SOCIAL INTERACTIONS IN CAPTIVE

HARBOUR PORPOISES (Phocoena phocoena)

© Solvin Zankl. Fjord&Baelt

Master thesis by Lara Delgado García

Institute of Biology
University of Southern Denmark
Supervisor: Magnus Wahlberg
August 2009
UNIVERSITY OF SOUTHERN DENMARK

SOCIAL INTERACTIONS IN CAPTIVE

HARBOUR PORPOISES (Phocoena phocoena)

M.S.c Thesis by Lara Delgado García

August 2009

Supervisor Magnus Wahlberg

Institute of Biology
University of Southern Denmark

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 ACKNOLEDGEMENTS

First I wish to thank Magnus Wahlberg, for his constant support and help,
from the most complex matters and teachings to the most rutinary-time consuming tasks,
always willing to help with endless patience and good mood. I want to thank him for
introducing me in the amazing whale world, contributing to my formation not only for the
master thesis topic but providing me a much broader biological base and scientific
experience, always allowing student to get implied in research, transmitting his curiosity
and truly scientific passion. It is not possible to remark all the innumerable details I need
to thank him. I wish to thank Hans Ulrik, who helped me through the experimental plan,
analysis and interpretation with absolute dedication, during hard times, and eventually in a
voluntary way. Thanks a lot to both my supervisors.
I also need to thank the trainers and employees at Fjord&Baelt Centre,
Kerteminde, Denmark for all their help and collaboration during the study, and for the
advices for the experimental plan. As well as the trainers and employees of the “Brown
bay” and SOS-dolphinen”, (Harderwijk Dolphinarium) Holland, for all their help for
preparing the stay, during the data collection and during the writing, always disposed to
gather and send information promptly (special thanks to Eligius Everaarts, Jolanda
Meerbeek, Lauro Marcenaro and Monique Timmer).
I would like to thank Ole Naesby and Lee Miller for their help and advices
for planning the master thesis, and with behavioural program searches. Also thanks to
Vibeke Hepworth, for technical help and warm support.
I would like to thank all the “Marine biological research centre crew” for their
cheerful company, strong support and friendship, for the uncountable hours shared that
have made my “stay” like being home (Caroline-Marie Vant Madsen, Coralie Barth,
Danuta Wisniewska, Inma Martin, Kim Lundgreen, Lee Miller, Meike Linnenschmidt,
Malene Agerled, Magnus Wahlberg, Morten Jørgensen, Parnuna Egede, Puk Faxe). Also
thanks to Ewa Borowska. And last, special thanks to my parents, my strongest basis, in the
hardest times, and in the farest distances, always supporting me whichever the decision
was.

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 FOREWORD

Passion, or at least some kind of motivation, is needed to achieve the smallest of

the goals of everyday life. A reason, or at least a belief, is necessary to do something. The
“more” or “less” important topics in which people invert their lives, is a matter of
perspective, and the perspective changes for each different individual, in each single
moment. From the extremely subjective point of view of passion, animal behaviour is for
me the most amusing and moving topic you can use your time on. Why we – animals –
behave as we do, which are the reasons for any of the actions or decisions we make,
becomes such an incredibly attractive question, that the desire of understanding what is
hidden behind every act or move becomes fundamental in my daily life. And the
inevitable bias makes me focus on the small details that may cause apparently random
actions. Sociality seems to me the only unavoidable human characteristic, and so social
behaviour appears to me as the basis of, at least, our society.
However, we humans are only a negligible self-centred piece of the huge puzzle of what is
possible for us to perceive, with our limited sensory system capabilities, as the rest of the
world. I am at any time puzzled by the diversity and complexity of nature, and the wish of
learning, of discovering, at least a little piece of what is left to know, makes me feel the
urge of start moving. Social behaviour possesses an attractive complexity that moves me. I
guess that including other individuals in the play is what makes it definitively interesting,
as this changes perspectives, and human social deflection arises. That it is why I get
completely entangled in it, vehement, without any chance to switch my attention to other
“boring” matters.

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 CONTENT

INTRODUCTION

The study of cetaceans……………………………………………………………...6

The study of social behaviour……………………………………………………...7
The harbour porpoise………………………………………………………………8
Taxonomy…………….…….…………………………………………………8
Morphology…………….…….……………………………………………….8
Biological parameters……….….……………………………………………..9
Habitat use and trophic ecology….…….……….…………………………...11
Distribution, abundance, status and conservation….……....…………..……12
Behaviour: what is known from the field…….….…………………….…….13
Group composition….…………….….……………………………………...14
Behaviour & group composition for a special case:
mother-calf pairs……………..……………………………………………..16
Social structure……….……………………………………………………. 18
Biological parameters of females & group composition:
comparison with other Odontocetes’ species………………………………19
Mating strategy: comparisons with other Odontocetes’ species…………...20
Communication…………………………………………………………….22
Chemical……………………………………………………………………...22
Tactile………………………………………………………………………...22
Visual…………………………………………………………………………23
Acoustic communication and echolocation……………………………..24
Interespecific communication signals……………………………………26
Intraspecific communication signals…………………………………….26
Behaviour: what is known from captivity………………………………….27
Andersen & Dziedzic (1964)................................................................28
Andersen (1969)...................................................................................29
Amundin & Amundin (1971).................................................................29
Amundin (1974b)..................................................................................32
Amundin (1974c)..................................................................................33

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 Kastelein & Staal (1997)......................................................................33
Nakamura et al. (1998).........................................................................34
Lockyer et al. (2003).............................................................................36
Desportes et al (2003)..........................................................................37
Kristensen (1999)........................................................................38
Benham (1999)............................................................................38
Wilson (1999)..............................................................................40
Jepsen (2002)...............................................................................42
Why the social structure is important…....……………………………………...43
The study of social interactions in harbour porpoises:
why studying captive animals…………………………………..……………….43
Aims of the study..………………………………………………………….…….45
Reference list……..………………………………………………………………46

ARTICLE MANUSCRIPT

Abstract……………………………………………………………………………55
Introduction…………………………………………………………………….…56
Materials and Methods…………………………………………………………...58
Results……………………………………………………………………………..66
Discussion …………………………………………………………………………75
Overall conclusions………………………………………………………………..89
Reference list………………………………………………………………………91

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 INTRODUCTION

THE STUDY OF CETACEANS

Studying cetaceans is in itself challenging and complex, and for investigating their
social behaviour the difficulties become even greater. Cetaceans spend the majority of
their time in quite inaccessible habitats. The dense and, compared to air, murky medium
they live in (seas and oceans) supposes the most obvious barrier for studying their
behaviour. Hence, the attraction of discovering the unknown makes studying cetaceans
extremely appealing for the curiosity-based scientific ideal. In addition, the potential
complexity cetaceans possess in their biological functions makes the research even more
interesting.
Cetaceans are long-lived animals which invest great resources into offspring care,
have large brains, and have developed special communication and scanning methods
(echolocation abilities) which allows them to perceive their environment and, in some
cases, communicate in uncommon and different ways in comparison with the majority of
animals. Hence, many cetaceans societies are among the most complex among the
mammals (Mann et al. 2000) but very little is known about them in comparison to
terrestrial animals.
Long-term studies in the wild for the most well-known species (killer whales
(Orcinus orca, e.g. Baird 2000); sperm whales (Physeter macrocephalus, e.g. Whitehead
& Weilgart 2000); humpback whales (Megaptera novaeangliae; e.g. Clapham 2000),
bottlenose dolphin (Tursiops truncatus; e.g. Connor et al. (2007), among others) have
provided a great basis for understanding cetacean societies, the evolutionary forces that
may have influenced shaping their biology, and help defining conservation strategies. Due
to the difficulties in studying cetaceans, scientists have developed ingenious and diverse
methods to provide varied and complementary glimpses in the biological overview of the
species biology (for a review, see Samuels & Tyack (2000); Mann (2000) and Whitehead
et al (2000)).

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 THE STUDY OF SOCIAL BEHAVIOUR

Behaviour can be defined in the simplest way as movement (Ridley 1986). Early
investigators on behaviour (such as Darwin, Heinroth and Lorenz) observed that any
behaviour is composed by repeated sequences. Such sequences were therefore called
behavioural “units”, and these allow observers to check their own and others observations,
and therefore permit rigorous testing of a certain hypothesis. Behaviour can also be
described my means of its consequences, and obtain the same “unit”, in both cases. In
conclusion, animals perform behaviour patterns that can be recognized by different
observers (Ridley 1986).
Animal behaviour as a science has earlier been accused of being subjective,
anecdotal and anthropomorphic. This may be one of the reasons why the development of
the scientific study of animal behaviour using systematic, quantitative methodologies for
testing hypotheses have developed exponentially (Houck & Drickamer 1996).
Social behaviour can be defined as a “behaviour involving two or more animals”,
and refers to all the ways in which animals influence each other, involving communication
(Deag 1980). Shannon & Weaver (1949) defined in their mathematical theory of
communication, that communication is the transfer of information, in this case from one
animal (sender) to another (receiver), by means of signals that can be distinguished from
the background noise to be detected, and have evolved for the specific communicative
purpose (Deag 1980). Communication is judged to have occurred when the Shannon-
Weaver information is transferred to the observer, i.e. when the behaviour
(communication) of one animal (sender) alters the probability of the behaviour of another
animal (receiver) (Deag 1980). The information transferred is typically a statement about
the environment, the physiology of the signaller, or its intentions (Deag 1980).
Interactions may occur among more than two animals at the same time. In addition
there may be unintended receivers, which “extract information from an interaction” a
phenomenon called eavesdropping (McGregor & Dabelsteen, 1996).
Hinde (1976) defined three levels in studying social organization. From the
lowest to the most complex level: “interactions between individuals”, “relationships” and
“social structure”. “Interactions” is the basis of social structure, the description needed to
take into account the quantity and quality of the social exchange. “Relationships” would
cover the interaction among individuals along time, and the structure or pattern of the
interaction. And, the “structure” of the group describes who and in which way is part of it,

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along time. Each level requires information from the previous level. Thus, inferences can
be made from one to the other but diverse and longitudinal studies are required to have a
complete comprehension of the social structure of a group and even more to be able to
generalize to the level of species that comprises population variations (Hinde 1976). The
study of social interactions cementing it in dyadic interactions, is a bottom-up approach
“starting the analysis from a secure base of description” (Hinde, 1976).
This thesis will provide information on the level of “interactions”, several insights
in the “relationships” of individuals and some suggestions and tendencies based on
hypothesis on the “social structure” of harbour porpoises (Phocoena phocoena),.

THE HARBOUR PORPOISE

Taxonomy

Harbour porpoises are small-sized cetaceans belonging to the family Phocoenidae

within the suborder Odontoceti – toothed whales and dolphins– (Bjørge & Donovan 1995;
Read et al. 1997). There are six living species of porpoises: the harbour porpoise
(Phocoena phocoena), the Burmeister’s porpoise (P. spinipinnis), the vaquita (P. sinus),
the finless porpoise (Neophocoena phocoenoides), the Dall’s porpoise (Phocoenoides
dalli) and the spectacled porpoise (Australophocoena dioptrica).
The harbour porpoise is the subject of this study. Two subspecies have been
recognized: P. phocoena phocoena in the Atlantic, and P. phocoena vomerina in the
Pacific. A third subspecies possibly exists in the Black Sea (P. phocoena relicta; Fajardo-
Mellor et al. 2006).

Morphology

The harbour porpoise derives its common English name from the Latin for pig
“porcus”. This is partly due to its physical appearance: its conical head does not have a
beak, and it has a short stocky body (Bjørge & Tolley, 2002).The harbour porpoise robust
body shape, and thick blubber layer is an adaptation to life in cold waters to minimize heat
loss (Read et al 1997). The general coloration of harbour porpoises is characterized by the
dorsal side being dark grey in contrast the chin and underbelly which are white, with a
greyish gradient in the mid-flanks. On each side of the head near the back of the mouth

8
grey stripes are present running back towards the flippers (Bjørge & Tolley, 2002). There
are differences in coloration, especially in the greyish zones, which allow for
differentiating individuals. Unfortunately it is not possible to use this in field studies, due
to the rapid surfacing which usually allow the observer only to see the small triangular-
shaped dorsal fin and dorsal parts of the body.
The harbour porpoise is one of the smallest cetacean species (Read et al 1997). It
exhibits sexual dimorphism, females being larger with an extended growing period
compared to males (e.g. Galatius 2005). Adult females are usually 153-163cm long and
weight 55-65kg. Adult males grow usually to 141-149cm and weight 46-51kg. These
averages mainly comprise North Atlantic harbour porpoises, female porpoises in the
waters of northern Japan have been reported to be larger in all age stages than females in
the north Atlantic (Gaskin et al. 1993). And even in the North Atlantic variations are seen
among populations (Lockyer 2003).

Biological parameters

Biological parameters of harbour porpoises have been obtained mainly from

information gathered from stranded and (by)caught animals. This sampling method
renders biases, especially in the age structure (Lockyer 2003). Studies in captivity have
complemented this knowledge, but such studies naturally have their own biases.
Main biological parameters inferred from stranded animals, by-catches, catches
and captive individuals are summarized in Table 1 in Danish, Japanese, Dutch waters and
the North Atlantic. The first three locations are selected because is where the three
facilities that keep harbour porpoises in captivity are located and the North Atlantic area as
a “general category” as is the best studied area.
From Table 1 it is evident that this species is characterized by a relatively short life
cycle compared to other toothed whales (Read et al. 1997). Harbour porpoises represent
one end of a continuum of Odontocete life histories. Compared to other cetaceans they
belong to the smallest species, mature at an earlier age, reproduce more frequently, and
live for short periods (Read & Hohn 1995). The larger size of females compared to males
is probably an adaptation for carrying a large fetus, as the calf needs to have a minimum
size to survive the energy loss by heat lost after birth (Galatius 2005). In an overall
perspective, the biological parameters for the species are constant but variations can be
observed among populations (Lockyer 2003), as seen in Table 1 for the studied locations.

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Table 1. Biological parameters of harbour porpoises in the North-Atlantic, Danish water, Japanese water and Dutch and British
waters. Information gathered from strandings, catches, bycatches and porpoises under human care (d=days, m=months, y=year,
max=maximum, min=minimum, cm=centimetres; SD=Standard Deviation). Footnotes are explained on the next page.

