PLoS ONE
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Turning preference in dogs: North attracts while south repels
DOI 10.1371/journal.pone.0245940 , Volume: 16 , Issue: 1
Article Type: research-article, Article History
Abstract

It was shown earlier that dogs, when selecting between two dishes with snacks placed in front of them, left and right, prefer to turn either clockwise or counterclockwise or randomly in either direction. This preference (or non-preference) is individually consistent in all trials but it is biased in favor of north if they choose between dishes positioned north and east or north and west, a phenomenon denoted as “pull of the north”. Here, we replicated these experiments indoors, in magnetic coils, under natural magnetic field and under magnetic field shifted 90° clockwise. We demonstrate that "pull of the north" was present also in an environment without any outdoor cues and that the magnetic (and not topographic) north exerted the effect. The detailed analysis shows that the phenomenon involves also "repulsion of the south". The clockwise turning preference in the right-preferring dogs is more pronounced in the S-W combination, while the counterclockwise turning preference in the left-preferring dogs is pronounced in the S-E combination. In this way, south-placed dishes are less frequently chosen than would be expected, while the north-placed dishes are apparently more preferred. Turning preference did not correlate with the motoric paw laterality (Kong test). Given that the choice of a dish is visually guided, we postulate that the turning preference was determined by the dominant eye, so that a dominant right eye resulted in clockwise, and a dominant left eye in counterclockwise turning. Assuming further that magnetoreception in canines is based on the radical-pair mechanism, a "conflict of interests" may be expected, if the dominant eye guides turning away from north, yet the contralateral eye "sees the north", which generally acts attractive, provoking body alignment along the north-south axis.

Adámková, Benediktová, Svoboda, Bartoš, Vynikalová, Nováková, Hart, Painter, Burda, and Roman: Turning preference in dogs: North attracts while south repels

Introduction

Dogs in two-choice experiments, when selecting between two dishes with snacks placed in front of them, 90° apart, left and right, prefer to turn either clockwise (“right-preferring”) or counterclockwise (“left-preferring”) or randomly in either direction (“irresolute”). This turning preference (or non-preference) is individually consistent in all trials but it is biased in favor of north if they choose between dishes positioned north and east or north and west, a phenomenon we denoted as “pull of the north” [1]. This phenomenon was particularly pronounced in older dogs, females, smaller and medium-sized breeds, dogs exhibiting a turning preference, and especially in the north-east choice. We suggested that “pull of the north” represents a further indication of magnetoreception in dogs, the other being non-random directional alignment during marking [2], which was, however, significantly changed when exposed to bar magnets [3], the ability to find a bar magnet [4], or the existence of the so-called "compass run" exhibited during homing [5].

We are, however, aware that for the ultimate evidence of magnetoreception, experiments in defined manipulated magnetic field and/or under conditions of disturbed magnetoreception are necessary. Moreover, the proximate reason for “pull of the north” remains unclear and should be at least hypothesized.

Laterality, i.e. a predictable, non-random preference for using one side of the body (limbs, brain hemisphere, sensory organs) spontaneously or if forced or restricted to choose between two sides, is a known phenomenon in humans and animals. Laterality may be inborn, imprinted, or entrained and has to be taken into account in maze and behavioral two-choice animal experiments [610].

Laterality in dogs has been intensively studied with regard to the motoric (efferent) aspect (paw laterality, Kong-test: [1115]; sensory (afferent) aspect [1618]; cognitive [19], and emotional aspects [2022]. Interestingly, and contrary to studies in humans, turning (directional, rotational) preference has remained understudied.

Most people are right-handed, yet tend to instinctively veer to the left upon entering a new space [23]. Interestingly, the counterclockwise action goes also for most athletic tracks, horse and car races, and for baseball players running the bases [24]. There is even evidence that the chariot races at ancient Rome's Circus Maximus ran counterclockwise, too [25,26]. So, in sports, where competitors enter the field of play from the outside of a traced circle, a right-directional choice would lead to a counter-clockwise motion. But when entering the field of action from within the circle—walking out of your apartment to take the dog for a walk, and encountering intersections—right directional choices would tend towards tracing a clockwise path [23]. Interestingly, in the countries, where people drive on the left side of the road, retail shoppers tend to turn counterclockwise—when navigating store aisles, while in the countries, where people drive and keep on sidewalks right, veer clockwise [23]. Tendencies of people to turn either direction are known to architects who use them to design shopping galleries to funnel shoppers in the wished direction [23].

While the preference to turn in a certain direction can be explained by individual inborn laterality (handedness) and experience (facilitation), or–e.g. in the context of our experiment of choice between two dishes, which is a visually guided task, through visual laterality—the “pull of north” is expected to have a magnetoreceptive ground. Examination of this phenomenon has a heuristic potential in getting insight into the very seat and mechanism of magnetoreception, which still remain enigmatic [27].

Sensory laterality (or asymmetry) has been described also in the context of spatial orientation in general and magnetoreception in particular. It has been found that homing pigeons rely more on the right olfactory system in processing the olfactory information needed for the operation of the navigational map [28]. An earlier study [29] has shown that the magnetic compass of a migratory bird, the European robin (Erithacus rubecula ), was lateralized in favour of the right eye/left brain hemisphere. However, it has been later demonstrated [30] that the described lateralization is not present from the beginning, but develops only as the birds grow older. In another study [31], it was shown that pigeons can perceive and process magnetic compass directions with the right eye and left brain hemisphere as well as the left eye and right brain hemisphere. However, while the right brain hemisphere tended to confuse the learned direction with its opposite (axial response), the left brain hemisphere specifically preferred the correct direction (angular response). The findings thus demonstrated bilateral processing of magnetic information, but also suggested qualitative differences in how the left and the right brain deal with magnetic cues.

