- In order to improve the welfare of dogs, we need to understand their behaviour, needs and development
- The specific capabilities of the beagle need to be considered when developing Refinements for purpose-bred laboratory-housed beagles
- Dogs are very familiar to humans, however this can lead to interventions being based on assumptions and "common sense" rather than on an evaluation of knowledge.
On this page
- The Beagle
- Natural history of the dog
- Puppyhood and development
- Social and cognitive abilities of the dog
The beagle possesses many of the characteristics which have been cited as advantages of using the dog in scientific research (see Dogs in Research). Its small size and amiable temperament make regular handling and procedures easier to conduct than in large dogs, while its history as a pack-living, working dog makes housing in large groups possible. The history of the breed can be traced back to the long-extinct Talbot dog (c. 11th Century) which gave rise to the Southern Hound. The beagle as a breed can first be identified from around 1830 . The continued popularity of the breed, both as a pet and as a working dog, can be attributed to its ability in scentwork and its temperament.
Beagles generally have a highly excitable temperament, scoring highest in a test of 'excitability' . Beagles are also prone to displaying "agreeableness" as a personality dimension, and are not prone to aggression , making them well-adapted for an environment which can involve intensive handling and group living. Beagles have a strong scenting drive: in a study reported in Scott and Fuller , beagles were able to find a mouse in a one-acre field in under a minute, compared to the next fastest breed, fox terriers which took 15 minutes. High drive to perform natural behaviours and the energy levels associated with a working, scenting breed should be taken into account in any programme of Refinements, providing opportunities to exercise and forage.
Natural history of the dog
The 33,000 year old skull of the "Altai dog". Photo credit: Ovodov et al.
While for other laboratory-housed species, in particular primates, we have a wild counterpart from which to obtain information on 'natural behaviour', this doesn't exist for the domestic dog. Instead, we need to piece together literature and information on the natural history of the dog, the process of domestication (which has influenced much of its behaviour and physiology), and the behaviour of free-ranging dogs who may be the closest analogue to a wild counterpart. These dogs typically form fluid groups, composed of more stable breeding pairs . Dogs are also crepuscular, with activity at its greatest around dawn and dusk .
All breeds of domestic dog (Canis lupus familiaris) are descended from a now-extinct subspecies of the grey wolf (Canis lupus, Serpell, 1995), which diverged along with the modern grey wolf between 27-40,000 years ago . DNA evidence has ruled out any involvement from non-wolf species in the dog lineage , although it is unclear which subspecies of C. lupus dogs are descended from. The genetic origin of the dog has been the subject of much inquiry for over 20 years.
Despite historical use of the wolf as a model for dog behaviour, the wolf is considerably different from the domestic dog, due to differences in selective pressure in the intervening millennia. It is hypothesised that a genetic bottleneck in the wolf population means that the ancestral sub-population from which dogs are descended would have been more genetically diverse and may have born little resemblance to the modern grey wolf population , meaning that modern wolves are unlikely to provide a valid model of domestic dog behaviour. Modern dogs are more closely related to ancient wolf fossils than they are to modern grey wolves .Therefore comparative studies between grey wolves and domestic dogs are of little use in gaining an insight into the natural behaviour and needs of the dog. Moreover, fossil records indicate that there have been domestic dogs in Europe for around 15,000 years, with dogs last sharing a common ancestor 18,800 years ago, although some dogs last shared a common ancestor 32,100 years ago pointing to multiple domestications in multiple locations .
A common physical characteristic of domesticated dogs is paedeomorphism (child-like features), caused by our selective breeding of child-like qualities such as large eyes, preference for eye contact and retaining puppy-like features normally lost in adolescent canids . Selective breeding has also favoured traits such as cooperation and tolerance for living in close contact with humans and other dogs, rarely seen in other, non-domesticated, canids.
Studies of dog personality traits have failed to establish a 'dominance' trait, a common misattribution resulting from observations of captive-housed wolves . 'Dominance' is commonly used to explain aggressive or territorial behaviours such as resource guarding. Increased aggression is associated with increased environmental stress and limited availability of highly-valued resources  so care must be taken to identify the cause of these behaviours, rather than misattributing to 'dominance'.
