**Early Recognition of Behaviour Problems in Shelter Dogs by Monitoring them in their Kennels after Admission to a Shelter**

### **Liam Clay 1,\*, Mandy Paterson 1,2, Pauleen Bennett 3, Gaille Perry <sup>4</sup> and Clive Phillips <sup>1</sup>**


Received: 28 September 2019; Accepted: 23 October 2019; Published: 28 October 2019

**Simple Summary:** Canine behaviour assessments are commonly used in shelters to identify behaviour problems in dogs prior to adoption. The aim of this study was to evaluate whether kennel monitoring of dogs could identify early signs of behaviour problems. Kennel behaviour was monitored for 38 dogs in their first five days in kennels at a shelter in Brisbane, Australia. This was compared to a formal assessment of exploratory, handling, play, run/freeze, and food guarding behaviour, as well as stranger and fake toddler interactions, and behaviour when the dog was alone, conducted five days after shelter admission. Kennel behaviours associated with fear, anxiety, and arousal in dogs were significantly correlated with the same behaviours in the formal assessment. With respect to outcomes, dogs that displayed more whining, tense body posture, standing leaning forward, panting, ears forward, less barking, lowered body and balanced/relaxed body posture, standing still, and standing by the wall had increased odds of failing the behaviour assessment. The study demonstrates that monitoring kennel behaviour could detect early signs of behaviour problems.

**Abstract:** Canine behaviour assessments are commonly used in shelters to identify behaviour problems in dogs prior to adoption. The aim of this study was to evaluate whether kennel monitoring of dogs could identify early signs of behaviour problems, thereby facilitating early intervention and better management of dogs displaying behaviour problems. Kennel behaviour was monitored for dogs (*n* = 38) in their first five days in kennels at a shelter in Brisbane, Australia. This was compared to a formal assessment of exploratory, handling, play, run/freeze, and food guarding behaviour, as well as stranger and fake toddler interactions, and behaviour when the dog was alone, conducted five days after shelter admission. Kennel behaviours associated with fear, anxiety, and arousal in dogs were significantly correlated with the same behaviours in the formal assessment. Positional correlations were also evident. With respect to outcomes, dogs that displayed more whining, tense body posture, standing leaning forward, panting, ears forward, less barking, lowered body and balanced/relaxed body posture, standing still, and standing by the wall had increased odds of failing the behaviour assessment. Over the five days in the kennel, the frequency and duration of fear-related behaviours decreased, suggesting a reduction in arousal as the dog became accustomed to the shelter environment. The study demonstrates that monitoring kennel behaviour could detect early signs of behaviour problems.

**Keywords:** behaviour; problems; assessment; canines; shelters; predict

#### **1. Introduction**

The largest Australian animal welfare organisation, the Royal Society for Prevention of Cruelty to Animals (RSPCA), received 40,286 surrendered dogs in the 12 months from July 2017 to June 2018 [1]. Reasons for dog relinquishment commonly include behaviour problems, e.g., inappropriate toileting, barking, digging, separation anxiety, fear, or aggression [2–4]. Entry to a novel shelter environment, plus alienation from its former owner, home, and routine, is likely to result in a potentially stressful form of social isolation in a surrendered dog [5]. Dogs experience fear and anxiety upon relinquishment to a shelter, with overt signs of stress sometimes persisting for several weeks after relinquishment [5,6]. Furthermore, as the length of time in a shelter increases, the detrimental impact on dogs' emotional state worsens [7–9]. Coping capacity differs considerably between individual dogs, with variable habituation to the environment and the same stressor being experienced as neutral or aversive [10–12]. Therefore, in order to reliably and effectively assess and monitor the mental well-being of surrendered dogs, it is important that early interactions with the novel environment are recorded to identify signs of negative affect, e.g., separation anxiety, which occur with high frequency in adopted dogs from shelters [13].

Behaviour assessments are used in shelters globally, assessing adoption suitability, identifying behaviour problems, and matching dogs with the most suitable adoptees [14]. Veterinarians also implement a variety of testing procedures for quality of life assessments in animals with medical and behavioural issues [15]. However, behaviour assessments in shelters have been recently criticised, due to both the nature and consequences of pass or fail assessment procedures and doubt about their ability to accurately predict behaviour problems [16]. It is claimed that they cannot accurately determine the frequency of false positive (identification of a behavioural problem that does not really exist e.g., aggression, which renders the dog unfit for adoption) or false negatives (failure to detect a behavioural problem during the test). Usually, dogs are removed from their kennel to undertake the test in a standard facility, through which many other dogs have passed. This single context assessment is likely to present a stressful situation for the dog, which is unlikely to replicate the best environment to examine their anticipated behaviour in the home in which they are adopted. For example, the presence of excreta from previous dogs, or potentially even odours from dogs previously tested, can affect the outcome of tests [17].

An alternative is to observe behaviour in their kennel (hereafter kennel behaviour), handler interactions, and interspecies behaviour, allowing them to be tested in the environment into which they are becoming settled. Kennel monitoring has been used previously in shelters to identify behaviour problems [18–20]. Furthermore, kennel behaviour monitoring could potentially be automated, using for example motion sensing or by programming computers to recognise specific behaviour patterns, e.g., escape attempts [15].

There is a need for better observational tools for assessment in shelters [21]. These could include assessing behaviour longitudinally in shelters, to account for plasticity, and the greater predictability of behaviour when measured over a period of time [20]. Therefore, the aim of this study was to compare the manifestation of behaviours in a structured assessment with behaviours observed in their kennel over the first five days in a shelter.

#### **2. Materials and Methods**

#### *2.1. Ethical Approval*

This study was granted ethical approval from the University of Queensland Animal Ethics Committee (AE04214). All dogs were owner-surrendered, and permission was obtained from the owners to enrol their animals into the study.

#### *2.2. Subjects*

Criteria for dogs to enter the study were that they were between six months and 10 years of age, had no predisposed medical conditions and had not been previously admitted to the shelter. Thirty-eight dogs (18 male, 20 female) of mean age 3.1 years (SEM 0.37 years) and weight 20.3 kg (SEM 1.43) that had been surrendered to the RSPCA Queensland's Animal Care Facility over a three month period were enrolled into the study. They represented the following 20 different breeds: Bull terrier (*n* = 9), Kelpie Cross (*n* = 6), Mastiff (*n* = 4), Beagle cross (*n* = 2), Staffordshire Bull Terrier (*n* = 2), and one each of Jack Russell cross, Alaskan Malamut, American Bulldog, Australian Cattle Dog, Australian Shepherd Cross, Border Collie, Boxer, Bull Arab cross, German Shepard cross, Husky cross, Labrador Retriever, Papillon, Poodle Cross, Portuguese Podengo, and Spoodle. All had been privately surrendered, with owners being required to declare the reasons for surrender.

#### *2.3. Housing and Feeding*

Dogs were housed in a single block of kennels, which held 16 dogs in individual kennels. Each kennel had a floor area of 3.5 m2 (120 cm <sup>×</sup> 180 cm), concrete floors and two solid walls separating each kennel and a gate opening into the kennel block, a fence opening out toward a garden area, a separate sleeping area with a raised bed, soft bedding, and toys. The dogs were fed twice daily with a combination of dry and wet food and had access to fresh water. Each dog received walks twice a day at 09:00 and 15:00 by shelter staff or volunteers.

#### *2.4. Behaviour Monitoring*

#### 2.4.1. Kennel

Dogs were observed on days 1–5, following surrender on day 1, for 60 min (07:30–08:30, before interactions with volunteers). Data were collected using two video surveillance cameras (KOBI CCD video cameras, Model: K-32HCVF, Taipei, Taiwan) placed in each individual kennel at a height of 3 m.

#### 2.4.2. Standard Behaviour Test

The standard RSPCA Qld behaviour assessment (RSPCA, 2018) was conducted on day 6, i.e., the day after the five days of kennel observations, as used by Queensland RSPCA shelters in each state to assess adoption suitability in shelter dogs. The assessment comprised a series of 10 tests of increasing provocation. Dog responses were scored based on frequency and durations of a variety of behaviours as described below. The tests were performed over 15 min with the following aids: a 1.8 m leash, tennis ball, plush squeaky toy, rope, plastic hand on a extend pole, bowl, raw hide or bone, and combination of wet and dry dog food.