Based on the hitherto knowledge and the above arguments,

    • We hypothesize that if “pull of the north” is due to magnetoreception (and indeed no other explanation is apparent), it should be demonstrated also in an artificial magnetic field shifted by magnetic coils, i.e. the artificially shifted magnetic North should exert the same effect as the natural geomagnetic North.
    • We expect that, consistently with results of the previous study [1] “pull of the north” is more pronounced in “lateralized” dogs and more in the North-East (N-E) combination than in the North-West (N-W) choice.

Furthermore, following questions can be raised (and should be tested) to get insight into the nature of the turning preference:

    3 Does the directional preference for turning correlate with motoric laterality (such as paw-laterality, i.e. “handedness”)?
    4 Is pull of the north a) symmetrical (bilateral, i.e. of the same strength in the clockwise as in counterclockwise direction), or b) asymmetrical (unilateral, i.e. stronger in one particular direction)?

Material and methods

Ethics statement

The study did not involve any disturbance or discomfort to the study subjects. The Professional Ethics Commission of the Czech University of Life Sciences in Prague has decided that according to the law and national and international rules, this study has not a character of an animal experiment and does not require a special permit.

Subjects

Altogether, 23 domestic dogs Canis familiaris (11 M, 12 F) from six breeds with pedigree and an average age of 4.8 (± 2.8) years (Table 1) were used in this study. The dogs were pets living in households. All the dog owners were present with their dogs at trials.

Table 1
List of the tested dogs and resulting indices of directional preference.
DogOwnerBreedSexAgePaw motorical lateralityInitial turning preferenceMean turning preference
AmalkaKBDachshund DF5511746
ArthurESDachshund NM2n.m.-32-45
AziziJSBeagleM66-419
BarcaLSFox TerrierF1206742
BertikKBDachshund DM68-29-48
BessyJAFox TerrierF8262242
FigyKBDachshund DF59-48
GofiJAFox TerrierF3-70-95-96
HardJAFox TerrierM2-46222
HugoKBDachshund DM3n.m.-25-17
HurvinekKBDachshund DM751-46-45
JimmyESDachshund NM2n.m.6035
KackaKBDachshund DF525-17-18
KukyKBDachshund DM7275040
NatyESMünsterländerM3n.m.-45-62
OffiJSBeagleF9-386
PeckaKBDachshund DF2-441729
PlysakKBDachshund DF210-37-60
PuntaKBDachshund DM3-1-8-34
RoxxyJSBeagleF91006267
ShedyESWeimaranerM5n.m.2740
SisiKBDachshund DF3n.m.1242
ZofkaKBDachshund DF2-205446
Paw motoric laterality = laterality index based on the Kong test; Initial turning preference Turning preference index in the first trials of each dog. Mean turning preference = = mean turning preference index over all trials of each dog. The value of the index can range from -100 to -25 (= left-turning dog) to 25–100 (= right-turning dog). Sex: F = female, M = male. Age is given in years. Dachshund N = normal-sized dachshund, Dachshund D = dwarf-sized dachshund, n.m. = not measured.

Experimental equipment

The experiment took place in a magnetic coil at the field research station Truba, Kostelec nad Černými lesy, (N 50°0.40480', E 14°50.11145'), a detached workplace of the Faculty of Forestry and Wood Sciences, Czech University of Life Sciences in Prague, Czech Republic. The magnetic coil (a Merritt coil, built according Kirschvink [32]) was 4 x 4 x 4 m and was located in a separate special building. It was shielded from radiofrequency waves. It was controlled from a separate building next to the coil building. The magnetic field in coils was manipulated by a MagFieldG control software through a GMP4 RJ4.01 control unit and three current amplifiers, each for the Bx axis, the By axis and the Bz axis. The generation system for GMP4 3D coil system was used to create a defined direct and slowly changing magnetic field and it served to drive the coil system to create a defined magnetic field.

Magnetic induction values in the Cartesian coordinate system (axis Bx = -3225 nT; axis By = 17800 nT; axis Bz = 45448 nT) were set for the experiment, thereby rotating the magnetic field by 90° magnetic North was shifted to the topographic (= geomagnetic) East. The magnetic field strength and inclination were maintained as for geomagnetic values for local geographic conditions. The magnetic coil space was used also for the control experiment to test the dogs under local geomagnetic conditions, while other experimental conditions were preserved identic, i.e. shielding of radiofrequency waves, avoiding other influences (wind, sun, outside sounds). The coil room was equipped with cameras (AXIS P5624-E 50HZ—PTZ IP camera, TD / N, 18x zoom, HD 720p, IP66, PoE +) for video recording of the entire experimental space, network speaker with SIP, PoE support (AXIS C3003-E NETWORK HORN SPEAKER, Double—sided audio) and microphone (AXIS T8353A MICROPHONE 3.5MM) at the control station to secure communication of the leading experimenter in the control workplace with two experimenters in the coil.

