Variation in reproductive traits of members of the genus Canis with special attention to the domestic dog (Canis familiaris)

Behavioural Processes 92 (2013) 131–142

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Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc

Variation in reproductive traits of members of the genus Canis with special attention to the domestic dog (Canis familiaris) Kathryn Lord a,∗ , Mark Feinstein a , Bradley Smith b , Raymond Coppinger a a b

Hampshire College, School of Cognitive Science, Amherst, MA 01002, USA Central Queensland University, Appleton Institute, 44 Greenhill Road, Wayville, South Australia 5034, Australia

a r t i c l e

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Article history: Received 8 June 2012 Received in revised form 6 October 2012 Accepted 24 October 2012 Keywords: Canidae Canis Dogs Reproductive behavior Feeding patterns Parental behavior

a b s t r a c t We compare differences in the reproductive strategies of “free-living” dogs with their wild relatives in the genus Canis, of which the dog is a very recently evolved member. The members of this genus display a greater range of parental motor patterns than generally seen in other species of Carnivora, including pair-bonding and extended parental care; parents regurgitate to offspring and provision them with food for months to as long as a year. But the domestic dog does not routinely display these genustypical behaviors. While this has generally been assumed to be a result of direct human intervention, humans have little reproductive control over the vast majority of domestic dogs. We analyze the low frequency of display of genus-typical behaviors and postulate that the dog’s reproductive behaviors are an adaptation to permanent human settlement and the waste resources associated with it. Adaptation to this environment has decreased seasonality, increased the fecundity of unrestrained dogs and reduced the need for prolonged parental care. The consequences of greater fecundity and reduced parental care are compared to the reproductive behavior of other species of the genus. © 2012 Elsevier B.V. All rights reserved.

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Reproductive activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Seasonality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. C. lupus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2. C. simensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.3. C. latrans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.4. C. mesomelas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.5. C. aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.6. C. adustus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.7. C. dingo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.8. C. familiaris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Age of first reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1. C. lupus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2. C. simensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3. C. latrans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4. C. mesomelas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5. C. aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.6. C. adustus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.7. C. dingo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.8. C. familiaris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Pair bonding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. C. lupus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. C. simensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. E-mail address: [email protected] (K. Lord). 0376-6357/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.beproc.2012.10.009

132 133 133 133 133 133 134 134 134 134 134 134 134 134 134 135 135 135 135 135 135 135 136

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K. Lord et al. / Behavioural Processes 92 (2013) 131–142

2.3.3. C. latrans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.4. C. mesomelas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.5. C. aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.6. C. adustus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.7. C. dingo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.8. C. familiaris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parental feeding behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Nursing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1. C. lupus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.2. C. simensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.3. C. latrans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.4. C. mesomelas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.5. C. aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.6. C. adustus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.7. C. dingo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.8. C. familiaris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Regurgitation and provisioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1. C. lupus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2. C. simensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3. C. latrans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.4. C. mesomelas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.5. C. aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.6. C. adustus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.7. C. dingo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.8. C. familiaris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Seasonality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Reproductive age and size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Pair bonding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Nursing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5. Regurgitation and provisioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6. Population implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction The genus Canis includes six incipient (inter-fertile) species: the dog (C. familiaris), the wolves (C. lupus and C. simensis), coyotes (C. latrans), jackals (C. aureus), and dingoes (C. dingo). There are two other members of the genus, the black-backed jackals (Canis mesomelas) and side-striped jackals (C. adustus) that are more distantly related and probably not interfertile with the others included in our review. We understand that there is an ongoing discussion of the nomenclature and classification of the current members of the genus (see Coppinger et al., 2010, for a review). The members of this genus exhibit reproductive behaviors not commonly found in the Carnivora or even other Canidae. African hunting dogs (Lycaon pictus) and several species of the South Amer˜ ican genus Pseudalopex (Munoz-Donos, pers. com.) are reported to have similar parental behaviors, but they are not inter-fertile with the domestic dog, which is our central concern. We have focused our discussion on differences in seasonality and parental behavior within the genus Canis, noting that the dog is atypical. The worldwide population of C. familiaris is unknown and difficult to calculate. One estimate is that there is approximately 1 dog for every 10 people (Wandeler et al., 1993), resulting in a figure of 700,000,000 dogs worldwide. This ratio varies dramatically regionally and Jackman and Rowan (2007) suggest that it is a relatively conservative figure. Alternatively, if we extrapolate from available calculations for individual countries (Rowan, pers. com.), based on landmass, we reach a figure of 1 billion dogs worldwide. If one assumes that all of the pet dogs in developed countries are restricted they would represent 17–24% of the dogs worldwide

136 136 136 136 136 136 136 136 136 136 136 136 136 136 136 137 137 137 137 137 137 137 137 137 137 137 138 138 139 139 139 139 140 140 140

(Table 1). This is most likely an over-estimation of restricted dogs. A survey by New et al. (2004) suggests that over 50% of litters born to U.S. households are unplanned. Thus, dogs that are not reproductively restrained comprise a naturally breeding population making up as much as 83% of the world’s billion dogs. These dogs are clustered in areas of human waste such as discarded food or food by-products, carcasses, kitchen wastes, fecal material or even corpses (Butller and du Toit, 2002; Daniels and Bekoff, 1989; Oppenheimer and Oppenheimer, 1975; Wandeler et al., 1993; R.C., pers. obs.). In many areas of the world concentrations of 700–1000 or more freely reproducing dogs/km2 are common around dumps, slaughterhouses, fishing ports, markets and other food processing and distributing areas (see Beck, 2000; Hsu et al., 2003; Reece, 2005; WHO, 2004, for examples). There is no evidence to suggest that humans have ever had control over the reproductive behavior of the vast majority of dogs, other than by culling. Consequently, it is plausible to think that any differences in reproductive behavior might be adaptations to a niche created by permanent settlement of humans and its associated waste products (Zeuner, 1963; Tchernov and Valla, 1997; Coppinger and Coppinger, 2001), and not by artificial selection as first claimed by Darwin (1858). In the following sections we review the literature on three general features of reproductive activity in Canis (reproductive seasonality, age of first reproduction, and pair-bonding), and compare three feeding behaviors (nursing, regurgitation, and provisioning). We analyze the low frequency of display of genus-typical behaviors in the dog and postulate that the dog’s reproductive behaviors are an adaptation to permanent human settlement and the waste resources associated with it, an issue that should not