The assessments were performed in a room (3 × 5 m) 20–30 m from the kennels, with one window and two half frosted doors, and a concrete floor with hospital-grade non-slip painted covering. All dogs were moved on lead from their kennel block to the assessment room. A single lead was attached to the wall for a 1.8 m leash to restrain the dog. During the assessment, one researcher acted as the handler, and a second person helped in observer interaction and implementing two tests requiring two people (Stranger and Fake toddler tests, described below). Data for all the following tests were recorded using a video recorder (Digital Video Recorder 1.1, Model: XQ-L400H, Manufacture: Kobi, Seoul, Korea).

#### Exploring the Room, One Minute

The handler entered the room, dropped the lead attached to the dog, and sat in the centre on a chair. Then, the observer started a timer and waited for 1 min without any interaction with the dog by either person.

#### Sociability to Handler

At the end of test 1, the handler called the dog to them in a friendly voice, remaining in the chair with no other body movement. If there was no response, a second attempt was made, and if still no response the handler clapped their hands on their lap and said 'come here' in the direction of the dog, trying at least three times to call the dog to them. When the dog came (at the first, second, or third call), the handler picked up the leash and then stroked the dog from the base of neck to tail three times. If the dog did not respond to the first, second, or third, call the handler approached the dog, picked up the leash, and gave the dog three strokes from the base of neck to tail. Following each stroke, the observer and handler counted 10 s, with behaviours exhibited noted.

#### Tolerance to Handling

The handler dropped the leash and held the dog's collar. With the dog standing, the other handler (in the standing position, or crouching if a small breed of dog) picked up the dog's rear inside foot, then the front inside foot, then reached over its back to pick up its rear outside foot, and finally the front outside foot. Each foot was held for 2 s. After picking up all four paws in this manner, the handler stood for 10 s with no dog interaction and finally removed the dog's leash.

#### Toy Interactions

A tennis ball, squeaky toy, and tugging rope were shown to the dog and gently thrown across the room, and the handler verbally engaged the dog in play. If the dog picked up the ball, the handler waited to see if it returned to the handler without encouragement. If it did not, the handler encouraged the dog to bring the ball back by calling his/her name and saying "come". If the dog still did not return, the handler went to the dog.

In both situations, the handler waited 10 s to see if the dog dropped the ball. If it did not, he/she asked the dog to "drop it". If the dog did not respond, then a second command was given, "give", and if necessary, a third attempt, "out", was tried. If the dog did not respond to these commands, the handler approached the dog carefully and removed the ball from the dog's mouth. These steps were repeated for a second throw, and after completion, the handler waited 10 s with no interaction before moving on to the next test.

#### Tag (Run and Freeze)

The run and freeze test was used to mimic a tag game. The handler gently moved the dog to the opposite end of the room and left it standing against the wall. Then, he gently moved one hand over its head, down toward the back to gently tap the rump area, and then ran across the room, laughing and waving arms, followed by suddenly stopping, folding his arms, and ignoring the dog. The tap, run, and freeze series was repeated a second time. The handler waited for 10 s after the run and freeze, ignoring the dog, before moving onto the next test. The dog was then placed back on the leash.

#### Resource Guarding

The handler tethered the dog to the wall for safety reasons, and proceeded to give the dog wet canned food, smeared in a bowl. The bowl was then placed near the dog at the end of the leash perimeter, allowing the dog to begin eating for 2 s. The handler then proceeded with a plastic hand, walking to the side of the dog while it was eating. Using the fake hand, the handler patted the dog on the head, continuing to stroke down its back and body twice. The fake hand was then placed 5 cm in front of the bowl and moved around in a semi-circle. The hand was then placed on the inside edge of the bowl and moved around the edge of the bowl next to the dog's face, without touching it. Finally, the bowl was pulled away from the dog using the fake hand. The bowl was then returned to the dog, which was observed for 10 s.

#### *Animals* **2019**, *9*, 875

The handler then gave the dog a pig's ear or bone, depending on dog's food interest, and it was allowed to chew it for 30 s. The steps above with wet food were repeated; then, the handler attempted to retrieve the food, asking the dog to "drop it", "leave it", or "give" before attempting to retrieve it by offering a higher value treat/food, e.g., the pig's ear.

#### Stranger Interaction

The handler placed the dog on a leash as the observer exited the room and returned dressed in a reflective vest, large brimmed hat and using a walking stick. The observer entered the room, and bent down to extend an open flat hand as if to pat the dog on the head. The observer then talked to the dog normally and stopped for 3 s, allowing the dog to approach. If the dog approached, the observer patted the dog on the top of its head for 3 s. If the dog did not approach, it was observed for 10 s, with an emphasis on any interaction between the handler and/or the observer.

#### Fake Toddler Interaction

The handler stood and held the dog's leash while the observer exited the area and returned carrying a toddler doll simulating a small child. Once the toddler was within the leash perimeter from the dog, the observer placed the doll on the floor facing the dog, with the doll's arm extended toward the dog. The handler allowed the dog to approach if it desired. If the dog did not approach the observer, it was observed for 20 s.

#### Time Alone

The handler and observer removed the leash from the dog and left the room for 2 min, with a video camera in the front of the room monitoring behaviour and vocalisations. Then, the handler and observer re-entered through the same door.

#### Behaviour with Another Dog

This test was conducted in a yard (10−20 m), allowing adequate space between the test dog and another dog, both with handlers. Each dog had a handler, who interacted with their dog by giving treats and ignoring the other handler and dog. The handler had a short, 1 m, leash, so that the dog walked close to the handler. At the start, both handlers walked parallel to each other, 5 m apart, with the dogs on the outside. If one or both dogs were reactive and pulled toward each other, the distance between the handlers was increased. If both dogs were relaxed and focused on their handler, the handlers moved the dogs to an exercise circle. If the dogs did not breach a minimum distance of 5 m between them, they were introduced on opposite sides of a fence. There followed a circling activity, which required one handler to stand still with their dog on no more than 1.5 m of leash while the other handler and their dog completed a circle around the handler. Handlers then swapped places and repeated the circling activity. If no adverse behaviours were displayed, the handler in the middle of the circle remained at that location, ensuring that the only tension on the leash was from the dog. The other handler identified the leash threshold of the dog in the centre and moved close enough to allow the dogs to be nose to nose, also ensuring that the only tension on their leads was caused by the dog pulling, not them pulling against the dog. Once the leads became loose, and the dogs stopped pulling against the handler, the handlers took a step closer to each other, allowing the dogs to interact if they chose. Leashes remained loose. If there were signs of adverse reactions or aggression, dogs were then separated by increasing the threshold.

#### *2.5. Behaviour Scoring*

Following preliminary observation of dogs in their kennel and during the formal behaviour assessment, an ethogram with 48 behaviours, classified as either long duration behaviours (for which the duration was recorded) or events (for which the number of occurrences was recorded) was devised. The behaviours focused on eight components: activities of the mouth, body, tail, tail movement, ears, eyes, position, and movement (Table 1). Descriptions of each behaviour are presented in Table 2 and their connection to emotions (Anxiety, Fear, Friendliness, Arousal, Aggression) [22–26] in Table 3. Kennel behaviours were continuously recorded over a 1 h period (07:00–08:00), and the formal behaviour assessments were recorded for all tests. Behaviour recording was assisted by coding software (BORIS) [27]. The following behaviour variables with no or only one occurrence were discarded: Squint, Whale eyes.


**Table 1.** Canine behaviours recorded for each body part, as well as positions and movement types.

**Table 2.** Behaviours measured, their descriptions and mean values (± SEM) for duration and frequency during kennel observations.



**Table 2.** *Cont.*

The RSPCA staff classified the dogs for adoption suitability following the formal behaviour assessment: (1) pass and ready for adoption, (2) some behaviour issues which should be addressed in a behaviour modification program, and (3) fail due to extreme behaviour problems. However, in the current study no dogs were classified under category 2.



#### *2.6. Statistical Analysis*

Results were analysed using Minitab 17, Lead technology Inc., Pennsylvania State University, Pennsylvanina, USA. Behaviours were entered as the percentage of the total observation time or percentage of the frequency of occurrence during their period in the kennel and during the behaviour assessment. These two were compared using multivariate general linear models with the following factors: reason for surrender, age, weight, animals, days since entry, and outcome (adopted/euthanized). Residuals were checked for normal distribution using the Anderson Darling test. Spearman's rank order correlations were computed between kennel and formal behaviour assessment variables. As comparisons with 38 other behaviours were made for each behaviour in each test of the behaviour assessment, results were corrected for false discovery using the Benjamini-Hochberg procedure [28]. The Bonferroni correction was rejected as it assumes independence in the individual tests. The Benjamini-Hochberg procedure ranks the P values for each test and compares P values to critical values [(rank/no. tests) x false discovery rate (selected as 0.20 as recommended by McDonald, 2014)]. All P values up to the critical one were considered to indicate a significant difference [28]. Correlations were further analysed on tests of the sample split according to owner surrender information, sex, adopted vs euthanasia, and daily behaviours. Linear and Binary Logistics Regressions were conducted to compare dog behaviour with RSPCA classification of outcomes and comparing behaviours over days for different tests. Two tests, Time Alone and Exploration of the Room, were subjected to additional logistic regression because of their predictive ability for kennel behaviour.