Comprehensive studies of dog personality have identified five major personality traits: "Playfulness," "Curiosity/Fearlessness," "Chase-proneness," "Sociability," and "Aggressiveness". These personality dimensions were developed by Svartberg and Forkman  based on behavioural data from 15,000 dogs of 164 breeds. Although not explicitly tested in this thesis, dimensions of personality such as the curiosity/fear dimension are known to influence an animal's interactions with its environment and may affect its welfare .
Puppyhood and development
The importance of early experience for the laboratory-housed dog cannot be underestimated. The early months of a puppy's development are a crucial window in which socialisation with conspecifics and humans can have a life-long positive impact, or conversely, their absence can have a negative impact. Puppies have limited organisational, sensory and motor abilities at birth . Their eyes and ears are closed and they do not respond to auditory or visual stimuli. However, they are born with developed tactile and thermal senses, responding to touch, pain, heat and cold . They also react to olfactory stimuli although this may be through taste rather than true olfaction. It is necessary to understand when and how well puppies can see, hear and feel to effectively implement any primary socialisation .
Jones  makes the following recommendations based on the acceptance of critical periods of development. As experiences during critical periods may well have life-long impact on the dogs, it is important to monitor these experiences. Modification of whelping beds to minimise stress to newborns and increase tactile and thermal comfort may be beneficial. Gentle introduction of light and sound and these abilities emerge may serve to desensitise pups to these. Desensitisation to unfamiliar stimuli during the period in which the startle response emerges may also be beneficial to the pups' future responses to unfamiliar stimuli.
In a six-year study of the effects of early experience on later life, Wilsson and Sundgren  found that the effect of puppy weight was particularly prominent in female dogs, with higher weights predicting higher activity levels and exploration during puppy tests and higher defence drive and 'hardiness' at adult tests. It was also found that changing the whelping bed substrate from corrugated cardboard to a soft bedding negatively affected puppies' resilience, and the authors suggest that the cardboard bedding may have simulated the effects of early handling.
Fox and Stelzner  also investigated the effects of early experience on puppies. In this study, puppies were grouped into a control group (raised under 'typical' conditions with the mother and experiencing daily human husbandry), a handling group (handled daily for the first five weeks of life) and an isolation group (raised identically for the first four weeks of life, then single housed in a darkened room with minimal human contact for the fifth week). Handling included exposure to light, sound, changes in position and orientation, temperature, and after three weeks, human play. When tested at five weeks, handled pups showed slightly superior coordination, were more active, more social and faster in a problem solving test (although none of these difference was significant). They also showed greater initial distress at separation from human handlers, which follows what we know about attachment-type patterns in dogs .
Conversely, control pups showed greater distress when placed in a novel environment but less so in response to separation from human handlers, suggesting that attachment patterns had not formed. ECG (electrocardiograph) testing also showed that handled pups had greater heart maturation than controls, as determined by greater amplitude in ECGs and on physical examination at necropsy. The isolation-reared pups were hyperalert (vigilant) and rarely rested, which prevented electroencephalograph (EEG) readings being obtained. ECG readings were instead taken while puppies were lying quietly or asleep in a darkened room and restrained in a copper-gauze box lined with foam rubber. The study demonstrated a considerable effect of handling or isolation on ECG and EEG results, with abnormal results in the isolated group and indications of advanced maturity and increased quality in the handled group, indicating that early husbandry practices can have considerable impact on puppy development.
More recently, Gazzano, Mariti, Notari, Sighieri and McBride  conducted an early handling programme with 43 puppies from breeding kennel and pet homes. Puppies were handled daily for the first three weeks of life and they were tested in isolation in a novel environment at eight weeks old. Puppies which had undergone handling were found to be more emotionally stable, had a longer latency to yelp, lowered duration of vocalising and greater exploratory behaviour in a novel environment. Meunier  reviewed socialisation programmes for laboratory-housed dogs and suggested that the most important factors are to develop a programme which succeeds in reducing distress through the implementation of training, desensitisation and socialisation tailored to the individual future experiences of the dogs.
