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Proc. R. Soc. B (2012) 279, 3083–3090
doi:10.1098/rspb.2012.0264
Published online 28 March 2012
A novel mammalian social structure in
Indo-Pacific bottlenose dolphins
(Tursiops sp.): complex male alliances
in an open social network
Srdan
Randić1, Richard C. Connor1,2, *, William B. Sherwin2
and Michael Krützen2,3
1
Biology Department, UMass Dartmouth, North Dartmouth, MA 02747, USA
Ecology and Evolution Research Centre, School of Biological Earth and Ecological Sciences,
University of New South Wales, Sydney, New South Wales 2052, Australia
3
Evolutionary Genetics Group, Anthropological Institute and Museum, University of Zurich,
Winterthurerstrasse 190, 8057 Zurich, Switzerland
2
Terrestrial mammals with differentiated social relationships live in ‘semi-closed groups’ that occasionally
accept new members emigrating from other groups. Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia, exhibit a fission – fusion grouping pattern with strongly differentiated relationships,
including nested male alliances. Previous studies failed to detect a group membership ‘boundary’,
suggesting that the dolphins live in an open social network. However, two alternative hypotheses have
not been excluded. The community defence model posits that the dolphins live in a large semi-closed ‘chimpanzee-like’ community defended by males and predicts that a dominant alliance(s) will range over the
entire community range. The mating season defence model predicts that alliances will defend matingseason territories or sets of females. Here, both models are tested and rejected: no alliances ranged
over the entire community range and alliances showed extensive overlap in mating season ranges and consorted females. The Shark Bay dolphins, therefore, present a combination of traits that is unique among
mammals: complex male alliances in an open social network. The open social network of dolphins is
linked to their relatively low costs of locomotion. This reveals a surprising and previously unrecognized
convergence between adaptations reducing travel costs and complex intergroup– alliance relationships
in dolphins, elephants and humans.
Keywords: alliances; ranges; social structure; social organization
1. INTRODUCTION
Mammalian social systems vary immensely along a range of
variables [1]. However, two particular traits are always
found together: complex social relationships and membership in a ‘semi-closed group’ with one or more reproductive
females. In such groups, members of one sex (usually
females) remain in their natal area or group, whereas members of the other sex disperse [2]. Semi-closed social groups
are often described by familiar terms such as a ‘troop’ of
baboons, a ‘pride’ of lions, a ‘community’ of chimpanzees
or a ‘pack’ of wolves. In these societies, an individual’s
bonds are normally limited to other group members,
whereas interactions between individuals of different
groups are typically hostile. Group defence may be performed by males (e.g. chimpanzees [3]), females (many
primates [4]) or both (e.g. lions [5]).
A few species that feature semi-closed groups have
what can be described as an ‘open social network’ above
the group level, where affiliative interactions may extend
to members of other groups with overlapping ranges.
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rspb.2012.0264 or via http://rspb.royalsocietypublishing.org.
Received 4 February 2012
Accepted 6 March 2012
For example, the African elephants’ (Loxodonta africana)
social system is based on stable ‘family groups’ of
female kin, and their offspring that associate with other
family groups to form ‘bond groups’ that are, in turn,
linked into larger ‘clans’ [6,7]. Multi-level societies
based on stable matrilineal groups are found in several
odontocetes, including killer whales (Orcinus orca) and
sperm whales (Physeter macrocephalus) [8,9]. In fact, the
behaviour and life history of elephants and sperm
whales have converged to a remarkable degree [10].
The social system of Indo-Pacific bottlenose dolphins
(Tursiops sp.) in Shark Bay, Western Australia, features a
fission – fusion grouping pattern with stronger associations
between adult males than adult females and bisexual philopatry [11]. The male dolphins form nested alliances.
Two or three males cooperate in ‘first-order’ alliances to
form consortships with individual females [12,13].
Teams of 4 –14 males cooperate in ‘second-order’ alliances to attack other alliances and to defend against
such attacks. Second-order alliances can persist intact
for over 15 years and may be considered the core unit
of male social organization in Shark Bay. Some secondorder alliances have ‘third-order’ alliance relationships
with other groups, which are also concerned with conflicts over females [14]. To mediate their bonds, males
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S. Randić et al. Dolphin open social network
use affiliative contact behaviours (petting and rubbing)
and possibly synchrony [15]. This complex system of
multi-level alliances has not been described in other
populations of Tursiops, so further references to ‘dolphins’
are specific to the Shark Bay population.