North
Japanese Dutch (g) and British (h)
Atlantic Danish waters
Waters waters
(a)
Strandings, Catches, and
Strandings, Captivity
catches, Captivity other sources Captivity Strandings and
catches and (Harderwijk
bycatches and (Fjord&Baelt) (dead (f) bycatches
bycatches dolphinarium)
sightings (b) (c) specimens) (e)
Max longevity found 24 y 11y 24 y (h)
The majority of the < 12 y <12 y (b)
population live
<5 y (females
Age at sexual found to be
3-4 y 3 y (b) mature at 3y) (g)
maturity ♀
>3y (h)
3y
Age at sexual 3-4 y 3 y (b)
(Testis size larger than the
max for immature testes)
maturity ♂
(i)
135 cm Longer than in
Length at sexual 127-135 cm
135cm (b)
(Testis size larger than the the North- >130cm
Max 160 cm max for immature testes) Max 163cm (h)
maturity ♂ Atlantic
(i) Max 158 cm
Longer than in
Length at sexual 138-147 cm the North- >
143cm (b)
maturity ♀ Max 184 cm Atlantic Max 189 cm (h)
Max 185cm
0.74-1.0
Not all
Alternately 1-2 y Every other year
Pregnancy rates females
(b) (d)
produce a calf
every year
mid-July-mid-
August (copulation
attempts) in 1998 (i)
More extended
July-mid-August than in Denmark.
August (b) (copulation & sperm Spermatogenetic
presence)
activity in March
Late-July-early-
(one individual
August (receptivity in
Seasonal June-August the female) in 1999
found) (g)
breeding/mating (o) (i)
18 August
(± 11.8 d) Peak testes size
July-August
(c) (presence of sperm) June-August
in 2000 (p) (max in August).
(h)
mid-July to October
(presence of sperm)
in 2001(p)
10 m (b)
Gestation 10-11 m <1y (h)
10.4m (c)
Peak in July.
Peak in late June More extended
early July (b) period than in
Most newborn 25th of July Denmark.
29th of
mid-May- calves observed in (stillborn) (k) Neonates from
Parturition April 5th of May (n)
mid-July July and August (b) May to October.
(stillborn)
8th of August (j) (g)
3 July (± 11.8 days)
(c) Peak in June -
July (h)
74.3cm
(SD7,8cm)
65-75cm 65-75 cm (b) 89cm (at 1m and min 63 cm
Size at birth Max 80cm Min 60cm (b) 3w) (l)
Max 80cm
max 97cm (g)

60-75cm (h)
Starting of fish eating >8 m >8 m (b) 1y and 7 m (l)
Size at weaning (fish <115 cm 116 cm (l)
eating)
Entirely independent
10 m <1y 11(m)
weaning
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(Footnots belonging to Table 1 on previous page)
a) Data from the comparative study of Lockyer (2003); b) Data from Lockyer & Kinze (2003); c) Börjesson
& Read (2003) dates of conception where back-calculated from fetal size and fetal growth rate was
estimated of 83 mm/month. The data shown is the one from the Baltic sea; d) Bjørge & Tolley (2002); e)
Data from Gaskin et al 1993; f) Nakamura et al (1998); g) Addink et al. (1995); h) Lockyer (1995); i) Data
from Desportes et al. (2003); j) Blanchet et al. (2008a); k) Blanchet et al. (2008b); l) M. Wahlberg personal
communication; m) Personal observation; n) Harderwijk dolphinarium stuff personal communication; o)
Data from Benham (1999), sexual behaviour based on behavioural observations (copulation attempts) and
physiological measures (presence of spermatozoa in vaginal smears) from the end of June to mid-August;
vaginal cytology suggested that late July-eary-August was the sexual receptive time; p) Data from Jepsen
(2002). Behavioural observations (done from March 2000 to March 2001), sexual behaviour observed from
April to mid-November, greatest activity in July-August. Vaginal smears (in 2000 and 2001) show presence
of spermatozoa in July-August 2000 and presence of spermatozoa from mid-July-early October 2001.

For instance, the breeding season has been reported to be strictly seasonal (e.g.
Møhl-Hansen 1954; Desportes et al. 2003) however, variations can be seen among
populations and among years in Table 1 (e.g. in captive porpoises in Kerteminde the
mating season seems to vary in different years).
Even though advances are being made in the knowledge of the species, the
biological parameters are still not well described (Haug 2003). Further investigations will
help understand their way of living and thus help us apply adequate conservation
measures.

Habitat use and trophic ecology

Harbour porpoises are mainly coastal dwellers, foraging near the sea bottom in
waters less than 200m in depth (e.g. Bjørge & Tolley 2002). Despite their predominant
coastal way of life they have also been observed in offshore waters, outside the continental
shelf in the North Sea (Börjesson 2003) and between Canada and Greenland (reviewed by
Edren 2009).
Porpoises are fish and squid eaters (e.g. Bjørge & Tolley 2002). The consumed fish
mainly consists of gadoids (e.g. cod) and clupeids (e.g. herring and sprat) of 10-25 cm
length, but diet varies geographically and seasonally (Kastelein et al. 1997).
Predominantly, harbour porpoises’ diet is composed by pelagic schooling fish (Wilson
1999), but some species of their diet are benthic (Bjørge & Tolley 2002).
The harbour porpoise has a short term energy storage capacity (e.g. Börjesson
2003, Lockyer et al. 2003), resulting in switches in their diet and foraging grounds
associated to changes in their preferred prey availability (Börjesson 2003).
Seasonal migrations have been observed between on shore and off shore locations
(e.g. Neave & Wright 1968), and movements parallel to the coast have also been observed.

11
The utilization of diverse areas at different times may be explained by a sum of factors,
such as the distribution of prey (e.g. Bjørge & Tolley 2002), environmental factors (Edren
2009), breeding areas (Lockyer & Kinze 2003), et cetera.

Distribution, abundance, status and conservation

Harbour porpoises are found throughout the Northern hemisphere (Read et al.
1997) in the temperate and cold regions (Andersen 2003). They are mostly distributed in
coastal areas of the North Atlantic and Pacific Oceans as shown in Figure 1. In the North
Atlantic, diverse subpopulations/populations have been found. Previously 18 putative
subpopulations/populations were suggested by Gaskin (1984), but this was later reduced to
13 (reviewed by Andersen 2003). The knowledge of the population structure will allow for
creating adequate guidelines for conservational strategies. Diverse techniques are used for
defining populations. In Danish waters, genetic studies (Andersen 2001, reviewed by
Edren 2009) and satellite-tagged porpoises have demonstrated that there are two
populations or subpopulations (Edren 2009).

Figure 1. The distribution of harbour porpoises (from Read 1997).

The number of harbour porpoise has suffered a sharp decrease since the last
century. However, only regional estimates are available for this species. The species, is
listed in the IUCN as least concern (Hammond et al. 2009), but appears in the appendix II
of the CITES − i.e. a species that is not in danger but may be endangered if measures are
not taken. In addition, some populations or subpopulations are endangered: the Baltic sub-
population is listed in the IUCN as critically endangered, and the Black sea subspecies as
endangered (Hammond et al. 2009).
Some measures have been taken to protect harbour porpoises. The species is to be
legally protected by creating MPAs (Marine Protected Areas) by the EU member states

12
according to the EC Habitat Directive (92/43/EEC; cited in Edren 2009). Assessing high
density areas of harbour porpoises is a focus for designing protected areas.
The harbour porpoise is threatened by a variety of anthropogenic influences, the
most important being the by-catch in fisheries (e.g. Edren 2009). Among other
anthropogenic threats the construction of offshore wind farms (Teilmann et al. 2008), fast
moving vessels and contamination can be mentioned (reviewed by Edren 2009).

Behaviour: what is known from the field

Harbour porpoises swimming and surfacing movements are quick but they rarely
leap out of the water. This surfacing behaviour characteristic from the species was defined
by Amundin & Amundin (1974) as smooth rolling, and described in detail by Amundin
(1974a) for captive animals.
In their study of porpoises’ behaviour in the wild, Amundin & Amundin (1974)
reported that the animals were observed to rest, logging in the surface for 5-10 seconds.
This has been observed also in captivity (e.g. Andersen & Dziedzic 1964). Longer resting
of up to half an hour was reported by Amundin & Amundin (1974) in hot summer days;
this long resting has been observed in both ill and healthy captive animals.
Amundin & Amundin (1974) described other variations of the normal smooth
rolling of porpoises while swimming. It has been observed to change when motor boats
get closer than 200m to the animals. The porpoises speed up and when rolling get higher,
plunge with a splash and breathe quickly and violently. This reaction has also been
observed in captive animals in fright-stress reactions (Amundin & Amundin 1971). The
animals avoided the boats by swimming away from, or under, them. It is interesting to
point out the difference in the so-called leaping behaviour (also called milling or
porpoising in other studies of various whale species) performed by porpoises and other
cetaceans. In harbour porpoises it is a higher rolling in comparison with the normal
smooth rolling, allowing to see all the body out of the water, but the animal never gets far
from the surface (e.g. Amundin & Amundin 1971; Amundin & Amundin 1974).
Amundin & Amundin (1974) also reported several fright-stress reactions when
groups of porpoises met with others. On one occasion a porpoise from one group
approached a mother-calf pair, and the mother-calf reacted by swimming fast in circles,
the calf exhibit the fear reaction described above - almost leaping our of the water – the
and mother-calf swam in the opposite direction of the other animal. Splashes and

13
disturbance of the water can be seen indicating fast swimming. Another encounter of two
alone animals showed the same pattern: fast swimming, and leaping.
A special type of fishing behaviour performed by a mother has been observed in
shallow waters of around 1.5 meter depth when the visibility was good, the animal
positioned vertically with the snout pointing the bottom presumably foraging (Amundin &
Amundin 1974); such behaviour was later to be called bottom grubbing. Harbour
porpoises have been seen to be involved in what seems cooperative hunting in waters of
Little Baelt (Denmark) (S. Andersen, pers. comm. and www.hvaler.dk).
Goodwin (2008) distinguished between feeding behaviour, travelling, social
interactions and avoidance behaviour in their study of habitat use of harbour porpoises in
two areas of southwest Britain. Feeding was defined when porpoises were observed
chasing or in association with fish, or nearby feeding sea birds. Travelling was defined as
constant movement in a fixed direction; when the porpoises where observed to change
direction, stay submerged or leave the area as a response to the presence of another
animal, object or marine vessel; this was defined as an avoidance. Resting was not only
including logging but also slow and unidirectional movements within a given area. It was
called Social interactions when porpoises where seen leaping, chasing, or surfacing at
high speed and when there was no evidence of feeding or directed travel. Social
interactions would therefore only comprise fear and aggressive responses as well as the
avoidance category sensu Amundin & Amundin (1974). When comparing behavioural
studies, it is capital to compare the definitions of the described behaviours as the naming
of behaviours can be confusing or even contradictory between studies.
Nor diurnal nor nocturnal patterns have been observed in harbour porpoises in the
wild, as harbour porpoises have been observed to dive continuously both day and night
(e.g. Teilman 2007, Linnenschmidt 2005). This is in agreement with what have been
observed in captivity (Andersen & Dziedzic 1964).

Group composition

The number of harbour porpoises in a group is usually reduced. It is reported to

range from 1 to 7 individuals in Blasket Islands (Ireland), with an average group size from
1.7 to 3.1 (Berrow et al. 2009). Only 2 calves were sighted in this study (i.e. an adult: calf
ratio 50:1); thus these groups were not mainly formed by mother calf pairs as it has been
proposed as the basic social structure of this species. Group size was observed to be

14
average around 2.7 individuals (SD = 1.8), ranging from 1 to 10 animals in the Bay of
Biscay and adjacent waters (Kizska et al. 2007). Hammond et al. (2002) reported that the
mean school size ranged from 1.4-1.6 in ship surveys in the North Sea and adjacent
waters. Goodwin (2008) reported the average group size of harbour porpoises to be 2.7
ranging from 1 to 10 individuals in Morte Point; and 2.5 in Lee Bay ranging from 1 to 6
individuals, both areas of southwest Britain. A review of older studies have reported the
same average range from 2 to 10 individuals, but larger feeding aggregations, seldom
more than 50 individuals, were also commonly observed (Wells et al. 1980). In Little
Baelt, feeding aggregations of adult porpoises are commonly seen during the summer
months (personal observation). Thus, in different areas the average group size tends to be
similar for the species, with larger aggregations seen in some areas.
Group composition has been pinpointed in few studies. For instance, Lockyer &
Kinze (2003) reviewed harbour porpoise encounters, group composition, and possible
calving areas in Danish waters. Studies from before 1990 were reviewed, and school sizes
are reported to vary from single individuals to a maximum of 100 individuals. The average
school size was 2.1. When analysing the most common group sizes, single individuals
where encountered 43% of the time, followed by pairs found in 35% of the encounters.
Schools of 10 or more animals accounted for 1.3% of the school sizes reported.
Some studies have considered time scales, for example it was reported that
the group sizes observed in the autumn were larger than those observed in the spring in
Canadian waters (Neave & Wright 1968). Møhl-Hansen (1954) described that larger
flocks were most abundant during November to February in Gamborg Fjord, Denmark,
and this fjord was established for several centuries as a hunting ground for this reason. In
contrast, in another Danish location, Isefjord, larger flocks were seen in the spring and
hunting was concentrated on that time. This shows that variations of group numbers are
found among areas and seasons.
Studies done at a shorter time scale have found variations within a month: Neave &
Wright (1968) observed that through a year survey in the same area in the Bay of Fundy,
Canada, monthly variations in the predominant group size were observed, and an overall
increase of porpoise density in July, August and September and a sharp decrease in the
winter being almost absent, and thus from this data, a seasonal migration was inferred.
Proportions of group number were monthly reported, for instance it was stated that the
group number became larger during the summer with very few single individuals reported,
groups of 5 or more, 3 and 2 being the most abundant group numbers in July.

15
Unfortunately, no statistical analysis was performed, and these high and low levels are
expected to be subjectively decided. But the fact that these monthly variations occur,
sheds more light on the group structure, and the social structure of porpoises. In this study,
differences were also found in the amount of sightings related to the distance from shore,
during the months of the year. In May and June, most of the animals are seen within 8
miles from shore. In July, 50% of the animals were seen more than 8 miles of shore in
contrast in September 70% of the sightings were done less than 8 miles from shore.
Interestingly, even more detailed variations of group size were reported by
Goodwin (2008). The distance from the shore and group size was statistically varying with
the time of the day; the group size decreased in the afternoon, being one individual and
pairs the most abundant. However, during the morning, similar proportions of groups
ranging from 1 to 6 animals were encountered.
In conclusion, due to all this variation in group size by the location and the time
(daily, monthly, seasonally, and yearly), studies at different times and on different spatial
scales should be done in order to provide some generalizations about group composition.
The average group number only cannot provide many more insights in to the social
structure and general biology without taking such variables into account.

Behaviour & group composition for a special case: the mother-calf pair

The only secure data on the age and sex composition of wild free ranging
harbour porpoise groups that can be obtained (without catching them) is the presence of
calves, due to their small size in comparison with their mothers. The dimorphism in male-
female sizes, females being slightly larger than males, cannot be assessed in the field.
However, even if it seems a minor detail, the information obtained of the group size when
calves are presents is of major importance as this gives insights into the social structure.
Additionally, calves below 1 year of age show the highest mortality (Lockyer 2003), and
to be able to protect these young animals it is necessary to understand their biology.
Lockyer & Kinze (2003) reviewed the group size when claves were present. Groups of
two porpoises were the most common observation (49%), corresponding to cow and calf;
followed by groups of 3 animals including a calf (32%), other combinations where
observed but were more rare, such as for example 4 animals including 1 calf (7.9%). The
largest group consisted of 17 individuals including 5 calves. A so-called nursery group
composed by several calves was observed in July in Little Baelt (personal observation).