#### **3. Results**

#### *3.1. Reasons for Dog Surrender*

The reasons for surrender were moving away or insufficient time to care for the dog (22.2%); dog being aggressive or escaping, or family issues (8.3%); medical concerns (5.5%); and arousal, barking, chasing, destruction, owner's death, resource guarding, or separation anxiety (2.8%).

#### *3.2. Emotional Characteristics of Dogs in Their Kennels That Were or Were Not Subsequently Euthanased*

#### 3.2.1. Emotional States of Dogs in Their Kennel

Over the first five days, dogs spent most time and had the highest frequencies of the following behaviours (Table 2): weight back, balanced body, and jumping up. Tail movement and position were spent in tail low and medium with still or slow movement, not wagging (Table 2). Ear position was most commonly ears back, then ears open, and finally ears forward. Eye direction was most commonly direct and diverting. In regards to position, dogs spent the most of the time in a kennel at the wire or front and the least amount of time in bed/sleeping or at the wall. Movement patterns were commonly standing, sit/lay, and pacing (Table 2). Over the five-day period, dogs spent 36% of their time in friendly behaviours, 25% displaying fear, 13% displaying anxiousness, 15% in high arousal, and 7% displaying aggression. Dogs' frequency of emotions differed from duration, with 33% of occurrences being high arousal, 25% friendliness, 24% anxiousness, 16% fear, and 2% aggression. Thus, friendliness and fear were displayed less frequently but for a longer duration compared with arousal and anxiousness, which were of short duration but more frequent.

Over the five-day period, there was a significant reduction in the frequency of fear-related behaviours, including tense body posture (*p* < 0.05), tail tucked (*p* < 0.05), and alert response in ears (*p* < 0.05) (Figure 1). There was increases in stiff and slow tail movement (*p* < 0.05) (Figure 1) and the duration of time spent at the front of the kennel (*p* = 0.016), wire of the kennel (*p* = 0.008), and in bed/sleep (*p* = 0.0019) (Figures 1 and 2).

**Figure 1.** The frequency of fear-related behaviours, alert ears, and tail behaviours over the first five days that dogs (*n* = 38) spent in a shelter.

**Figure 2.** The frequency of position over the first five days that dogs (*n* = 38) spent in a shelter.

There were reductions in time spent panting (*p* < 0.001) (and corresponding increase in mouth open or closed, *p* < 0.001), a reduction in lowered (*p* < 0.008) and tense body posture (*p* < 0.001), and reductions in tucked tail and stiff tail movement, and a corresponding increase in slow tail movement (*p* < 0.05) (Figure 3).

**Figure 3.** The duration of fear-related behaviours, arousal behaviours, and tail behaviours over the first five days that dogs (*n* = 38) spent in a shelter.

#### 3.2.2. Relationship between Kennel Behaviour and Outcome for the Dogs

Comparing behavioural characteristics of dogs that were adopted or euthanized, the latter had an increased duration of tense body posture overall, but inspection of changes over time revealed that this was mainly on the first day, with this behaviour declining over time in both sets of dogs (*p* = 0.001) (Table 4, Figure 4). Conversely, dogs that were adopted, which generally exhibited more mouth open/closed behaviour, had similar levels to euthanased dogs by day 5. Dogs that were adopted had a greater frequency of balanced/relaxed posture, but this declined over time, in contrast to euthanased dogs, which had little evidence of decline over time (*p* = 0.004). Jumping kennel was more common in euthanased dogs, and this declined over time in both euthanased and adopted dogs (*p* = 0.03) (Figure 5).

**Figure 4.** The duration of behaviours over the first five days that adopted or euthanased dogs (*n* = 38) spent in a shelter.

**Figure 5.** The frequency of behaviours over the first five days that adopted or euthanased dogs (*n* = 38) spent in a shelter.



D = Duration, F = Frequency.

*3.3. Emotional Characteristics of Dogs in the Behavioral Assessment That Were or Were Not Subsequently Euthanased*

#### Behaviour of Dogs in Formal Behaviour Assessment

In the behaviour assessment, dogs spent 39% of their time in friendly behaviours, 17% displaying fear, 17% displaying anxiousness, 24% in high arousal, and 3% displaying aggression. Considering the frequency of behaviours, 26% were incidences of high arousal, 41% friendliness, 19% anxiousness, 12% fear, and 2% aggression.

Total scores for each behaviour were obtained from the formal behavioural assessment and categorised into emotional domains (Anxiety, Fear, Friendliness, Aggression, and Arousal). See Table 5 for Pearson's correlations of scores, with significance levels corrected using the Benjamini-Hochberg procedure.


#### *Animals* **2019** , *9*, 875


#### *Animals* **2019** , *9*, 875

**Table 5.** *Cont.*



Almost all correlations were statistically significant but ranged from weak to strong for both positive and negative correlations. There were positive correlations between the following behaviours that we associated with Fear: ears back, lip licking, lowered body, lowered head, shiver, tail low, tail tucked, tense body posture, weight back, and yawning; Anxiousness: fast, high tail, jumping, licking, lip licking, medium tail, pacing, panting, stiff tail, tense body posture, weight back, weight forward, and yawning. There were positive correlations between the following behaviours that we associated with Aggression: biting, ears forward, growling, high tail, lip licking, lowered head, medium tail, snapping, standing, stiff tail and still tail, and targeting gaze. There were positive correlations between the following behaviours that we associated with Arousal: barking, diverting gaze, fast and high tail, jumping up and off, licking, medium tail, mouthing, pacing, panting, weight forward, and whining. There were positive correlations between the following behaviours that we associated with Friendliness: balanced body posture, body curve, direct eye contact, ears forward and open, fast tail, handler interaction, jumping, medium tail, play behaviour, relaxed body, slow tail movement, sniffing, soft eye contact, wag loose, and walking.

#### *3.4. Relationship between Kennel Behaviour and Formal Behaviour Assessment*

There were positive correlations between anxiety, fear, and arousal behaviours displayed in kennels and in the formal behaviour assessment: whining, diverting eye contact, lip licking, panting, barking, jumping up, ears alert and forward, ears back, lowered body and tense body posture, tail tucked and stiff, and body weight back (*p* < 0.02) (Table 6). In addition, there were positive correlations between position in the kennel (at wall, wire, and at front door) and locations in behaviour assessment (at wall, window, and door) (*p* < 0.02) (Table 7).


**Table 6.** Significant (*p* < 0.05) Spearman Rank correlation coefficients between behaviours recorded in kennel and the formal behaviour assessment of shelter dogs (*n* = 38), listed for the emotional states of Arousal, Fear and Anxiety.

*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; 0.05.

**Table 7.** Significant (*p* < 0.05) Spearman Rank correlation coefficients between locations recorded in kennel and formal behaviour assessment of shelter dogs (*n* = 38).


*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; 0.05

#### 3.4.1. Exploration of Room

Comparing exploration of the room in the behaviour assessment with kennel behaviours, there were significant correlations between many duration and frequency behaviours in the anxiety, arousal, and fear emotional states (Table 8). Nearly all correlations were positive, demonstrating that for most behaviours recorded in the kennel were related to those exhibited in the behavioural assessment. Only two—whining and lip licking—were negatively related, suggesting that these are not reliable indicators of the room exploration test.

**Table 8.** Spearman Rank correlation coefficients between behaviours recorded in kennel and behaviours exhibited during the 'exploration of room test' in the behaviour assessment of shelter dogs (*n* = 38) within the emotional domains of arousal, fear, and anxiety.


*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; *0.05.*

#### 3.4.2. Time Alone Assessment

Similarly, comparing the time alone assessment with kennel behaviours, there were also significant correlations between many duration and frequency behaviours in the anxiety, arousal and fear emotional states (Table 9). Nearly all correlations were positive, demonstrating that most behaviours recorded in the kennel were related to those exhibited in the time alone assessment. Only three—whining, fast tail, and direct eyes—were negatively related, suggesting that these are not reliable indicators of the time alone test. There were also positive correlations between locations (Table 10).