Experimental procedure

Dogs were tested indoors, in a room housing the magnetic coils, and should make the choice between two identical dishes. The dishes were placed at a distance of 2.9 m from the point of release of the dog, always a plus and minus 30° from the starting point. Both dishes contained the same treats and dogs were always allowed to empty both. After placing the dishes, the dog was ready for the starting point and waited to obtain a permit to go to a dish. The dogs could not see the placement of the reward dishes. Three experimenters were involved in the experiment; two were present in the magnetic coil (the owner was guarding the dog and prohibited it from seeing the preparation procedure, and the other was preparing the placement of the rewarded dishes), the third experimenter was in the control room using a microphone and headsets to communicate with the two other colleagues, changed the experimental magnetic conditions (switching between control and experimental conditions) according to a randomized schedule and recorded the results (direction of dog first choice) (Fig 1). Note that this person was the only one who knew the actual position of the magnetic North inside the coil.

Experimental setup as monitored from above by a camera placed at the ceiling of the room, showing the sequence from release of the dog (A) to its choice of one of two dishes (D).
Fig 1
Experimental setup as monitored from above by a camera placed at the ceiling of the room, showing the sequence from release of the dog (A) to its choice of one of two dishes (D).

Each dog was tested in three to five test series under the control conditions with the magnetic North (mN) being 0°, and in the same number of test series in an artificially shifted magnetic field with mN = 90° (where magnetic north was set on topographic east). The order of the test series (control first, shifted field second or shifted field first, control second) was taken into account. Tests series were performed at different days, at different daytimes, evenly distributed over the whole day.

Because a series included four trials in each dish combination alignment (i.e. N-E, E-S, S-W, and W-N), individual dogs experienced either 48 or 80 trials (in 12 or 20 complete series) in which their turning preference (first dish choice) was recorded under control conditions and the same number of records was gathered for experiments in the shifted magnetic field. The difference in the number of series and trials experienced by individual dogs was given by their availability for our study.

In addition, the dog's identity, date, time, sequence of trials combinations, and the order of the trials in the respective series were recorded.

Paw preferences

To determine paw preference (motoric laterality of dogs), a modified Kong test [e.g. 12,16,33] was used. In this test, it is recorded with which paw (left or right) the dog holds a Kong, a dog toy (KONG Company) when trying to get the food stuffed inside. A plastic yoghurt cup was used instead of Kong. The inner walls and bottom of the cup were covered with a dog's delicacy such as lard, cream cheese. Each dog was tested at home in an open area for 10 minutes while the dog played with the cup and tried to lick it out and the number of touches with either paw was recorded. Simultaneous touches with both paws were also recorded but were not included in the calculation of the index of laterality. The dogs who did not touch the cup during test of paw preference are excluded from the analysis of the Kong test.

Data analyses

From the recorded choices for each dog, in each trial, the left and right turning preferences were summed, for all four combinations (W-N; N-E; E-S; S-W) separately. For data analysis, the turning preference index was calculated in tests performed in the control and shifted magnetic field. The formula (R-L / R + L) x 100 was used, where the R = right and L = left sides are the total numbers of the first choice of left or right dishes. The laterality index for the paw preference (Kong test) was calculated using the same formula. The value of the index can range from -100 to -25 (= left-pawed dog) to 25–100 (= right-pawed dog). Dogs with index values between -24 and 24 were considered ambilateral. For the turning preference, altogether ten indices (LI) were calculated; one for each dish combination alignment (N-E, E-S, S-W, and W-N), i.e. four altogether in the control conditions and four altogether in the shifted magnetic field conditions. Furthermore, we calculated one mean index for control conditions and one mean index for shifted magnetic field (S1 Table). The dogs were divided in turning preference left-preferring, right-preferring or irresolute (ambilateral) preference according to [33] based on results of the first trials (Initial turning preference in Table 1). Generalized Linear Model (GLM) contained the interaction between Magnetic field and Turning preference classes.

From the recorded choices, preferences for either left or right turn were calculated for all test combinations (N-E, E-S, S-W, W-N) within each trial, and the sum of all trials of each dog. Index of directional preference was then calculated (according to the above formula) for each dog.

All data were analyzed using the SAS System (SAS, version 9.4). For calculating Spearman correlation coefficient we used PROC CORR. To analyze the factors affecting the directional preference index (dependent variable) we used a multivariate Generalized Linear Mixed Model (GLM, PROC MIXED). We constructed two GLMs. The models were applied as a fixed-effect models designed for the repeated measures, i.e., in SAS, with REPEATED = order of testing and the SUBJECT = Name of the dog with compound symmetric covariance structures for repeated measures (TYPE = cs). The first GLM was constructed with the predicted fixed factors Magnetic coil in an interaction with the Turning preference classes, and then we added other variables listed in S2 Table in case they could affect the directional preference index. None of these variables appeared significant and therefore we will not mention them in the text any more. Least squares means (LSMEANs) were calculated for the categorical fixed effects by computing the mean of each treatment and averaging the treatment means. These means of means were then used to compare the factors.

The second model was designed to estimate repeatability of the directional preference across experimental conditions. The GLM contained the only fixed factor Magnetic coil. We calculated repeatability as the intraclass correlation coefficient [34] by adding the RCORR option to the REPEATED.

Independently, mean directional compass preference based on the frequency of first choices in a given combination in all pooled trials was calculated for each dog using circular statistics with Oriana 4.02 (Kovach Computing). Grand mean vectors were then calculated on the base of those mean dog vectors for all the dogs, and subgroups with respect to turning preference, experimental condition, sex, and age.