16
 Amundin & Amundin (1974) observed in the wild a mother-calf pair during
8 days. They returned to the bay where the observations where made once/several times
per day getting as close to land as 20 meters where the water was only 1 meter deep. The
mother-calf pair swam slower and breathed more frequently than single animals. The calf
was observed to perform exaggerated, high rolls when swimming, described to look like
attempts of leaping caused by the inexperience in performing the normal smooth rolling
when breathing. During the observations made on the first calf born and surviving in
captivity, such exaggerated high rolls were performed by the new-born calf during at least
two weeks after. Later on the calf learned to perform the adult-characteristic smooth-roll
(Delgado et al. in prep.). These developmental-caused behaviours provide a new tool to
asses the age of the calves (without the necessity of catching them to measure them to
infer their age). It is thus very likely that the calf observed by Amundin & Amundin
(1974) was less than a month old.
Amundin & Amundin (1974) observed in the mother-calf pair described
before, that the mother bottom grubbed by her own while the calf swam alone, going as far
as 30 meters form the calf. The cow was never observed to fetch the calf, instead it was
always the calf that approached to the mother. Acoustical communication was not studied,
but its use was hypothesized for the mother and calf to find each other. Clausen et al. (in
prep.) have found that calves produce a “calling” sound when separated/away from their
mothers, probably the same described by Amundin & Amundin (1971) and Amundin
(1991) from young porpoises in stressful situations.
It is also interesting to point out, that the mother-calf pair in the Amundin &
Amundin (1974) study was observed in very shallow waters. It has been suggested that
porpoises go to shallower areas to give birth and breed (Meek 1918, reviewed by
Amundin & Amundin 1974). Amundin & Amundin (1974) also reported that the mother-
calf pair tended to swim by themselves, and a stressful reaction was described when
another porpoise approached the dyad. In August 2008 during a 10-day study at Fyns
hoved in Denmark, a mother calf-pair was observed to get close to the shore, where the
depth was around 2m. These animals were the only ones seen to get that close to the shore
in this study and the cow-calf pair always swam alone, agreeing with the observations
described above (personal observation).
Teilmann et al. (2007) studied the time allocation and diving behaviour of harbour
porpoises in Danish and adjacent waters by means of satellite tags. Two adults and two
calves that were accidentally trapped in pound nets were tagged, among other porpoises.

17
Genetic analysis were made to asses the relatedness of the animals, and one adult-calf, was
seen to be mother-calf; while the other adult-calf pair trapped together was found to be
half siblings or cousins. The related adult-calf (not mother-cow) separated after a day of
the release, which indicates that long-term allomaternal care did not seem to be performed.
The cow-calf pair was observed to swim together for the remaining 43 days of the tag
attachment, and as the calf was estimated to be 10 months old at the time of tagging, this
information shows that the mother-calf maintained a close bond during more than 11
months.
The Teilmann et al. (2007) study gives the first empirical data of a mother-calf
bond along time that is not based on inferences from expected times of birth and weaning
from stranded or bycaught animals. The data suggests that complete weaning or at least
the break of the affiliative bond is not achieved before 11 months after birth. Even if this
conclusion is based in only one mother-calf pair, it is interesting to highlight because of
being the first information of this kind and delay the time of weaning reported to be
around 8-10 months (Lockyer 2003; Møhl-Hansen 1954). In agreement with this
observation of long mother-calf dependence, the calf born in captivity as described above
was completely dependent on the mother and did not start to eat fish until an age of 1y and
3 months (M. Walhberg, pers. comm.). This is much later than what has been previously
observed to be the beginning of weaning (around 8months, eat fishing but probably still
nursing; Lockyer 2003; Lockyer & Kinze 2003) and also much later than the age of
complete weaning (around 10 months, only eating fish Lockyer 2003). Even if this
observation might be influenced by the fact that the calf was held in captivity, should be
considered as it is obtained with exact timing and age.

Social structure

There is an almost absolute lack of knowledge of the social structure of harbour

porpoises, apart from the average number of group composition as discussed above. Some
hypothesis of the (gender) group composition based on the expected breeding time, and
weaning, and relative group number have been suggested, but as it is not possible to sex
animals by means of observations in the field (except for mother-cow pairs , or by
capturing animals), they are pure suggestions with very little empirical basis. For instance,
Neave & Wright (1968) suggested that the peaks of single and pairs of porpoises in May
in the Bay of Fundy (Canada) might be migrating pregnant females that travel alone or

18
 with other pregnant females, male groups, mating pairs, etc. No empirical data has
however been presented to confirm this yet.
The most trustable information comes from Møhl-Hansen (1954) from groups of
animals captured together. However, as stated by the author, this “group composition”
might be just individuals that were close by and were caught together with no significant
social bonds between them. But, at least the animals caught together were in the same
area at the same time. Most of the potential schools (school defined by Norris & Dohl
(1980) as “any aggregation of aquatic animals that regularly swim together as a unit”),
consist of both sexes, but “not infrequently” small flocks are made up of exclusively
males. Møhl-Hansen cites some examples 7♂:1♀, 10♂:0♀, 7♂:0♀, 9♂:2♀, 8♂:0♀, and
reports the opposite proportion to not be common e.g. 6♀:1♂, being in that case 4 adult
females with 3 young, one of them the male. The author suggests that adult males are
probably travelling in schools separated from females, and hypothesises that females
travelling alone with their young might be trapped together with “male flocks”, but this
cannot be known for sure. Additionally, these data come only from hunting done in
November-February, which reduce these suggestions to that time frame.

Biological parameters of females & group composition: comparisons with other

Odontocetes’ species

There are some Odontocetes that share similar habitats and life history
patterns with harbour porpoises. The social structure of species with similar life history
parameters may be expected to show some common features, and are reviewed in Table 2.

Table 2. Biological parameters and group number of Odontocete species sharing a similar habitat and life history with
harbour porpoises (Phocoena phocoena) are presented. The lengths presented are the average for females when available, or
average for the species otherwise. All the other information corresponds to the average for the species. (cm=centimetres,
y=year, m=months max= maximum).

Common name Species Length Age at Gestation Interbirt Longevit Habitat Group size
maturity h interval y
Harbour porpoises (b) Phocoena phocoena 158 cm 3-4 y 10-11 m 1-2 y 24 y Inshore and 2.7 (from 1 to
(average shelf 10) (k)
max)

Spectacled porpoise Australophocoena 200 cm Early 24 y (max) Inshore and 2

(d) dioptrica maturation shelf

Commerson’s dolphin Cephalorhynchus 170 cm 6y 12 m 18 y Inshore 6

(a) commersonii
Hector’s dolphin (a) Cephalorhynchus 130 cm Inshore 4
hectori
White-beaked dolphin Lagenorhynchus 260 cm 10 m Shelf 10
(a) albirostris
Finless porpoise (a) Neophocoena 160 cm 5.5 y 11 m 2y 23 y River and 6
phocaenoides inshore

19
Vaquita Phocoena sinus 150 cm >3 y (e) 21 y (max) Inshore (e, g) 2 (e, g)
(g) (e)
Burmeister’s porpoise Phocoena 185cm 11-12 m 1 y (f, h) Inshore and 5 (up to 70) (f)
spinipinnis (f) (h) shelf (f)
Dall’s porpoise Phocoenoides dalli 187 cm 4.4 y 12 m 1y 35 y (c ) Shelf and 10 (up to 100)(c)
(c) (c) (c, i) (c, i) deep waters
(c) 2 (from 1 to 7,
small and fluid
Inshore (i) composition) (i)

a) Data reviewed by Whitehead & Mann (2000), table 9.1; b)Data from Lockyer (2003); c) data from Ferrero
& Walker (1999); d) Natalie & Goodall (2002); e) Rojas-Bracho & Jaramillo-Legorreta (2002); f) Reyes
(2002); g) Vidal (1995); h) Reyes & Van Waerebeek (1995); i) Willis & Dill (2007); j) E.g. Edren (2009); k)
E.g. Goodwin (2008) in Morte Point (southwest Britain).

The knowledge of the social structure of the species listed in Table 2 is very
limited. Probably the best well known social structure of inshore Odontocetes species is
the one form Dall’s porpoises (Phocoenoides dalli). Dall’s porpoises have been reported
to breed every year, and the group composition has been seen to change seasonally, the
average group number reported to be 2 showing a fluid pattern (Willis & Dill 2007). Male-
male dyadic associations have been observed, and newly calved females have been found
to associate a month after parturition with one male probably during all the mating period
(Willis & Dill 2007).
The common constraint that has been proposed to relates life history of female
cetaceans and the environment is as follows “large, slow-reproducing animals are not
found in inshore or freshwater environments” (Whitehead & Mann 2000). And therefore,
Odontocetes having a quick life cycle could be expected to be living in rich inshore
environments. However, no clear correlations can be made in this respect on social
structure, as other causes may have helped causing these adaptations. In addition, the
mean group size (what is mostly known from the species reviewed in Table 2) is a very
poor measure of the social structure because many other variables influence the range of
the group sizes encountered.

Mating strategy of harbour porpoises: comparisons with other Odontocetes’ species

The mating strategy is of great importance in order to outline the social

structure of harbour porpoises. The testes size, sexual dimorphism and the presence or
absence of secondary sexual characteristics provides some indications on the mating
system of a species. Big testis size is correlated with sperm competition. Aguilar &
Monzon (1992) showed that in general, cetaceans have larger testis size than terrestrial
mammals. Delphinids, Phocoenids, Kogiids and Balaenids have larger testis than those of

20
other mammals of similar body sizes. Species of these families will probably have a
mating system based on sperm competition –i.e. females mate with multiple males –,
while species with smaller testes may compete for mates through aggressive interactions.
The mating system of a species can be outlined from fighting ability among males and
sperm competition (e.g. Connor et al. 2000b). In monogamous species, the fighting ability
of males and sperm competition will be generally low. In species where males mate with
multiple females during their entire oestrous period, selection for sperm competition will
be low, but the fighting ability high. Selection for fighting ability and sperm competition is
expected to be high if males compete for access to females but females mate with multiple
males. And in last term, selection for sperm competition will be high and fighting ability
low if males do not compete for females and females mate with multiple males (Connor et
al. 2000b).
Harbour porpoises have been reported to have the greatest relative testis size,
comprising 4% of their body weight, from the 133 species of mammals compared by
Kenagy and Trombulak (1986). Due to the big size of harbour porpoise’s testes, sperm
competition is expected to occur, which points to extreme multimale (promiscuous)
breeding in this species. And the reverse sexual dimorphism, with females being larger
than males, and males not having any “weapon” or secondary sexual characteristics that
could be used in fighting, shows that males probably do not compete by means of male-
male fighting for females (Jefferson 1990).
Different mating systems than the one for harbour porpoises are expected for
the other inshore Odontocetes from which some information is known. Lagenorhynchus
(white-beaked dolphin) exhibits large testis and high sexual sized dimorphism, indicating
a multiple-mating breeding system both with sperm competition and male-male
competition (Connor et al. 2000b). On the contrary, the smaller Cephalorhynchus
(Hector’s dolphin and Commerson’s dolphin), have relative small values of sexual size
dimorphism and smaller testes, and thus less sperm competition is expected, and also less
fighting is assumed in this species. Dall’s porpoises (Phocoenoides dalli) have a large
sexual dimorphism, males being larger than females, and small testes, having also
secondary sexual characters expected to function for male-male competition or female
choice. Because of these characteristics, Dall’s porpoises were thought to have a
polygynous mating system (Jefferson, 1990); however it has lately been shown by Willis
& Dill (2007) that mate guarding, i.e. “the male closely attends and defends a fertile
female from extra-pair matings” (Willis & Dill 2007) is the mating strategy occurring in

21
the species. Males associate with a female and her new offspring a month after parturition,
and this dyadic association probably lasts through the mating period. This matches
perfectly with the reduced testes size which predicts low copulation frequency, and
therefore explains the “guarding need”. The males’ larger body size allows them to defend
females alone, and male alliances, as observed in bottlenose dolphins (Connor 2007) are
not needed (Willis & Dill 2007).
Less information is known about the mating strategy of other inshore species
(Table 2), but they do seem to differ from harbour porpoises. Spectacled porpoises
(Australophocaena dioptrica) have a significant degree of sexual dimorphism in both size
and shape of the dorsal fin (reviewed by Jefferson, 1980). Also in Burmeister’s porpoises
(Phocoena spinipinnis), males are significantly larger than females (Reyes & Van
Waerebeek 1995; Reyes 2002).

Communication

As stated before, social behaviour involves communication (i.e transmission of

information, in its basic form, including a sender and at least a receiver). The sensory
systems of cetaceans have evolved very differently from terrestrial animal systems, due to
the physical characteristics of the medium they live in. Therefore, communication has also
been shaped differently in marine mammals. (Tyack 2000).
Chemical communication is not really well known in marine mammals. However,
some hypotheses on the use of pheromones among cetaceans have been suggested in
bottlenose dolphins, spinner dolphins and gray whales (reviewed by Norris & Dohl, 1980).

Tactile communication plays a very important role in most cetacean species.

Dolphins and whales rub and caress each other with different parts of the body which
maintains affiliative relationships among them (Tyack 2000). Harbour porpoises do the
same (e.g. Andersen & Dziedzic 1964, Amundin & Amundin 1971, this thesis).
Sexual contacts have been shown to have social and communicative functions in
addition to procreation; for instance sexual activity in male-male groups has been
observed in grey whales and delphinids (Tyack 2000). It has also been seen in harbour
porpoises, probably as a rank-stating method (Amundin & Amundin 1971, Amundin
1974c). And copulation has been observed in individuals that are not sexually mature,

22
both in dolphins (Connor et al. 2000a) and in harbour porpoises (Amundin & Amundin
1971, Kastelein & Staal 1997, this thesis).
Nursing has been suggested to have a communicative-affiliative function in
addition to the nutritive function, keeping and reinforcing the mother calf-bond (Brodie
1969). This is in agreement with what observed in harbour porpoises, as a 1years 6months
old captive calf is observed to continue trying to nurse (Delgado et al. in prep.).
Aggression in harbour porpoises mainly fills a communicative function. No
physical effects have been observed in aggressive manifestations. Information transfer
rather than physical consequences are expected to be the basis of aggressive
communication in this species. (Andersen & Dziedzic 1964, Amundin & Amundin 1971,
Amundin 1974c, this thesis).