Associations among adult female dolphins in Shark
Bay are variable but never as strong as those between
the most strongly bonded males [16]. There are no
reports of females forming alliances against other females
in Shark Bay, and in over 25 years, there has been only
one observation of females forming a temporary coalition
against young males [13]. Individual female ranges are
not congruent but form an overlapping mosaic in our
study area [17]. These findings indicate that the social
structure in Shark Bay is not based on female defence
of ranges or groups as is common in many mammals [18].
Although fission–fusion group formation is found in
a wide range of species [19], the pattern of sex-specific
bonds in the Shark Bay dolphins is much closer to that of
common chimpanzees (Pan troglodytes) and spider monkeys
(Ateles spp.) than other terrestrial mammals [3,19]. However, there is no evidence that the male dolphins defend a
community territory such as male chimpanzees and
spider monkeys [3,20–23], suggesting an unprecedented
combination of male alliance relationships in an otherwise
open social network [24]. This issue is of general interest
for two reasons. First, the relationship between social cognition and large brain evolution has received considerable
attention [25], and animals with complex social relationships but living in an open social network would face
novel cognitive challenges (reviewed by Connor [24]). In
semi-closed social groups, individuals may not only know
the other members of their group, but they may also learn
the dominance rank and primary kin relationships of
group members. Such ‘social knowledge’ may be critical
to their reproductive success (e.g. they might refrain from
forcibly taking food from a smaller individual if that individual has a larger sibling). In an open social network, the
social knowledge individuals can acquire about others
they encounter will be highly variable and limited for
individuals encountered infrequently. Assessing risk in
potential conflicts may be difficult: an opponent may have
gained new allies since he or she was last encountered. Furthermore, discovering a novel social structure in dolphins
raises questions about which aspects of their biology and
ecology might permit such a deviation from the terrestrial
‘norm’, thus broadening our understanding of mammalian
social evolution.
(a) Alternative models and predictions
Despite the apparent lack of a community boundary in
Shark Bay [24], previous research has not been able to
exclude two models based on Clutton-Brock’s [18] category
of ‘multi-male groups with spatial defence by males’.
The ‘community defence’ (CD) model is derived from the
common chimpanzee/spider monkey social system, where
individual females travel in smaller areas of a larger community range that is patrolled and defended by males [3,20,21].
Given the nested structure of dolphin alliances, the equivalent to a chimpanzee patrol might be performed by a
group of male dolphins belonging to a single second-order
alliance or even more than one second-order alliance.
Thus, the CD model predicts: (i) that at least one or more
second-order alliances will range over (¼patrol) the entire
Proc. R. Soc. B (2012)
study area (¼community), and (ii) that these alliances will
overlap with the ranges of all other second-order alliances
in the community. We note that, given the hundreds of dolphins residing in our previous study area of 250 km2, the
dolphin community would have to be much larger than
any known chimpanzee community. Travelling around
such a large territory would be quite feasible for dolphins.
Dolphins enjoy a low cost of locomotion and day ranges of
odontocetes are typically an order of magnitude greater
than those of similar-sized terrestrial mammals [26].
Typical travelling speeds of dolphins in our population are
3–5 km h21, which would allow them to traverse the full
length of our study area along the peninsula (50 km) in a
12–18 h period.
The ‘mating season defence’ (MSD) model postulates that
male groups defend smaller territories or sets of females
during the mating season. For example, males might shift
from using larger non-mating season ranges, where they
concentrate on foraging to improve body condition, to
smaller mating season ranges for female defence. The
MSD model predicts that allied males will occupy exclusive
ranges during the mating season months of September–
December. However, observations off Scotland [27]
suggest that groups of bottlenose dolphins might defend
mobile ranges. A finding of overlapping mating season
ranges might conceal a system where spatial defence shifts
on a shorter timescale as mobile sets of females are
defended by particular alliances. To allow for this variant
of the MSD model, we also examined the extent to which
alliances overlap in the females they consort with.
To test the predictions of the CD and MSD models,
we examined ranging and behaviour of over 120 adult
males in an expanded 600 km2 study area (figure 1), in
the period from 2001 to 2006. These males associated
in 12 second-order alliances and five ‘lone trios’ (i.e.
trios without second-order affiliations [14]).
2. METHODS
(a) Field observations
Male association, behavioural and ranging data were collected
through surveys and focal follows during the same five-month
field season for 6 years (2001–2006, from July through to
November). This period covered the first three months
(September to November) of the five-month peak breeding
season, as well as August, when alliance behaviour and consortship rates increase [28,29]. Surveys represent brief encounters
(at least 5 min) of dolphin groups during which we record a variety of data, including time and global positioning system (GPS)
location, as well as group composition, based on photographic
identification [30]. A group was defined as all individuals that
were observed together based on a 10 m ‘chain rule’ [16].