Results

Paw preference (motoric laterality, Kong test)

Following the a priori set criterion, out of altogether 17 dogs tested, 3 dogs were classified as left-lateral, 6 as right-lateral, and 8 as irresolute (ambi-lateral) (Table 1). There was no apparent effect of sex, age, breed or owner on this type of laterality. The correlation between the Kong and overall turning preference tests was rather weak (rs = 0.317, P = 0.22).

Turning preference under the control (mN = 0°) and experimental (mN = 90°) conditions

Following the a priori set criterion, out of altogether 23 dogs tested, 6 dogs were classified as clockwise-preferring (right-lateral), 7 dogs as counterclockwise-preferring (left-lateral), and 10 as irresolute (ambi-lateral) (Table 1). There was no significant difference in turning preferences of individual dogs between control conditions (mN = 0°) and the shifted magnetic field conditions (mN = 90°) (Fig 2). There was a variation in the turning preference index according to the magnetic north direction and Turning preference classes (F(23, 131) = 4.59, P<0.0001, Figs 2 and 3). For the dogs with clockwise turning preference, there was a trend towards increasing the turning preference index from NE, SE, SW and NW. In other words, the clockwise turning dogs exhibited the lowest turning preference index in the combination North-East. However, only the difference between NE vs NW and between NE and SW, and only in the shifted magnetic field, reached the level of significance (P = 0.05) (Fig 2 left). For the dogs with counterclockwise turning preference, the most intensive counterclockwise preference was shown in SE orientation in comparison with NW and partly NE, while the weakest preference was in shown in the NW combination. Significant differences were achieved in the shifted magnetic field in SE vs NW, and under control conditions in NE vs SE, SE vs NW, SW vs NW (Fig 2, middle). No trend nor differences were detected for dogs showing irresolute turning preference (Fig 2, right).

Turning preference index.
Fig 2
(Least Square Means ± SE) for clockwise-preferring (left), counterclockwise-preferring (middle), and irresolute (right) dogs under the conditions of the magnetic North (mN) = 0° (control) and mN = 90° (shifted magnetic field) for the four particular combinations of the placement of dishes.Turning preference index.
Numbers in each quadrant (in the respective four compass combinations: N-E, E-S, S-W, W-N) show mean values of turning preference indices calculated from individual dogs and pooled across all trials (both control and shifted magnetic field conditions).
Fig 3
The value of the index can range from -100 to -25 (= left-turning dog) to 25–100 (= right-turning dog). Data were partitioned by turning preference (left figure shows clockwise turning preference, right figure shows counterclockwise turning preference; irresolute dogs were not calculated. The green arrow over the dog's head in the centre of the circle indicates the direction of view of the (supposedly) dominant eye which guides turning direction, while the red arrow shows the direction of view of the contralateral eye, supposed to exert "pull of the north" if heading northwards. Green arrow outside the circle designates the preferred direction of turning, the shorter red arrow designates "pull of the north".Numbers in each quadrant (in the respective four compass combinations: N-E, E-S, S-W, W-N) show mean values of turning preference indices calculated from individual dogs and pooled across all trials (both control and shifted magnetic field conditions).

There was significant bias from the overall turning preferences in the eastern hemisphere, expressed as the "pull of the north", in that a dish placed eastwards was more frequently chosen than a dish placed southwards and a dish placed northwards more frequently chosen than a dish placed eastwards, resulting in an average (theoretical) preference for NNE (Fig 4, Table 2). In a more differentiated view, this result was due to a dominant preference of females and/or clockwise preferring dogs for North (over East) and to an additional weaker pull of the East over South in males and/or counterclockwise preferring dogs. "Pull of the north" in irresolute dogs was indicated but not significant (Table 2, Figs 2 and 3).

Mean preference for compass direction of a dish with snacks of the first choice.
Fig 4
Angular means over dogs preferring to turn clockwise, those preferring to turn counterclockwise, dogs which were irresolute in their preference, and over all dogs. The arrow indicates the grand mean axial vector (μ) calculated over all angular means. The length of the mean vector (r) provides a measure of the degree of clustering in the distribution of the mean vectors. The inner circle marks the 0.05 level of significance border of the Rayleigh test. See Table 2 for statistics.Mean preference for compass direction of a dish with snacks of the first choice.
Table 2
Circular statistics for frequencies of choices of a dish placed in different cardinal compass directions in front of a dog in dual choice experiments, where the dog chose between north or east, east or south, south or west, west or north.
VariableAll trialsmN = 0°mN = 90°1st series2nd series
Number of dogs tested2323232323
Mean vector (μ)21°43°350°22°17°
Length of mean vector (r)0.4850.5570.4640.3470.566
Circular standard deviation69°622°71°83°61°
95% Confidence interval (-/+) for μ349°-53°16°-70°316°-23°335°-68°351°-44°
99% Confidence interval (-/+) for μ339°-63°7°-78°305°-34°321°-82°342°-52°
Rayleigh test (Z)5.4027.1344.9452.7667.378
Rayleigh test (p)0.0044.92E-040.0060.0613.68E-04
Variablemalesfemalesclockwise preferringcounterclockwise preferringirresolute
Number of dogs tested11126710
Mean vector (μ)44°48°
Length of mean vector (r)0.5170.5290.6370.6550.356
Circular standard deviation66°65°54°53°82°
95% Confidence interval (-/+) for μ358°-90°318°-42°318°-53°9°-90°279°-87°
99% Confidence interval (-/+) for μ344°-105°304°-56°303°-68°354°-103°252°-113°
Rayleigh test (Z)2.9393.3572.4313.0051.268
Rayleigh test (p)0.0490.0310.0840.0430.288
Each compass direction was offered with the same frequency. Mean vectors in this table represent thus grand mean vectors. Cf. Fig 4.