Visual communication plays a major role in cetacean lives. It was long

believed that they had a poorly developed visual system, but it has recently been shown to
be the opposite (Mass & Supin 2002). Observations of captive dolphins have shown that
they are able to catch fishes in the air, perform precise jumps to reach targets above the
water. And vision is needed in air where echolocation does not operate (Tyack 2000, Mass
& Supin 2002). Mass & Supin (2002) reviewed that vision plays an important role in
social interactions, in discriminating individuals and species, as well as preys, in
orientation, reproduction and defense. In-air vision has been reported to be nearly as acute
as underwater vision; In-air vision is likely to have a role in foraging, surveillance and
orientation (Tyack 2000). The visual sense complements the echolocation skills of
Odontocetes, and is expected to be of main importance in daylight and at close range
(Tyack 2000).
As specific examples, both aggressive and sexual interactions involve visual
signals at close range that function as communicative displays (Tyack 2000). For instance
in harbour porpoises, jerked noddings, sideward turn as aggressive displays, being more
intense when resemble biting (open mouth); and belly exposure and S-posturing as sexual
and submissive displays (Andersen & Dziedzic 1964, Amundin & Amundin 1971, this
thesis).
The range at which vision can be used in the water is limited to a few meters
and daytime. Oddly enough, riverine cetaceans (the Amazon river dolphin (Inia
geoffrensis) and the tucuxi (Sotalia fluvialis)) living in turbid and low-transparent water

23
does not exhibit a significant regression in their visual system, with the exception of the
Indian river dolphin (Platanista gangetica).

Acoustic communication and echolocation. Cetaceans have excellent

hearing and a specialized vocalization system, both optimized for functioning under water.
This allows them to communicate with elaborate acoustic signals (Tyack 2000). In
addition, Odontocetes can echolocate. Echolocation is “the ability to produce high-
frequency (ultrasounds, not audible for humans) clicks and to detect echoes that bounce
off objects” (Tyack 2000). Echolocation is mainly used for orientation and prey detection
(Au 1993).
Sounds with higher frequencies are absorbed faster than those of lower
frequencies .This may be a major reason why the majority of the sounds used for
communication in Odontocetes are of low frequencies so that they can optimize the range
at which they can be detected. On the contrary small targets produce higher backscatter by
high frequency signals or shorter wavelengths, and because higher frequencies are needed
for efficient echolocation (Tyack 2000). There are also other characteristics than the
frequency of the sounds to take into account for defining features that are best for
communication and for echolocation, for instance the intensity of the sound and its
directionality.
Harbour porpoises are only using clicks – very short and relatively
broadband transient signals used for communication and echolocation –as communicative
sounds (Amundin 1991, Nakamura 1998, Clausen et al. in prep.). No frequency modulated
whistles are produced as in many delphinids (Popper 1980). The clicks of harbour
porpoises are narrow band and of very high frequency, centered around 110-140 kHz.
They are about 50-100 µs long (Villadsgaard et al 2007).
Amundin (1991) reported that harbour porpoise clicks consisted of two frequency
components, the omnidirectional low frequency one (LF) at around 2kHz, and the
directional high frequency one (HF) at around 130kHz, both being the result of the same
generation process. It was shown that the click repetition rates varied among behaviours
observed simultaneously, suggesting its social communication function. The specific click
frequency, using the LF component, could be associated with agonistic behavioural
displays, distress and sex related calls. Lately it has been discussed that the LF component
it is probably not used for communication due to its extremely low intensity (100dB re 1
µPa). And the detection range of harbour porpoises of this component is much smaller

24
than the HF component in any direction to the whale. Therefore it may be regarded to be a
by-product of the sound generator, and not a dedicated pulse produced for communication
(Hansen et al. 2008). However, even if the LF component is a by-product of the
production of the HF one, the LF component can be used as an indicator of the HF
component when repetition rate is concerned and therefore, their rate patter can be
correlated with behaviours and provide information on the communicative function of the
sounds (Amundin 1991).
Nakamura et al. (1998) associated 10 behaviours with the click pattern (number of
clicks, click-interval, and sound pressure level) of the HF component. They found the
click-intervals during snouting (defined by Amundin & Amundin 1971 as sideward turn)
being significantly shorter than those associated with other behavioural categories. This
showed that the repetition rate patterns of the HF component clicks conveyed
communicative information, as suggested by Amundin (1991).
Clausen et al. (in prep) also showed that the repetition rate pattern of the HF
component clicks conveyed communicative information, finding more click repetition rate
of the sounds linked to other behaviours. The behaviours with a sound correlate were
aggression1, contact call (from a calf towards her mother), echelon behaviour – the calf
swimming underneath the mother, closely related to nursing and sleeping in dolphins,
defined as infant position2 (McBride & Kritzler 1951; Reid et al. 1995)– and to some
extent grooming3. In addition, it was demonstrated that the repetition rate pattern in
aggressive encounters did not differ in three different contexts and interactions between
different individuals.
The main differences in the acoustic communication used by harbour porpoises by
means of using ultrasonic clicks, as compared to dolphins, is that the range at which the
sounds can be transmitted is much smaller, and that the sounds can convey less
information than for example frequency modulated whistles (Amundin 1991; Tyack
2000). The communicative system is therefore, constrained by or constraining the social
structure. A dichotomy has been stated taking into account communicative sounds and
gregariousness, species producing whistles are much more gregarious, forming schools of
up to several hundred animals; on the other hand non-whistling species tend to be less
gregarious forming small groups or being solitary (Herman & Tavolga 1980).

1
Corresponding to sideward turn defined by Amundin & Amundin (1971)
2
Not to be confused with echelon position were the infant swims besides the mother (McBride and Kritzler
1951, reviewed by Jacobsen 2003).
3
Defined by Amundin & Amundin (1971).

25
 Tyack (2000) categorized communication signals according to their function,
dividing them into interspecific and intraspecific signals.

Interspecific communication signals. The fact that communicative signals can be

intercepted by prey or predators, have probably shaped the communicative signals of
cetaceans. Harbour porpoises have high-frequency signals above the hearing threshold of
bottlenosed dolphins and killer whales, avoiding being intercepted by their main predators;
additionally, harbour porpoises have sensitive hearing in the frequency range of dolphin
whistles and killer whales. The predators, on the other hand, have poor hearing in the
frequency range where porpoises echolocate and communicate. Therefore, porpoises are
able to detect and avoid them (reviewed by Clausen 2008 and Morisaka & Connor 2007).

For intraspecific communication signals, the differential functions (according to

Tyack’s (2000) classification) that have been observed or can be expected, are: signals for
increasing the chances of mating, agonistic relationships or fighting assessment, parent-
offspring recognition, cohesion and coordination in a group and individual differentiation
or the maintenance of individual-specific social relationships. However, these functions
may be expected depending on the social characteristics of the species.
For harbour porpoises, small groups have been reported, but also less frequently
larger aggregations. The cohesion of the small group sizes can be maintained with the
communication at short range possible for porpoises, which might show that close
communication is the major need for the species. The larger conspecific aggregations
could be explained by fixed routes (migrations), stationary food aggregations, or common
meeting places for example for breeding (synchronized breeding in different areas),
defined by the coast line and bottom topography (Amundin 1991, Amundin & Amundin
1974, Norris & Dohl 1980).
Cohesion and coordination of large groups as observed in dolphins would not be
required by harbour porpoises, as the groups can probably keep in contact using ultrasonic
clicks, and thus their inability to produce omnidirectional cohesive-coordinator whistles
would reflect the lack of this larger structural requirement as observed by Herman &
Tavolga (1980). Hector’s dolphins (Cephalorhynchus hectori), another inshore species
with an average group size of 4, also uses only clicks for communication (Dawson 1988).

26
 A possible mating call was observed by Amundin (1991). This short-range call
together with visual displays and the fact that porpoises meet at common feeding areas,
seems sufficient to permit the sexes to meet for mating in this species.
Aggressive sounds have been demonstrated in porpoises, as reviewed above
(Clausen et al. in prep.), as well as a visual display (reviewed below). Hierarchies have
also been observed in captivity associated with visual behaviours. This functional category
has been observed and is only expected to occur at close distances.
Amundin (1991) suggested that individual differentiations could be observed in the
“mating call” and other sounds; however Clausen et al. (in prep) did not find any
individual differentiation in the communicative sounds. It should be taken into account
that other sensory capabilities could be used for differentiating individual identity as for
example different colour patterns. However, no investigations have been done in this
respect. It is not known, at which range the individual-recognition is present in harbour
porpoises, but reduced to its basic form mother-calf recognition is necessary; and probably
the recognition of the small-group components, even if the partnership was not lasting
long, is expected. However, until which point, or how many animals can be recognized, is
far from being know in this species as it is just started to be hypothesized in the far much
more well-known dolphins, after many years of studying individuals from diverse
populations (Connor 2007).
Parent-offspring recognition is expected but how it is performed is not known.
Clausen et al. (in prep.) showed that considering the so-called active space – the distance
at which a transmitted signal can be detected by the receiver– of acoustic communication
in porpoises, to keep contact by means of acoustical signalling a maximal distance
between mother-calf should be around 20 meters. It may be however that wild porpoises
use higher intensities than captive ones when signalling, giving a greater active space
(Villadsgaard et al. 2007, reviewed by Clausen et al. in prep.). The mother and the calf
may not always be in acoustic contact, as mother-calves have been observed to be
separated by up to 30 meters (Amundin & Amundin 1974, P. Sabinsky, pers. comm).

Behaviour: what is known from captivity

In this thesis an effort has been made to compile and summarize what is know
from the behavioural studies of harbour porpoises in captivity. Some studies were made in
the 1960s and 1970s, and some others (Benham 1999; Kristensen 1999, Wilson 1999 and

27
Jepsen 2002) have been published as short reviews (Desportes et al. 2003), and two are
published in other languages than English: Swedish (Amundin & Amundin 1971) and
Japanese (Nakamura et al. 1998). The review will be done in chronological order and the
inconsistencies in the nomenclature of behaviours within the different studies will be
clarified. The definitions of the behaviours will be reviewed, to be able to compare them.
The focus will be centred on the social behaviour, reporting the social-related remarks.

Andersen & Dziedzic (1964) published the first behavioural descriptions of

captive harbour porpoises. Eight animals where observed at different times of the year,
and qualitative observations and descriptions explaining sexual behaviour were made.
This study also gave some insights on dominance and aggression, fear and playing
behaviour, as well as resting, learning with other anecdotal observations. The animals
were kept for this study in two indoor-tanks, four harbour pens, and one open air canvas,
of different sizes in diverse combinations.
Courtship and sexual behaviour was observed during about a month and a half
−late May, June− when 3 sexual mature females and 2 males (one of which was sexually
mature) were enclosed together in the indoor tanks (of 15.6m3 and 78m3). Stereotyped
courtship displays were observed consisting of: companionship, chasing, stroking and
cross-swimming, belly-exposure, posturing, rubbing, mouthing, and erection. However,
copulative behaviour− intromission and ejaculation− were never observed. It was stated
that in a later date of their observations, intersexual contact increased.
This display is similar to those of other marine mammals, and some behaviours
which may cause confusion due to a same name but a different description are described
in Table 3.
Table 3. Definitions of behaviours by Andersen & Dziedzic (1964) that may lead to confusion from causes
explained in the text.
Companionship Swimming in both intra and intersexual pairs that often change composition.
Chasing Prolonged male-female pairs swim keeping tactile contact by means of the flippers, flukes or dorsal fin. Called
prolonged companionship (Tavolga & Essapian 1957) in the bottlenose dolphin.
Stroking A male swim above a female stroking his flukes against her dorsal fin.
A male approached the female crossing her pathway from behind in an acute angle, and swam over her. Stroking
Cross-swimming can occur during cross-swimming.
Rubbing Defined as “broad tactile intersexual contact” by rubbing the sides of the body against each other when
swimming in the same direction.
Some behaviours that have been described as sexual behaviours or courtship,
involve behaviours like close swimming in pairs (companionship, chasing) and grooming4

4
Grooming defined by Amundin and Amundin (1971) see below.

28
(rubbing, stroking, cross swimming) may be included in the display, but they also have a
social non-sexual function as have been seen to occur during the non-mating season not
related to sexual activities (this thesis).
Harbour porpoises were reported to be inventive and play with balls, sea stars,
seaweeds, fishes, and other objects. They were easily scared even after being kept in
captivity for a long time. Behaviours annotated to be reactions of fear were described as
speeding up, swimming in small circles keeping away from the stimuli and irregular
respiratory pauses. Harbour porpoises were never observed to be aggressive against
humans. And aggression among animals did not occur very often. Aggression was only
observed when 5 animals were kept together during the
mating season, when the young males were observed to
attempt to bite and or swimming towards the side of their
companions, however tooth marks or scratches were not
observed. The resting position (Figure 2), the blowhole out
of the water, and the tail bent ventrally, was observed to
Figure 2. Resting position in
Harbour porpoises (Phocaena occur 4-5 times per hour with a duration of 4-5 seconds.
phocaena). From Andersen &
Dziedzic (1964), Fig. 7.
The activity pattern seemed similar during day and night.
Feeding was also observed at night. As a remarkable
anecdote with social implications: one animal was found dead, and during the half an hour
before the finding no sounds were heard in the pool where the two animals were kept
together.

Andersen (1969) described the epimeletic behaviour – care giving towards another
animal (Caldwell & Caldwell 1966) – of harbour porpoises. Some cases of nurturant
behaviour – care giving to a juvenile – among older (some juveniles) animals towards very
young sick ones were reported. The animals helped the ill ones to float on the surface to
breath. The same was observed among same aged animals, one of them being ill.
However, the author reports that epimeletic behaviour was not always observed when ill
animals were with conspecifics, not even in the presence of dying suckling calves with
adult females, and therefore the causes that may elicit the behaviour remain unclear.

The other basic descriptive paper of porpoise behaviour was done by Amundin &
Amundin (1971) published in Swedish. Here I rely of an unofficial translation kindly
made by M. Wahlberg. The study was done based on three sub-adult males (one year old)

29
observed during April to September. Some considerations should be highlighted, for
instance the clarification and a better description of the social stroking called by the
authors grooming and detailed descriptions of aggressive behaviours.

Grooming is defined as stroking of two porpoises “by swimming one by another,

where the passer-by touches the other’s dorsal fin or side” the other porpoise contributes
by slowing down its speed, as shown in Figure 3. It does, therefore expand and describe in
much more detail the rubbing described by Andersen & Dziedzic (1964). It is pointed out
in the paper by Amundin and Amundin (1971)
that the dorsal fin of porpoises is supplied
with ceratinous humps used by conspecifics as
a way of scratching each other and to remove
dead skin. This definition confers a social and
hygienic-healthy function, as seen in primates
and other animals, and the name grooming
reflects this analogy. As empirical evidence
they explain that porpoises that were isolated
and with skin problems due to the sensitivity
to the chloride of the water, after being put
with other conspecifics started immediately to
groom, and after some hours the skin was
normal and the skin fragments were visible in Figure 3. Grooming behaviour of Harbour
porpoises (Phocoena phocoena) from Amundin
the water. Also, porpoises rubbed themselves & Amundin (1971).
against irregularities in the pool when isolated, and this was not observed any more when
other animals were introduced in the pool. In relation to sound production, grooming was
performed silently, only few series of clicks were emitted.
Stress reactions were described in accordance with Andersen & Dziedzic (1964) as
porpoises swimming closer and faster when scared, staying more underwater and
breathing more explosively. A sound was correlated with this behaviour and being
described like a “long-stretched sound from a sheep”, with and acceleration of the click
repetition rate and constant clicking afterwards. The mean average duration of this call
was 3s. It should be taken into account the age of the animals, being one year old, Clausen
et al. (in prep) stated that the sound emitted by a calf when separated from her mother,
could be the sound described as a stress reaction in this very young animal. The young

30
porpoises in the study by Amundin and Amundin (1971) emitted the sound when
separated from each other during a big storm, when hungry, and when they were frustrated
after not performing correctly, the training requirement and not getting a reward.