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Table 1 Summary of pet dog population in developed countries. Country United States Canada Europe Australia New Zealand Japan Total

Number of pet dogs 72,114,000 6,070,783 73,643,400 3,405,000 475,072 12,522,000

Source AVMA (2007) Perrin (2009) European Pet Food Industry Federation (2010) Australian Companion Animal Council (2010) Pfeffer and Heath (2010) Nippon Zenyaku Kogyo Co (2008)

168,230,255

be confused with claims about the evolutionary origins of the dog. 2. Reproductive activity 2.1. Seasonality Reproductive seasonality is the tendency for sexual activity, mating and parturition to occur during the same annual period. Reproductive seasons are thought to be the result of changes in the distribution of sunlight effecting photosynthetic production. Parturition tends to be timed to coincide with seasonal blooms of food, which Geist (1998) terms “productivity pulses.” In wild Canis spp., parturition occurs at the beginning of a pulse (Bekoff and Wells, 1986; Bernard and Stuart, 1992; Bryan et al., 2006; Moehlman, 1983, 1986, 1987). Seasonal fluctuations in day length and subsequently production pulses are less exaggerated on the equator than at other latitudes (Geist, 1998). 2.1.1. C. lupus Northern gray wolf males and females become sexually active once a year from December through early April depending on the latitude (Haase, 2000; Mech, 2002). The majority of pups are born in April (March–June) (Asa et al., 1990; Rausch, 1967; Seal et al., 1979). In a given geographic region litters of pups are synchronously born within a week and a half (Harrington et al., 1983), though parturition may vary as much as a month from one year to another in the same area. Mech (2002) indicates that there is a correlation between latitude and whelping, with pups arriving later in higher latitudes. Captive wolves are similarly seasonal (see Fig. 1). 2.1.2. C. simensis Ethiopian wolves breed once a year. We found no reference to male seasonality. The breeding period may vary by as much as four months between particular years, with pups whelping from September through December in Bale Mountain National Park in southern Ethiopia (latitude: 7◦ N). Within a given year pups are born in a 1–3 week period (Sillero-Zubiri et al., 1998). 2.1.3. C. latrans Coyote males and females become sexually active in December and whelp in March through May (Gier, 1968; Gipson et al., 1975; Green et al., 1984; Hamlett, 1938). The coyote reproductive season may vary from year to year. Gier (1968) reported that ovulations in and around Manhattan, KS (latitude: 39◦ 11 N) occurred in a sixweek range from year to year from the beginning of February to mid-March. But within years, ovulations ranged over a four-week period. Gese et al. (1989) reported that 13 of the 16 litters observed during their four-year observation period in Colorado (latitude: 37◦ 10 N) were born within two weeks during April. Carlson and Gese (2008) reported that coyote estrus is synchronized and occurs within a four-week period between mid-January and mid-February in Utah (latitude: 41◦ 68 N). Hamlett (1938) surveyed the reproductive capacity of coyotes from 13 states and found that there was up

Fig. 1. Number of conceptions (A) of domestic dogs – golden retriever and Labrador retrievers (N = 141), (B) captive dingoes (N = 36), and (C) wolves (N = 37) plotted against the length of daylight over the 2008 calendar year. Dog and dingo breeding facilities are located within 50 km of Melbourne, Australia; wolf breeding facility located in Battle Ground, IN.

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to a two-month difference in the beginning of the breeding season between some states, though most began in February. In a few instances, Hamlett found reports of pregnant females still suckling a litter, suggesting the possibility that some coyotes can be seasonally polyestrous. Harrington et al. (1987) reported a single case of a captive female coyote breeding on January 14th and March 22nd of the same year. Given the rarity of these reports, however, it seems exceptional rather than a species-typical trend for seasonal polyestrous cycles. 2.1.4. C. mesomelas Black-backed jackal males and females are seasonal (Bernard and Stuart, 1992; Bingham and Purchase, 2002). Moehlman (1983, 1986), reporting on two populations in Tanzania – Lake Ndutu (latitude: 3◦ S) and the Serengeti Plain (latitude: 2◦ 34 S), found whelping to occur between July and September, coincidental with a boom in the rodent population. Loveridge and Macdonald (2001) found peak mating season in Zimbabwe (latitude: 18◦ 45 S) to be in June and July. Fairall (1968) recorded births over multiple years in Kruger National Park (latitude: 22◦ 25 S–25◦ 32 S) ranging from August to October. Bingham and Purchase (2002) reported that C. mesomelas has a synchronized estrus within a given population. Over an eight-year study, Bothma (1971) found that breeding in the northeastern portion of South Africa (latitude 30◦ 33 S) starts at the beginning of July and ends at the beginning of October. Bernard and Stuart (1992) reported, over a four-year study, that mating in Cape Province (latitude: 33◦ 13 S) was from late May through August. These data suggest that like the gray wolf, C. mesomelas breeding/whelping seasons occur later the further the population is from the equator. 2.1.5. C. aureus The timing of golden jackal births, both in the wild and in captivity, suggests they are seasonal breeders. No reference was found to male seasonality. Pups are born from December to March, during the wet season in Tanzania (latitude: 3◦ S) (Moehlman, 1983) or when ungulates arrive in their habitat (Moehlman, 1986). Zuckerman (1953) reported from the London Zoo (1850–1864 latitude: 51◦ 32 N), births as early as March 13th and as late as April 14th. 2.1.6. C. adustus Side-striped jackal females are seasonal, though we found no data for males (Bingham and Purchase, 2002). Loveridge and Macdonald (2001) found the peak-mating season of C. adustus in the west of Zimbabwe (latitude: 18◦ 45 S) to occur in June and July. Bingham and Purchase (2002) found estrus in northeastern Zimbabwe (latitude: 17◦ 49 S) occurred from the beginning of July to the beginning of August by examining 45 culled females. 2.1.7. C. dingo Dingo males and females are seasonal, producing one litter of pups each year (Catling, 1979; Catling et al., 1992; Jones and Stevens, 1988). Thompson (1992) found that over a nine-year period on the lower Fortescue River in northwestern Australia (21◦ 22 S), pups were born from the middle of May through the middle of August, with more pups being born in July than any other month. He estimated the breeding season to occur from mid-March to early June. Catling et al. (1992) reported that both wild and captive dingoes in Central Australia (25◦ S) bred from March to July. They also reported that captive dingoes in Canberra (35◦ S) bred from April to July. Jones and Stevens (1988) reported in a four-year study that female dingoes in Victoria (37◦ S) were either in estrus or conceived between January and April. Captive dingoes in the London Zoo (latitude: 51◦ 32 N) whelped pups from February through March, and a small subset whelped in October