**Table 9.** Significant (*p* < 0.05) Spearman Rank correlation coefficients between behaviours recorded in kennel and behaviours exhibited during the time alone test in the behaviour assessment of shelter dogs (*n* = 38) within the emotional domains of arousal, fear, anxiety, and friendliness.


*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; *0.05.*


**Table 10.** Significant (*p* < 0.05) Spearman Rank correlation coefficients between locations recorded in kennel and the time alone test of shelter dogs (*n* = 38).

3.4.3. Relationship between Outcomes for the Dogs and Summarised Behaviour Results

Comparing the time spent in the various behaviours for dogs that were adopted with those that were euthanased, dogs that displayed more barking, balanced or lowered posture, or positioned by the wall in the kennel assessment, or balanced/lowered posture or pacing in the behaviour assessment, or balanced posture or jumping up in the time alone test had an increased likelihood of being adopted (Table 11). Those that displayed more tense body posture in the kennel test or sitting/lying in the behavioural assessment were more likely to be euthanased.

**Table 11.** Time spent in behaviours in the kennel, the formal assessment and time alone test of dogs (*n* = 38) that were adopted or euthanased, with Odds Ratio and Confidence Interval (CI) tested by binary logistic regression.


*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; *0.05*. K: Kennel B: Behaviour assessment T: Time alone.

Comparing the frequency of the various behaviours for dogs that were adopted with those that were euthanased, dogs that displayed more barking in the kennel assessment or balanced posture in the kennel or behaviour assessment or the time alone test had an increased likelihood of being adopted (Table 12). Those that displayed more panting in the kennel assessment, lowered head, or scanning in the behaviour assessment were more likely to be euthanased.


**Table 12.** Frequency of behaviours in the kennel, behaviours in the formal assessment and time alone test of dogs (*n* = 38) that were adopted or euthanased, together with the significance of the difference tested by binary logistic regression.

*p* <sup>&</sup>lt; **0.01**, *<sup>p</sup>* <sup>&</sup>lt; *0.05*; K: Kennel B: Behaviour assessment T: Time alone.

#### **4. Discussion**

One solution to increasing adoptability of shelter dogs is the early detection of behaviour problems followed by modification programs aimed at helping dogs develop desired behaviours. Longitudinal monitoring of behaviours using both kennel and formal behaviour assessment information to help create comprehensive insight of the dog's behaviour can help achieve this aim [20]. Recent studies have pointed to the uncertainty of single behaviour assessments [16], but the work of Goold and Newberry and this current research clearly demonstrate the benefit of continual monitoring. Continual monitoring allows correct identification of behavioural cues associated with separation-related behaviours, anxiety, fear, arousal, and friendliness. To identify these behavioural cues using monitoring tools in the first five days allows behaviour modification to be implemented to help these dogs to cope effectively in a socially isolating environment. Using a formal behaviour assessment, as customarily practiced in shelters, as a single context assessment of a dog's behaviour creates an ineffective profile of stable behavioural tendencies.

#### *4.1. Behaviour in the Five Days after Surrender*

This study focused on behaviour observations in the first five days after admission to a shelter and compared these to behaviour identified in a formal behaviour assessment. Over the first five days after admission, dogs displayed decreasing tense body and tucked tail, which are probably the best indicators of fear in the dogs. Previous studies that found that over the first five days after relinquishment to a shelter dogs will experience social isolation due to the breaking of social bonds with previous companions/owners [5,6]. Prior studies report numerous contradictory indications of the extent to which shelter dogs adapt over time, displaying behavioural and physiological indicators of positive and negative stress [29]. Some studies report a reduction in stress and fear related behaviours over time in shelters [6,10,30], whereas others indicate that dogs display acute signs of negative stress and fear due to the high novelty of the shelter environment [29,31]. Although environmental factors influence these behaviours, including new olfactory, auditory, and sensory stimulation, dogs can either have a positive or negative coping style, thereby demonstrating effective or ineffective ability to cope in a new environment [21,29,32]. These diverse results are likely to be due to differences in resources offered by shelters.

The ability to monitor kennel behaviours associated with positive and negative stress or coping styles can help identify changes in the quality of life (QoL) of dogs in shelters [15,33]. Identifying dogs that have a deterioration in positive behaviours allows early treatment. Interestingly, dogs that were deemed not suitable for adoption had higher durations of tense body posture in-kennel and increased frequency of jumping behaviour in kennel. Conversely, positive behaviours, including a balanced/relaxed body posture, had lower frequency of occurrence in dogs suitable for adoption.

Another interesting finding in the present study is the association between positive behaviours that include friendliness in dogs in the first five days, which agrees with previous studies [6,10,20,30]. These findings highlight the benefit of longitudinal monitoring of behaviour in shelter kennels to identify stable behaviours that included docility and friendliness [20].

#### *4.2. Behaviours in Assessment*

Anxiousness, arousal, and fear tendencies correlated with its corresponding emotional domain in the behaviour assessment (Table 5), indicating a positive relationship with the domains identified in kennel and behaviour in the standardized assessment. Previous research by Mornement [26] in behaviour assessments in Australian shelters indicated fear and friendliness were the only behaviours that were predictive. Other research using similar test protocols with social (stranger and toddler interactions) and non-social stimuli reported fear related behaviours as found in this research [34,35]. As stated previously, the effect of acute stress and social isolation in dogs when relinquished to a novel environment have the ability to dramatically change behaviour. Thus, the result of increased fear, arousal, and anxious behaviour found in the kennel and at assessment (Table 4) suggest time-independent coping mechanisms that a dog may implement to help respond to the changing environment [21,36,37]. The results go beyond the previous study, suggesting that if coping mechanisms are ineffective at helping the dog cope with the environment, then those behavioural tendencies can manifest into behaviour problems that can be identified in an assessment.

#### *4.3. Comparison between Kennel and Behaviour Assessment*

The comparison of kennel behaviour and the formal behaviour assessment indicates that kennel behavioural cues associated with fear, anxiety, and arousal were confirmed in the formal behaviour assessment (Table 6). Furthermore, in the analysis of the position in kennel, we confirmed that position in the behaviour assessment was associated with front of kennel, door, and wall in each situation (Table 7).

Once the formal assessment was separated into component parts, specifically exploration of room and time alone, there were associations between behaviours found in these tests and kennel behaviours reflecting separation-related behavioural cues, anxiousness, arousal, and fear (Tables 8 and 9). Separation related behaviours are associated with increased whining, pacing, excessive salivation, barking, jumping in orientation of owner's departure, and escaping behaviour [38]. Studies show that separation-related behaviours can be correctly identified in video analysis of dogs in their time alone once the owner has left [18]. Furthermore, a study by Blackwell et al. [39] into the identification of separation-related behaviours in shelters showed the importance of using a time-alone test to assess dogs with behaviour problems. The results clearly demonstrate the positive predictive value of the time alone test to identify separation related behaviours [39]. Separation-related behaviours have been identified as a common problem post adoption [13]. Therefore, to identify these issues early is the key to early treatment, which could lead to an increase in the likelihood of successful adoption and therefore decreasing euthanasia. The findings with respect to fear are consistent with that of Mornement [26], who identified its predictive validity. Research by Tiira et al. [40] outlined high comorbidity between different anxieties, showing that fearful dogs had significantly higher noise sensitivity and separation anxiety.

Dogs with behaviours associated with separation-related problems, such as arousal and fear, were less likely to be deemed adoptable (Tables 11 and 12). Dogs that displayed friendly, low arousal, and docile behaviours were more likely to be adopted (Tables 11 and 12). Behavioural issues that have been linked to reasons for relinquishment of dogs include separation-related behaviours, arousal, and fear [41–46]. In contrast, behaviours that adoptees look for in dogs are associated with friendliness toward people, docility, and low arousal [47]. Thus, increasing positive behaviours and decreasing separation-related behaviours, fear, and high arousal are critical to increase adoptability, thereby decreasing euthanasia. Early recognition of ineffective behaviours and coping mechanisms allows

shelters to implement behaviour management programs before behavioural problems manifest [48,49]. Behaviour assessments are comprised of numerous tests that allow for a snapshot of a dog's behaviour that is multifactorial. Therefore, a paradigm shift should occur in shelters to implement assessments as continuous tools to monitor a dogs' behaviour over time. Once unsuitable or problem behaviours are identified, shelters can create effective modification plans to allow issues to be solved before manifesting into serious behavioural problems. Using assessments in shelters to identify past behaviours in the previous home or to predict future behaviour is difficult. However, using assessments as a tool to understand the behaviour of dogs in conjunction with continual kennel monitoring and everyday interaction may allow identification of behavioural issues and ineffective coping mechanisms. Further research into monitoring of behaviours associated with the manifestation of behavioural problems in shelters is warranted.