Agonistic behaviour was described in

detail in the Amundin & Amundin (1971) paper.
They noted diverse ways of threatening, escapes
and what they defined as aggression-inhibitive
behaviour. Threatening was mostly seen by
means of a sideward turn of the head and frontal
part of the body with closed and less often open
mouth towards the head of the threatened
porpoise, as shown in Figure 4. The intensity of
the aggression is greater if during the sideward
turn it hits its antagonist with the snout. Hitting
was only seen once. There is a characteristic
sound that occurs simultaneously with
aggression, as reviewed above. The frequency of
the aggressive behaviour was several times per
hour during the first introductions of one
porpoise that the other already was familiarized
two. A few days after the introduction,
aggressive sounds were rare and only observed a
few times a week.
Figure 4. Aggressive sideward turn in Another type of aggressive behaviour
harbour porpoises, from Amundin &
Amundin (1971), Fig 1. described by Amundin & Amundin (1971) was
jerked noddings that were seen to occur either
directed or not directed (as a sign of frustration) towards another animal. Pushing the
antagonist while nodding was also observed and supposed to be of a more intense nature
than jerked noddings or sideward turn. Noddings were usually performed with closed
mouth, and less often with open mouth. This open mouth aggressive behaviours have
never been observed to be followed by biting, and this is corroborated by the fact that
scars have never been found. This could outline the already described biting behaviour

31
observed by Andersen & Dziedzic (1964) that was also stated to not leave any mark; and
is therefore the same as an aggressive sideward turning, touching with open mouth.
A behaviour that was defined as an aggression reducer is a short beat with the tail
when swimming. However is not entirely clear which function this behaviour has.
Related to hierarchy, Amundin & Amundin (1971) point out that a ranking
order seems to exist in porpoise groups just as in bottlenose dolphin groups. The hierarchy
was not of absolute character, as it seemed to vary in strength and in diverse activities. In
the three animals, two did not have a clearly established rank but were dominant over the
third one.
Homosexual behaviour was observed in the three young male porpoises; this
has been seen to be a common behaviour among sub-adult delphinids, and especially
among dominant adults. This was performed in the same way as the heterosexual activity
already described in porpoises by Andersen & Dziedzic (1964), by means of grooming
when it is directed to rub the genital area, belly exposure −also observed between male-
male and female-female by Andersen & Dziedzic (1964)−, erection and intromission
attempts. Amundin & Amundin (1971) state that a ranking order can be observed during
homosexual activities, being the less dominant playing more often the female role, as it
has also been observed among dolphins.
Masturbation was observed in the three young porpoises by means of
erection while posturing, also called S-display. A specific audible sound was associated
with this behaviour, and it was possible to distinguish individuals by means of the sound
with the smallest animal having the weakest clicks. Erections were also observed in
conflict situations.
Other playing behaviours where described as blowing water on objects
(insects on the surface, balls), playing together with balls, grooming, having an object in
between, and other swimming games as changes in speed, creating waves, picking up
objects. Learning was observed in several occasions by observing the other animals during
experiments.

Amundin (1974b) published a paper on how playing could reduce the stereotyped
cage habit behaviour caused by the animal being alone for two months in an empty pool.
Concluding that enrichment in artificial environments is a need for welfare. Some new
descriptions of fear reactions and playing were made. Social interactions with the male
were absent when stereotyped behaviour was high, and increased when stereotyped

32
behaviour decreased, showing that sociality in porpoises is also a sign and a need for
welfare.
Stress - fear reactions were concordant with the ones already described (Andersen
& Dziedzic 1964, Amundin & Amundin 1971) and it was again explained that when
panicking the normal surfacing behaviour of porpoises −described by Amundin 1974a−
was performed in a long flat jump at high speed (leaping, described also from field
observations above). The duration of those behaviours are also correlated with how
frightening they were: the longer the more frightening or stressful.
Some toys were reported to be much more attractive, frightening, or uninteresting
than others. The playing behaviour in porpoises was also described as not aggressive in
comparison with dolphins. It was seen than even in unnatural pools the bottom grubbing
(Amundin & Amundin 1974) behaviour observed in the wild was also performed in
captivity.

In Amundin (1974c), a displacement behaviour – i.e. a behaviour that arises as a

result of a conflict, when equal drives are confronted together – is discussed: the function
of a “sudden underwater expiration through the blow hole”. It is shown that when a
conflict arises, the animals react by releasing air form the blowhole, being the expiratory
part of coughing desinhibited. Homosexual activities with a partner of similar rank did
produce this conflict and the air release was observed. There lack of settled rank in the
homosexual behaviour in two harbour porpoises, both three years old, was statistically
significant. Dominance is seen in the animal performing the male role, but both did
perform it equally. Also aggression was considered in order to analyse rank, one animal
threatening (sideward turn) significantly more than the other, and thus, it was mostly
dominant in other context than homosexual activity. The aggressive threatens as a
response of homosexual attempts, the reaction to that aggression, avoidance, or no
reaction, were considered but the reduced number of aggressions related to homosexual
behaviour did not allow statistical analysis. Observations were done from April to
September.

Kastelein & Staal (1997) studied swimming behaviour of harbour porpoises under
different conditions in human care, at the Netherlands Cetacean Research and
Rehabilitation Centre of the Harderwijk Marine Mammal Park. Demonstrating that the
space of the enclosure and its environmental quality –the presence of natural objects (sand,

33
rocks) and marine life (such as star fish, jellyfish, crabs and fish) – as well as the presence
of conspecifics, had a strong influence in harbour porpoise’s swimming patters. The
presence of a conspecific made the stereotypical swimming behaviour of a harbour
porpoise in a small concrete pool (8.6m x 6.4m and 1.2m deep) disappear: the distribution
and frequency of surfacing changed, as well as the swimming pattern, and social
interactions were observed. The swimming behaviour of the animals changed markedly
from the small pool to a larger peen (34m x 20m; 3.2m deep at the sides and 4.7m deep in
the centre). This shows that a richer, more natural environment increases the welfare of the
animals.
Homosexual interactions between a juvenile male (with a length of 122cm at that
time of the study, not expected to be sexually mature), and a calf, estimated to be around
3months old (length 92cm), were often observed in 11 sessions of 15min made during
September and October in the small pool. The same juvenile male (at that time around
138cm) and a juvenile female (143cm of length) observed during 11 session of 15min
were observed to surface simultaneously and close together in May in the larger pen; no
sexual interactions were observed but the observational conditions were much worse than
in the small pool, and their synchronic close breathing indicated a social bond, as has also
been shown in dolphins and other cetaceans (e.g. Connor et al. 2006; Perelberg & Schuster
2008).

Nakamura et al. (1998) published the paper called “Threat clicks of captive
harbour porpoises, Phocaena phocaena” in Japanese, and therefore very few people have
had access to it. Here I rely of an unofficial translation kindly made by T. Ishigami. The
behaviour of the animals was quantitatively measured, but no statistical analysis was
performed as the main focus was on the relation between behaviour and acoustics. A
captive group of 5 harbour porpoises − one male and four females − were observed during
three days in late April (from 25th to 27th). The animals were enclosed in a concrete
outdoor pool, 6m in diameter and 1.5m depth (42,4m3 volume). The behaviour of the
animals was correlated with sound, as reviewed in the Chapter “Acoustic Communication”
above. However, even if it was not the main aim of the study, comprehensive behavioural
observations were performed and presented showing the frequency of occurrence of each
behaviour of the male towards the females, the females towards the male, and each female
towards the others. All this information provides very interesting knowledge of the social
structure and directionality of specific behaviours in these groups of captive porpoises of

34
 different ages and sexes. This is extremely useful
as a basis to compare with the present study. The
most interesting behavioural categories used
were as follows. Pushing up described as
epimeletic behaviour in harbour porpoises
(Andersen, 1969), rubbing (i.e. grooming,
Amundin & Amundin 1971), pecking (i.e.
pushing, Amundin & Amundin 1971), chasing5
(aggressively pursuing another animal), close
swimming, close floating and snouting (i.e.
sideward turn Amundin & Amundin 1971).
The animals had their name assigned
according to their length and gender, N1(152cm),

Figure 5. Frequency of behavioural being the male; N2(170cm) a pregnant female

categories performed by the male towards
that delivered two days after the end of the study,
the females. Fig. 4 from Nakamura et al.
(1998). N3(151cm), N4(148cm) and N5(128cm) being
the females.
Regarding the males’ behaviour towards the
females (Figure 5) was reported to direct, most of his
interactions towards the oldest female (N2). The male
was reported to perform towards the oldest female:
“courtship behaviour” because of the performance of
rubbing and pecking, (according to Amundin &
Amundin (1971) being just affiliative and aggressive
behaviours respectively); “accompanying behaviours”
because of high frequencies of close swimming, close
floating and pushing up, and “aggressive behaviours”
as the male was reported to direct to the oldest female
a high frequency of chasing and snouting. In contrast
the male was described to interact towards the other Figure 6. Frequency of behavioural
categories performed by the females
females (N3, N4 and N5) mostly through chasing and towards the male. Figure 5 from
Nakamura et al. (1998)
snouting, defined as “intimidations”.

5
Do not confuse with chasing as described in Andersen & Dziedzic (1964).

35
 Unfortunately no statistical analysis was performed, and the above-mentioned
descriptions of high and low levels are thus subjective interpretations. The figures are
presented here so that the actually measured data can be observed. In Nakamura et al.
(1998)’s paper, the word “frequency” refers to the counts of the respective behaviours (e.g.
in Figure 5, 6 and 7). The study was conducted during 21.43 hours, and thus, the frequency
of a certain behaviour – i.e. the number of times it occurs per hour – can be calculated.
Females behaved towards the male, as follows (Figure 6). N4 and N3 were
reported to behave frequently towards the male. N4, interacted mostly through snouting.
N3 performed mostly rubbing towards the male, cross swimming and close swimming
were also reported. N2, the oldest female, was mostly resting at the surface, but responded
to behaviours of the male by rubbing and close swimming. N4 directed mostly aggression
towards the male, snouting that ended with peaking (in this case an aggressive but not
sexual function was linked to the behaviour according to the author).
Among females
(Figure 7), the authors
report that the highest
values of interaction were
among N2:N3, N4:N5, and
N4:N3. The higher
behaviours among N3
towards N2, were diving,
rubbing and close floating,
Figure 7. Frequency of behavioural categories performed by each which were attributed to the
female towards the others. Table 1 from Nakamura (1998).
same “accompany function”
described for the male and N2. The snoutings directed from N2 to N3, were seen as a
response of N3 rubbing and close swimming with the male. The same was seen in N4,
which directed aggression towards N3 just after N3 was rubbing with a male. It was also
reported that N4 and N5 were mostly rubbing and close swimming.
This study by Nakamura et al. (1998) shows social interaction, qualitatively
described but based on quantitative data, and was until then the most consistent study of
social interactions among harbour porpoises that had been performed.

Lockyer et al. (2003) made 24-hour watches of two harbour porpoises: Freja, a
2.5-year –old female, and Eigil, a 3.5 year-old male (two of the animals also studied in

36
this thesis), in October 1998, and in February 1999, in a 15x36m 3.5 average depth pen in
a seminatural environment (pool area 1890m3) at Fjord and Baelt in Kerteminde
(Denmark). The budget activity of the two animals was reported, including the percentage
of “social interactions” which included close swimming, touching, and sexual display. No
data was given on the absolute amounts of each of these behaviours. There were no
definitions of neither touching nor sexual display. Thus it cannot be know which of them
were actually observed and in which amounts. Each animal was observed for 8 hours each
(20min per hour each) per day, as only two animals were together, all the interactions
were directed to the other animal, and thus the frequency of interaction the first day
(October) was of an average of 0.376 interactions/hour. The second day (February), 0.26
interactions/hour were reported. Excluding sexual activity (if it was actually observed) the
interactions described were affiliative, and thus give information of the affiliative
interaction at that age in those dates.

Desportes et al. (2003) presented all the projects on the reproductive

function of harbour porpoises made until that time at the Fjord&Baelt, Kerteminde
(Denmark) since the animals arrived to the centre (April 1997). The studied animals were
a male, Eigil, and a female, Freja (the same animals studied above in Lockyer et al. 2003,
and two of the individuals also studied in this thesis). In some studies a third female, Nuka
(arrived in April 1999, and died in February 2000), was observed. Diverse techniques and
approaches were used to gain insights in the reproductive biology –i.e. blood collection
for hormonal analysis, ultrasound examination of ovaries uterus and testes, vaginal and
prepucial smears and behavioural observations (including studies by Kristensen (1999);
Benham (1999); Wilson (1999) and Jepsen (2002)) –. The animals were enclosed in the
same pen described in Lockyer et al (2003) for the studies. The results provides
information on the biological parameters of the species (e.g. age at sexual maturity
according testes volume, and breeding time by means of the majority of sexual behaviour
observed and in some studies confirmed mating by means of presence of sperm in vaginal
smears) that have been reviewed and included in Table 1.
The behavioural observations on sexual behaviour done during training
sessions (observations done from April 1997 to December 1998) showed sexual activity
all the months from October 1997 (the male estimated to be two years old, immature)

6
Frequencies calculated from percentage of time interacting in Table 2, as interaction were considered
reciprocal and average of Eigil and Freja values are presented.

37
until August 1998. However, in observations done from June to November 1998 in the
evening, as a part of Kristensen’s (1999) study, sexual behaviour was absent in June,
September, October and November. It was therefore concluded by Desportes et al. (2003)
that probably the frequent observations of sexual behaviour may be due to the specific
position of the female during training sessions (the female logging straight and immobile
at the surface stationed towards the trainer) that would have elicited a sexual response in
the male. Males have also been seen to try to mate with females while stationed in front of
the trainers in Harderwijk dolphinarium (Harderwijk trainers, pers. comm.). Thus it is not
recommended to study sexual behaviours in porpoises during such circumstances.

Kristensen (1999) (reviewed by Desportes et al. 2003) studied the sexual

behaviour in the male harbour porpoise and its hormonal correlates during 1998.
Behavioural observations were conducted form mid-June to the end of November during
18 days. At that time the male was 3 years old. He became sexually mature in May 1998
(based on testes size), when the only female present (Freja) was two years old, and
immature. Results presented show non-sexual contact, erections and mating attempts.
Sexual behaviour was observed from July to mid August, erections ranging from 41 per
hour to 15 per hour, and mating attempts observed a maximum of 26 times per hour and a
minimum of 13 per hour (during the time sexual interactions were observed, numbers
obtained from Fig 6 from Desportes et al., 2003). Non sexual contacts (that due the lack of
more information will be considered affiliative interactions) were observed in 12 of the 18
days observed, from the end of June to the beginning of September, and one day in
November, being the highest level in August with 28 non-sexual contacts per hour.

