The Social Dog. Behavior and Cognition

402 Pages·2014·17.531 MB·English

by  Juliane Kaminski and Sarah Marshall-Pescini (Auth.)

The Social Dog
Behaviour and Cognition
Edited by
Juliane Kaminski
Psychology Department, University of Portsmouth, Portsmouth, UK
Sarah Marshall-Pescini
Dipartimento di Fisiopatologia Medico-Chirurgica e dei Trapianti,
Sezione di Neuroscienze, Università degli Studi di Milano, Milan, Italy
Comparative Cognition, Messerli Research Institute, University of
Veterinary Medicine, University of Vienna, Vienna, Austria
Wolf Science Centre, Ernstbrunn, Austria
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Preface
The domestic dog seems to be the new star in behavioural research. Forgotten
for some time, it has been rising again in the past two decades. Research on dog
behaviour and cognition has exploded, with so many papers being published
that it is hard to keep track. There are probably many reasons why research
with dogs has increased so substantially, one being that several researchers have
raised the hypothesis that dogs might have evolved specialized social skills as
a result of living with humans and adapting to the human environment. This
hypothesis has sparked the interest of both the scientific community and a wider
audience, reflected in many of the contributions to this volume.
The main purpose of this book is to summarize the growing body of research
on dogs’ social behaviour and cognition, as well as to highlight some of the con-
troversial issues and open questions still needing answers. The intention is to
make this exciting new field more accessible to scholars from both similar and
different fields, to students, and to dog specialists whose practical work with
dogs is informed by the research highlighted throughout the book. Our empha-
sis, reflected in the organization of this volume, has been to draw the reader’s
attention both to studies focusing on dog-to-dog social interactions as well as
those directed at a deeper understanding of the dog-to-human relationship, since
we think both are necessary to gain a more complete understanding of dogs.
This project was endorsed enthusiastically by both the publishers and
the many scientists who have contributed to the book. Indeed, we combine
13 original contributions, from 27 authors and co-authors, from many disci-
plines including biology, veterinary science, and psychology. The diversity of
the authors’ scientific backgrounds allows the reader to gain ‘a feel’ for how
dogs are being studied, from many different perspectives. Each contribution is
a review of a particular topic pertaining to dogs’ social behaviour and/or cogni-
tion and is written to stand alone. However, each chapter is also a ‘slice of the
cake’, and as a whole the result is an interdisciplinary book that provides an
overview of progress in understanding many aspects of dogs’ social behaviour
and cognition.
Juliane Kaminski
Sarah Marshall-Pescini
xi
Contributors
Roberto Bonanni Department of Neuroscience, University of Parma, Italy
Juliane Bräuer Max Planck Institute for Evolutionary Anthropology, Leipzig,
Germany
Oliver Burman University of Lincoln, Riseholme Park, Lincoln, UK
Simona Cafazzo Wolf Science Center, Ernstbrunn, Austria
Juliane Kaminski Psychology Department, University of Portsmouth,
Portsmouth, UK
Anna Kis Institute of Cognitive Neuroscience and Psychology, Research Centre
for Natural Sciences, Hungarian Academy of Sciences, Budapest, Hungary;
Department of Ethology, Eötvös University, Budapest, Hungary
Enikő Kubinyi Department of Ethology, Eötvös University, Budapest, Hungary
Sarah Marshall-Pescini Comparative Cognition, Messerli Research Institute,
University of Veterinary Medicine, University of Vienna, Vienna, Austria; Wolf Sci-
ence Centre, Ernstbrunn, Austria; Dipartimento di Fisiopatologia Medico-C hirurgica
e dei Trapianti, Sezione di Neuroscienze, Università degli Studi di Milano