Repeatability of turning preference

A single factor of Magnetic coil was not significant (F1, 22 = 1.16, P = 0.86). On the other hand, Repeatability was high (r = 0.76).

Discussion

Turning preference did not correlate with the motoric paw laterality (Kong test). Apparently, both types of preferences are controlled by different proximate mechanisms / pathways. This conclusion is consistent with earlier findings [35] showing that visual (sensory) and paw (motoric) laterality in dogs are independent of each other. None of the dogs had any previous experience with emptying cups (i.e. Kong-type tests). None of the dogs used in this study had a history of being trained "Heel" to come and follow the master at her/his left (or right) side. Consequently, their turning preferences can be considered natural, spontaneous, inborne, and not entrained. Accordingly, there was no significant difference in the turning preference in particular dogs between the first and second experimental series and there was no effect of the respective owner. Interestingly, among the dogs who turned clockwise there were more females, while among the dogs turning counterclockwise there were more males. The sample was, however, too small to allow any general conclusion with regard to the effect of sex on turning preference. In fact, no clear effect of sex on turning preference was found in a previous study (with a different composition of the study sample) [1].

Consistently with results, of the previous study in open field [1], the turning preference was consistent for each particular dog for all combinations of placement of dishes also in an interior with uniform walls, no apparent landmarks, and no sun or wind cues. Concordantly with the results of the previous study, this preference was slightly, yet significantly disturbed (or pronounced) in that the north-placed dishes were more frequently chosen than would be expected according to the average turning preference of each particular dog. Most important in the context of the present study is the finding that, magnetic and not topographic, north affected the mentioned bias.

The detailed analysis shows, however, that the "pull of the north" is a more complex phenomenon, involving also "repulsion of the south". These effects are unilateral: the clockwise turning preference in the right-preferring dogs is more pronounced ("accelerated") in the S-W combination, while the counterclockwise turning preference in the left-preferring dogs is "accelerated" in the S-E combination. On the other hand, N-E combination decreases ("decelerates") clockwise turning preference in the right-preferring dogs, while in the N-W combination, the counterclockwise turning preference in the left-preferring dogs will be reduced. In this way, in the total, south-placed dishes are less frequently chosen than would be expected, while the north-placed dishes are apparently more preferred. Since "rotational deceleration" is stronger in N-E than the N-W combination, while the "acceleration" is stronger in the S-E than in the S-W combination, the resulting theoretical mean preference is for Northeast.

It may be of relevance and significance in this context that the analysis of published results on magnetic alignment behaviour in a variety of vertebrate species revealed that magnetic alignment typically coincides with the north-south magnetic axis, however, the mean directional preferences of an individual or group of organisms is often rotated clockwise from the north-south axis [3638]. The deviation from the magnetic north-south axis could originate at different levels in the sensory hierarchy: it could be related either to asymmetries at the sensor level or to functional brain asymmetries, i.e. central processing.

Although the mode of the perception of the magnetic compass direction in animals remains enigmatic [27], findings from behavioral, histological, neuroanatomical, and electrophysiological studies have led to several physically viable theoretical models that might also apply to dogs. Two mechanisms are most widely discussed in the literature: the magnetite-based mechanism and the radical-pair mechanism.

Perhaps the most intuitively appealing mechanism to explain magnetosensitivity in animals is the idea of a small permanent magnet inside the animal that acts like a compass needle [39]. Magnetite-based sensors may be located anywhere in the body, they do not need to be concentrated in (paired) organs and they can be very tiny.

Another proposed mechanism for magnetoreception in animals is based on an effect of the magnetic field on the quantum spin states of a photo-excited chemical reaction that forms long-lived, spin correlated radical pair intermediates (radical pair mechanism; [40,41]. It is believed to occur in the specialized retinal cells [42,43]. It is assumed that the magnetic field may generate a “visual” pattern of varying light intensity, color, and/or contrast superimposed on the normal visual scene [40,44,45]. The model suggests that north or south “patterns” are more clearly recognizable and easier to be followed than east or west “patterns”. Accordingly, and alternatively, the “pull of the north” could be also interpreted as a “deflection / repellence by the east or west”.

Given that the choice of a dish in our experiment was visually guided, we may postulate that the turning preference was determined by the dominant eye, so that a dominant right eye resulted in clockwise, and a dominant left eye in counterclockwise turning. Assuming further that magnetoreception in canines is based on the radical-pair mechanism [46,47], a "conflict of interests" may be expected, if the dominant eye guides turning away from north, yet the contralateral eye "sees the north", which generally acts attractive, provoking body alignment along the north-south axis. To test this hypothesis, visual dominance (eyedness) in particular dogs should be studied in an independent test, e.g. sensory jump test [35].

Magnetic alignment might have an adaptive function in that it provides a global reference frame that helps to structure and organize spatial behavior and perception over many different spatial scales. For example, one possibility is that magnetic alignment helps to put the animal into register with a known orientation of a mental (cognitive) map, reducing the complexity of local and long-distance navigation, and reduces the demands on spatial memory [44]. This would be analogous to strategies used in human orientation; it is much simpler and intuitive to navigate when the navigators align themselves with a physical map (i.e. the users rotate their body direction to coincide with the alignment of the physical map), rather than to navigate by mentally rotating the physical map to align with the user’s orientation. Therefore, we suggested that the mental map in animals is fixed in alignment with respect to the magnetic field [2,38]. Indeed, important component(s) of the cognitive map may be derived from the magnetic field (see below) and spontaneous magnetic alignment behavior may help to place the animal into register with this map. This relatively simple alignment strategy would help animals to reliably and accurately ‘read’ their cognitive map and/or extend the range of their maps when exploring unfamiliar environments. Accordingly, animals of different taxa were frequently reported to prefer to head about northwards when feeding (reviewed in [3638]).