Benham (1999) studied the behaviour of the older female (Freja) specially
focusing on her role during sexual activities and courtship behaviours, that was estimated
to be 3 years old at that time. The other animals present at that time where Eigil, a 4 years
old male, and Nuka, which had arrived to the centre in April 1999, estimated to be 1 year
old (115cm of length at arrival). Observations were done from the last week of June to the
first week of September of 1999, in 36 days of observations, during evening dedicated
observations.
Sexual activity was seen to be high in early July, and had another peak in early
August. Vaginal cytology showed that the receptive time for Freja was late July, early
August, but spermatozoa were found from late June to early August. It was seen that the

38
male had the leading part in the sexual activity initiating the approaches, but the female
allowed copulation by cooperated in sexual activities or avoided them. Two new
behaviours were described: roll and hover performed by the female. Roll was described as
the female twisting or rolling as a response to a mating attempt, avoiding it. In contrast in,
hover, the female remained motionless as a response of a mating attempt, allowing it, and
usually copulation was achieved.
Even if sexual activity was higher at those reviewed times, and spermatozoa only
observed in a reduced period, sexual behaviour was observed during all the observed days
(last June to first September). The maximum frequency of mating attempts per observation
were 46 attempts/hour and the average for all the period was 8.3 mating attempts/hour.
Grooming7 was also measured between the focal animal (Freja, the older female)
and the other animals; and aggression among the focal animal and the male. And the
magnitude orders at which they occurred are reported. Grooming of Freja with Eigil was
infrequent, only observed in 18 out of the 36 days (mainly observed from 2nd July to the
18th of August), with frequency values that ranged from a minimum of 0 to a maximum of
4 grooming/hour, and a mean frequency of 0.4 event/hour. In contrast with Nuka,
grooming was observed during all the observational period in 34 of 36 days, with
frequency values that ranged also from a minimum of 0 to a maximum of 31
groomings/hour, the average of all days was 9.8 groomings/hour. Thus, the affiliative
bond among the females was stronger than among Freja-Eigil. The general trend for all the
“proximity and affiliative” behaviours with both animals decreased during the
observational period (statistically correlated with day).
Aggression8 and chasing9 were also reported among Eigil and Freja. Aggression
from the male towards the female was observed only 3 out of the 36 days of the study,
values ranged from a minimum of 0 to a maximum of <1 day, the average frequency in all
the observed time was reported to be 0.04 events/hour. In contrast, the aggression of the
female directed towards the male was observed more often, in 11 of the 36 days, with a
maximum of 4agreessions/hour and an average of 0.4 events/hour for the whole period.
Chasing was seen more often than aggression, (aggression is a quickly behaviour and it
would probably have been missed more easily than chasing that is much more apparent).
Eigil chasing Freja was observed in 16 observations, with a maximum frequency of 3

7
The same definition as Amundin & Amundin (1971).
8
I.e. sideward turn, Amundin & Amundin (1971).
9
Defined as Nakamura (1998).

39
events/hour, and an average of 0.5 chases/hour for the 36 days. As seen in sideward turn,
chasing was also more often directed from Freja to Eigil than opposite. The female chased
the male in 33 days from the 36 observed, with a maximum frequency per observation of
22 chases/hour, and an average of 2.3 events/hour in the whole period. All this frequencies
prove basis of sexual activity levels, aggression and affiliation at that time (considering the
age of the animals and the environment).
It is interesting to highlight that Benham (1999) points out that stroking, cross
swimming, posturing, and mouthing, described by Andersen and Dziedzic (1964) were
never observed. Mouthing10 was also described by Amundin & Amundin (1971) with an
aggressive function, and by Nakamura (1998)11 and posturing was also observed by
Amunidn & Amundin (1971) in sexual related contexts.

Wilson (1999) described the behaviour of Nuka, the one year old female that had
arrived to Fjord&Baelt in April of that year. Her time budget at that time of the year
(mating season) and that age, and her differential relationships with the older porpoises,
the male Eigil and the female Freja shows that the interactions with the older animals were
initiated by the older (dominant) ones. As well an age-related development and
familiarization with the environment was concluded to be seen in the focal juvenile
female. The observations were done at the same time as Benham (1999) observations, and
thus some values and tendencies have already been described above. The study was
conducted from the 7th of July to the 7th of September in 1999.
Quantitative measures were used on the defined behaviour, but detailed
descriptions and qualitative observations were also done, which permits a better
understanding of the social interactions, and behaviour of harbour porpoises.
Bottom grubbing, as observed in the wild (Amundin and Amundin, 1974) was
observed as a common behaviour of the harbour porpoises in the semi-natural
environment. The young female, showed playful behaviours very often. Playing was
observed by diverse relaxed motor patterns, changing directions and depths when
swimming. For instance, the young animal was seen to lay vertically on the surface with
the tail directed downwards. In between bottom grubbing events, upward glides were
performed obliquely to the surface. Dropping and recatching objects (jellyfish and sea

10
reviewed above as a more aggressive display of touching (touching with open mouth) (Amundin &
Amundin 1971)
11
Nakamura (1998) called it biting.

40
stars), as already described by Amundin and Amundin (1971) and Andersen and Dziedzic
(1964), were also seen. The calf was observed swimming along the surface belly upwards.
All behaviours were reported to seem to occur in bouts. Behaviours such as
grooming12, playing, bottom grubbing, swimming alone and sexual activities were more
likely followed by the same kind of behaviour. Grooming was observed to be more
frequent when sexual activities peaked, therefore, social interactions were clustered, and
bottom grubbing and playing were performed alone, mixed with lonely swimming
patterns.
Grooming among females followed the motor pattern described by Amundin &
Amundin (1971). However, it was observed with the male in very few occasions, and the
rubbing observed among male-female was seen to be quickly and with “rostrum contact”
(i.e. aggression), and therefore it should not be considered the same social interaction. And
this description should be then applied for the grooming observed between Freja and Eigil
in Benham (1999).
Belly exposures were seen to be directed female-male, and male-female but also
female-female. The immature female, Nuka, was also participating in sexual activities,
and seen to collaborate (i.e. hover, described by Benham, 1999, and lifting the tailstock
when copulation occurred).
Considering overall proximity measures of the focal animal with the others, close
swimming (in the study called “free swimming with Eigil/Freja”) was more often
observed with the older female than with the male, the same seen with close resting, and
with grooming that was observed 88% of the time with the female and 12 % of the time
with the male. If orders of magnitude are considered, grooming between Nuka and Freja
was on average in all the period of a frequency of 12.6 + 8.5 + 3.8 (grooming events/hour)
corresponding with grooming divided in diverse categories (i.e. and a total average of
affiliative interactions of 25 event/hour) with maximums of 36.6 + 24.4 + 13.7 events/hour
(i.e. around a maximum of 75 affiliative interactions per hour).
Aggression toward Nuka was (by means of chasing) was seen on an average 2.5
chases/hour with a maximum of 8 events/hour. In contrast with the chases directed by
Freja to Nuka, being on average 0.5 chases/hour, with a maximum of 6.2 per hour. Nuka
did not direct any aggression to the older female, and less aggression than received by any

12
Grooming, same definition as Amundin & Amundin (1971), divided in subcategories that will be
considered together in this review.

41
of the adults towards the male, on average 0.2 chases/hour with a maximum of 1
chase/hour observed.
As overall conclusions on the frequencies and durations of interactions, the author
reports that they decrease at the end of the sexual season (male-female and female-
female). The stronger female-female relationship, in comparison with the one between the
female and the male, was proposed to be caused by a) a mother-calf relation, b) a
dominant-subdominant relation or c) caused by the mating period. As observations were
only done in the sexual season, and the female-female relation seemed to decrease towards
the end of the study, as well as the female-male one.

Jepsen (2002) studied the sexual behaviour in a female harbour porpoise and
hormonal correlates. The animals studied were Eigil, at that time a 5years old male; and
Freja, being 4 years old. Behavioural observations were done from March 2000 to March
2001. Vaginal smears were collected from January 2000 to October 2001. Spermatozoa
were present in the vaginal smears of Freja from July to early September 2000 and from
mid-July to early October 2001 (see Table 1). Thus, an overall seasonality in the sexual
behaviour was observed according with the receptivity of the female. Desportes et al.
(2003), reviewing this study, reports that females were not seen to initiate the mating
behaviours but exhibited specific behaviours that decided the outcome of the matting
attempts.
Focusing the attention on the behavioural observations, it is necessary to point out
that sexual behaviour was observed from the beginning of April to mid-November (being
both adult animals), and thus observations of sexual activities were much more extended
than the specified “mating season”. The reasons might be several, an artefact of captivity
by the presence of both genders, or that the mating season is more extended than
previously estimated but that conceptions are restrained by the female receptivity.
Whichever the reason is, it is very important to highlight these finding, as is the first time
a study of sexual behaviour in mature animals has been done during such an extended
period.
Jepsen (2002), reports that social interactions among Freja (female)-Eigil (male)
were observed parallel to sexual interactions, being both low from April to mid July, both
higher from mid-July to mid-August, and both lower again, on average remaining low
until December. Sexual and social behaviour were not observed from December to April
(however, observations were done once per month, instead of every second week, in

42
December, January and March, and observations were not done in February). Sexual and
social behaviour were significantly higher during the mating season than during the rest of
the year.

WHY THE SOCIAL STRUCTURE IS IMPORTANT

Population parameters such as dispersal, reproductive success and mortality are

strongly affected by the social structure (Whitehead, 2008). The social structure can also
act as an evolutionary force by means of inclusive fitness − “interactions between relatives
on one another's fitness” −, that leads to social selection (Hamilton, 1964); or by means of
the evolution of reciprocal altruism − “cooperation of non-relatives” − (Trivers 1971).
Additionally, social structures can explain the evolution of sexual size dimorphism,
signalling systems and cognition (reviewed by Whitehead 2008). And the degree and
pattern of spread through individual-to-individual depends on social structure, as for
example the transference of information (Lusseau 2003), or disease (Whitehead 2008).
Therefore, behaviour in general, and especially social structure, has a major importance in
conservation issues (Sutherland 1998). The knowledge of behavioural aspects, such as
mating systems, breeding systems, and general social structure, helps in predict in which
specific way it is necessary to act in conservation strategies (and for assessing
management units); and this necessary approach has been largely lacking (Sutherland
1998). As formulated by Whitehead (2008): “Social structure is important, and scientists
should study it”.

THE STUDY OF SOCIAL ORGANIZATION IN HARBOUR PORPOISES:

WHY STUDYING CAPTIVE ANIMALS

Cetaceans have been kept in captivity since at least 1860 (Defran & Pryor 1980)
and since then a great diversity and number of species has been kept in aquaria. It should
be therefore expected a huge amount of species-typical behaviour descriptions, but this is
far from being the reality (Defran & Pryor 1980). Some behavioural work has been done
in the most well-known species, mainly in the bottlenose dolphin (e.g. McBride & Hebb

43
1948; McBride & Kritzler 1951; Tavolga & Essapian 1957 in dolphins; Recchia 1994 in
belugas; among others) however the general tendency have shifted towards studies in
natural settings, which is reasonable and necessary to obtain descriptions on behaviour not
constrained by animals in captivity. However passing by the unique opportunities that can
be gained from studying animals in oceanaria would be inexcusable due to the perfect
observational conditions that are difficult to obtained in the wild (Defran & Pryor 1980).
Very few anecdotal observations have been made underwater in the field due to the
difficulties observing, and therefore most of what is known from details of social
interactions comes from captive groups (Norris & Dohl 1980).
The study of social organization of harbour porpoises has an additional
inconvenience. Individual identification is the basic knowledge needed for the study of
social interactions, and photo identification – one of the most efficient techniques for
studying wild cetaceans– has been proven not to be possible in harbour porpoises (Graner
2003). As harbour porpoises have very reduced differentiable features among individuals
(Graner 2003). Therefore, captive situations offer the best possibility of studying social
interactions, having a complete overview of the behavioural scene where interactions
occur and being able to individually identify the animals that are interacting. Genetic
studies and satellite telemetry13 of animals caught together, are also potential ways of
achieving insights in the social structure, but animals pertaining to the same group would
be need to be actively caught and or marked; requiring high economic and effort
investments.
Despite the fact that the observed relationships may be influenced by the captive
situation, and the stock of animals kept together is completely artificial, bonds and
avoidances, aggressiveness and affiliation will give information about natural links or
rejections. And the social structures observed in captivity tend to reflect the general
structure in the wild (Nakamichi & Kato 2001). Also, comparative and field studies have
demonstrated that fundamental social patterns are conserved specially in “naturalistic
captive environments” (reviewed in Wilson 1999).
Porpoises was a difficult species to keep in captivity during the first 20 years of
trying (Read et al. 1997). However, the situation have changed since the development of
adequate husbandry techniques as has been developed and employed in e.g. the

13
As two pairs of individuals accidentally caught together had already provided some insights on their
relatedness and posterior proximity patterns (Teilmann et al. 2007).

44
rehabilitation centre for stranded porpoises in Harderwijk (Read et al. 1997). Therefore,
the possibilities for performing studies in captivity are now better than ever.

AIMS OF THE STUDY

Little is known about the social interactions in harbour porpoises. The aims of this
study have been centred on quantifying (quantitave measures) the differential interactions
among animals of different sex and age, at different times and different environment, and
thus provide some insights in to the possible social structure of the species.
Two main aims can be highlighted: First, obtain information on the biology and
possible natural links may help understanding the natural social pattern. Second, studying
social interactions in captivity will give some basis for future management of harbour
porpoises in aquaria. To successfully keep animals in captivity, knowledge is required on
adequate transport, husbandry and medicine of each species, as well as a comprehension
of their sociobiology (Defran & Pryor 1980). The attention will be focused on the specific
following questions:
- Which kinds of interactions are observed among harbour porpoises and at
which levels.
- Are animals observed to have differential bonds with specific animals?
Differences by gender, age of the porpoises, and by the time the bonds are
observed.
- How is the relation of young with adult porpoises?
· Has any alloparental-care behaviour been observed?
· Are males especially aggressive towards young?
- How is the relation among same sexed animals? And among male-females?
- How is the mating strategy?
· Do males compete among them for mating, do they form coalitions?
· Do females and males have a non-sexual bond? Or interactions between
males-females only occur related with sexual activity?

45
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 ARTICLE MANUSCRIPT

Social interactions in captive harbour porpoises

(Phocoena phocoena)

Lara Delgado, Magnus Wahlberg and Ulrik Nørum

In prep.