Although care was taken to distribute the spatial search effort
as evenly as possible throughout the study area, our ability to
do so was somewhat limited by weather conditions.
Focal alliance follows ranged in duration from 1 to 8 h.
During follows, we kept a continuous record of behaviour
and group membership, with a focus on documenting consortships, following Connor et al. [31]. Members of second-order
alliances formed first-order alliances (consorted females)
with each other, cooperated in conflicts with other groups
and generally shared half-weight association coefficients
greater than 20 [12,16]. These associations were obvious in
the field and distinct in cluster diagrams [14].
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Dolphin open social network
S. Randić et al.
3085
N
Cape Peron
Shark Bay
Guichenault Point
Peron Peninsula
Cape Rose
Monkey Mia
Dubaut Point
Denham
0 1.5 3
6
9
12
km
Figure 1. Study area and sighting locations.
During the study, we observed that particular secondorder alliances had third-order alliance relationships with
other groups [14]. It is possible that such associations are
based partly on joint defence of an area or females. Thus,
to examine the question of whether allied males maintained
exclusive access to a set of females (as predicted by the
MSD model), we grouped first- and second-order alliances
into putative third-order alliance groups (sensu [14]) and
compared lists of consorted females between groups.
(b) Analysis
Data on male alliance membership were taken from surveys
and focal alliance follows. GPS location data were analysed
using ARCVIEW v. 9.2 software. For each individual male,
sighting points from the study period were plotted based on
Proc. R. Soc. B (2012)
latitude and longitude, using a universal transverse Mercator
projection with a WGS84 map datum. Hawths analysis tools
for ARCGIS toolkit’s algorithms [32] were used to translate
projected points into corresponding surface areas, which
were spatially referenced. To avoid autocorrelation, a maximum of one sighting point per individual per day was used,
thus enabling each sighting to be considered an independent
data point. To calculate the total home range for each secondorder alliance, we included sighting points for all the individual members of a given alliance during the study period, but
limited each individual to one point per day.
To test the CD model, ranges were estimated using the
minimum convex polygon (MCP) method. The MCP
range estimation method is the most conservative test of
the CD model because it includes outlier points and thus
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S. Randić et al. Dolphin open social network
Cape Peron
N
Shark Bay
Guichenault Point
Peron Peninsula
Cape Rose
alliance name (alliance size)
BB (3)
PD (7)
BL (8)
PHG (3)
CB (6)
FCB (3)
GG (6)
RHP (3)
RR (7)
SK (3)
HC (7)
HH (6)
SJ (11)
WC (10)
KS (14)
PB (12)
XF (8)
Monkey Mia
0 1.5
3
Dubaut Point
6
9
12
km
Figure 2. Alliance ranges calculated using the minimum convex polygon method.
maximizes the estimated degree of overlap between alliance
ranges. To test the MSD model, we estimated alliance core
ranges during the mating season using the fixed kernel density
estimation (FKDE) method [33]. For the FKDE method, a
smoothing factor (hadj [34]) of 1.574 was chosen as optimal,
given the number and spacing of sighting points, to provide
sufficiently continuous home range estimates, without overly
inflating range size or artificially placing a part of the range
on an impossible location (e.g. on land). FKDE output cell
size was set at 100 m. We followed the common practice of
using the 50 per cent point density volume contour to represent the core home range [35] of the animal, and 90 per
cent volume contours were taken to represent the entire
range for comparison with the MCP method.
For further details on methods and results, including analyses of individual male ranges with respect to sample size,
Proc. R. Soc. B (2012)
the number of males in an alliance and a comparison with
female ranges, see the electronic supplementary material.
3. RESULTS
(a) Tests of the community defence and mating
season defence models
We found no evidence supporting either the CD or the
MSD models. The key prediction of the CD model was
that at least one second-order alliance would range over
the entire study area. However, even with generous
MCP range estimates, there were no individuals or alliances whose ranges overlapped all other alliances in the
study area (figure 2). The largest FKDE-estimated
alliance range size was 133 km2, and the largest
MCP-estimated range size was 229 km2, compared with
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Dolphin open social network
S. Randić et al.
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Cape Peron
N
Shark Bay
Guichenault Point
Peron Peninsula
Cape Rose
alliance name (alliance size)
BB (3)
PD (7)
BL (8)
PHG (3)
CB (6)
FCB (3)
GG (6)
RHP (3)
HC (7)
HH (6)
SJ (11)
WC (10)
KS (14)
PB (12)
XF (8)
Monkey Mia
RR (7)
SK (3)
0 1.5
3
Dubaut Point
6
9
12
km
Figure 3. Alliance core ranges during the peak-mating season, calculated using the fixed kernel density estimation method.
