Volume 107, September 2015, Pages 159–173
- Open Access funded by European Research Council
- Under a Creative Commons license
Open Access
Highlights
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- We tested neophobia and exploration in dogs and wolves.
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- Dogs were quicker to approach, but showed less interest in, novel objects.
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- Presence of conspecifics enhanced approaches to, and exploration of, novel objects.
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- Our findings suggest risk sharing mediates cooperation in wolves and dogs.
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- We assume the differences between wolves and dogs to be an effect of domestication.
Exploration
is important for animals to be able to gather information about
features of their environment that may directly or indirectly influence
survival and reproduction. Closely related to exploration is neophobia,
which may reduce exposure to danger, but also constrain explorative
behaviour. Here we investigated the effects of social relationships on
neophobia and exploration in wolves, Canis lupus, and dogs, Canis familiaris.
Eleven pack-living wolves reared by human foster parents and 13
identically raised and kept dogs were tested in a novel object test
under three different conditions: (1) alone, (2) paired with a pack mate
and (3) together with the entire pack. Dogs were less neophobic than
wolves and interacted faster with the novel objects. However, the dogs
showed overall less interest in the novel objects than wolves, which
investigated the objects for longer than the dogs. Both wolves and dogs
manipulated objects for longer when paired or in the pack than when
alone. While kinship facilitated the investigation of novel objects in
the pair condition in both wolves and dogs, rank distance had opposite
effects. Our results suggest that the presence of conspecifics supported
the exploration of novel objects in both wolves and dogs, particularly
within kin and that this may be interpreted as risk sharing. The reduced
latency to approach objects and less time spent exploring objects in
dogs compared to wolves may be interpreted as an effect of
domestication.
Keywords
- dog;
- domestication;
- exploration;
- neophobia;
- relationship;
- wolf
Exploration
is important for animals to be able to gather information about
features of their environment that may directly or indirectly influence
survival and reproduction. Exploring animals may collect information
about food distribution and abundance, shelters, predators, escape
routes or potential mates (Dall et al., 2005, Heinrich, 1995, Mettke-Hofmann et al., 2002, Renner, 1988 and Schwagmeyer, 1995). To acquire such knowledge, an individual may assess its environment alone (Day, Kyriazakis, & Rogers, 1998), by social learning or by using public information (Swaney et al., 2001, Valone and Templeton, 2002, Visalberghi and Adessi, 2001 and Visalberghi and Fragaszy, 1995).
Closely
related to exploration is neophobia with highly neophilic animals being
quick to approach and explore a novel object, while highly neophobic
animals are slow to do so (Day, Coe, Kendal, & Laland, 2003).
Neophobia is linked to exploration because individuals only explore if
they are interested in an object and the same is true for active
avoidance. Thus objects can be neither explored nor avoided out of sheer
disinterest/lack of perceived relevance. Accordingly, neophobia has
been defined as ‘the avoidance of an object or other aspect of the
environment solely because it has never been experienced and is
dissimilar from what has been experienced in the individual's past’ (Stöwe, Bugnyar, Heinrich, & Kotrschal, 2006,
p. 1079). Neophobic responses can therefore reduce exposure to danger
but they can also constrain explorative behaviour and thus opportunities
for learning and innovating (Stöwe, Bugnyar, Heinrich, et al., 2006 and Stöwe, Bugnyar, Loretto, et al., 2006).
Depending
on a species' ecology and the animal's motivation, individuals approach
and investigate changes in their familiar environment with different
latencies and for variable periods (Day et al., 2003, Mettke-Hofmann et al., 2005, Mettke-Hofmann et al., 2002 and Stöwe, Bugnyar, Heinrich, et al., 2006).
This may also be affected by social context. For example, the presence
or action (handling or food intake) of a conspecific facilitated the
acceptance of novel food in gerbils, Meriones unguiculatus ( Forkman, 1991), zebra finches, Taeniopygia guttata ( Coleman & Mellgren, 1994), capuchin monkeys, Cebus apella ( Visalberghi and Fragaszy, 1995 and Visalberghi and Addessi, 2000), rats, Rattus norvegicus ( Galef, 1996 and Galef and Whiskin, 2000), keas, Nestor notabilis ( Huber, Rechbergen, & Taborsky, 2001) and house mice, Mus musculus domesticus ( Valsecchi, Bosellini, Sabatini, Mainardi, & Fiorito, 2002).
In contrast, delay and inhibition of approach/acceptance of novel food
in a social context have been observed in chum salmon, Oncorhynchus keta ( Ryer & Olla, 1991), Atlantic salmon, Salmo salar ( Brown and Laland, 2001 and Brown and Laland, 2002) and great tits, Parus major ( van Oers, Klunder, & Drent, 2005).