Karen McComb School of Psychology, University of Sussex, Falmer, UK
Ádám Miklósi Department of Ethology, Eötvös University, Budapest, Hungary
Daniel Mills Animal Behaviour Cognition and Welfare Group, School of Life
Sciences, University of Lincoln, Riseholme Park, Lincoln, UK
Katalin Oláh Institute of Cognitive Neuroscience and Psychology, Research Centre
for Natural Sciences, Hungarian Academy of Sciences, Budapest, Hungary;
Department of Cognitive Psychology, Eötvös University, Budapest, Hungary
Péter Pongrácz Department of Ethology, Biological Institute, Eötvös Loránd
University, Budapest, Hungary
Emanuela Prato Previde Dipartimento di Fisiopatologia Medico-Chirurgica e
dei Trapianti, Sezione di Neuroscienze, Università degli Studi di Milano, Segrate,
Italy
Angelo Quaranta Department of Veterinary Medicine, Section of Behavioural
Sciences and Animal Bioethics, University of Bari ‘Aldo Moro’, Italy
Friederike Range Comparative Cognition, Messerli Research Institute, University
of Veterinary Medicine, Vienna, Austria; Medical University of Vienna, Vienna,
Austria; University of Vienna, Vienna, Austria; Wolf Science Centre, Ernstbrunn,
Austria
Victoria Frances Ratcliffe School of Psychology, University of Sussex, Falmer, UK
David Reby School of Psychology, University of Sussex, Falmer, UK
xiii
xiv Contributors
Marcello Siniscalchi Department of Veterinary Medicine, Section of Behavioural
Sciences and Animal Bioethics, University of Bari ‘Aldo Moro’, Italy
Barbara Smuts Department of Psychology, University of Michigan, Ann Arbor, MI,
USA
Anna Magdalena Taylor School of Psychology, University of Sussex, Falmer, UK
József Topál Institute of Cognitive Neuroscience and Psychology, Research Centre
for Natural Sciences, Hungarian Academy of Sciences, Budapest, Hungary
Borbála Turcsán Department of Ethology, Eötvös University, Budapest, Hungary
Paola Valsecchi Dipartimento di Neuroscienze, Università degli Studi di Parma,
Parma, Italy
Emile van der Zee School of Psychology, University of Lincoln, Brayford Pool,
Lincoln, UK
Zsófia Virányi Comparative Cognition, Messerli Research Institute, University
of Veterinary Medicine, Vienna, Austria; Medical University of Vienna, Vienna,
Austria; University of Vienna, Vienna, Austria; Wolf Science Centre, Ernstbrunn,
Austria
Helen Zulch Animal Behaviour Cognition and Welfare Group, School of Life
Sciences, University of Lincoln, Riseholme Park, Lincoln, UK
Chapter 1
The Social Dog: History and
Evolution
Sarah Marshall-Pescini1,2,3 and Juliane Kaminski4
1Dipartimento di Fisiopatologia Medico-Chirurgica e dei Trapianti, Sezione di Neuroscienze,
Università degli Studi di Milano, Milan, Italy, 2Comparative Cognition, Messerli Research
Institute, University of Veterinary Medicine, University of Vienna, Vienna, Austria, 3Wolf Science
Centre, Ernstbrunn, Austria, 4Psychology Department, University of Portsmouth, Portsmouth, UK
1.1 WHERE DO DOGS’ SOCIALITY AND SOCIO-COGNITIVE
ABILITIES COME FROM? THE CANID STORY
The explosion of studies on dogs’ social behaviour and cognitive abilities since
the turn of the twenty-first century has been impressive (see Bensky et al., 2013,
for a comprehensive review), and the many hypotheses as to the causes behind
dog’s remarkable socio-cognitive abilities have engendered lively debates in
journals and at conferences. However, most debates revolve around the wolf–
dog comparison (the wolf being dog’s closest living relative), neglecting the fact
that the dog’s canine family is much larger and shows some unique and intrigu-
ing features that may well have played a role in allowing dogs’ emergence as our
favoured social companions. Hence, in the first part of this chapter, we intro-
duce dogs’ canine family, presenting some of these intriguing social features
and highlighting some of the characteristics that may have played a fundamen-
tal role in allowing the emergence of one species’ unique history with humans.