and November (Zuckerman, 1953). Dingo seasonality varies in response to environmental conditions. Males in hot and arid environments exhibit a true annual cycle while in other habitats males are capable of breeding all year, although there is a sharp seasonal peak in prostate weight, testes weight, and sperm count (Catling et al., 1992; Corbett, 2001; Jones and Stevens, 1988). In periods of drought, testes responded several months later than during flush periods, and for females, uterine weight can be delayed several months (Catling et al., 1992). 2.1.8. C. familiaris Domestic dogs are not seasonal, regardless of whether they are free-living or under direct human control (Boitani et al., 2006; Engle, 1946; Gipson et al., 1975). Females come into estrus every seven months on average (Boitani et al., 2006; Macdonald and Carr, 1995); males are constantly capable of reproducing (Gipson et al., 1975; Haase, 2000). Pups can be born at any time of year (Boitani et al., 2006; Macdonald and Carr, 1995). However, under certain environmental conditions whelping may be concentrated at particular times of the year: free-living pups in India, for example, tend to be born between October through March, during late monsoon season and winter (Chawla and Reece, 2002; Oppenheimer and Oppenheimer, 1975; Pal, 2001). A comparison of seasonality between domestic dogs, captive dingoes located in Melbourne, Australia (37◦ S, 144◦ E) between 1999 and 2008, and captive wolves located in Battle Ground, IN (40.31◦ N, 86.50◦ W) between 1977 and 2012 is presented in Fig. 1 and illustrates the differences between the dog and a wild type under controlled conditions. Dates of conception for litters of domestic dogs (Guide Dogs Victoria), captive dingoes (Dingo Discovery and Research Centre), and captive wolves (Wolf Park), calculated by subtracting 63 days from known date of birth, were plotted against the length of daylight across the calendar year. Differences in seasonality were evident: domestic dog females conceived during all months of the year – they are not seasonal – whereas dingo females only conceived during the period between January and July. Alternatively, wolf females primarily conceived between late January and early March. The general picture of seasonality in wild types with respect to latitude is illustrated in Fig. 2. 2.2. Age of first reproduction The onset of sexual maturity is not a purely genetic characteristic (Fox, 1978; Medjo and Mech, 1976). Estrus is a function of attaining adult body size, physical condition and social synchrony, along with environmental variables. Delayed maturity in all Canis spp. can be a result of poor resource availability (Fuller et al., 2003). 2.2.1. C. lupus Northern gray wolf females breed after they disperse from their natal pack, usually in their second or third year (Mech, 1970; Peterson et al., 1984; Rausch, 1967; Young and Goldman, 1964). In captivity, wolves have bred and produced young in their first year (Medjo and Mech, 1976; Seal et al., 1979). 2.2.2. C. simensis Ethiopian wolves reach sexual maturity at two years (SilleroZubiri et al., 1996). 2.2.3. C. latrans Coyotes are able to breed successfully in their first year. Gier (1968) found that 10–50% of yearling females have pups, but this varies year to year. By the second year a majority of females are

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Fig. 2. Latitude and whelping times in wild Canis.

breeding, but the exact percentage still varies year to year (Gier, 1975; Gipson et al., 1975). 2.2.4. C. mesomelas Black-backed jackals begin breeding in their second year (Bingham and Purchase, 2003; Ferguson et al., 1983). Ferguson et al. (1983) note that black-back jackals have reproduced in their first year when raised in captivity. He also found that some physically mature but underweight animals do not breed in their second year. 2.2.5. C. aureus Golden jackals have been observed to breed in their first year, but those that stay with their parents delayed breeding for a year or two (Moehlman, 1983, 1987; van Lawick-Goodall and van LawickGoodall, 1970). 2.2.6. C. adustus Side-striped jackals will breed at one year of age (Bingham and Purchase, 2003). However, data are limited and this may vary with food availability. 2.2.7. C. dingo Dingoes can reproduce in their first year in flush conditions, but most do not bear pups until they are two years of age (Breckwoldt, 1988; Catling et al., 1992; Jones and Stevens, 1988). Jones and Stevens (1988) reported that estrus was variable, occurring between one and four years of age, with only 36% of females and 63% of males breeding before two years, while 97% of males over three years old reproduced.