Some limitations are associated with this research that future studies should consider. To allow for comprehensive behaviour analysis of dogs, previous home environment could be taken into consideration. Therefore, we should try to more accurately represent behaviour in the home. Our sample size was relatively small, but due to the nature of the study, which identified changes in behaviours over time on single dogs, it is not seen as a major restriction. Finally, the limitation of variability between each shelter should be taken into consideration and warrants further study.

#### **5. Conclusions**

Previous research suggests that behaviour assessments are ineffective, focusing on the lack of their accurate predictability of behaviour. However, in this study, we found that behaviour assessment information can be related to behaviour over the previous days since relinquishment to the novel environment. Effectively monitoring kennel behaviour allows early recognition of problems. Numerous authors have recommended continual monitoring procedures to help identify key behavioural problems as early as possible. This research has demonstrated numerous correlations between kennel behaviour and that displayed during formal assessments. We suggest that shelters should use continuous monitoring techniques at the same time as supporting automated behaviour problem recognition. Continuing to use formal assessments and incorporating longitudinal monitoring of behaviour to help identify dogs unable to cope effectively in shelter environments may also provide useful additional information of dog behaviour problems. Such monitoring allows early implementation of training modification, thereby increasing adoptability of dogs that once would be deemed unadoptable.

**Author Contributions:** L.C., M.P., P.B., G.P., and C.P. conceived the project. L.C. drafted the paper and all authors had input into modifying it into the present format.

**Funding:** This research received no external funding.

**Acknowledgments:** The authors acknowledge the assistance of RSPCA Queensland.

**Conflicts of Interest:** Mandy Paterson declares that she works for the RSCPA Qld. Liam Clay declares that RSPCA Qld funds his studentship. Apart from this, no other author has any conflict.

#### **References**


© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

### *Article* **Forgotten, But Not Lost—Alloparental Behavior and Pup–Adult Interactions in Companion Dogs**

#### **Péter Pongrácz \* and Sára S. Sztruhala**

Department of Ethology, Eötvös Loránd University, Pázmány Péter sétány 1/c, 1117 Budapest, Hungary; sztruhalasara@hotmail.com

**\*** Correspondence: peter.pongracz@ttk.elte.hu

Received: 30 October 2019; Accepted: 14 November 2019; Published: 21 November 2019

**Simple Summary:** Companion dogs are vastly popular animals; however, we know surprisingly little about their natural parental behaviors. Meanwhile, although wolves, dingoes, and, to an extent, even free-ranging dogs show several forms of alloparental behaviors, the parental care among companion dogs is thought to be solely provided by the mother. We circulated an international survey for dog breeders, asking them about the forms of alloparental behaviors they observed among their dogs, as well as further interactions between the puppies and other adult dogs at home. Our results show that allonursing and feeding of the pups by regurgitation is a widespread phenomenon among companion dogs. The behavior of young puppies regarding, for example, their reaction to other dogs' barking was also influenced by the timing of their access to the other dogs at the breeder's home. Based on the breeders' observations, sexual status and age of the other dogs affected the way they interacted with the puppies, and also the way the puppies' mother interacted with them. These results highlight the importance of dog–puppy interactions during the early weeks of life, an often neglected area compared to the well-known elements of puppy socialization with human beings.

**Abstract:** Socialization with humans is known to be a pivotal factor in the development of appropriate adult dog behavior, but the role and extent of dog–dog interactions in the first two months of life is rarely studied. Although various forms of alloparental behaviors are described in the case of wild-living canids, the social network of companion dogs around home-raised puppies is almost unknown. An international online survey of companion dog breeders was conducted, asking about the interactions of other dogs in the household with the puppies and the pups' mother. Based on the observations of these breeders, our study showed an intricate network of interactions among adult dogs and puppies below the age of weaning. Alloparental behaviors (including suckling and feeding by regurgitation) were reportedly common. Independent of their sex, other household dogs mostly behaved in an amicable way with the puppies, and in the case of unseparated housing, the puppies reacted with lower fear to the barks of the others. Parousness, sexual status, and age of the adult dogs had an association with how interested the dogs were in interacting with the puppies, and also with how the mother reacted to the other dogs. Our study highlights the possible importance of dog–dog interactions during the early life of puppies in forming stable and low-stress interactions with other dogs later in life.

**Keywords:** behavior; dog; alloparental care; puppies; breeders

#### **1. Introduction**

The species-specific traits of dogs (*Canis familiaris*) are mostly inseparable from the process of domestication. The evolutionary changes in the socio-cognitive capacities [1,2], behavior [3,4], anatomy and physical appearance [5,6], as well as the physiology [7,8], are most often evaluated with regard to the differences between dogs and their closer or more distant wild-living relatives. More recently, researchers concentrated on the behavioral and cognitive features [9,10], both as proximate and ultimate factors behind the adaptation of dogs to the anthropogenic niche, with only a few exceptions—for example, genetic changes that could affect the carbohydrate metabolism in dogs were also highlighted as assumed key factors behind domestication [11,12]. Although differences in the reproductive biology of dogs (e.g., switching from being monestrous to a mainly diestrous cycle), when compared to their closest wild relative, the grey wolf (*Canis lupus*), are also apparent among the crucial changes, and have also been modeled by the well-known silver fox project conducted in Novosibirsk, Russia [13], the reproductive behavior of companion (or "family") dogs is rarely discussed in scientific literature, apart from various issues covered by veterinary science (e.g., [14,15]). As the reproduction of companion (and working) dogs is mainly planned, supervised, and restricted by human caretakers [16,17], this segment of dog behavior remains almost untouched by ethologists. Furthermore, alloparental behavior and paternal caretaking of the young, two factors which are considered uniquely typical for a wide selection of canid species [18], are literally unknown among companion dogs, and have only recently been discovered in the free-ranging dog populations [19,20].

Free-ranging dogs are often considered to be the "ecologically most successful" variants of domestic dogs due to their vast number (according to some estimations, around 800 million worldwide—[21]) and ubiquitous presence in and around human settlements. Subsequently, it is assumed that free-ranging dogs provide the best opportunity to understand the biology of dogs [21], as free-ranging dogs have been adapting to their environment for many generations without excessive artificial selection by humans. However, when it comes to parental behavior, seemingly, there is a considerable difference, even among free-ranging dogs. This has led to such widely differing observations, which have either stated that lack of alloparental care is one of the reasons why mortality rate of young pups is very high among free-ranging dogs (in Italy—[22]; in Mexico—[23]), or described more or less sporadic, but existing paternal/alloparental caretaking (in India—[20,24]). In their exhaustive review on canid reproduction, Lord and colleagues [25] assumed that since domestic dogs became dependent on human resources, they mostly lost the need for alloparental caretaking (i.e., because they have a stable food supply); meanwhile, the same ecologically predictable food resources made it possible that the sexual behavior of dogs also mostly lost the strict seasonality that is typical to wild canids. This feeding ecology-based theory gains further (indirect) support from the observations made with dingoes—feral dogs in Australia that became isolated from other Southeastern Asian dog populations around 3.5–5 thousand years ago [26]. These dogs sustain themselves mainly by hunting large prey—consequently, they have retained many typical features of the reproductive behavior of wolves (e.g., alloparental care—[27], monestrus—[18]), because these seem to support the lifestyle of apex canid predators.

Very little is known about the natural interactions of juvenile (pre- and around weaning period) dogs and their older canine companions (kin and non-kin) in the case of companion (pet) and working dogs. Contrary to dog–human interactions during puppyhood, which were recently investigated from multiple aspects and considered to be a crucial part of the "process of proper socialization" [3,28–30], the behavior and effect of adult dogs on puppies in the home environment have received much less interest from investigators. Among the most likely reasons for this is the difficulty of conducting observations at the owners' home, or the highly variable social environment (i.e., there is no standardized or "natural" social structure at breeders' homes that would include roughly the same kinds of adult dogs around the puppies). Consequently, although there are data about the interactions of dog puppies with other dogs at public areas [31], as well as pup–pup interactions within the litter (e.g., the ontogeny of playful behavior [32]), our knowledge of pups' interactions with familiar, but not necessarily related adult dogs from the household is very limited. The exception is the interaction with the mother—as the extent and style of maternal care was found to have fundamental effects on later behavior in working dogs (e.g., drug seeking dogs—[33]; police dogs—[34]). However, except for the work of [35] regarding the feeding of the pups by regurgitation, we do not know of any studies on alloparental behavior within pet dog groups, and indications of paternal care are missing as well.

