to implement, the new method allowed

TA BL E 3 Palatability results for each false-bottom bowl trial: first choice and intake ratio; with “first choice” the first bowl selected and
“intake ratio” the ratio of quantities eaten in both bowls

Trial Bowl Product codes First choice (%) Intake ratio (%) First choice significance Intake ratio significance

1 A KP1/P1 46 52 NS NS
B KP1/P1 54 48

2 A KP1/Water 13 15 *** ***


B KP1/P1 87 85

3 A KP1/Water 38 32 NS ***
B KP1/SI 62 68

4 A KP1/P1 30 43 ** *
B KP1/P2 70 57

Results of Chi-squared test for first choices, and T test for intake ratios: NS: p > .05; *: .05  p < .01; **: .01  p < .001; ***: p  .001.
KP1: Nutritionally balanced kibbles, coated with fat and P1.
P1, P2: respectively, a premium and super-premium commercial meat-based palatant differing in composition.
SI 5 simple ingredient; / 5 separation to locate each product above/under the grilled separation.

PETEL ET AL. | 5 of 7

TA BL E 4 Comparison of the average intake ratio between the multiple paired comparison test presentations in owned dogs (Hall et al.,
different false-bottom bowl trials 2017). However, on one occasion (Trial 3: K1/SI versus K1/Water), the
Adjusted average of first choice result did not correlate to the final intake ratio. The dogs
Reference Tested quantity consumed in apparently needed more information (flavor, as well as smell) to discrimi-
bowl bowl tested bowl (%)
nate between both products, as emphasized by the product effect on
KP1/P1 KP1/P2 60 the final intake ratio. This could be explained either by a lack of intensity
KP1/water 14
of the odor of SI, or by interactions between SI’s odor and the kibble
KP1/water KP1/SI 62 taste, as the dog needs to sample both bowls before choosing.
KP1/P1 85 This introduces several limitations of the method. The first could
be the olfactory intensity of the substance that is placed under the
KP1: Nutritionally balanced kibbles, coated with fat and P1.
P1, P2: respectively, a premium and super-premium commercial bowl separation. This could be under the dog’s olfactory threshold, or it
meat-based palatant differing in composition. may be too intense, and hence, repellent for the dog. To explore inten-
SI 5 simple ingredient; / 5 separation to locate each product above/
sity and detection issues further, the FBB method should be used with
under the grilled separation.
various concentrations of the tested olfactory stimuli to determine
their perceptible-, appealing-, or repulsive levels, and to investigate
measurement of significant dog’s preferences, depending upon the
dogs’ odor thresholds.
olfactory stimuli placed under kibbles. As the FBBs set-up does not
Moreover, the FFB set-up is subject to interactions between the
modify the kibbles, only their odor; these results most likely indicate
kibbles and the hidden substance’s odor, which cannot be controlled.
the impact of odor on the dog’s food choice.
The interactions between food matrix and odor, that may create poten-
It is interesting to note that the addition of a drilled separation into
tially new perceived flavors, are widely known in food analysis. They
a standard feeding bowl provides the advantages of a simple set-up
can be due to food composition, texture, or humidity (Dalla-Rosa, Pittia,
that closely resembles meal conditions, and a technique to evaluate
& Nicoli, 1994; De Roos, 2003; Perreault, 2007; Seuvre, Philippe,
odor perception without any training phase required, as the entire
Rochard, & Voilley, 2007). However, similar interactions occur when
panel of dogs ate confidently. This set-up was designed to compare
odorant substances are applied directly on kibbles, as the kibble core
dogs’ responses to potential odors in food and/or non-food substances.
releases its own aromas. In literature, some examples used specifically
According to these results, the FBB method allows the detection and
to avoid sensorial interaction with the product during the selection pro-
the discrimination by the dogs of hidden substances’ odor. Dogs seem
cess have been used (Araujo & Milgram, 2004). However, in these
to be able to discriminate between water and simple or complex ingre-
studies, which rely on an operant conditioning approach, information
dients, and between different complex ingredients, based on their
related to odor perception is either missing or not relevant.
odor. It is worth mentioning that while SI was not perceived by humans
The FFB method might have another limitation. In the study, the
(unpublished data), it was perceived and preferred over no smell (water)
dogs’ perception and discrimination abilities were assessed through the
by dogs. Had the dogs even selected water over SI, this result would
selection of a food bowl, which implies assimilation of detection and
still have indicated that dogs can perceive and discriminate between
food decision. In the case of nonsignificant results during the trials, it
the two products.
would have been difficult to discern between the absence of odor
In this study, olfactory information seems to drive food selection in detection and subsequent food decision capacity and the lack of inter-
dogs, as illustrated by the congruence between the first choice and the est in the odor by dogs. Dogs could have integrated the information
respective intake ratio (higher intake ratio for the first selected bowl). about the odor, but decided that this was not relevant in the situation
This result is supported by previous research results obtained using (Hall et al., 2017).
Moreover, even if several research projects indicate that olfaction
Evaluation of panel effect on false-bottom bowl results
TA BL E 5
is critical for dogs to differentiate between preferred and non-
(ANOVA 5%)
preferred food products, it is still not clear if the odors of the preferred
Trial n8 Bowl Products Size effect Gender effect Meal effect foods are more appealing (Hall et al., 2017). This hedonic consideration
2 A KP1/Water 0.8574 0.8838 0.1546 is as complicated to define for dogs, as for any other nonverbal species,
B KP1/P1 as we cannot conclude about their choice decision criteria, but can

3 A KP1/Water 0.945 0.2367 0.5693 only make inferences based on their feeding behavior (Day, Kergoat, &
B KP1/SI Kotrschal, 2009). Expressed preference can be linked to different
parameters, such as intensity or novelty effects that cannot be certainly
4 A KP1/P1 0.495 0.7682 0.8371
attributed to hedonic appeal. Food appreciation in dogs may be uncov-
B KP1/P2
ered by using other complementary approaches, such as behavioral
KP1: Nutritionally balanced kibbles, coated with fat and P1. studies, and by monitoring arousal level (Kostarczyk & Fonberg, 1982;
P1, P2: respectively a premium and super-premium commercial meat-
based palatant differing in composition. Travain et al., 2016).
SI 5 simple ingredient; / 5 separation to locate each product above/ Another concern was linked with food rejection (Houpt et al.,
under the grilled separation. 1978). As dogs do not have the opportunity to taste the substance that

6 of 7 | PETEL ET AL.

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mittee for a company, or consultancy for, or receive speaker’s fees Kitchell, R. L. (1978). Taste perception and discrimination by the dog.
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