We suggest that the described simple turning test has a high heuristic potential and should be extended for tests of visual laterality and be performed under a wider array of experimental conditions to get more insight into the very mechanism, seat and function of magnetoreception.

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20 Oct 2020

PONE-D-20-31110

Turning preference in dogs: north attracts while south repels

PLOS ONE

Dear Dr. Burda,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

The reviewers believed there was merit to the study, but also that they lacked all the information necessary to make firm conclusions on the result's validity and the conclusions drawn.  Specifically, both reviewers felt the methods sections was not sufficiently clear.  I believe that much more attention to the methods will be needed for publications.   Specifically the clarification of abbreviations, and the number of trials and what where the indices were used.  I felt that the description of how the experimenters were blinded also needed a great deal more clarity - e.g., state very concisely who interacted with the dogs, and who new the location of magnetic north in each experiment.  

The results appeared to leave the reviewers with several more questions.  It is unfortunate that Fig4 was missing for the reviewers, however, both reviewer #1 and #2 had additional important questions on the interpretations of figs 2 and 3.  Although new experiments may not be needed, Reviewer #1 had some important questions regarding dog-owner interactions that should be addressable and would hopefully help eliminate some potentially trivial explanations for the North pull.   Additional questions on eye-laterality were brought up in response to the discussion.  I believe these are important questions from reviewer #1 and please try to answer if possible. If you cannot answer them, these limitations of current knowledge should be at least addressed in the discussion. 

There were also questions regarding the role of the eyes in magnetic detection.  Unless you have experimental data that addresses this, I believe this can also be handled in the discussion by referring to data from other vertebrate systems and clearly drawing the inferences.  

==============================

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Reviewer #1: There were a few places where I was a little confused about the method. For example the paragraph beginning on Line 193. I was confused about how many total trials dogs had and what exactly what meant by first choice. The sentence on Lines 220-222 I found similarly confusing. What were the 10 indices? There were not 10 mentioned so I wasn’t sure what was being explored here.

Do other studies show similar patterns in laterality? That is, that about half of the dogs do not have a preference? Is laterality preference (or lack thereof) independent of the task? Or could a dog have a preference for one paw on a kong task and a preference for another paw on a different task? It could be helpful to show that the dogs’ paw laterality isn’t just random but is stable within dogs either by citing work that demonstrates that it is so or by giving these dogs a second laterality test and showing that they are consistent.

I think the talk of eye dominance is interesting, but the authors’ case would be significantly strengthened by demonstrating that such eye preferences exist. In other words, is there a simple eye dominance task that the authors could do to assess the dogs’ eye dominance? Given that so much of their discussion is based on the assumption about eye dominance it would strengthen the paper significantly to show that such eye dominance exists and tracks with their predictions.

Similarly, is there evidence that dogs have magnetic field receptors in their eyes?

The authors mention that the dogs do not have a history of coming to heel, but I wonder about other types of owner interactions. Do owner handedness or owner turning preferences track with dogs’ preferences?

There are a few awkward sentences (lines 85-88; 132-134)

Where is Figure 4?

Reviewer #2: In earlier outdoor experiments, dogs were found to prefer the North direction and avoid South, when choosing between two food dishes placed in front of them. In this paper, the authors repeat these experiments indoors under controlled conditions, and by shifting the north direction of the magnetic field, they demonstrate that this preference is based on the magnetic field.

In the introduction, the questions are clearly stated. The description of the experimental procedure appears rather cryptic and suffers from the use of many abbreviations. The result part is hard to read. I have problems to derive from Fig. 2 a “pull of the north”, and also in Fig. 3, it is unclear what the numbers in each quadrant mean. Fig. 4 is missing altogether.

The best part of the paper is definitely the discussion. I welcome the authors’ attempt to propose a promising idea for explaining why so many animals show a magnetic alignment.

**********

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7 Dec 2020

Dear editor, dear reviewers,

we appreciate very much your interest in our study and attention given to our manuscript and the very thoughtful and constructive comments aimed to improve our contribution. We have carefully considered all of them, and we response to them point by point and describe how we changed the manuscript (below, in blue print). Thank you very much for giving us the chance to revise and amend the ms and for taking the revised version and our rebuttal into consideration.

Best regards

Hynek Burda

On behalf of all coauthors

Comments and summary of the academic editor

Editor points out the need for:

clarification of abbreviations, and the number of trials and what where the indices were used.

This clarification was requested also by the reviewers and we respond specifically below. Also, we have addressed these points in the revised ms.

the description of how the experimenters were blinded (e.g., state very concisely who interacted with the dogs, and who new the location of magnetic north in each experiment).

We describe this on lines 177-185 of the revised ms. We added further information which points out the way of blinding the experiment.

Fig4 was missing

This is indeed unfortunate and we apologize. The figure has been uploaded now. Please note that the statistical values in Table 2 have partly changed. This is because we based the figure now on the attribution of dogs to laterality categories according to results in the first trials (and not to mean laterality indices) to ensure comparability of all figures.

both reviewer #1 and #2 had additional important questions on the interpretations of figs 2 and 3.