2.2.8. C. familiaris Studies on free-living animals report that male and female dogs breed in their first year (Boitani et al., 1995; Ghosh et al., 1984/85; Wandeler et al., 1993). However, ‘restricted dogs’ vary greatly according to size. Small female house dogs 8–15 kg often come into season at seven months after birth, while large females 30–40 kg may not come into season for a year and a half.

2.3. Pair bonding Pair-bonded wild Canis may share territories year round, and defend their territory cooperatively. Males display aggression toward unfamiliar males, and females toward unfamiliar females. Canis spp. breeding pairs care for offspring (Carter and Keverne, 2002; Kleiman, 1977; Sillero-Zubiri et al., 1996). Monogamy – exclusive mating between pair-bonded individuals – is rare in mammals but may be characteristic of wild members of the genus Canis (Kleiman, 1977). The necessary genetic studies have not been conducted for most members of the genus Canis to confirm the exclusivity of pairs, but there is data to support at least social (or behavioral) monogamy in wild Canis spp.

2.3.1. C. lupus Wolves exhibit long-term pair bonding (Kleiman and Eisenberg, 1973; Macdonald and Moehlman, 1982; Mech, 1970); there are, however, some rare reported cases of polygyny (Mech and Nelson, 1989). Mated pairs maintain a shared territory (Harrington and Asa, 2003) and both parents raise the young (Ballard et al., 1991; Fentress and Ryon, 1982; Harrington and Mech, 1982; Mech et al.,

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1999; Mech, 1970; Packard, 2003; Paquet et al., 1982; Young and Goldman, 1964). 2.3.2. C. simensis Ethiopian wolves form pair bonds, but genetic data have shown that extra-pair copulations do occur. Sillero-Zubiri et al. (1996) found that alpha females mated with the alpha male in her pack as well as males from other packs. Alpha females rebuffed mating attempts from all but the alpha male within their own pack. It is common for both males and females to remain with their natal pack, with offspring inheriting their parents’ positions in the pack (Sillero-Zubiri et al., 1996). 2.3.3. C. latrans Coyotes form long-term pair bonds and are genetically monogamous (Andelt et al., 1979; Andelt, 1985; Bromley and Gese, 2001; Carlson and Gese, 2008; Hennessy et al., 2012). Pairs share resources (Andelt et al., 1979; Andelt, 1985; Bekoff and Wells, 1986; Bromley and Gese, 2001) and defend territories (Camenzind, 1978; Gese, 2004). Both coyote parents care for young (Andelt, 1985; Andelt et al., 1979; Camenzind, 1978; Mengel, 1971; Silver and Silver, 1969; Way et al., 2001) And, recent genetic research has confirmed the exclusivity of mated pairs (Hennessy et al., 2012). 2.3.4. C. mesomelas Black-backed jackals form lifelong pair bonds (Moehlman, 1980, 1987). Pairs occupy the same territory and defend it from intruders (Moehlman, 1979, 1980, 1983; Wyman, 1967). Moehlman (1987) observed that territories marked by only the male or female of a pair were not effective in keeping away intruders. Members of mated pairs are highly aggressive toward members of the same sex, guarding their mates from members of the opposite sex (Moehlman, 1987). They also exhibit affiliative behaviors such as food sharing and mutual grooming (Moehlman, 1983). Both parents are involved in care for young (Rowe-Rowe, 1982; Moehlman, 1979). 2.3.5. C. aureus Golden jackals generally form long-term pair bonds, though they have occasionally been observed to switch mates (Moehlman, 1987). Pairs protect a mutual territory through tandem pair marking (Kleiman, 1977). Both members of the mated pair care for young (van Lawick-Goodall and van Lawick-Goodall, 1970; Moehlman, 1986). They also demonstrate affiliative behavior such as social grooming (Golani and Keller, 1975; van Lawick-Goodall and van Lawick-Goodall, 1970). 2.3.6. C. adustus Side-striped jackals form long-term pair bonds (Bingham and Purchase, 2002). Pairs stay in relatively close contact (less than 200 m) throughout the year and both care for young (Atkinson et al., 2002; Carter and Keverne, 2002; Kleiman, 1977; Loveridge and Macdonald, 2001). 2.3.7. C. dingo Dingoes form long-term pair bonds, defend shared territories and cooperatively care for young (Corbett, 2001; Corbett and Newsome, 1975; Thompson, 1992, 1992b). 2.3.8. C. familiaris Domestic dogs do not form pair bonds. Free-living females may show a preference for particular males over others, but they are promiscuous (Daniels, 1983; Ghosh et al., 1984/85). Males occasionally stay in the same general locale as females after copulation (Pal, 2005; Boitani et al., 1995), but this is most likely a function of shared resource availability (Boitani et al., 1995). Males