The importance of handling from birth is clear, as well as introducing an examination table and health checks at an early age. Where breeding takes place within the same site as the animal unit, incorporating measures such as these into standard early rearing practices may increase the resilience of the dogs before they reach the experimental unit, where additional training for specific procedures can be introduced without the need for remedial handling. Similarly, breeding companies which supply dogs to industry must be able to provide an even greater level of resilience in dogs which are subject to additional stressors such as transport and acclimatisation.
Habituation and desensitisation to procedures and equipment is also recommended prior to the brief pre-study habituation typical of toxicology studies. Despite the wealth of literature and supporting evidence for the implementation of training, specifically positive reinforcement training, for dogs, very few examples of such research being applied in the laboratory setting exist and as such the costs and benefits to welfare are poorly understood.
Stages of development
Puppies' development was first described in phases by Scott & Fuller , who
identified four phases of development:
|0-5 days||Characterised by a lack of response of the audio-visual system|
|5-18 days||Adult postural reflexes appear, the eyes begin to open and a weak startle response may be present|
|18-28 days||Emergence of positive orientation towards audio and visual responses, puppy reflexes of rooting and urination on stimulation disappear, adult sensory reaction (startle, avoid cliff edge) appear and motor activities emerge|
|28 days-adulthood||Adult behaviours emerge. Puppies are capable of recognising humans/littermates visually and auditorily|
Building upon this, Jones  described the stages of development in more detail, detailing the emergence of key reflexes and the responses associated with them, which are described in the table below. Introducing gentle stimuli such as changes in sound, texture and light as the eyes and ears open may help to increase resilience in later life by providing a variety of sensory experiences.
The emergence of sexual maturity may vary between breeds of dogs, and in the beagle, the onset of puberty occurs between 6-12 months, with sexual maturity reached at between 9-12 months. Growth and food consumption increases from five to approximately ten months, where it begins to level off and most dogs in safety assessment are considered adult at 12 months . However, typical use of dogs in safety assessment occurs at an age of nine months or younger. This means that many of the opportunities to influence behaviour and resilience in later life occur at an age when many dogs will be in the breeding facility before being transferred to a dog facility. The stressors associated with transport and acclimatisation to a new facility mean that early opportunities for desensitisation in the breeding facility are particularly important to future welfare. This places special responsibility on breeders to take the opportunities to positively influence behaviour and resilience in later life as these opportunities occur at an age when many dogs will be in the breeding facility before being transferred to a dog facility.
A detailed description of the sensory capabilities of the dog can be found in Prescott et al., .
Social and cognitive abilities of the dog
The result of our history of cooperation in a shared environment has led to the dog developing abilities to communicate with and understand humans which in some ways exceed those of nonhuman primates. Dogs demonstrate an understanding of human eye gaze similar to that of human infants and exceeding that of the dog's ancestor, the wolf (Canis lupus) or the chimpanzee (Pan troglodytes, [24,25]). Dogs are able to identify when they are being spoken to and follow pointing cues.
More importantly, dogs are also greatly influence by human-given social cues. This ability to influence dogs' choices through social referencing means that interactions with dogs, particularly when referencing potentially aversive stimuli. In the context of dog use in scientific research, it is important to exploit this social referencing ability to ensure that positive associations are formed with staff, equipment and procedures.
1. Youatt, W. (1845). The Dog. London: Knight & Co.↩
2. Fogel, B. (1990). The dog's mind: Understanding your dog's behavior. New York: Macmillan. ↩
3. Kraeuter, K. (2001). Training your beagle. New York.: Barron's Educational Series.↩
4. Scott, J. P. & Fuller, J.L. (1965). Genetics and the social behavior of the dog. Chicago: The University of Chicago Press.↩
5. Spotte, S. (2012). Societies of wolves and free-ranging dogs. Cambirdge: Cambridge University Press.↩
6. Beck, A. M. (1973). The ecology of stray dogs: a study of free-ranging urban animals. West Lafayette: Purdue University Press.