54
 Social interactions in captive harbour porpoises
(Phocoena phocoena)

Lara Delgado1*, Magnus Wahlberg1,2 and Ulrik Nørum3 ¤

1 Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark.
2 Fjord & Baelt, Margrethes Plads 1, 5300 Kerteminde, Denmark.
3 National Environmental Research Institute, Silkeborg, Denmark

ABSTRACT

There is an almost absolute lack of information on the social structure of harbour porpoises (Phocoena
phocoena). Such knowledge is necessary for adequate conservation measures, and for appropriate
management of individuals kept in aquaria. Therefore, social interactions of two harbour porpoises’ groups
kept in captivity in Kerteminde, Denmark (4 animals) and Harderwijk, Holland (6 animals), were studied by
means of quantitative analysis of the affiliative, aggressive and sexual interactions between the individuals
of each group.
The average levels of aggression per individual were found to be 1.7 (± SEM 0.8, maximum level 4)
aggressions/hour in Kerteminde. And the highest frequency of affiliative interactions was 29.2
interactions/hour between a mother and her calf.
Sexual interactions were observed in Harderwijk at the end of May, and sexual interactions were never
observed in Kerteminde in December and January. This reinforces the assumptions of seasonality in the
mating behaviour inferred in the field by indirect techniques. And that seasonality seems to be maintained in
captivity.
An immature female (2y) showed higher levels of sexual activity than the older individuals. Females decided
the outcome of the sexual interactions. All males attempted to mate with no preference towards any certain
female, and all males had the same mating possibilities. Neither coalitions nor hindering was observed
among males. This is the first empirical data supporting the promiscuous mating system usually assumed in
this species. Furthermore it suggests that juveniles are more sexually active than mature animals, and that
females choice decides the outcome of a sexual interaction. Homosexual interactions were observed among
the males in Harderwijk.
Male-female affiliative interactions were only observed during the mating season This hints they probably
have a sexual function. In contrast female-female affiliative interactions were observed both during and
outside the mating season. Male-male affiliative associations occurred during the mating season, but whether
it is also occurring outside the mating season is not known. The average duration of affiliative interactions
per pairs was significantly shorter during the non-mating season than during the mating season.
A significantly stronger affiliative bond in Kerteminde was found among a mother-calf pair, than the
affiliations among the oldest female (12y) and a younger one (5y), the younger probably subdominant as
inferred from the direction of aggressive interactions.
In Harderwijk the male-female, female-female and male-male affiliative interactions observed had a similar
strength (during the mating season). The adult mature males affiliated together. The mature female had a
social bond with all the males supporting the link of male-female affiliation with a sexual function, as any
male affiliated with the immature female. The immature male (2y) affiliated with the younger mature male
(9y); and the immature female (2y) affiliated with the mature female (4y) supporting that young affiliate
with an older animal (the next in age), but was not observed in Kerteminde between the mature (5y) and
immature (2y) females. Aggression was higher in the adult females than in the immature porpoises.
Many social interactions were observed with a diversity of social displays performed. Additionally different
directions of interactions depending on sex, age and season were clear, showing that sociality is an important
feature in the biology of the species, and complex interactions are present.

Keywords: social structure, harbour porpoise, captivity, affiliation, aggression, sexual

interactions, bond.
*Corresponding author: Tel: 0034 646 11 58 01. E-mail address: lara_6_a_secas@hotmail.com

¤ The third author, Ulrik Nørum, has not been able to comment on all the text of this manuscript at the time of printing this thesis. His
comments will be included before the submission of the paper to a journal.

55
 INTRODUCTION

Harbour porpoise (Phocoena phocoena) is one of the smallest species of toothed

whales, and mainly inhabits coastal areas of the North Atlantic and Pacific Oceans (Read
et al. 1997). Their life history can be described by a relatively quick life cycle in
comparison with other Odontocetes (Read et al 1997). Harbour porpoises mature at 3-4
years of age, have a gestation period of 10-11 months (Lockyer 2003), and live an average
of 12 years up to 24 (Lockyer 2003). Harbour porpoises have, like other toothed whales,
large brains (Tyack 2000) and they use both acoustic and visual displays as a part of a
broad behavioural repertoire to interact with conspecifics (Andersen & Dziedzic 1964,
Amundin & Amundin 1971, Amundin 1991, Nakamura et al. 1998, Clausen et al. in
prep.). These characteristics predispose them for social complexity. To find their prey they
echolocate, using extremely high-frequency short signals (Møhl and Andersen 1973),
identical to the ones used for acoustic communication (Amundin 1991, Clausen et al. in
prep.).
Little is known about the social structure of this species, and it has long been
considered to be rather asocial, or even solitary (e.g. Evans 1980). The scarce knowledge
of harbour porpoises’ social structure can be summarized in mother-calf bonds, seen to
last for at least 11 months (Teilmann et al. 2007), and from what we know of the average
group size. The average group size is around 2-3 animals, usually ranging from 1 to 10
individuals (e.g. Kizska et al. 2007; Goodwin 2008; Berrow et al. 2009); however, larger
aggregations of up to 100 individuals have also been reported (Lockyer & Kinze 2003). A
great variability has been seen in the group composition depending on the geographical
area, the distance from shore, the season and the time of the day (Møhl-Hansen 1954;
Neave & Wright 1968; Goodwin 2008), probably due to a sum of factors such as the
distribution of prey (e.g. Bjørge & Tolley 2002), environmental factors (Edren 2009) and
breeding areas (Lockyer & Kinze 2003).
The knowledge of harbour porpoise social structure lags far behind from what is
known from some other cetacean species, such as killer whales (Orcinus orca; e.g. Baird
2000); sperm whales (Physeter macrocephalus; e.g. Whitehead & Weilgart 2000);
humpback whales (Megaptera novaeangliae; e.g. Clapham 2000), and bottlenose dolphins
(Tursiops truncates; Connor 2007). The major reason for this is that it is virtually
impossible to individually identify animals in the field (Graner 2003). This means that on
of the basic tools for studying social structure in cetaceans, photo-identification, cannot be

56
used for this species. Not even gender differences can be distinguished in wild harbour
porpoises as it can be done in other cetaceans (as for example in Dall’s porpoise
(Phocoenoides dalli); Willis & Dill 2007). The only insight on group composition can be
obtained by the clear differential size of calves and their mothers.
Thus, more detailed knowledge of the relationships, gender, duration of
associations and other insights of social patterns between individual porpoises cannot be
obtained from visual observations of animals in the field. Therefore, scientists must rely
on other techniques to derive such information. Studies of animals in captivity offer a
great possibility. Even though the captive situation influences the animals’ behaviour,
social relationships, bonds and avoidances, aggression and affiliation, can give
information on behavioural patterns also occurring in wild groups of animals, as social
structures that are observed in captivity tend to reflect the general social structures in wild
populations (e.g. Nakamichi & Kato 2001).
Some previous studies in captive harbour porpoises have provided insights
into the social and sexual interactions, especially during the mating season (Nakamura et
al. 1998; Desportes et al. 2003). However, most of the previous investigations have
centred on other topics. Earlier papers on this subject were descriptional in their nature
identifying the behavioural repertoire of the animals: sexual, social and epimeletic
behaviour (Andersen & Dziedzic 1964; Andersen 1969; Amundin & Amundin 1971;
Amundin 1974a, Amundin 1974c), welfare and enrichment: stereotypic behaviour
decreasing with changes in the environment and the presence of a conspecific (Amundin
1974b; Kastelein & Staal 1997). Also, sounds production has been correlated with specific
behaviours (Amundin 1991; Nakamura et al. 1998; Clausen et al. in prep).
This study aims at providing basic insights into the social structure of two groups
of captive harbour porpoises by means of quantitative analysis of their social and sexual
interactions. Two study locations were chosen to hopefully be able to derive more general
conclusions.
The behavioural observations were made on the four animals kept in Kerteminde
(Denmark) in January and on six animals kept in Harderwijk (Holland) in May. The
observation periods in Kerteminde were chosen to optimally complement data from
previous studies, and the one in Harderwijk was chosen to be during the mating season.
Basic knowledge of links among the individuals, that will help understanding their social
pattern, were obtained. This information will help to give some basis for future
management of harbour porpoises both in the field and in aquaria.

57
 MATERIALS AND METHODS

The study subjects were two groups of captive harbour porpoises (Phocoena
phocoena), one group kept at Fjord&Baelt in Kerteminde (Denmark), and the other in
Harderwijk dolphinarium (Holland).

Kerteminde
Animals
At FoB, all four harbour porpoises (Phocoena phocoena) were studied: three were
females of different ages and one male. Biological information of the animals is presented
in Table 1. The youngest animal, the first animal born and survived in captivity, Frigg,
was parented by Freja and Eigil (Blanchet et al. 2008). The other three animals were taken
from pond nets where they were accidentally bycaught (e.g. Desportes et al. 2003).

Table 1. Biologicla data of the harbour porpoises kept at Fjord&Bælt, Kerteminde (Denmark). ID, name,
gender, estimated age, length and weight at the time of the study, location of bycaught, date of arrival, estimated
age at arrival, and length at the first measure are shown. *This measure was taken at age 1m and 3w. **This
measure was taken at 3m and 1w. ***Very inaccurate, as the animal was moving during measurement. D:
Denmark, y: year, m: months and w: week.

Estimate Length Weight Estimated Estimated

Location of Housed Length at
ID Name Gender d age Dec 09 Dec 09 time of birth age at
catch since arrival (cm)
Dec 09 (cm) (kg) **** arrival
F1 Freja F 12y 6m 156 58,3 D: Korsør 07/04/1997 June, 1996 10m 127,5

4y and 8 D: Fjellerup early spring,

F2 Sif F 147 48,7 23/07/2004 2 to 12 m 106
to18m Strand 2004

F3 Frigg F 1y 4m 116 31*** Born at FoB 08/08/2007 August, 2007 Born at FoB 89*

M1 Eigil M 13y 6m 141 44,9 D: Korsør 07/04/1997 June, 1995 1y 10m 130,5

For a comparison of individuals between the two facilities, the animals have been
assigned an ID depending on the gender, and the relative lengths of the animals of the
same gender, in decreasing order as decreasing the length (Nakamura et al. 1998). The
ages of Sif, Freja and Eigil were estimated based on their lengths when arriving at the
centre, and their growth curves (Wahlberg et al. in prep).

Environment

The behavioural observations were conducted at FoB, where the harbour porpoises
are housed in a semi-natural outdoor enclosure in the harbour of Kerteminde. The pool has
natural rocky and sandy bottom, and it is separated from the harbour by nets, which

58
provides natural environmental conditions of water flow and quality, tidal currents,
temperature, and also allows the entry of small-sized flora and fauna into the enclosure.
The enclosure is 15m x 36m with an average depth of 3.5m ranging from about 2 to 4m
(Lockyer et al. 2003). The enclosure is divided into two pens, separated by a net with
gates. During the time of the study the animals were usually separated in combinations of
two individuals in each of the two pools during the centre opening hours (8AM to 4PM).
Sometimes during the day, and always during the nights, the gates were open allowing the
four porpoises to freely swim between the two enclosures. During the observations the
four animals were gated together into the smaller 11xs14 m pen. The animals could be
viewed within the area with an open water surface covering 9x13 meters, and they would
disappear out of site when swimming under the floating pontoons covering on the sides of
the pool. It should be considered that the four animals were usually not kept together in
the small pool.

Data collection
Acoustic and visual data were simultaneously recorded in Kerteminde during the
observations. Visual data was collected from a height of 5m overlooking the experimental
pool with a Philips LTC3361/32 video colour camera digitalized with an AV400 Grabster
card connected via USB to a laptop computer. Acoustical data was recorded with two
calibrated hydrophones, Reson 4014 (sensitivity: -187dB re 1V/µPa at 130kHz),
horizontally separated by one meter along the one of the shorter sides of the pool. The
signals were filtered with a highpass filter of 10kHz and a lowpass filter of 200kHz, and
amplified 40 dB, with a custom built amplifier, fed through two porpoise echolocation
click detectors, and digitalised by the Grabster card for synchronization of sound and
video.
All the behavioural observations and all analysis of the videos were performed by
the same observer. Frequency and the duration of behaviours were counted by means of
the shareware “Etholog Version 2.2” (Ottoni 2000), where the output can easily be
transferred to Excel for further analysis.

Behavioural sampling
One hour of continuous recordings were made after sunset, at ten days in
December (2nd, 3rd, 6th, 8th) and January (8th, 10th, 14th, 22nd, 28th, 29th) in 2008/9, being a
total of 10 hours of observations. Observations dates were randomized among days with

59
 appropriate weather during December and January. To maximize visibility, and avoid
disturbances on the animals’ behaviour, observations were performed after the sunset with
artificial lights illuminating the experimental pool, as harbour porpoises show neither
diurnal nor nocturnal patterns in their behaviour (Andersen & Dziedzic 1964; Teilman
2007).
The animals were marked with innocuous baby-cream to be able to identify them.
Each animal was observed continuously during one hour, except when they swam under
the pontoons. Video recording were observed several times to describe the behaviour of
each animal. The sampling method used would be the defined by Altman (1974) as
“Sampling all occurrences of some behaviours”14 –recording all occurrences of social
interaction in the group– or “focal sampling” –each individual being the focal animal
during 10 hours– if the reduced amount of time each individual was not visible is
disregarded.
Harderwijk
Animals
Six males and females of different ages held in Harderwijk dolphinarium were studied. A
seventh harbour porpoise, not included in the study, was separated from the others (a
pregnant female soon to give birth). They were all stranded animals rehabilitated in SOS-
dolphinen. Most healthy animals of sufficient age are released after rehabilitation, but
these animals were kept for various reasons indicated in Table 2, together with other data
of the animals.

Table 2. Biological data of the harbour porpoises kept in Harderwijk dolphinarium (The Netherlands). ID, name, gender,
estimated age, length and weight at the time of the study, location of stranding, date of arrival, estimated age of arrival, length at the
first measure, and the cause for the animals not being released when they were rehabilitated are shown in the table.

Length Estimated
Estimated Weight Apr Location of Housed Estimated Length at Cause for not
ID Name Gender Apr 09 age at
age Apr 09 09 (kg) stranding since time of birth arrival (cm) release
(cm) arrival
3y 10m (2y
F1 Ellen F 142 44 N: Domburg 03/03/07 01/06/2005 1y 9m (9m) 117 Heart problems.
10m)

F2 Agnes F 3y 10m 140 50 N: Ameland 02/03/06 01/06/2005 9m 110 Problems on her eyes.

F3 Siepy F 1y 10m 129 40 N: Ameland 22/08/07 01/06/2007 2-3m 99 Too young

M1 Daan M 11y 10m 132 42 N: Oost Capelle 19/01/98 01/06/1997 7-8m 99 Too young

M2 Jordi M 8y 10m 123 31 WG: Langeoog 14/03/01 01/06/2000 9-10m 93 Too young

M3 Bram M 1y 10m 115 33 N: Zeeland 20/02/08 01/06/2007 9m 97 Heart problems

14
The same as “behavioural sampling” with “continuous” regime (Martin and Bateson 1993).

60
Of the three animals with medical problems, Agnes, could not see with one eye, but that
did not cause her any remarkable problem in captivity, and her behaviour cannot be
differentiated from a healthy porpoise. Bram and Ellen, having heart problems, did show
differences in their behaviour compared to the other animals. They stayed in more shallow
areas of the pool and spent more time resting than the others. This was especially
pronounced with Ellen. All the animals were included in the study, but Ellen’s social
behaviour should not be regarded as being typical for porpoises; Bram, on the other hand,
had a social behaviour which could not be differentiated from the other animals’, even
though he spent significantly more time resting when not interacting with the others.
The same system of ID used in Kerteminde was assigned to the animals in
Harderwijk. Age estimations were done assuming first of July as the birth date, and fitting
the length at arrival in the expected general growth curve for harbour porpoises. Births
were assumed to occur in July, in accordance with Lockyer (2003) that reported a peak for
births from mid-May to mid-July for the North Atlantic harbour porpoises (more
specifically most births have been reported in July in Dutch waters, according to Addink
et al. 1995). However, Ellen was estimated to be one year older than Agnes but had a
similar length on her arrival, so her real age may actually be one age younger as indicated
in the parenthesis of Table 2.