do not guard females for exclusive reproductive access; temporary social groupings of males around females in heat are usual (Daniels, 1983; Fox, 1978; Ghosh et al., 1984/85; Oppenheimer and Oppenheimer, 1975). Males do not assist females with the rearing of young (Boitani et al., 1995; Macdonald and Carr, 1995; Nesbitt, 1975). 3. Parental feeding behavior 3.1. Nursing Parental feeding in Canis spp. begins with nursing by the mother (allonursing by other females does occur, but it is rare). Nursing is a diagnostic feature of Mammalia. Neonates are born exhibiting a stereotypic sequence of nursing motor patterns (Fuller and Dubois, 1962; Hall and Williams, 1983; Levy, 1934; Scott, 1963). Suckling bouts are terminated by the nursing female, as satiation does not terminate suckling behavior (Hall and Williams, 1983). Nursing is energetically expensive, but suckling provides food with low energy expenditure for pups. Weaning can vary within a species depending on the nutritional state of the female. 3.1.1. C. lupus Gray wolf pups are reported to be weaned between 5 and 10 weeks of age (Hayssen et al., 1993; Packard, 2003; Young and Goldman, 1964). There are rare cases of communal denning (including allonursing) by wolves both in the wild (Mech, 1970; Packard, 2003) and in captivity (Paquet et al., 1982) when more than one female has a litter. 3.1.2. C. simensis Ethiopian wolf pups are reported to stop nursing entirely at 10 weeks (Sillero-Zubiri et al., 2004). Sillero-Zubiri et al. observed 20 litters, 8 of which had females other than the mother nursing pups (in at least two of the 8 cases, the allonursing females had lost their own litters). 3.1.3. C. latrans Coyotes have been observed to wean pups from 6 to 16 weeks (Bekoff and Wells, 1986; Gier, 1975; Silver and Silver, 1969). Gier (1975) reported that about 10% of the litters he observed consisted of two age groups in the same den, which may account for the apparently long nursing period. 3.1.4. C. mesomelas Black-backed jackals wean their young between 8 and 9 weeks (Moehlman, 1979, 1986). Ferguson et al. (1983) reported two cases of communal denning. 3.1.5. C. aureus Weaning in golden jackals occurs between 8 and 9 weeks (van Lawick-Goodall and van Lawick-Goodall, 1970; Moehlman, 1986). We found no reports of allonursing in golden jackals. 3.1.6. C. adustus Side-striped jackal pups are weaned at between 8 and 10 weeks (Ginsberg and Macdonald, 1990). We were unable to find any references to allonursing in this species. 3.1.7. C. dingo Dingo pups are nursed for 7–10 weeks (Breckwoldt, 1988; Thompson, 1992). Allonursing has been observed in a wild population in central Australia, where two females had dens within 20 m of each other, and one was observed feeding four of her own pups and two of her neighbours’ (Green and Catling, 1977). Allonursing

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has been seen in a captive C. dingo colony (Corbett, 1988), where a subordinate female continued to nurse after her pups were killed. 3.1.8. C. familiaris Dog mothers nurse their young for 5–10 weeks (Martins, 1949; Pal, 2008, 2005; Scott and Fuller, 1965). Although uncommon, allonursing has been occasionally observed in dogs; Pal (2005) reports two breeding females with adjacent dens nursing each other’s pups. Daniels and Bekoff (1989) reported a similar observation of two females giving birth in the same den. 3.2. Regurgitation and provisioning Canis spp. regularly regurgitate partly digested food to their offspring, a rare phenomenon in the order Carnivora. Most Canis adults will regurgitate when a pup gives the appropriate begging signal. The young of most Carnivore species including Canis are also provisioned with chunks of meat from large prey or whole small prey items. Canis spp. pups will follow parents to food. 3.2.1. C. lupus Adult wolves begin to regurgitate to pups between 4 weeks (Mech, 1970) and 6 weeks of age (Packard et al., 1992). The breeding male and female and helpers (usually siblings from previous years) regurgitate to pups (Fentress and Ryon, 1982; Harrington and Mech, 1982; Mech, 1970; Mech et al., 1999; Packard, 2003; Paquet et al., 1982). Wolf pups receive approximately two regurgitations a day (Fentress and Ryon, 1982; Packard, 2003; Paquet et al., 1982), although rates as low as 0.67 feedings a day (five a week, both regurgitation and provisioned food) have been recorded in captivity (Fentress and Ryon, 1982). Pups begin to eat pieces of meat brought to them by pack members at 6 weeks (Packard et al., 1992). Packard et al. (1992) reported that by 8 weeks, in addition to regurgitations, pups were provisioned with an arctic hare/day. Pups follow the pack to kills beginning at 10 weeks (Packard et al., 1992; Packard, 2003). While capable of foraging on their own, pups as old as a year have been observed receiving regurgitations from their parents (Fentress and Ryon, 1982; Harrington and Mech, 1982; Mech, 1995; Mech et al., 1999). 3.2.2. C. simensis Regurgitations and provisioning of pups with small rodents begin at 5 weeks (Sillero-Zubiri et al., 2004). Individual members of the pack provisioned and regurgitated to 6-month-old pups, and occasionally to yearlings (Sillero-Zubiri et al., 2004). On average the female feeds pups (whole rodents or regurgitations) twice as often (0.12 times) per hour as the male. Male and female helpers were also observed feeding pups between 0.03 and 0.06 times per hour (Sillero-Zubiri et al., 2004). 3.2.3. C. latrans Coyotes begin to regurgitate to pups between the second and third week (Gier, 1975; Silver and Silver, 1969). The lactating female, her mate, and often helpers, regurgitate to pups (Andelt et al., 1979; Gier, 1975; Silver and Silver, 1969; Way et al., 2001). References for the rates of regurgitation in C. latrans were lacking. Provisioning of pups with small carcasses begins at 4–6 weeks (Gier, 1975). Gier (1975) reports that by 3 or 3.5 months pups are fed entirely with small carcasses or pieces of larger carcasses, and no longer receive regurgitations. In the wild, the parents and helpers feed pups until 3–5 months (Harrison and Harrison, 1984; Harrison et al., 1991). It is unclear whether this food is regurgitated or carried, as these studies are based on scat and radio collar data.