It is not unlikely that the delay/inhibition reported in these studies
was caused by dominance rank differences (and associated risk of
agonistic interaction) between the participating individuals ( Brown and Laland, 2001, Brown and Laland, 2002, van Oers et al., 2005 and Ryer and Olla, 1991). Individual ravens, Corvus corax,
for example, approached a novel object faster when tested alone than
when paired with a conspecific, but they spent more time close to, and
manipulating the novel object in dyads or in groups ( Stöwe, Bugnyar, Loretto, et al., 2006).
This study showed that social relationships mattered: ravens approached
a novel object faster when paired with siblings than nonsiblings and
dominant males approached the novel object first when in a dyad with a
female, but not when with a male ( Stöwe, Bugnyar, Loretto, et al., 2006).
Wolves, Canis lupus,
are cooperative, group-hunting animals that provide communal care for
the pups in a kind of helper system supporting the exclusive
reproduction of the dominant pair ( Mech & Boitani, 2003). Moreover, wolves also defend their territories ( Mech and Boitani, 2003 and Mech and Boitani, 2004) and kills ( Kaczensky, Hayes, & Promberger, 2005)
together. A pack usually consists of the reproductive pair and their
offspring of 1 or more years; however, many variations of this theme
have been observed ( Packard, 2003). The pack is structured according to a sex–age graded hierarchy that reflects the composition of the family group ( Packard, 2003). Domestic dogs, Canis familiaris, although phylogenetically closely related to wolves ( Pang et al., 2009, Savolainen et al., 2002 and Scott and Fuller, 1965), differ fundamentally not just genetically ( Axelsson et al., 2013) in regard to their closeness to humans, but also in their breeding system and, possibly, other cooperative interactions ( Boitani and Ciucci, 1995 and Butler et al., 2004; but see Bonanni, Valsecchi, & Natoli, 2010). Similar to wolves, free-ranging dogs may form stable social groups ( Cafazzo, Valsecchi, Bonanni, & Natoli, 2010) consisting of several unrelated males and females. Feral dogs form a relatively steep, sex–age graded dominance hierarchy ( Cafazzo et al., 2010). Particularly during feeding on dumps or on carcasses, aggression tends to be high ( Boitani et al., 1995 and Macdonald and Carr, 1995),
which may make it less costly for them to explore a new source of food
alone rather than in a group. Moreover, while free-ranging dogs, similar
to wolves, defend their territories together ( Boitani et al., 1995 and Macdonald and Carr, 1995), they usually do not raise pups cooperatively ( Boitani et al., 1995 and Daniels and Bekoff, 1989; but see Pal, 2005), nor is it clear how closely they cooperate during hunting ( Boitani et al., 1995 and Macdonald and Carr, 1995).
If
dogs are indeed less cooperative than wolves within groups of
conspecifics, it may be predicted that also with novel objects,
potentially perceived as a source of danger, wolves might rely more on
support from conspecifics than dogs. For example if the social context
mediates the expression of an individual's personality by either
synchronizing its behaviours to the behaviour of its partner or by
increasing individual differences between the partners (King, Williams, & Mettke-Hofmann, 2015),
wolves could be more prone to synchronize than dogs because, in
general, cooperativeness with conspecifics is more important for their
daily survival than for dogs. On the other hand, in social mammals the
presence of a familiar conspecific has been shown to be more effective
for social buffering, namely in alleviating acute stress responses,
compared to the presence of an unfamiliar conspecific (Kiyokawa, Honda, Takeuchi & Mori, 2014).
Therefore in potentially stressful situations, as when confronted with a
novel object, the presence of a conspecific might be a valuable
resource reducing the potential stress, which might be the same for dogs
and wolves.
While wolves
have experienced various degrees of persecution and exploitation from
humans during the last centuries, potentially selecting for greater
neophobia (Fritts, Stephenson, Hayes, & Boitani, 2003), dogs have undergone the opposite selection through the domestication process (Clutton-Brock, 1995, Hare and Tomasello, 2005 and Thorne, 1995). It has been argued that neophilia is an adaptive consequence of selection by living in association with humans (Kaulfuβ & Mills, 2008),
suggesting that dogs should be inherently less neophobic than wolves,
which may also decrease the dependency on a group in their approach of
novelty, as compared to wolves. Still, wolves may be more strongly
interested in novelty than dogs, because the potential costs or benefits
of contact with novelty may be greater in the former than in the latter
because of their reliance on prey rather than relatively stable food
resources.
In this study, we
compared the responses of identically raised and kept pack-living wolves
and dogs to novel objects presented in three different conditions:
alone, as a pair with a pack mate and with the entire pack. The aim was
to investigate how the social context and relationship between pack
members influenced their neophobic responses and explorative behaviour.
