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      Influence of Maternal Care on Behavioural Development of Domestic Dogs ( Canis Familiaris) Living in a Home Environment

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          Abstract

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          Maternal care in dogs and its impact on the behavioural development of puppies has become the subject of growing research interest. In order to determine the effects of maternal care on the behaviour of family dog puppies, maternal care during the first three weeks after birth was observed in 12 litters of puppies reared in a home environment (72 puppies). The behavioural responses of the puppies were assessed at two months of age, in an arena and an isolation test. In both tests, the amount of maternal care was found to be positively associated with some stress behaviours and, in the arena test, also with the puppies’ interest in an unfamiliar person who was present during the test. These behaviours are similar to those observed during the separation of other young mammals from an attachment figure with which they have a high quality of bond. Amount of maternal care was also found to be negatively associated with exploration and play. The difference in results between the present study and our previous study involving laboratory dogs reared in relative social isolation suggests that the developmental trajectory of puppies is influenced by a combination of maternal behaviour and social and physical environmental enrichment.

          Abstract

          Maternal care has been shown to affect the development of the brain, behaviour, social skills and emotional systems of the young of many mammalian species including dogs. The aim of the present study was to determine the effects of maternal care on the behavioural responses of family dog puppies towards environmental and social stimuli. In order to do this, maternal care (licking puppy’s ano-genital area, licking the puppy, nursing and mother-puppy contact) during the first three weeks after birth was assessed in 12 litters of domestic dog puppies reared in home environments (total = 72 puppies). The behavioural responses of puppies were assessed in an arena and an isolation test, which were performed when the puppies were two-month old. Data were analysed using principal components analysis and projection to latent structures regression. A systematic relationship was found between maternal care and behaviour in both tests. In the arena test, maternal care was found to be positively associated with approach to the stranger, attention oriented to the stranger, time spent near the enclosure, yawning, whining and yelping (R 2Y = 0.613, p = 8.2 × 10 −9). Amount of maternal care was negatively associated with the number of squares crossed and the time spent individually playing with the rope. In the isolation test, the amount of maternal care was positively associated with standing posture, paw lifting, and howling, and it was negatively associated with yawning, lying down and nose licking (R 2Y = 0.507, p = 0.000626). These results suggest that the amount of maternal care received during early life influences the pattern of behavioural responses and coping strategies of puppies at two-months of age. On the basis of these findings it could be speculated that early maternal care contributes to adaption to the environment in which family puppies are developing, with particular regard to social relationships with people.

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          Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.

          Variations in maternal care affect the development of individual differences in neuroendocrine responses to stress in rats. As adults, the offspring of mothers that exhibited more licking and grooming of pups during the first 10 days of life showed reduced plasma adrenocorticotropic hormone and corticosterone responses to acute stress, increased hippocampal glucocorticoid receptor messenger RNA expression, enhanced glucocorticoid feedback sensitivity, and decreased levels of hypothalamic corticotropin-releasing hormone messenger RNA. Each measure was significantly correlated with the frequency of maternal licking and grooming (all r's > -0.6). These findings suggest that maternal behavior serves to "program" hypothalamic-pituitary-adrenal responses to stress in the offspring.
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            Nongenomic transmission across generations of maternal behavior and stress responses in the rat.

            In the rat, variations in maternal care appear to influence the development of behavioral and endocrine responses to stress in the offspring. The results of cross-fostering studies reported here provide evidence for (i) a causal relationship between maternal behavior and stress reactivity in the offspring and (ii) the transmission of such individual differences in maternal behavior from one generation of females to the next. Moreover, an environmental manipulation imposed during early development that alters maternal behavior can then affect the pattern of transmission in subsequent generations. Taken together, these findings indicate that variations in maternal care can serve as the basis for a nongenomic behavioral transmission of individual differences in stress reactivity across generations.
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              Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat.

              The mothers of infant rats show individual differences in the frequency of licking/grooming and arched-back nursing (LG-ABN) of pups that contribute to the development of individual differences in behavioral responses to stress. As adults, the offspring of mothers that exhibited high levels of LG-ABN showed substantially reduced behavioral fearfulness in response to novelty compared with the offspring of low LG-ABN mothers. In addition, the adult offspring of the high LG-ABN mothers showed significantly (i) increased central benzodiazepine receptor density in the central, lateral, and basolateral nuclei of the amygdala as well as in the locus ceruleus, (ii) increased alpha2 adrenoreceptor density in the locus ceruleus, and (iii) decreased corticotropin-releasing hormone (CRH) receptor density in the locus ceruleus. The expression of fear and anxiety is regulated by a neural circuitry that includes the activation of ascending noradrenergic projections from the locus ceruleus to the forebrain structures. Considering the importance of the amygdala, notably the anxiogenic influence of CRH projections from the amygdala to the locus ceruleus, as well as the anxiolytic actions of benzodiazepines, for the expression of behavioral responses to stress, these findings suggest that maternal care during infancy serves to "program" behavioral responses to stress in the offspring by altering the development of the neural systems that mediate fearfulness.
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                Author and article information

                Journal
                Animals (Basel)
                Animals (Basel)
                animals
                Animals : an Open Access Journal from MDPI
                MDPI
                2076-2615
                05 December 2017
                December 2017
                : 7
                : 12
                : 93
                Affiliations
                [1 ]Department of Veterinary Sciences, University of Pisa, Viale delle Piagge, 2, 56124 Pisa, Italy; cmariti@ 123456vet.unipi.it (C.M.); csighier@ 123456vet.unipi.it (C.S.); agazzano@ 123456vet.unipi.it (A.G.)
                [2 ]Queen Mother Hospital for Small Animals, Royal Veterinary College, Hawkshead Lane, North Mymms, Hertfordshire AL9 7TA, UK; jbowen@ 123456rvc.ac.uk
                [3 ]Department of Psychiatry and Forensic Medicine, Autonomous University of Barcelona, 08193 Bellaterra, Spain; jaumefatjo@ 123456gmail.com
                Author notes
                [* ]Correspondence: giovanna.guardini@ 123456gmail.com ; Tel.: +39-050-2216837
                Author information
                https://orcid.org/0000-0001-6747-0961
                https://orcid.org/0000-0001-7127-4680
                https://orcid.org/0000-0001-9649-2027
                Article
                animals-07-00093
                10.3390/ani7120093
                5742787
                29206131
                11b99461-37e6-4334-9209-00e5c1a988f0
                © 2017 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/).

                History
                : 02 October 2017
                : 03 December 2017
                Categories
                Article

                behaviour,dog,early experiences,maternal care,mother-puppy interactions,puppy

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