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3.2.4. C. mesomelas Black-backed jackal parents and helpers regurgitate to pups (Moehlman, 1979; Rowe-Rowe, 1982) beginning at 3 weeks (Moehlman, 1986). Mated pairs feed their pups 0.318 times per hour, or 53 times per week (Moehlman, 1986). Pups are reliant on parental feeding until 14 weeks (Moehlman, 1979, 1986) at which point they begin to forage for themselves on small prey and fruit. Early foraging activity is supplemented by parental feeding through 8 months (Moehlman, 1986). Helpers beyond their first year occasionally receive food from other adults (Moehlman, 1986). 3.2.5. C. aureus Golden jackals begin to regurgitate to pups at 3–4 weeks (van Lawick-Goodall and van Lawick-Goodall, 1970) at an average rate of approximately once every 2 h until 14 weeks (Moehlman, 1986). Direct provisioning does not appear to be a common strategy. van Lawick-Goodall and van Lawick-Goodall (1970) note that on the infrequent occasions when golden jackals carried meat to pups, this incited other scavengers to attempt to steal the food – a situation avoided by eating and then regurgitating food to pups. They also observed that the first time pups were brought a large piece of meat (back leg of a gazelle) was at 10 weeks. 3.2.6. C. adustus Loveridge and Macdonald (2001) suggest that parents and helpers feed pups; however, this species is fairly cryptic and difficult to observe, and the authors did not report how pups were fed. Atkinson and Loveridge (2004) reported that parents regurgitated to pups every 2–3 h overnight, but this seems to be inferred from black-backed jackals, as they cite Moehlman (1979). No reports were found on how long feeding persists. 3.2.7. C. dingo Dingo parents and non-breeding helpers regurgitate to pups (Corbett and Newsome, 1975; Thompson, 1992) beginning at 15 days (Breckwoldt, 1988). No rates of regurgitation have been reported for dingoes. Pups receive regurgitations as late as 8 weeks. While no age is given, Thompson (1992) observed adult pack members provisioning pups with large food items such as kangaroo legs. Similarly, Corbett and Newsome (1975) reported female adults bringing pups a rabbit a day, although the ages this occurred are not given. Pups follow the pack to kills starting at 9 weeks; pups as old as 20 weeks have been observed being fed (Corbett and Newsome, 1975; Thompson, 1992). 3.2.8. C. familiaris Regurgitation by adult dogs to pups is reported, but it is rare to see pups being regularly fed in this manner. Malm (1995) reported that 43% of 131 dog breeders, randomly polled, observed a mother regurgitate to young on at least one occasion. Only 3% observed a male regurgitating to pups on at least one occasion, and 19% saw a dog other than the parents regurgitate to pups. Pal (2005) reported that among free-living dogs in and around dumps in India, mothers regurgitated to pups from 6 to 10 weeks of age, 5 times per week. He also observed one incident of a male regurgitating to pups over the course of 10 days starting when the pups were 9 weeks old. One study reports on two female dogs provisioning their suckling pups with meat-covered bones (part of the mother’s diet) in the laboratory (Martins, 1949). 4. Discussion Unrestricted domestic dogs differ significantly from other members of the genus Canis in both the quality and frequency of their reproductive and parental behaviors (Table 2). Of the six reproductive and care-giving categories we reviewed, dogs resemble other

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Table 2 Summary of differences in reproductive cycling and parental care behavior in Canis spp. Species

Seasonal

Pair bonding

Regurgitation

Provisioning

Independence

C. familiaris C. lupus C. simensis C. latrans C. mesomelas C. aureus C. adustus C. dingo

N Y Y Y Y Y Y Y

N Y Y Y Y Y Y Y

N (rare) Y Y Y Y Y Y Y

N (rare) Y Y Y Y Y Y Y

10–11 weeksa,b 5–8 monthsc,d 6 monthse 4–5 monthsf,g,h 8 monthsi 8 monthsi 6–8 monthsj 3–6 monthsk,l,m

a b c d e f g h i j k l m

Macdonald and Carr (1995). Pal (2008). Mech and Boitani (2003). Pulliainen (1965). Sillero-Zubiri et al. (2004). Harrison and Harrison (1984). Harrison et al. (1991). Harrison and Gilbert (1985). Moehlman (1986). Ginsberg and Macdonald (1990). Corbett and Newsome (1975). Corbett (2001). Thompson (1992).

Canis spp. only in age of reproductive activity, nursing behavior and weaning age. It is remarkable that this recently derived member of the genus Canis does not exhibit seasonality, pair-bonding, regurgitation or provisioning of pups by males or helpers, and only rarely and sporadically engage in parental regurgitation or provisioning. 4.1. Seasonality It has been suggested that loss of seasonality in the domestic dog has resulted either from a lack of selective pressure encountered in the domestic environment (i.e. people directly provide shelter and food) (Haase, 2000; Packard et al., 1985), or from direct artificial selection for increased fecundity (Boitani et al., 2006; Fox, 1978; Malm, 1995; Martins, 1949). We argue that natural selection has favored the loss of seasonal reproductive behavior as an adaptation to continuous availability of human refuse – a reliable food source that is less dependent on seasonal variations in sun, water, or other yearly environmental cycles. In contrast to wild Canis, the food supply of dogs does not occur in seasonal pulses. Unrestricted dog populations scavenge from humans who have long-term food storage capabilities and tend to discard waste uniformly over a year (Medina, 2007). Peri-equatorial villages tend to have reliable and continuous food supplies, including kitchen wastes and fecal materials, as do city dumps and slaughterhouse and food processing areas. That does not imply that waste food is unlimited or that there are not regional and seasonal effects on human waste in higher latitudes, as well as effects of migratory and nomadic cultural patterns. Drought, human starvation and pestilence will obviously have effects on a dog population, which is behaving in an obligatory symbiotic way with humans. Titcomb (1969) reports people eating dogs in response to such conditions. Seasonal uniformity in the availability of human waste products does not suggest that the actual quantities of available waste in a given year are not a limiting variable. The total population of dogs, like any other species, is limited by quantity and quality of the resource. But the lack of a seasonal food pulse favors continuous reproduction such that growing pups do not compete for limited resources with the entire yearly crop of offspring. In addition, survival of young is always dependent on the limits of food resources and population density. Thus, reproduction uniformly distributed over time allows dogs a rapid recovery from both density-dependent and density-independent mortality.