For reasons discussed above, we predicted that wolves would be overall
more neophobic than dogs towards human-related objects (Clutton-Brock, 1995, Fritts et al., 2003, Hare and Tomasello, 2005 and Thorne, 1995),
approaching the objects slower than dogs, but possibly exploring novel
objects more thoroughly than dogs as novelty may lead to potential
benefits or costs that are greater for wolves than for dogs. Moreover,
owing to the inherently higher cooperativeness of wolves towards
conspecifics (Boitani et al., 1995, Kaczensky et al., 2005, Mech and Boitani, 2003, Mech and Boitani, 2004, Pal, 2005 and Range and Virányi, 2015),
we expected a greater facilitating influence of the presence of
conspecifics on the exploratory and neophobic behaviour of wolves than
dogs, that is, wolves would approach the novel objects faster and
explore the objects for longer when tested with a pack member or the
entire pack. We also expected that when tested alone this effect would
be larger in wolves than dogs; that is, there would be no or little
influence of the presence of a pack member in dogs.
Methods
Ethical Note
No
special permission for use of animals (wolves and dogs) in such
sociocognitive studies is required in Austria (Tierversuchsgesetz 2012 –
TVG 2012). The relevant committee that allows running research without
special permissions regarding animals is Tierversuchskommission am
Bundesministerium für Wissenschaft und Forschung (Austria).
Subjects
We tested 11 wolves and 13 dogs raised and kept the same way at the Wolf Science Center, Austria (for details see Table 1).
All animals were hand-raised after being separated from their mother at
approximately 10 days after birth. During the first 5 months of their
lives, the puppies had 24 h contact with their human hand-raisers. At
the age of 2–3 months, the puppies were gradually socialized with the
older animals (dogs with dogs and wolves with wolves) and at the age of 5
months they were integrated into their respective packs. Individual
packs were not natural families, as older individuals were not the
parents of the younger ones. In all packs but one (pack 5), at least one
pair of siblings was present. Both wolves and dogs lived in three packs
(Table 1) in 2000–8000 m2
enclosures with natural vegetation such as trees and bushes. Each
enclosure contained two or three shelters and the dogs also had access
to indoor shelters year-long. Water was available ad libitum. Wolves
were fed two or three times a week, dogs on a daily basis, wolves mainly
with carcasses of rabbits and deer, dogs mainly with dry food, owing to
the different specific dietary requirements of wolves and dogs (Axelsson et al., 2013).
- Table 1. Individual data for all the wolves and dogs housed at the Wolf Science Center (Austria)
Species Subject Sex Birth date Puppy origin Sibling Pack no. Wolf Apache Male 19 May 2009 Zoo Basel, Switzerland Cherokee 1 Aragorn Male 4 May 2008 Game park Herberstein, Austria Shima 1 Cherokee Male 19 May 2009 Zoo Basel , Switzerland Apache 1 Geronimo Male 2 May 2009 Triple D Farm, Montana, U.S.A. Yukon 2 Kaspar Male 4 May 2008 Game park Herberstein, Austria – 1 Kenai Male 1 Apr 2010 Quebec, Canada Wapi 3 Nanuk Male 28 Apr 2009 Triple D Farm, Montana, U.S.A. – 2 Shima Female 4 May 2008 Game park Herberstein, Austria Aragorn 1 Tatonga Female 21 Apr 2009 Triple D Farm, Montana, U.S.A. – 2 Wapi Male 1 Apr 2010 Quebec, Canada Kenai 3 Yukon Female 2 May 2009 Triple D Farm, Montana, U.S.A. Geronimo 2 Dog Asali Male 13 Sept 2010 Szeged, Hungary Binti 4 Bashira Female 13 Sept 2010 Paks, Hungary Hakima 5 Binti Female 13 Sept 2010 Szeged, Hungary Asali 4 Bora Female 2 Aug 2011 Györ, Hungary Layla 6 Hakima Male 13 Sept 2010 Paks, Hungary Bashira 4 Kilio Male 18 Dec 2009 Paks, Hungary Maisha 5 Layla Female 2 Aug 2011 Györ, Hungary Bora 6 Maisha Male 18 Dec 2009 Paks, Hungary Kilio 4 Meru Male 1 Oct 2010 Velence, Hungary – 5 Nia Female 21 July 2011 Paks, Hungary – 5 Nuru Male 24 June 2011 Paks, Hungary Zuri 6 Rafiki Male 30 Nov 2009 Tengelic, Hungary – 4 Zuri Female 24 June 2011 Paks, Hungary Nuru 6
From
puppyhood on, all animals were regularly trained and participated in
different behavioural tests. During the training sessions, they were
usually separated from the rest of the pack. Wolves and dogs were
exposed to the same type of experiences and the same behavioural tests
at the same age from puppyhood on. At the age of 3–10 weeks, all
subjects participated in several tests where they were confronted with
novel objects in a room. It is unlikely that these early tests
influenced the current tests in any specific way since, first, all
animals (dogs and wolves) were exposed to the same objects; second, they
were tested in a very different context (inside versus outside; human
handler present in puppy tests versus absent in the current setting)
and, finally, the time elapsed since these early tests (>2 years).