1.1.1 Introducing Dogs’ ‘Canine’ Family
The domestic dog belongs to the Canidae family, consisting of 35 related species
that diverged within the last ten million years (Wayne et al., 1997; Ostrander &
Wayne, 2005). In recent years, there has been considerable interest in the evolu-
tionary relationships between canids that has resulted in analyses based on both
morphological (Berta, 1987; Tedford et al., 1995; Lyras & Van Der Geer, 2003;
Zrzavý & Řičánková, 2004) and molecular data (Wayne et al., 1987; Wayne
et al., 1989), including, more recently, DNA sequencing (Wayne et al., 1997;
Bardeleben et al., 2005; Linblad-Toh et al., 2005; Wong et al., 2010). The devel-
opment of methodologies for the sequencing of DNA has allowed researchers to
The Social Dog. http://dx.doi.org/10.1016/B978-0-12-407818-5.00001-2
Copyright © 2014 Elsevier Inc. All rights reserved. 3
4 SECTION | I Theoretical Aspects
reconstruct the dog’s family tree, with a certain amount of accuracy (although a
few grey areas still exist).
Taken together, current results converge in showing three major groupings
within the dog’s family: (1) the red fox–like canids, (2) South American canids,
and (3) wolf-like canids. Together, these three clades contain 93% of all living
canids. A separate lineage comprising the grey fox seems to be the most primi-
tive and suggests a North American origin of the living canids about ten million
years ago (Ostrander & Wayne, 2005; Bardeleben et al., 2005; Lindblad-Toh
et al., 2005; Graphodatsky et al., 2008) (see Figure 1-1).
When one looks more closely at the wolf-like canids, results place grey
wolves as the closest living ‘cousins’ of domestic dogs, followed by a close
affiliation with coyotes, golden jackals, and Ethiopian wolves. These phylo-
genetic relationships imply that the dog has several close relatives within its
genus, confirmed by results showing that all members of Canis can produce
fertile hybrids, and several species may have genomes that reflect hybridisation
in the wild (Wayne & Jenks, 1991; Gottelli et al., 1994; Roy et al., 1996; Adams
et al., 2003). Closest to the Canis group are the dhole and African wild dog (thus
completing the members of the wolf-like canids). Dhole and African wild dogs
do not, however, form a monophyletic group, and their exact relationship to the
Canis genus is still somewhat unclear (Bardeleben et al., 2005; Zhang & Chen,
2011). Finally, results from genetic analyses also appear to support an African
origin for the wolf-like canids because the two African jackals are the most basal
members of this clade (Lindblad-Toh et al., 2005).
1.1.2 Evolution of the Canid Brain: A Socially Driven
Phenomenon?
Studies on the evolution of canids show that this family separated from the other
mammals around 40 million years ago. Interestingly, a shift in canid encepha-
lisation and architectural reorganisation of the brain (i.e., expansion of the pro-
rean gyrus at the anterior end of the neocortex, general increase in the amount of
infolding of the frontal lobe, and expansion of the prefrontal cortex; Radinsky,
1969, 1973; Lyras & Van der Geer, 2003) appears to have occurred sometime
in the late Miocene or early Pliocene period, roughly coinciding also with a
sudden taxonomic diversification (Van Valkenburgh, 1991) and expansion of
global grasslands (Cerling et al., 1997). Based on these data, authors have put
forward a number of suggestions as to the possible causes driving these changes
in the brain.