In most of the wild species between-year variation in reproductive timing is greater than within-year variation. This suggests that day length may not be the primary signal for ovulation. The onset of sexual behavior in wolves is later in more northerly latitudes in spite of the fact that day-length increases more rapidly at higher latitudes. Dingoes appear to be more sexually responsive as daylight shortens. Clearly there must be some signal for reproductive onset other than day-length. In the same vein, equatorial latitudes have considerably less variation in the annual light cycle than higher latitudes, resulting in a less dramatic photosynthetic pulse and consequent impact on reproductive activity. Nevertheless the equatorial species C. aureus and C. simensis are seasonal although they do not appear to respond to increasing daylight. Several authors (Oppenheimer and Oppenheimer, 1975; Pal, 2008; Totton, 2009) note that unrestricted dogs in India are reactive to seasonal ‘pulses’ such as rainy seasons or changes in distribution of the prey base. Some such synchronizing factor may be generally responsible for seasonality in Canis, but at present it is unclear what this may be. Dogs are a-seasonal and are often described as diestrous. They can indeed have two estrus periods a year, roughly six months apart; however, the limited literature suggests that on average freeliving dogs come into estrus every 7 months (Boitani et al., 1995). Given that this varies from 6 to 12 months between individuals, and the cycles of individuals can vary by several months (Boitani et al., 1995; Macdonald and Carr, 1995), it is likely that the timing of estrus periods is largely dependent on how fast the female can regain body weight and fat to recycle. Under the best of circumstances dogs are capable of whelping 2 litters in a 12-month period, but wild Canis are not. Furthermore, if conditions are poor, wild Canis spp. may miss an entire breeding season. 4.2. Reproductive age and size Unlike the wild Canis spp., dogs can come into estrus whenever they reach mature body weight and do not have to wait for the next breeding season. While numerous descriptions of restricted dogs assert that the domestic dog is the most variable canid species in size, unrestricted dogs tend to be uniformly medium-sized (see Ortolani et al., 2009; Totton, 2009, for examples). There is some clinal variation, but populations are strikingly consistent. This size uniformity in free-living populations worldwide suggests natural selection. Unrestricted dogs can attain sufficient size and often become reproductively active within their first year.

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Seasonality also plays an important role in reproductive age. In every Canis spp. other than the dog, the first possible reproductive season of their lives occurs when they are approximately 10 months of age. If these animals have not yet attained a sufficient size to reproduce, they have to wait another year to become reproductive. Of the eight species we have discussed, only the dog and the side-striped jackal are claimed to regularly reproduce in their first year. Most species vary on reproductive onset depending on food availability (e.g. C. latrans) or in the case of wolves, which are a relatively large species, rarely reach sufficient size until their second breeding season at 22 months. Territoriality also contributes to the reproductive age of wild Canis spp. Young animals must not only be physically capable of breeding, but also must establish a territory which is dependent on the age structure of the population and the saturation of the niche. The non-territorial and promiscuous dog, by contrast, can reproduce as soon as it is physically capable in the same dump it was born in. Given the lack of seasonality and its ability to reproduce earlier, it is easy to see why dogs would have relatively high fecundity (Reece et al., 2008). 4.3. Pair bonding The selective advantage of pair bonding for females is clearly a function of the help provided by the male in protecting territory and food sources, along with male care-giving behaviors being directed to her pups. Lactation and puppy care are energetically expensive (Greco, 2009; Oftedal and Gittleman, 1989; Ontko and Phillips, 1958). Several observers note that females often either do not participate in feeding pups or have greatly reduced post-nursing behaviors, which presumably allows them to regain reproductive readiness more quickly (Fuller et al., 2003; Oftedal and Gittleman, 1989). Care-giving behaviors are energetically expensive for the bonded male as well, and are only a selective advantage if they are displayed to its own pups. Therefore, same-sex territorial defense limits the chances of extra pair copulations and increases the likelihood of monogamy for wild Canis spp. We found no references suggesting that dogs pair-bond. We also found no references to parents directly feeding pups after the tenth week. Dog pups, unlike their wild counterparts, do not need to hunt and kill their food, and have the capacity to forage on their own at 10 weeks (Macdonald and Carr, 1995; Pal, 2008). This early independence decreases the necessity of energetically expensive parental care-giving behaviors. Both male and female dogs are sexually promiscuous and litters can have more than one father. The selective advantage for the female rests in increasing the genetic variation within her litters; for males it increases their reproductive access and variation among their offspring. 4.4. Nursing Nursing of pups is similar for all the species in the genus, including the dog. The onset of nursing is at birth, and the offset occurs some four to ten weeks postpartum. Allonursing has been reported in all species of the genus except C. aureus and C. adustus. We are inclined to interpret allonursing and communal denning as byproducts of circumstances where females have had litters in close proximity, or where mothers have lost a litter but continue to be disposed to allow suckling. We found no data that suggest that allonursing improves puppy survival in any Canis spp. 4.5. Regurgitation and provisioning Regurgitation to and provisioning of offspring by the pairbonded males and helpers is a trait that is characteristic of all species within the genus Canis – except the dog. In wild Canis spp.