In this study, we conducted a detailed, international internet questionnaire about alloparental behavior and pup–adult dog interactions within companion dog groups that live at the homes of dog breeders. We surveyed not only the existence of alloparental nursing and feeding of pups by regurgitation, but we also covered such behaviors as the mother dog's reaction to other adult dogs around her offspring, and the pups' reaction to other household dogs' barking. We analyzed whether the aforementioned behavioral variables were dependent on the circumstances of how the pups were kept—especially with regard to their isolation from the other dogs in the home. Based on the literature about the reproductive biology of free-ranging dogs [36] and dingoes (e.g., [18]) (both of which are not under direct human control), it can be assumed that alloparental behavior emerges in dogs as a functional response of the temporal predictability and ease of access to food [25]. As companion and working dogs in private or professional kennels are steadily provided with easily accessible food, one could assume that the need for alloparental and paternal care is minimal to non-existent. However, as an alternative hypothesis, one could expect that even companion dog populations have retained the capacity of providing alloparental care, as we do not know about active selection that would go against this capacity in dogs under human management.

#### **2. Materials and Methods**

#### *2.1. Ethical Approval*

This study was carried out in accordance with national and international ethical guidelines (e.g., American Psychological Association, Hungarian Psychological Association). Participation was voluntary; we handled all data obtained confidentially, and anonymized the questionnaires after data collection. The Ethical Committee of Eötvös Loránd University reviewed and approved the study. Ethical permission number: PEI/2016/003.

#### *2.2. Development of the Survey*

Two questionnaires were created in Hungarian and English languages, and both versions were disseminated via social media and email. Questionnaire 1 (https://goo.gl/forms/u7Q4ti2jglUHfKy63) was the main endeavor with a complex set of items, while Questionnaire 2 (https://forms. gle/ceRXWfrw4tEmtAUZ6) served to collect additional information regarding adult dogs' food regurgitation to puppies. It took approximately 10–15 min to complete Questionnaire 1, and 5 min to complete Questionnaire 2. Data from Questionnaire 1 were recorded between October 2017 and April 2018. Questionnaire 2 (focusing on solely the regurgitating behavior) was circulated between 8–19 of October 2018.

Nonprobability convenience sampling was used, as the questionnaires were distributed via social media, predominantly by sharing them in various Facebook groups, dedicated to the breeding of specific dog breeds, or breeding of purebred dogs in general. We repeated the call for participation weekly on the social media platforms along the course of the survey. Additionally, the surveys were also sent via email to dog breeders on the basis of personal acquaintances of the authors—however, this resulted in only about 10% of the total sample.

#### *2.3. Subjects*

Participation in the survey was voluntary and anonymous; however, participants could provide their name and/or contact address on a non-mandatory basis. No form of incentive was offered for the participation.

Our first sample consisted of 77 dog breeders from 11 countries, who reported their observations of 45 dog breeds. Our second sample from Questionnaire 2 consisted of the observations of 36 dog breeders from 3 countries and 28 dog breeds (see Table 1).


**Table 1.** Distribution of breeders according to countries and participation in the questionnaire surveys. In the column marked with "Total", the numbers represent the sum of individual respondents (of each breed) who completed either Questionnaire 1 or 2. FCI = Fédération Cynologique Internationale.


**Table 1.** *Cont*.

Breeders who completed the questionnaire had to meet the following criteria: They raised at least one litter of puppies a priori the completion of the questionnaire; they keep at home a minimum of one more dog of any age, in addition to the mother of the puppies. We requested that the breeders answer the questions regarding their observations on their "entire experience" of their past litters bred.

#### *2.4. Variables*

The questionnaires covered the first 8 to 12 weeks of the puppies lives which are spent in their breeders' home. During this period, the puppies normally experience various new stimuli (both social and asocial). Towards the end of this period, puppies start to show an almost complete set of social behaviors, including playful, agonistic, and communicative interactions with not only their kin [37], but also towards humans [38].

Beyond the demographic details, the questionnaires contained items that were aimed at the following interactions between the mother, other dogs, and the puppies:


adults start barking, show aggression towards the puppies, puppies show aggression towards adults, were excluded due to the very sporadic or missing answers to these options.


We analyzed the possible associations among the aforementioned parameters and the following factors:


In the case of the items that included the puppies' or their mother's interaction with "another dog", there were separate options for the following categories of dogs:


The following categories were used as fixed factors in the statistical analysis.

Dog breeds categorized according to the FCI (Fédération Cynologique Internationale) system. For the statistical analysis, we had a large enough sample size from only three FCI breed groups: Group 1 "Sheepdogs and Cattledogs", Group 2 "Pinscher and Schnauzer—Molossoid, Swiss Mountain, and Cattledogs", and Group 9 "Companion and Toy Dogs".

Dog breeds were categorized according to their genetic distance from the wolf (*Canis lupus*) (based on [39]). Three out of the ten groups had a large enough sample size for statistical analysis: "Working Dogs", "Herding Dogs", and "Mastiffs".

#### *2.5. Data Analysis*

For the statistical analysis, we used the IBM SPSS statistical program (version 22.0, Armonk, NY, USA). Raw data are available online as a Supplementary Materials.

The alloparental behavior was handled as a binary variable (presence/absence) and its association with the fixed factors was analyzed by generalized linear models (GzLM) with the binary logistic method. The same method was used when we analyzed the adult dogs' behavior to puppies in general situations. The binomial test was used to analyze the occurrence of regurgitating behavior (presence/absence). The puppies' reaction to adult dogs' barking was analyzed by ordinal regression. We used GzLM with ordinal logistic to find out whether there were differences in the adult dogs' behavior towards the puppies' whining and in the mother's reaction towards the adult dogs. We used sex, previous parental experience, sexual status, and age of the adult dogs as independent variables.

In the case of models where there were two or more independent variables, the two-way interactions were also included in the analysis. Alpha was set at 0.05 in each test.

#### **3. Results**

#### *3.1. Alloparental Behaviors (Including Nursing, Licking, Cleaning, But Not Regurgitation)*

From the 77 responses to Questionnaire 1, we found in 61% of the cases that breeders observed the presence of alloparental nursing behaviors. We found no significant association between the adult dogs' caretaking behavior and any of the fixed factors (GzLM with binary logistic—housing method of puppies κ2(2) = 3.022, *p* = 0.221; timing of separation of the puppies κ2(2) = 2.349, *p* = 0.309; aggressive behavior with the puppies κ2(1) = 0.245, *p* = 0.621; FCI breed groups κ2(2) = 0.294, *p* = 0.863; and genetically clustered breed groups κ2(2) = 0.539, *p* = 0.764).

#### *3.2. Feeding of the Puppies with Regurgitation*

From the 41 breeders who responded to Questionnaire 2, 34 reported that he/she observed mother dogs regurgitating to their puppies. By setting the chance level to 0.5, according to the binomial test, this ratio is significantly above chance level (*p* < 0.001). However, one could also expect that mothers will almost always feed their litters by regurgitation (parallel with the pariah dogs, [36]), therefore we ran the binomial test again with the chance level set at 0.99. The abovementioned observed ratio is significantly below this (*p* < 0.001). We also investigated the occurrence of alloparental regurgitative feeding. From the 41 responses, 18 breeders reported observations of other (i.e., not the mother) dogs providing food by regurgitation to the puppies. Based on the very sporadic incidence of this behavior, based on the literature about free-ranging dogs [20,36], we set the reference ratio near zero (0.01). The observed ratio was significantly higher than this (binomial test, *p* < 0.001).

#### *3.3. The Puppies' Reaction to the Other Dogs' Barking*

We found a significant association with the housing method of puppies (ordinal regression—κ2(2) = 9.363, *p* = 0.009). Based on the post-hoc comparisons (Table 2), puppies show the weakest reaction to the barking of adult dogs when they are not separated from the other dogs; meanwhile, they show fear or they join in barking with the others when they are kept partly or fully separated from the other dogs in the household (Figure 1). A similar, but non-significant trend was found in the case of the timing of separation of puppies (ordinal regression—κ2(2) = 4.631, *p* = 0.099), where again, puppies that are never separated from the other dogs showed the weakest reaction to other dogs' barking according to the breeders' observations. We found no further significant associations between reaction to other dogs' barking and the fixed factors (ordinal regression—aggressive behavior with the puppies κ2(1) = 0.628, *p* = 0.428; FCI breed groups κ2(2) = 1.112, *p* = 0.573; and genetically clustered breed groups κ2(2) = 0.598, *p* = 0.742).