We react below and in the revised ms.

Although new experiments may not be needed, Reviewer #1 had some important questions regarding dog-owner interactions that should be addressable and would hopefully help eliminate some potentially trivial explanations for the North pull. Additional questions on eye-laterality were brought up in response to the discussion.

We address these important and interesting points below and in the revised ms.

Reviewer #1:

There were a few places where I was a little confused about the method. For example the paragraph beginning on Line 193. I was confused about how many total trials dogs had and what exactly what meant by first choice.

Looking at the sentence with time lag, we see also the problem and agree with the reviewer. We have reworded the sentence and specified the numbers as follows:

Because a series included four trials in each dish combination alignment (i.e. N-E, E-S, S-W and W-N), individual dogs experienced either 48 or 80 trials (in 12 or 24 complete series) in which their turning preference (first dish choice) was recorded under control conditions and the same number of records was gathered for experiments in the shifted magnetic field. The difference in the number of series and trials experienced by individual dogs was given by their availability for our study.

The sentence on Lines 220-222 I found similarly confusing. What were the 10 indices? There were not 10 mentioned so I wasn’t sure what was being explored here.

Again, we agree with the reviewer and apologize. We have changed the text as follows:

For the turning preference, altogether ten indices (LI) were calculated; one for each dish combination alignment (N-E, E-S, S-W, and W-N), i.e. four altogether in the control conditions and four altogether in the shifted magnetic field conditions. Furthermore, we calculated one mean index for control conditions and one mean index for shifted magnetic field.

Do other studies show similar patterns in laterality? That is, that about half of the dogs do not have a preference? Is laterality preference (or lack thereof) independent of the task? Or could a dog have a preference for one paw on a Kong task and a preference for another paw on a different task? It could be helpful to show that the dogs’ paw laterality isn’t just random but is stable within dogs either by citing work that demonstrates that it is so or by giving these dogs a second laterality test and showing that they are consistent.

Concerning general laterality behavior in dogs: These are relevant questions, but it is not really what this study set out to address. There are published papers on laterality in dogs on a variety of behavioral tasks which we mention and cite (reference numbers 6-22), however, what we can say is that laterality, as measured by the Kong test, cannot account for the turning preference exhibited by the dogs evaluated. Indeed, this is a strength of the study rather than a weakness, as it uncouples handedness/lateral dominance (motoric laterality) and magnetic turning preference (presumably a sensory laterality). Similarly, it was shown in an earlier report (Tomkins et al. 2010, a newly added reference) that visual (sensory) and paw (motoric) laterality are independent of each other (see also the point below).

I think the talk of eye dominance is interesting, but the authors’ case would be significantly strengthened by demonstrating that such eye preferences exist. In other words, is there a simple eye dominance task that the authors could do to assess the dogs’ eye dominance? Given that so much of their discussion is based on the assumption about eye dominance it would strengthen the paper significantly to show that such eye dominance exists and tracks with their predictions.

Unfortunately, at the current stage of research, given the (wo)manpower and current lockdown-like restrictions we're not going to carry out an additional eye dominance experiment to satisfy this request. For sure, and as we state in the text, it is an inspiration and suggestion for follow-up research. We can, nevertheless, bolster the argument of eye dominance with previous studies from vertebrates, with a focus on mammals that show eye dominance/laterality plays a large role in behavioral ecology. There's lots of examples from birds (where different eyes can specialize on different tasks – either for foraging or for surveillance; the eye dominance with reference to magnetoreception in birds was reported in Refs.29-30, cited in our manuscript). Moreover, eye dominance = ocular dominance = eye preference = eyedness is a well known phenomenon to human ophthalmologists (see Wikipedia and basic literature cited there) and there is no reason to assume that dogs would be different from humans in this respect. Indeed, there is one paper published explicitly on this topic, which, unfortunately, was not cited in the first version of the ms, but, fortunately, came to our notice now to be cited in the revised version (Ref. 35 in the revised version).

Similarly, is there evidence that dogs have magnetic field receptors in their eyes?

There is no direct evidence, but it has been suggested multiple times for canines in previous published studies (Refs. 45-46) and it has been discussed as the putative magnetoreception mechanism in terrestrial vertebrates (Refs. 39-44), with subterranean mammals who evolved under completely different environmental/ecological contexts, being the exception (Ref. 37). Given the robust support for a photoreceptor based mechanism in closely related taxa, it is an interesting hypothesis to propose and is justified based on previous findings from a diverse array of vertebrates, including mammals.

The authors mention that the dogs do not have a history of coming to heel, but I wonder about other types of owner interactions. Do owner handedness or owner turning preferences track with dogs’ preferences?

Unrelated to the study and the use of different magnetic field alignments clearly shows that the pull of magnetic north mediates these behaviors. It might be interesting look at some of these other factors, however the study design was intended to address the questions outlined in the last paragraph of the introduction.

There are a few awkward sentences (lines 85-88; 132-134)

In fact the sentence on lines 85-88 is a word-by-word citation from an English book (Ref. 23).

We have shortened it and slightly reworded it now and hope that it became more straightforward.

Also the second criticized sentence was reworded.

Where is Figure 4?

As admitted above – this was an unfortunate omission and the figure 4 has been uploaded now.