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the pair-bonded male and female and helpers, whether they are related or not, regurgitate partly digested food to puppies. This behavior is elicited by puppy begging behaviors and continues for months. For a behavior that is (almost) unique to Canis, it is somewhat surprising that there have been so few studies attempting to measure the benefit to wild populations. Among domestic dogs, reports of either male or female dogs regurgitating to pups are exceedingly rare, and we found no reports of this behavior after weaning (Martins, 1949; Pal, 2008). After weaning, dog pups are independent of parenting and must compete with adults as well as other juveniles for available food. Helpers are common in all the wild species of Canis but not in the dog. Helpers are animals other than members of the bonded pair, which regurgitate and provision puppies. Helpers are most often the young from a previous season, although unrelated animals have been observed regurgitating to pups. Adult wolves that were hand-raised in captivity will spontaneously regurgitate to unrelated begging pups (Fentress and Ryon, 1982; K.L., pers. obs.), further suggesting that the behaviors of regurgitation and begging are innate motor patterns. Moehlman (1979) argued that jackal helpers contribute to the inclusive fitness of closely related litters. She also claims that C. mesomelas helpers increased the overall number of surviving pups by 1.5 on average. Alternatively, it has been argued (Macdonald et al., 2004) that resource availability governs helper behavior. He observed that territory size in carnivores is based on the availability of prey, which is unevenly distributed. A reproductive pair of carnivores will defend the smallest territory possible that will provide enough food for them and their offspring to survive. When this smallest defensible territory has more than enough food for the pair, it is beneficial for young to remain in the territory rather than disperse. Offspring from previous seasons will regurgitate to younger siblings. In lean years, however, helpers do not regurgitate and instead will steal food from pups (Ballard et al., 1991; Harrington and Mech, 1982). When food is plentiful, pup survival is improved or unaffected by the presence of helpers (Ballard et al., 1987; Mech et al., 1999; Moehlman, 1979; Peterson et al., 1984). But when food is scarce, survival of pups is negatively impacted by the presence of offspring from prior years (Bekoff and Wells, 1986; Harrington and Mech, 1982). Helping behavior has not been reported for dogs.

4.6. Population implications C. familiaris no longer displays the typical seasonal reproductive pattern of the genus Canis as well as parental feeding behaviors associated with pair-bonding, regurgitation and provisioning. The reduced of display of these genus-typical behaviors by dogs is regularly assumed to be maladaptive. We might expect it to reduce survivorship in any given litter (Packard et al., 1985; Haase, 2000; Daniels, 1983; Martins, 1949; Malm, 1995; Boitani et al., 2006; Fox, 1978). However, weaned dog pups are able to feed themselves: the waste niche is continuously available and food within this niche, although limited, does not require adult hunting behavior to obtain it. Therefore dogs can produce a large number of puppies annually, evenly distributed over the year at reduced parental energetic expense. Since neither parent is investing in long-term energetically expensive care-giving behavior, they can redirect that energy into continuous production, which leads to higher fecundity. The wild types have all their pups in the same seasonal period. Wild pups are not capable of efficiently caring for themselves until they reach the adult adaptive size and shape, which can be as much as two years or more depending on conditions. Dogs occupy a niche which allows juveniles to be independent of parents at a much earlier age.

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In stable populations high fecundity generally leads to higher pup mortality, especially in post-weanlings which are competing with adults for limited resources (see Ortolani et al., 2009; Totton, 2009 for a discussion of population structures). This results in skewing the population toward nursing pups and adult dogs (Ruiz-Izaguirre and Eilers, 2012). The higher rate of juvenile mortality has been misinterpreted as an inability of dogs to maintain their numbers without recruitment (Beck, 1973; Daniels, 1983). Dog populations living in marginal areas (sink populations) may be sustained by recruitment (Boitani et al., 1995; Daniels and Bekoff, 1989; Macdonald and Carr, 1995). If, however, the average age of the adult is four years, then a 5–8% pup survival to reproductive age is enough to sustain the population. Moreover, when adult populations oscillate dramatically, the increased fecundity and lack of seasonality would allow for a more rapid replacement. 5. Conclusion We have reviewed the literature on three general features of reproductive activity in the genus Canis (reproductive seasonality, age of first reproduction, and pair-bonding), and compare three parental feeding behaviors (nursing, regurgitation, and provisioning). The domestic dog is a-typical in that it is not seasonal, females tend to breed at a younger age, and they do not pair-bond but rather both males and females are promiscuous. Dogs typically nurse pups but rarely regurgitate, or provision them. Parental care ends after weaning. A number of authors have concluded that the reduction of genus-typical reproductive behaviors of dogs was the result of “relaxed selection” because of direct care and protection by humans or was the result of direct selection by humans for an increase in fecundity (Boitani et al., 2006; Fox, 1978; Haase, 2000; Malm, 1995; Martins, 1949; Packard et al., 1985). Alternatively, we suggest that the low frequency of these behaviors is an adaptation to a new niche, created by permanent settlement and stationary human refuse. This waste niche releases dogs from the high transportation and acquisition cost of finding and processing live prey typical of other members of the genus. The relative ease of finding and processing food year round makes extended parental care and seasonality maladaptive. Reducing parental care and breeding multiple times/year increases their fecundity. The increase in fecundity has the consequence of an increased juvenile mortality when population levels reach carrying capacity. However, dogs are better able to refill the niche after density-dependent and density-independent increases in mortality. Thus, we suggest free-living dogs are a self-sustaining population adapted to survive on human refuse, and the 83% of this planet’s dogs living in this niche seem to be doing very well. Acknowledgments Thanks to Lyn Watson at the Dingo Discovery and Research Centre, Toolern Vale, Victoria, Australia; Guide Dogs Victoria, Victoria, Australia; and Patricia Goodman at Wolf Park, Battle Ground IN, for providing us with birth records. Thanks also to Lorna Coppinger for editorial revision; and Bret Bard, Tracey Butchart, David Macdonald, Ramon Escobedo Martinez, Elise McMahon, Lynn Miller, Christian ˜ Munoz-Donos, Andrew Rowan, Claudio Sillero-Zubiri and Michael Sutherland for help and discussion on many points. References American Veterinary Medical Association, 2007. U.S. Pet Ownership and Demographics Sourcebook. Author, Washington, DC. Andelt, W.F., 1985. Behavioral ecology of coyotes in south Texas. Wildl. Monogr. 94, 3–45.

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