**Table 2.** Parameter estimates of the puppies' reaction to other dogs' barking as a function of the method of housing of the puppies (ordinal regression). "Barkreact" 0–2 levels show an increasing intensity of fearful/joining reaction when other dogs bark. "Separation" 1–3 levels show a decreasing extent of separating the puppies from the other dogs during the time spent at the breeder's house. \* this parameter is set to 0 because it is redundant.


**Figure 1.** Association between the housing method of the puppies ("separation" 1–3 shows a decreasing level of isolation of the puppies from other dogs) and their reaction to other dogs' barking (mean ± 95% confidence interval (CI)).

#### *3.4. Adult Dogs' Reaction to the Puppies' Whining*

We found no difference between the reaction of the puppies' father and other adult male dogs (GzLM with ordinal logistic—κ2(1) = 0.606, *p* = 0.436). In the case of the adult female dogs' age, reproductive status (intact vs. spayed), and parousness (had offspring vs. did not have offspring previously), we found a significant association between the age of the female dogs and their reaction to the puppies' whining (GzLM with ordinal logistic—age κ2(2) = 8.564, *p* = 0.014). According to the post-hoc comparisons (Table 3), female dogs under 1 year of age showed the strongest reaction (including either sniffing, or even more intense, mother-like behaviors, such as licking, lying beside, or attempting to nurse) to the puppies' whining (Figure 2).

**Table 3.** Parameter estimates of the reactions of adult female dogs to the whining of the puppies as a function of age, reproductive status, and parousness (had offspring or not). GzLM with ordinal logistic. \* this parameter is set to 0 because it is redundant.


**Figure 2.** Association between the female dogs' age (1 = younger than one year; 2 = adult; 3 = older than 8 years) and the intensity of their reaction to the puppies' whining (mean ± 95% CI).

Neither the reproductive status (κ2(1) = 2.442, *p* = 0.118) nor the parousness (κ2(1) = 2.341, *p* = 0.126) of the adult females had significant association with reaction to the puppies' whining. We did not find any significant interactions between the factors. According to the breeders' observations, the parousness of the adult dogs (including both males and females) had a significant association with their reaction to the puppies' whining (Table 4; GzLM with ordinal logistic—κ2(1) = 5.795, *p* = 0.016), where parous adult dogs react more intensely than the nulliparous ones (Figure 3). Sex itself did not have a significant effect (κ2(1) = 2.240, *p* = 0.134), and we did not find significant interaction between the factors.

**Table 4.** Parameter estimates of adult dogs' reaction to the whining of puppies, as a function of their sex and parousness (0 = did not have puppies; 1 = had puppies). GzLM with ordinal logistic. \* this parameter is set to 0 because it is redundant.


**Figure 3.** Adult (male + female) dogs' reaction (mean ± 95% CI) to the whining of puppies in association with the parousness of the adults (0 = did not have puppies; 1 = had puppies before).

#### *3.5. Adult Dogs' Reaction to Puppies in General Situations*

Adult males' reactions did not show a difference between the puppies' father and other males (GzLM with binary logistic—κ2(1) = 0.000, *p* = 1.000). The age (GzLM with binary logistic—κ2(2) = 8.300, *p* = 0.016) and reproductive status (κ2(1) = 6.293, *p* = 0.012) of female dogs showed a significant association with their reaction to the puppies—according to the post-hoc comparisons (Table 5), less than 1 year old females and the intact females were more likely to react with playful interest to the puppies' presence than the older or spayed females (Figure 4). The parousness of the females did not have a significant effect on this parameter (κ2(1) = 0.271, *p* = 0.603). The sex (κ2(1) = 0.451, *p* = 0.502) and parousness (κ2(1) = 0.164, *p* = 0.686) of the other adult dogs in the household, as well as the interaction of these factors, did not show a significant association with the reaction to the puppies in general encounters.

**Figure 4.** The association between the amicable reaction (mean ± 95% CI) of female dogs to puppies as a function of their reproductive status (0 = spayed, 1 = intact).


**Table 5.** Parameter estimates of the female dogs' behavior with the puppies in association with their age, reproductive status, and parousness (did not have puppies or had puppies before). GzLM with binary logistics. \* this parameter is set to 0 because it is redundant.

#### *3.6. The Reaction of the Mother of the Puppies to Other Dogs in the Household*

In the case of other adult male dogs, we did not find a significant difference between the reaction of the mother to the father of the puppies or other adult male dogs (GzLM with ordinal logistic—κ2(1) = 1.091, *p* = 0.296). When we analyzed the reaction of the mother to other females in the household, according to the breeders' observations, there was a significant association with the other females' age (GzLM with ordinal logistic—κ2(2) = 13.090, *p* = 0.001), and we also found a significant interaction between the reproductive status and parousness of the other females (κ2(1) = 12.183, *p* < 0.001). According to the post-hoc comparisons, mother dogs are less friendly with other adult females than with juveniles or older females. Furthermore, mother dogs are the least friendly with nulliparous, intact females (Table 6). This result was strengthened by another analysis, where we tested the association with the sex and parousness of other dogs in the household. Besides the two significant main effects (GzLM with ordinal logistic—sex κ2(1) = 12.784, *p* < 0.001; parousness κ2(1) = 15.090, *p* < 0.001), we also found a significant interaction (κ2(1) = 5.732, *p* = 0.017). According to this, mother dogs are the least friendly with nulliparous females by the observations of the breeders.


**Table 6.** Parameter estimates of the mother dogs' reaction (agonistic, neutral, friendly) to other females in the household as a function of the other females' age, reproductive status, and parousness. Significant interaction (\*) between reproductive status and parousness is included. GzLM with ordinal logistic. \* this parameter is set to 0 because it is redundant.

#### **4. Discussion**

In this study, we surveyed an international sample of active dog breeders, with questions aimed at the various forms of alloparental caretaking of the puppies, the interactions between puppies and other dogs apart from the mother, plus the interactions between the mother dog and other dogs at the same home. Based on the breeders' reports, alloparental nursing can be considered widespread in companion dogs, although its presence is significantly less than 100%. Other forms of nurturing the puppies (i.e., regurgitation) is typical for the mothers, and additionally provided by other dogs in slightly less than 50% of the cases as well. The presence of alloparental caretaking was not associated with the type of breed, or with the way the puppies were separated (or not) from the other dogs. The puppies showed a stronger reaction to other dogs' barking if they were kept at least partially separated from other dogs in the household. Paternity (including both the father of the puppies or an unrelated male) did not have significant association with the dogs' reaction to the puppies' whining and with the dogs' playful behavior with the puppies. Mother dogs also reacted similarly with the father of the puppies and other males. Young female, parous dogs showed stronger interest towards the whining of the puppies; and the young/sexually intact females behaved more playfully with them. In turn, mother dogs were reported as being the least friendly with other females that were either adult, or intact, nulliparous ones.

Before the detailed discussion of the results, we should consider some limitations of our study. As it was a questionnaire survey, we entirely relied on the expertise and experiences of the breeders who reported on the behavior of their dogs. Therefore, in the future, targeted behavioral tests would be useful for validating the key findings about the various dog–dog interactions—however, we should also keep in mind that conducting experiments in the homes of dog owners/breeders has its difficulties/limitations, too. The sample size was relatively low in our study, partly caused by the rather strict rules of participation (only breeders were invited with actual experience of raising at least one litter of puppies in the past with other adult dogs around). In any case, a more comprehensive survey would be beneficial (preferably involving more participants from non-European countries), especially which includes a more complete set of dog breeds from preferably each breed groups based both on the artificial (FCI) and genetic clustering. Finally, the scope of our survey was limited by the way in which the questionnaire was distributed—the utilization of internet and social media has its benefits (one can reach participants quickly and technically with no geographic limitations); however, potentially knowledgeable participants can also be left out because they do not use these means of communication.

Compared to the detailed comparative work done on the parental behavior of wild canids [25], and even on free-ranging dogs [36], empirical studies are noticeably lacking for companion dogs. Companion and working/service dogs are usually bred with close human supervision (e.g., [40,41]); therefore, the circumstances and, many times, even the process of parental care can be considered as more or less artificial compared to wild dogs. Apart from veterinary and animal breeding texts (e.g., [17,42]), scientifically accumulated information is surprisingly sparse regarding the maternal (see review [43]) and alloparental behaviors, as well as the interaction between the puppies and other adult dogs, in the first two months of life.