According to some authors, they may simply have been a by-product of
a rapid taxonomic diversification in the new environment (Andersson, 2005);
however, considering the energetic expenditure of big brains, it would seem
more probable that such an expensive adaptation would be driven by some major
adaptive advantage. Work by Van Valkenburgh and colleagues puts forward the
possibility that, in fact, the onset of cooperative pack hunting (Van Valkenburgh
Chapter | 1 The Social Dog: History and Evolution 5
100 Arctic fox
100 Kit fox
100
100 Corsac fox
52
67 98 81 Ruppell’s fox
99 100 Red fox
100
Cape fox
100
(4) 96 Blanford’s fox
100 Fennec fox
75
100 Raccoon dog
Bat-eared fox
Short-eared fox
Crab-eating fox
100
100 – Sechuran fox
80 81 – 99 Culpeo fox
– 100 – 99 – Pampas fox
100 99 99 Chilla
100 93
100 Darwin’s fox
Hoary fox
96 Maned wolf
100 100 Bush dog
100 100 Side-striped jackal
100 3–4 100 Black-backed jackal
100 9–10 Myr Golden jackal
100
Myr 75 100 93 Dog
100 99 78 100 Grey wolf
100
100 Coyote
92 (2)
100 Ethiopian wolf
6–7.4 78
(9) Myr 100 Dhole
African wild dog
100 Grey fox
100 Island fox
100 Black bear
100 Giant panda
100 Northern elephant seal
100 Walrus
FIGURE 1-1 Branch colours identify the red fox–like clade (red), the South American clade
(green), the wolf-like clade (blue), and the grey and island fox clade (orange). (From Lindblad-Toh
et al., 2005.)
et al., 2003; Van Valkenburgh et al., 2004) may have driven this change. How-
ever, Finarelli’s (2008) analysis, taking into account a larger sample of both
extinct and living canids, suggests that encephalisation increased in the three
major living clades (wolf-like, fox-like, and South American canids) at the same
time, yet most of the smaller-bodied canids (except for the South American
bush dog) are not cooperative hunters. The trait that most canids share, however,
6 SECTION | I Theoretical Aspects
is ‘monogamy’ (defined as a single male and single female mating exclusively
with each other over multiple reproductive cycles) and (to differing extents)
the cooperative rearing of the young. Hence, these authors suggest that it may
have been these traits driving encephalisation and that pack hunting would then
have emerged as a second-order adaptation, facilitated by, but not directly caus-
ally related to, the reorganisation of the canid brain. This hypothesis seems to
be plausible given another study showing that, among mammals and birds in
general, it is not the size of the social group that correlates with brain size (as
in primates), but instead it is species that live in pair-bonded social systems that
have the largest brains (when phylogeny and a range of life history and ecologi-
cal variables are partialled out; Shultz & Dunbar, 2007; Dunbar, 2009).
1.1.3 The Sociality of Canids’ Mating System: Pair Bonding
and Cooperative Pup Rearing
Taken as a whole, the dog’s canine family is one of the most fascinating
amongst carnivores. As a start, they are the most widespread, with at least one
species inhabiting every continent except Antarctica (although dogs, of course,
live there as well), and some spread over entire continents (Sillero-Zubiri et al.,
2004). Perhaps more interestingly for the purpose of this book, canids have a
number of interesting social adaptations, starting from their mating system.
Most species in this family are monogamous, a rare trait amongst mammals,
but a potentially characteristic trait for canids (Kleiman, 1977, 2011). However,
there is considerable interspecific variation in mating systems among canids,
and polygamy, polyandry, and monogamy have been documented (Bekoff et al.,
1981; Moehlman, 1989; Geffen et al., 1996; Carmicheal et al., 2007): for exam-
ple, red foxes, Arctic foxes, and coyotes appear to adopt a largely monogamous
strategy (Sillero-Zubiri et al., 2004; Hennessy et al., 2012; but see Carmicheal
et al., 2007), whereas a recent study using genetic analyses to determine parent-
hood across multiple populations of African wild dogs found that there was,
in fact, a greater than previously reported incidence of reproductive sharing in
that both beta females and males (and not just the dominant pair as previously
thought) played a significant role in producing young (Spiering et al., 2010),
suggesting a more promiscuous strategy in this species.