Reviewer #2: In earlier outdoor experiments, dogs were found to prefer the North direction and avoid South, when choosing between two food dishes placed in front of them. In this paper, the authors repeat these experiments indoors under controlled conditions, and by shifting the north direction of the magnetic field, they demonstrate that this preference is based on the magnetic field.

In the introduction, the questions are clearly stated.

We are pleased by this assessment.

The description of the experimental procedure appears rather cryptic and suffers from the use of many abbreviations.

The reviewer might be right but the problem can be solved only on costs of losing some details or lengthening the text and making it even less understandable. Importantly, all abbreviations are either known units (nT = nanotesla), or are commonly used in the literature of this kind and in any case explained when first used (M = male, F = female, N = North, magN = magnetic North, etc.), or explained when used in a formula (R = right, L = left) or they specify marks of the used software or hardware (which information is important for those who would like to assess suitability of our equipment or replicate the experiments and equip their labs. Finally, there are, abbreviations which are of importance and interest only for statisticians who themselves are familiar with statistical Analysis system (SAS), e.g. LSM for Least squares means, GLM (generalized linear model), etc. Again, all these abbreviations are explained when first mentioned. Repeating whole descriptions in each sentence instead of using these abbreviations would not make the text more fluent, readable and understandable. Omitting these and not mentioning these models would, for sure, be criticized by statisticians.

The result part is hard to read.

We reworded and complemented the text.

I have problems to derive from Fig. 2 a “pull of the north”

The reviewer is very attentive. There was a mistake in the Figure 2a. The corresponding author uploaded mistakenly an earlier and incorrect version of the figure. Sorry for that error and thank you for finding it. The correct version is uploaded now and the figure is explained in more detail.

and also in Fig. 3, it is unclear what the numbers in each quadrant mean.

Description of the Fig. 3 is reworded as follows:

Fig 3: Numbers in each quadrant (in the respective four compass combinations (N-E, E-S, S-W, W-N) show mean values of turning preference calculated from individual dogs and pooled across all trials (both control and shifted magnetic field alignments). Data were partitioned by turning preference (left figure shows clockwise turning preference, right figure shows counterclockwise turning preference; irresolute dogs were not calculated. The green arrow over the dog's head in the…….. (the further description of the figure remains unchanged).

Fig. 4 is missing altogether.

As admitted above – we apologize for this unfortunate omission. The figure 4 has been uploaded now.

The best part of the paper is definitely the discussion. I welcome the authors’ attempt to propose a promising idea for explaining why so many animals show a magnetic alignment.

We appreciate this opinion.

Submitted filename: Response to reviewers Adamkova 2020.pdf

5 Jan 2021

PONE-D-20-31110R1

Turning preference in dogs: north attracts while south repels

PLOS ONE

Dear Dr. Burda,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

Along with the two reviewers, I believe your manuscript is very nearly ready for publication. I appreciate the detail with which you address the reviewers comments and concerns.  Reviewer #1 had some last edits that you may wish to consider.  Please consider these edits before returning the manuscript.  I would especially like you to consider a change to the Fig1 legend that would make the meaning of the measures more apparent to someone less familiar with the experimental approach.   Please also read through closely to make sure you catch any other existing typos before resubmission. 

Congratulations on a very nice paper.       

==============================

Please submit your revised manuscript by Feb 19 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Reviewer #1: Some minor things:

Lines 153-162 — paragraph should be in past tense

Line 219 tense shift

Line 244 “according to based on” (redundant)

Line 326 “more frequently" need to add "chosen”

In the figure caption for Fig 1 please give a sense of what these numbers mean. - ie - left and + right? We don't need the full explanation that comes later in the text, but a sense of what these numbers are telling us would be helpful at this point.

I still find the figures confusing, but I’m not an expert on how to present these results with turning preference so I leave it to the other reviewer and the editor's expertise.

Reviewer #2: The text is considerably improved, and it is now easier to follow the argumentation of the authors. I think that the paper can be published now.

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7 Jan 2021

Dear Prof. Roman,

we are pleased about the positive views of the reviewers and appreciate also the careful editing of the manuscript by the reviewer #1:

We accepted all but one suggestions:

Lines 153-162 — paragraph should be in past tense

Corrected

Line 219 tense shift

Corrected

Line 244 “according to based on” (redundant)

We have not changed this sentence, because "based on first trials" is here a complementary information, a fact, which should be pointed out

Line 326 “more frequently" need to add "chosen”

Corrected

In the figure caption for Fig 1 please give a sense of what these numbers mean. - ie - left and + right? We don't need the full explanation that comes later in the text, but a sense of what these numbers are telling us would be helpful at this point.

The reviewer means probably Table 1 and/or Figure 3. We complemented the caption in both cases as suggested.

I still find the figures confusing, but I’m not an expert on how to present these results with turning preference so I leave it to the other reviewer and the editor's expertise.

We assure the reviewer that this way of illustrating the results is common in the literature dealing with spatial orientation.

Once again, many thanks for considering our manuscript and ist academic processing.

With best regards and wishes for a prosperous and healthy new year

Hynek Burda

On behalf of all coauthors.

Submitted filename: Adamkova response to reviewers.pdf

11 Jan 2021

Turning preference in dogs: north attracts while south repels

PONE-D-20-31110R2

Dear Dr. Burda,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Gregg Roman, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:


20 Jan 2021

PONE-D-20-31110R2

Turning preference in dogs: north attracts while south repels

Dear Dr. Burda:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr Gregg Roman

Academic Editor

PLOS ONE

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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