Table 1. Average range sizes (in km2) for lone trios and
second-order alliances in Shark Bay.
MCP
90% FKDE
50% FKDE
mean
s.e.
n
minimum
maximum
144.92
92.31
25.56
14.83
6.78
2.04
17
17
17
57.77
48.15
14.60
273.02
132.90
45.68
the study area size of over 600 km2 (table 1). Furthermore, the ranges of some second-order alliances did not
overlap at all (figure 2).
The key prediction of the MSD model was that males in
different second- or third-order alliances should show no or
minimal overlap of ranges or female consorts during the
Proc. R. Soc. B (2012)
mating season. However, conservative 50 per cent FKDE
estimates of core ranges showed extensive mating season
overlap among second-order alliances, including those
that did not share a third-order alliance membership (e.g.
alliances SJ and PB, PD and RR, BL and CB; figure 3).
Data from a single mating season show the same pattern
(see the electronic supplementary material).
There was also extensive overlap in the females consorted by different male groups. Sixty-five females were
documented in three or more consortships (range 3– 17,
mean 6.4). Only one female, observed in three consortships, was observed with a single second-order alliance
and only seven females (11%) were consorted by
males from a single third-order alliance. Thirty-two
(49%) of the 65 females were consorted by three or
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S. Randić et al. Dolphin open social network
more second-order alliances belonging to three or more
third-order alliance groups. Thirty-one of those 32
females were observed in at least two consortships
(range 2 –12) in a single season. Over the course of that
season, all 31 were consorted by males from more than
one (range 2– 5) second-order alliance, belonging to
between two and four third-order alliances.
4. DISCUSSION
(a) A novel mammalian social system: an open
social network or ‘unbounded’ dolphin society
We found no evidence that the large and complex social network in Shark Bay, comprising hundreds of bottlenose
dolphins, is a closed group defended by males. We also
found no evidence that males defend smaller ranges or
groups of females within this network. Instead, there is
extensive overlap in the ranges of alliances and in the
females they consort with. Combined with earlier work on
females, these results lead to the conclusion that Shark
Bay bottlenose dolphins live in an open social network
with a mosaic of overlapping female and male ranges.
The total extent of the Shark Bay dolphin social network is unknown, and it may be continuous throughout
the dolphins’ habitat in the bay. A much larger social network is suggested by the fact that, in addition to the males
that were the focus of our study, there were at least
another 100 adult males that we encountered one or
more times in different parts of the study area. We
expect that the core ranges of these males partially overlap
with or are beyond our study area.
It is unlikely that kinship can offer a complete explanation for the male dolphin network in Shark Bay. Male
dolphins do not maintain strong bonds with their mothers
and while they form male–male bonds from an early age
[11], the second-order alliances ‘crystallize’ when males
are in their teens, after a long juvenile period [36]. The combination of ubiquitous alliance formation among males and
a slow life history where females give birth to single calves
separated by several years militates against males being
able to rely consistently on close kin for allies [24]. Relatives have been found among some close allies in smaller
second-order alliances, but males were unrelated in one
large, 14-member second-order alliance [37].
(b) Comparison with terrestrial mammals
The terrestrial mammal most often compared with bottlenose dolphins is the common chimpanzee (Pan troglodytes)
[11,38]. Shark Bay bottlenose dolphins have a very
‘chimpanzee-like’ fission–fusion grouping pattern, stronger male–male than female–female associations and
they have very similar life histories [39]. However, we
found here that the dolphins do not live in semi-closed
male-defended communities such as chimpanzees.
While the other great apes do not share as many features
of social organization with the Shark Bay dolphins, their
social boundaries may be less clearly defined or social interactions between groups more tolerant than in chimpanzees,
whose intergroup relationships are exclusively hostile [3].
In striking contrast to common chimpanzees, some (but
not all) bonobo (Pan paniscus) communities enjoy peaceful
interactions when they meet [40]. A bounded chimpanzeelike community structure has not been found in orangutans
(Pongo pygmaeus), whose ‘diffuse’ social system is described
Proc. R. Soc. B (2012)
as ‘neighbourhoods, where residents know many others,
but know them less well as the home range overlap
decreases’[41]. Western gorillas (Gorilla gorilla) live in
one-male groups, but have been described as having a ‘dispersed male network’ on the basis of tolerant interactions
among related male silverbacks that have overlapping
ranges [42]. However, in none of these species does the
greater tolerance between groups translate to alliance formation between groups that might be comparable with
the complex nested alliances we find in dolphins. Among
other non-human primates, claims that Hamadryas
baboons (Papio hamadryas) have more complex male alliances than those found in other baboons have been
challenged [13]. Humans live in semi-closed groups and
exhibit intergroup alliance formation. This is achieved, at
least in part, by maintaining relationships with kin that
have dispersed to other groups [43].