7. Skoglund, P., Ersmark, E., Palkopoulou, E. &Dalen, L. (2015). Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Current Biology, 25, 1-5.↩
8. Vila, C., Savolainen, P., Maldonado, J. E., Amorim, I. R., Rice, J. E., Honeycutt, R. L., Crandall, K. A., Lundeberg, J. & Wayne, R. K. (1997). Multiple and ancient
origins of the domestic dog. Science, 276 (5319), 1687-1689.↩
9. Freedman, A. H., Gronau, I., Schweizer, R. M., Ortega-Del Vecchyo, D., Han, E., Silva, P. M., Galaverni, M., Fan, Z., Marx, P., Lorente-Galdos, B., Beale, H., Ramirez, O., Hormozdiari, F., Alka, C., Vil, C., Squire, K., Geffen, E., Kusak, J., Boyko, A. R., Parker, H. G., Lee, C., Tadigotla, V., Siepel, A., Bustamante, C. D., Harkins, T. T., Nelson, S. F., Ostrander, E. A., Marques-Bonet, T., Wayne, R. K. & Novembre, J. (2014). Genome sequencing highlights the dynamic early history of dogs. PLoS Genetics, 10 (1), e1004016.↩
10. Thalmann, O., Shapiro, B., Cui, P., Schuenemann, V., Sawyer, S., Greenfield, D., Germonpre, M., Sablin, M., L_opez-Gir_aldez, F., Domingo-Roura, X. et al. (2013). Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science, 342 (6160), 871-874.↩
11. Gould, S. J. (1994). Eight little piggies: Reflections in natural history. WW Norton & Company.↩
12. Mech, L. D. & Boitani, L. (2003). Wolves: behavior, ecology, and conservation. Chicago: University of Chicago Press.↩
13. DeVries, A. C., Glasper, E. R. & Detillion, C. E. (2003). Social modulation of stress responses. Physiology & Behavior, 79 (3), 399-407. ↩
14. Svartberg, K. & Forkman, B. (2002). Personality traits in the domestic dog (Canisfamiliaris). Applied Animal Behaviour Science, 79 (2), 133-155.↩
15. Panksepp, J. (2011). The basic emotional circuits of mammalian brains: Do animals
have affective lives? Neuroscience & Biobehavioral Reviews, 35 (9), 1791-1804.↩
16. Fox, M. & Stelzner, D. (1966). Behavioural effects of differential early experience in the dog. Animal Behaviour, 14 (2-3), 273-281 ↩
17. Jones, A. (2007). Sensory development in puppies (Canis lupus f. familiaris): Implications for improving canine welfare. Animal Welfare, 319-329. ↩
18.Wilsson, E. & Sundgren, P.-E. (1998). Behaviour test for eight-week old puppies heritabilities of tested behaviour traits and its correspondence to later behaviour. Applied Animal Behaviour Science, 58 (1-2), 151-162. ↩
19. Gacsi M., Miklosi A., Varga, O., Topal, J. & Csanyi, V. (2004). Are readers of our face readers of our minds? Dogs (Canis familiaris) show situation-dependent recognition of human's attention. Animal Cognition, 7: 144–153.↩
20. Gazzano, A., Mariti, C., Notari, L., Sighieri, C. & McBride, E. A. (2008). Effects of early gentling and early environment on emotional development of puppies. Applied Animal Behaviour Science, 110 (3), 294-304.↩
21. Meunier, L. D. (2006). Selection, acclimation, training, and preparation of dogs for the research setting. ILAR Journal, 47 (4), 326 347. ↩
22. Gad, S. C. (2006). Animal models in toxicology. Boca Raton: CRC Press Taylor and Francis Group.↩
23. Prescott, M., Morton, D. B., Anderson, D., Buckwell, A., Heath, S., Hubrecht, R., Jennings, M., Robb, D., Ruane, B., Swallow, J. & Thompson, P. (2004). Refining dog husbandry and care: Eighth report of the BVAAWF/FRAME/RSPCA/ UFAW Joint Working Group on Refinement. Laboratory Animals, 38 (SUPPL. 1), S1:1-S1:94. ↩
24. Hare, B. & Tomasello, M. (2005). Human-like social skills in dogs? Trends in Cognitive Sciences, 9 (9), 439-444.↩
25. Kubinyi, E., Viranyi, Z. & Miklosi, A. (2007). Comparative social cognition: From wolf and dog to humans. Comparative Cognition & Behavior Reviews, 2, 26-46.↩