Our results show that alloparental caretaking behaviors (allonursing, regurgitating of food) are widespread among dogs that are kept by hobby breeders. Fostering of the young has a solid ecological basis in such species as the super-social members of the *Canidae* family (gray wolf; African wild dog *Lycaon pictus*; dhole *Cuon alpinus*). Among others, Riedman [44] lists the following factors that, along the course of evolution, could facilitate alloparental caretaking to develop: "(1) Prolonged or energetically intensive parental investment; (2) small groups with tight kinship bonds; (3) highly social or cooperative group structure; and (4) young that are raised in high density breeding colonies". From these, the first three conditions are typically true of the abovementioned wild canids—however, they are harder to interpret in the case of companion, or even-free ranging dogs. If we consider the latter (pariah, or village dogs) as the most valid ecotype of domestic dogs [21], we should notice that the change in feeding ecology (being mainly a scavenger instead of a hunter of large prey, [45]) could be the main driving force behind the alteration of reproductive and parental behavior in the majority of dogs. Scavenging does not require adults to act cooperatively—neither during the hunt, nor when provisioning the lactating mother and the young. Furthermore, in free-ranging dogs, the freshly weaned juveniles become mostly a competitor for the adults [21]; therefore, their role as "helpers" for the next generation is limited or non-existent. Interestingly, our results, as well as in the earlier study of [35], show a considerably common occurrence of alloparental behaviors among companion dogs. The apparent difference compared to the infrequently observed foster-behaviors among free-ranging dogs [19,20] could be the result of the complex effect of different levels of food competition, human intervention, and, in part, the density of animals around the breeding mother/puppies (see condition #iv by Riedman [44]). Based on this, we can hypothesize that the capacity for alloparental caretaking is steadily present in the domestic dog, even in the population of pets and working dogs where the conditions for both the breeding and caretaking of the young are highly artificial. The competition for resources is rather strong among free-ranging dogs [46], thus alloparental behaviors may be less adaptive (given that scavenging is the main type of food procurement). In companion dogs, alloparental behavioral tendencies are rarely discouraged—according to our results, its occurrence was not affected by the method of puppy-raising that the breeders chose. Somewhat surprisingly, we did not find a breed effect; however, this could be explained by the low sample size of individual breed groups. One could hypothesize that those breeds that are more closely related to wolves would show stronger alloparental tendencies. Although basal (or "ancient") breeds were not represented well enough in our sample, the fact that we did not find a difference between the occurrence of alloparental behaviors among breed groups, with such widely varying functions as herding vs. toy/companion or belonging to the mastiffs vs. herding dogs, it shows that alloparental behaviors were probably less affected by recent functional selection of dogs.

Keeping conditions reportedly affected the puppies' reactivity to other dogs' barking—the breeders observed the weakest reaction (i.e., lower levels of fearfulness, or tendency to join the others barking) in those puppies that were kept together with the other dogs in the household without any restriction. Although the first couple of months are considered crucial in the proper socialization of young dogs [47], and successful socialization is unequivocally considered a key factor in avoiding problem behaviors in dogs (e.g., [48]), still, the majority of scientific studies concentrate on the events of socialization that typically follow the puppies' departure from the breeder's home (e.g., [29,30]). Relatively few papers target the early interactions between the living environment and puppies still with their mother (e.g., [49]). In a few earlier studies (such as [50]), it was shown that early isolation of the puppies resulted in a decreased level of interactivity later with conspecifics. However, most studies have focused on dog–human interactions (e.g., [3,51]), because, in the case of companion and working dogs, the main measure of their success as adults depends on their fit to the human environment. Therefore, the observations reported in our study have a relevance from the aspect that the chance to interact uninterruptedly with other dogs from a very early age can improve young dogs' behavior regarding dog–dog interactions. It is important to see, however, that the familiarity between the young puppies and the other adult dogs they interact with also can play a crucial role in the behavioral development of the juvenile dogs. Earlier, it was found [52] that the younger the puppy was when its new owners introduced it to other dogs, the higher the chance became that later the dog showed undesired aggression towards conspecifics. Adding these findings to our results, one could conclude that the predominantly amicable interactions (including alloparental care) with familiar dogs at the breeder's home could provide the best experience for young puppies with their conspecifics; meanwhile, owners should be careful with the early exposure of the puppies to possibly negative experiences with unknown dogs at public areas [52]. So far, this particular aspect of environmental effects on behavioral ontogeny has only been marginally covered by other studies (e.g., [33,53]), where the focus has mainly been on other behaviors, such as interactions with the physical environment or with humans.

We did not find a difference between the behavior of adult male dogs with the puppies, whether the particular dog was the father of the puppies or not, and the mother dog's reaction to the males was also independent from the paternal status of the males. This result is in parallel with the reports on free-ranging dogs, where sometimes, more than one male dog was observed to be loosely associated with particular litters [36].

Friendly interactions were reportedly facilitated with the puppies if the other dog was a young, sexually intact female. Sexual status was also important in the case of the other dogs' reaction to the whining of the puppies—besides the young females, intact and parous dogs showed stronger interest towards whining puppies. Interestingly, in a recent laboratory study, Lehoczki et al. [54] found no association between the sexual status, parousness, or sex of adult dogs and their responsiveness to playbacks of separation calls of puppies. Besides the option that breeders may misinterpret their dogs' behavior, it is also possible that dogs behave differently in an artificial laboratory setting compared to a realistic situation at home when puppies are truly present. In the case of highly social canid species, fostering (alloparental helping) behaviors are facilitated by several factors [18]: Monestrum (which prevents deliberate further pregnancies in most females along the season) and an unusually long diestrous (pseudopregnancy) phase (which puts the non-pregnant, usually young females into a hormonal state that facilitates maternal behaviors). As monestrum and alloparental helper behavior are definitely present in some dogs (dingoes, [27]), as well as pseudopregnancy, which is a pronounced feature even in companion dog females [55], our results (i.e., young females are among the most attentive to whining puppies and respond to puppies in the friendliest manner) are in line with the literature. Breeders also reported that older, intact, and parous dogs showed heightened interest towards whining puppies and were more likely to play with the puppies—this behavior can be expected, according to Schradin et al. [56], who, besides the neoteny-helper hypothesis, highlighted another way of alloparental care: The parent–helper scenario. According to the latter, even adult members of the group can show helping behavior with the puppies, if their endocrine system mimics the changes otherwise typical to the lactating mother.

Finally, breeders reported some level of discrimination by the mother dog regarding her interactions with other dogs in the household. Mothers showed the most agonistic behaviors with other females, if those were either adult, or intact, nulliparous ones. One should take into consideration, of course, that the distribution of sexes and age cohorts were uncontrolled in our sample, which could have an effect on the statistical reliability. On the other hand, there are reports of protective mother dogs (in free-ranging dogs, [57]), with an emphasis on the most frequent agonistic interactions among the adult females [58]. Paul and colleagues [19], however, showed that in free-ranging dogs, grandmothers may provide help with their daughters' puppies. As in our study, the mother dogs showed higher aggression against intact, nulliparous females, the observations made on companion dogs and on free-ranging dogs (that were accepting help from their mothers) are not excluding each other. However, in general, the reportedly higher occurrence of agonistic behaviors in dog mothers against other (intact) females can be explained as a result of avoiding possible resource competition, and even a probability of infanticide (which is observed among female wolves, [59]).

#### **5. Conclusions**

Based on the observations of companion dog breeders, our study shows an intricate network of interactions among adult dogs of the household and puppies below the age of weaning. Alloparental behaviors and amicable interactions from the adult dogs dominated the scene, with an eventual stress-reducing effect on the behavior of puppies in the case of alarm barks of the adults. The role of dog–dog interactions during the first two months of life might be an important factor for proper socialization and later problem-free behavior with future canine partners.

**Supplementary Materials:** The following are available online at http://www.mdpi.com/2076-2615/9/12/1011/s1, raw data file (puppy\_survey)—this file includes the data which were used for the statistical analyses.

**Author Contributions:** Conceptualization, P.P. and S.S.S.; Methodology, P.P. and S.S.S.; Formal analysis, P.P.; Investigation, S.S.S.; Data curation, P.P. and S.S.S.; Writing—original draft preparation, P.P. and S.S.S.; Writing—review and editing, P.P.; Visualization, P.P.; Supervision, P.P.; Project administration, S.S.S.

**Funding:** This research received no external funding.

**Acknowledgments:** The authors are thankful to Celeste Pongrácz for checking the English of this manuscript. **Conflicts of Interest:** The authors declare no conflicts of interest.

#### **References**


© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

#### *Article*