While it remains unclear if the nested intergroup
relationships found in African elephants are commonly
featured in an alliance context (e.g. two family groups
against others), they do associate, like the dolphins, in a
large open social network. But otherwise, elephant social
organization is fundamentally different from the Shark
Bay dolphin society. Unlike the dolphins, elephant society
is based on stable units of female kin and their offspring
[44], although individuals are capable of forming strong
bonds with non-relatives when relatives are not available
[45]. The core matrilineal units are apparently formed
by a process of fission, as subordinate females become
grandmothers [6,44]. The changes we observe in the
male dolphins’ first-order and sometimes even their
second-order alliance relationships [36] would not be
expected in an elephant-like kinship system.
Outside of mammals, the most intriguing parallels with
the dolphin social system are found among small parrots
such as green-rumped parrotlets (Forpus passerinus), and
conures (Aratinga spp.). Although the basic unit of
social structure is the male – female pair, these species
exhibit an extensive fission –fusion grouping pattern, preferential associations beyond the pair bond [46] and have
converged with the dolphins in the use of individually
distinctive contact calls [46,47]. Young male greenrumped parrotlets are sometimes found in pairs before
they find a mate [48]. Future studies should reveal
whether these birds have an open social network or any
alliance structure outside of the pair bond.
(c) Low cost of locomotion, overlapping ranges
and nested alliances: convergence in dolphins,
elephants and humans
It is interesting that mammalian brain size evolution produced peaks in such otherwise disparate taxa: elephants,
humans and some odontocetes (dolphins and sperm
whales). Connor [24] argued that the same selective
environment was common to all three groups: an extreme
degree of mutual dependence based on high infant vulnerability in species that are already investing heavily in
each offspring. Given this mutual dependence, individuals were in reproductive competition with the same
individuals their lives depend on, favouring increasingly
sophisticated abilities in the arena of social cognition.
Another area where ‘the big three’ have apparently
converged is in their low costs of locomotion. The low
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Dolphin open social network
cost of locomotion in dolphins has already been noted;
elephants have the lowest cost of locomotion recorded
for any terrestrial mammal [49], and the evolution of
bipedal locomotion endowed humans with greatly
reduced locomotion costs relative to the other apes [50].
Clearly, a lower cost of locomotion does not necessarily
lead to complex social systems but it could have contributed
to the evolution of enhanced social cognition and the complex intergroup–alliance relationships found in hominids,
cetaceans and elephants. At a given population density,
cheaper travel and concomitantly larger ranges would
have increased the rate that individuals and groups encountered each other in competitive contexts, favouring larger
groups and alliances [51], and perhaps intergroup relationships that are sometimes cooperative rather than hostile or
merely tolerant. These changes would have directly
impacted two factors that are thought to impose selection
for enhanced social cognition: the number of social relationships an individual maintains [52], and the additional
cognitive burden imposed by negotiating a multi-level
group/alliance structure [13].
Humans maintain relationships with other groups by
remaining in contact with dispersed kin and by cultural
identity [53] and are thus said to be ‘released from the constraint of proximity’ [43]. However, multi-level alliance
formation in humans was probably also favoured by their
large overlapping ranges associated with the evolution of
bipedal locomotion. Humans and bottlenose dolphins are
the only two species that exhibit nested male alliances
within a social network [12,24]. Some of the profound
differences between human and dolphin social organization
(e.g. dolphins do not exhibit pair bonds or male parental
investment) may relate to the fact that humans are tied to
a home base or hearth (see Wrangham [54]), whereas dolphins are not.
6
7
8
9
10
11
12
13
14
The University of Massachusetts at Dartmouth approved
the study.
This study was supported by grants from the Australian Research
Council (A19701144 and DP0346313), the Eppley Foundation
for Research, Seaworld Research and Rescue Foundation,
W. V. Scott Foundation, the National Geographical Society’s
Committee for Research and Exploration and NSF (1316800).
We thank Jack Bradbury, Steve Beissinger and Phyllis Lee for
email discussions on parrots and elephants. Accommodation
was very generously provided by the Monkey Mia Dolphin
Resort. Permits were obtained from the West Australian
Department of Environment and Conservation. Many
generous people helped out with this project.
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