Canids are also unique in that intraspecific variation in mating systems may
be as great as interspecific variation (Moehlman, 1989); for example, swift
foxes, Arctic foxes, and urban red foxes may all live either in monogamous
pairs or polygamous groups depending on their ecological context (Baker et al.,
2004; Kamler et al., 2004; Carmicheal et al., 2007; and see Geffen et al., 1996
for a comprehensive review of canid social flexibility). Indeed, it appears that
the choice between a monogamous or polygamous strategy may even change
within the same population, most probably in relation to food availability (red
foxes: von Shantz, 1984; Zabel & Taggart, 1989). Such flexibility is not con-
fined to the fox-like canids; indeed, Ethiopian wolves show a similar level of
Chapter | 1 The Social Dog: History and Evolution 7
flexibility depending on ecological factors affecting food availability (Sillero-
Zubiri et al., 1996; Marino et al., 2012).
Alongside pair bonding, canids also show a variety of parental care strate-
gies. In some species, mostly the female appears to care for the young—the
most common strategy in mammals (e.g., bat-eared foxes and swift foxes: Kam-
ler et al., 2004; Poessel & Gese, 2013); however, in others, male provisioning
of both pups and lactating females occurs (e.g., black-backed jackals, red foxes,
coyotes: Moehlman, 1989; Zabel & Taggart, 1989; Gese, 1998); and in yet oth-
ers, both breeding individuals and their older offspring (that delay dispersal:
Emlen, 1991) are involved in pup rearing (e.g., grey wolves, African wild dogs,
dhole: Fritts & Mech, 1981; Malcolm & Marten, 1982; Creel & Creel, 2002;
Sillero-Zubiri et al., 2004; Venkataraman & Johnsingh, 2004). In fact, coop-
erative breeding, involving also the non-breeding pack members and including
‘helping behaviour’ such as den-site attendance; provisioning (including regur-
gitation); play; and grooming are perhaps among the defining characteristics of
a number of canid species (Macdonald, 1979; Moehlman, 1986; Mech et al.,
1999; Packard, 2003).
Such helping behaviour has been shown to have an adaptive value in a num-
ber of cooperative breeding species (banded mongoose: Hodge, 2005; meerkats:
Russell et al., 2007), although evidence in the canid family has been harder to
obtain (Gusset & MacDonald, 2010; but see Wright, 2006, for paternal invest-
ment on pup rearing success in bat-eared foxes and helper effect in red wolves;
Sparkman et al., 2011). However, sociality in many canid species is not just
apparent in pup rearing but emerges strongly also in relation to hunting and
territorial defence.
1.1.4 The Sociality of Canids’ Hunting and Defence Strategies
Canid hunting strategies vary widely, ranging from species that feed largely
solitarily on fish and insects, like the short-eared dog (Sillero-Zubiri et al.,
2004), to hypercarnivore species that hunt in packs, such as the African hunt-
ing dog, bush dog, wolf, and dhole (Venkataraman et al., 1995; Creel & Creel,
2002; Mech & Boitani, 2003; Sillero-Zubiri et al., 2004). Hunting techniques
are intimately linked with sociality levels in canids, because species that hunt
cooperatively are also described as the most social. Indeed, a number of authors
have suggested that pack hunting may be the major force behind canid social-
ity (Alexander, 1974; Pulliam & Caraco, 1984; Clark & Mangel, 1986). Group
hunting, in theory, may allow the capture of larger prey. However, the cause and
effect of such an argument may be difficult to tease apart: do some canid species
live in larger groups because in so doing they can hunt larger prey, or does the
availability of predominantly larger prey ‘oblige them’ to live in groups? In a
chapter reviewing the topic, MacDonald et al. (2004) suggest that at present the
evidence cannot tease these two alternatives apart, although novel methods of
modelling hunting success seem to suggest that, at least in African wild dogs,