Environment

The observations were conducted at the Harderwijk dolphinarium (Netherlands),

where seven harbour porpoises are housed in a concrete pool with chlorinated water,
divided in three areas. The studied animals had access to the biggest pool of dimensions
15.5x7m, with a depth of 2.4m and the separation area of 6.2x3.9m and a depth of 1.2m.
The separation pool was communicated by a gate with the third area where the pregnant
animal, not included in this study, was located; with whom the other animals could
maintain visual and acoustical communication through the gate. During the two hours of
observations the animals did not have access to the shallow area. However, differences in
the behaviour caused by the decrease of available space could not be tested due to the
reduced amount of time they where observed in that situation.

Data collection

Data was collected by direct observations by the same observer as in Kerteminde. The
animals were observed in situ and the duration of the behaviours was measured with a stop

61
watch. It was not possible to use neither video nor sound recordings in this study, and no
behavioural programs were used.

Behaviour sampling
The animals in Harderwijk were observed for 14 hours, spread out during daylight hours
of three consecutive days (29th of April until 1st of May, 2009). During the opening hours
of the dolphinarium (9AM-5PM) the observations were stopped while the trainers fed the
animals and cleaned the pool. Observations were continued as soon as the trainers were
not in the vicinity of the pool. After closing hours the observations were stopped every
hour.
For individual identification, the animals were marked with innocuous baby-cream
just as in Kerteminde.
The sampling method used here can not be considered focal sampling, which
would have been the most desired sampling method in a study like this. However, all
efforts were made to approximate to this method as much as possible. The sampling
method should instead be strictly considered ad libitum (Altman 1974). The pool was
scanned and any social interaction observed was recorded (recording its occurrence), and
followed until it was over (recording its duration), then a new scan was performed. The
main problem of ad libitum sampling is to have lost specifically a type of behaviour, or an
animal (Altman 1974). Thus, this method may inflict biases by the observer. However,
randomisations and an observation schedule were used to avoid this as much as possible.
Every 15 min one animal was chosen as the focal animal, but interactions between other
individuals were also recorded if possible, having the focal animal still in view.
Simultaneous observations of several interactions were conducted whenever possible. To
obtain the maximum amount of comparable data in a consistent way, it was prioritised to
record events – counts of occurrence (Altman 1974) – rather than the duration of each
behavioural event.
The method described here may lead to an underestimation of the total amount of
interactions. The frequency of occurrence in the results below should be regarded as an
approximation for further studies, because some interactions might be missed during the
14 hours. Still, with the amendments described above, the results are regarded as being
perfectly comparable for the animals observed in the same facility.

62
 Considered behaviours
The behaviours included in the study (in both facilities, Kerteminde and
Harderwijk) were chosen by taking into account that the main aim was to elucidate the
social interactions among harbour porpoises. Hence, only behaviours directed towards
another individual and therefore could imply an interaction between them, were recorded.
The ethogram used is shown in Table 3.
For all behaviours their occurrence was counted (as an event sensu Altmann 1974).
The duration of the behaviour (its state sensu Altman 1974) was only recorded if the
behaviour lasted longer than 5 seconds. Duration was recorded to provide insights to the
strength of social interactions. Therefore, some behaviours were always counted as events
(see ethogram) because of having a short duration. Behaviours whose duration depend on
other functions than sociality (close resting, and close fishing), their duration was not
measured.
The behaviours have been categorized in different classes when the social
interaction had a clear function. Behaviours can be affiliative and strengthening bonds, or
aggressive when the receiver answers with avoidance or aggression. Sexual behaviours
were classified separately. The neutral category includes behaviours that may be
considered as an indicator of tolerance, due to the captive condition. Thus, close resting
may have a strong affiliative character in the wild, but in captivity distances are
constrained by the dimensions of the pool, and therefore this behaviour should be regarded
as permissive (some couples actively avoid each other) rather than affiliative. Swimming
behind was understood as the actor trying to affiliate but the receiver not allowing it, and
not classified in any category.
Close fishing could only occur in Kerteminde, where small fishes were present in
the semi-natural environment. Close resting and swimming behind were not recorded in
Harderwijk to keep focus on recording behaviours having the clearest linking and avoiding
functions.
Sideward turn in Kerteminde was defined when the characteristic sound and
motion pattern were observed; in Harderwijk, however, no sounds were recorded and thus
this behaviour was only determined by means of the motion of the animal. Because the
motion pattern of this behaviour is very subtile, it is likely to have been missed at some
occasions in Harderwijk, so that an underestimation of the frequency of occurrence might
be expected from this facility.

63
Table 3. Ethogram. Showing the functional category at which the behaviours have been assigned (affiliative, aggressive,
neutral, sexual, dominance display), the name and description of the behaviours observed, and the recording method
(event=count of a behaviour; duration=duration of the behaviour). *Behaviours that were not recorded in Harderwijk.

Recorded
Behaviour Description
as
Animal resting on the surface is pushed up from below by another animal. Previously
Pushing up described by Nakamura et al. (1998), also reported by Andersen (1969). Event
The calf swims under the tailstock of the mother keeping pace with her momentum,
Infant placing the top of its head just touching the posterior extremity of her abdomen. Described Event
swimming in bottlenose dolphin related with nursing and sleeping (e.g. McBride & Kritzler 1951;
Reid et al. 1995).It was, however, observed that sometimes after grooming the porpoises Duration
stayed in infant position.[0]
AFFILIATIVE

Echelon The calf swims by the side of the mother in close proximity, sometimes touching, on one Event
side of the cow slightly over her trunk, just below her dorsal fin (e.g. McBride and Kritzler
swimming 1951, reviewed by Jacobsen (2003)). Providing the calf hydrodynamic advantages Duration
(reviewed by Jacobsen (2003)). Observed to breathe in synchrony.
Two animals swim near each other – at a distance no greater than one body length – in the
same direction during >5seconds, usually surfacing in synchrony when breathing. Event
Close
Described by Andersen & Dziedzic (1964) as companionship between male-female giving
swimming it a sexual function. However, it has been defined in many delphinids with a social Duration
affiliative function (e.g. Perelberg & Schuster, 2008).
Stroking of two porpoises “by swimming one by another, where the passer-by touches the
Event
Grooming other’s dorsal fin or side” the other porpoise contributes by slowing down its speed
(Amundin & Amundin 1971). Grooming tends to occur in bouts, where both animals
Duration
groom each other. Grooming was considered in this study as grooming bouts.
Event
Swimming Swimming behind another animal, following its direction for a duration > 5s, keeping a
behind* distance no larger than one body length.
Duration
Fishing close to another animal, at a distance no greater than one body length. Fishing
could be described, even if not always small fishes could be observed, when the animals
Close fishing* were grubbing in the bottom (Amundin & Amundin 1974), when swimming frequently
NEUTRAL

(less than a second) changing directions, and positioning in the vertical axis, sometimes Event
swimming up to the surface and head-down. Or, when the porpoises were observed to
chase, move their head, probably echocolocating, towards the nets of the enclosure where
fishes where hiding.
Close resting Resting “logging on the surface with the blowhole out of the water and the tail bent
ventrally” (Andersen & Dziedzic 1964) near another animal, at a distance no greater than Event
* one body length.
Snouting towards another animal turning the head and frontal part of the body with closed
and less often open mouth towards the head of the threatened porpoise; having an
aggressive function (Amundin & Amundin 1971). Aggressive behaviour have a duration of
Sideward abut 1second (Amundin & Amundin 1971).
Event
turn (*)
AGGRESSIVE

* A sound correlated with aggression was used to define aggressive interactions. The
aggressive sound is characterized by an “up-sweeping, high repetition rate click-trains”
(Clausen et al. in prep). When listened through a click detector, the signal sounds like a
steadily increasing pitch, ending in a very high frequency tone. The sound as the behaviour
lasts about a second.
The sideward turn ended in the aggressor touching the other animal with its snout.
Pushing Supposed to be a more intense nature of aggression (Amundin & Amnundin 1971).
Event
Aggressive interaction, where one animal chases another one in a high speed, preceded by
Chasing a sideward turn or a pushing, or ended by them. Not to be confused with the sexual chasing Event
described by Andersen and Dziedic (1964).
Belly One animal turns its body to show its belly to a porpoise nearby (Andersen & Dziedzic
1964) Event
exposure
SEXUAL

Mating A male approaches another porpoise from behind with an erection, and tries copulation at
attempt high speed, without succeeding. The trunk is bended and directed towards the genital area. Event
(erection)
Intromission A male copulates with a female. Ejaculation is not known. Event
DOMINA

Mating
A male approaches another male porpoise from behind and performs the same movement
attempt Event
NCE

patterns than for “mating attempt” but not erected.

(not erection)

64
Data analysis

Some of the data was sorted by means of custom-made programs in MatLab (ver.
6.2, MathSoft, Inc.). The resulting data was statistically analysed with Microsoft Excel
(ver. 2000, Microsoft Corporation) and SAS (ver. 9.1.3. SAS Institute Inc.).
The data on affiliative interactions was tested by individuals and grouped per
couples considered the interaction mutual. In contrast, in aggressive and sexual
interactions, directionality (i.e. who interacted towards whom) was considered and
statistically tested for.
Counts. The counts of affiliative, aggressive and sexual interactions were summed
in for all the observation days and divided by the quantity of hours observed (10 hours in
Kerteminde, 14 hours in Harderwijk) variation among days (i.e. differences in behaviours
frequency per hour, in Kerteminde) or within hours in Harderwijk, were not considered as
being the objective to obtain an overview of the bond among animals, and variations are
expected among hours/days. Data was presented in the figures in units of frequency
(counts of interactions/hour, for clarity of comparisons). However, statistical analyses
were performed on the total counts for all the observed time. When comparing data
between Harderwijk and Kerteminde (Figures 3) the Harderwijk data was scaled to
number of counts per 10 hours (by dividing the counts by 14 and multiplying them with
10).
Statistical analyses for testing differences among individuals or couples were done
with Chi-square tests (Zar, 1999). If significant differences were found (i.e. some of the
individuals or couples showed different levels of interactions, but who differs from whom
is not known) pair-wise comparisons of the individuals or couples tested were performed,

by means of pair-wise Chi-square tests with Yates correction: (were

fi, is an observed value, and is an expected value), to correct for the degrees of freedom
being 1 (comparing two individuals at a time). Adjusting the final p-value of the pair-wise
comparisons with Bonferroni correction (i.e. Bonferroni adjusted p’=p* number of
comparisons) as multiple comparisons were performed on the same data. If a p values was
smaller than 0.05 the difference was considered being statistically significant (Zar,
1999).These analysis were done with Microsoft Excel.
Duration. Only the duration of some behaviours was measured (see Table 1). The
mean duration of affiliative behaviours (grooming, close swimming and infant swimming,

65
because of having similar durations and being related behaviours, and excluding echelon
swimming for having a longer duration and only occurring among mother-calf) was
statistically tested to check for differences among facilities and among pairs of animals.
The data was normally distributed (after log-transformation), not having homogeneity of
variances (the “Two sample test for variances”, showed unequal variances P<0.0001,
SAS). Data was tested for differences among facilities with a “Two sample t-test for
means with unequal variances” by means of SAS (Zar 1999).
Testing for differences among pairs in the mean duration of affiliative behaviours
was done with ANOVA (factor: pair), with the normally distributed log-transformed data.
Posterior pair-wise comparisons among couples of animals were done with Bonferroni
multiple comparisons correction (Zar 1999).

RESULTS

Social interactions are presented, first comparing individuals and pairs of animals
interacting (general categories) in the two groups of animals studied, and then interactions
found within each facility are pinpointed.

Sexual behaviours were observed in Harderwijk (observations made in the end of

April until the first of May); but no sexual interactions were observed in Kerteminde
(observations made in December and January).

Individual differences were found in the total number of affiliative behaviours

between the animals in Kerteminde (X32= 500; p<0.05) and also for the animals in
Harderwijk (X52= 170; p<0.05). Individual differences were also seen in the aggressive
interactions between the animals in Kerteminde (X32= 87; p<0.05) as well as between the
animals in Hardewijk (X52= 34; p<0.05). Individual differences in the total number of
sexual interactions in Harderwijk (X52 = 176 p<0.05) were also observed. Pair-wise
comparisons (see Materials and Methods) were performed to test which individuals
differed from which within each facility, and the results are shown in Figure 1.

66
 Frequency of interaction of each Frequency of interaction of each animal in H
animal in K 45
45
40
40
a
35

Interactions/hour
35
Interactions/hour

30
30 b
Sexual Sexual
25 25
Agressive Agressive
20 20 Affiliative
A Affiliative
15 15
A 2
10 10 1 1
c a ab ab
5 5 2 1 1
B C a A b A A b
C a B B
0 0
F1 F2 F3 M1 F1 F2 F3 M1 M2 M3

Kerteminde Harderwijk
Individuals Individuals

Figure 1. Frequency at which each harbour porpoise interacted affiliatively, aggressively or sexually in both facilities.
The contribution of each behavioural category (sexual, aggressive and affiliative) to the total amount of interactions is shown.
Individuals from left Kerteminde (observed 10 hours) and right Harderwijk (observed 14 hours) are shown. Affiliative,
aggressive and sexual interactions per individual are statistically compared between the animals of the same facility.
Affiliative interactions (green): animals with no uppercase letters (e.g. A) in common differ significantly in the amount of
affiliative interactions. Aggressive interactions (red): animals with no lowercase letters (e.g. a) in common differ significantly
in the amount of aggressive interactions. [0]Sexual interactions (white): animals (from Harderwijk) with no numbers in
common differ significantly in the amount of sexual interactions (e.g. 1).

The observed frequencies of behavioural events in Harderwijk are probably an

underestimation of the total number of occurrences due to the sampling method used there
(see Material and Methods above) Therefore the frequencies of behavioural occurrences
reported from the two facilities cannot be directly compared. Results from both places
have been plotted together to provide a general overview, but the amounts of interactions
of each animal should only be compared within each facility.
In Kerteminde, because of the sampling method used (see Material and
Methods), we believe that all behavioural interactions occurring during the observational
period were observed, and thus the frequencies of behaviours in Kerteminde can be
compared with other studies. The highest frequency of occurrence of affiliative
interactions directed towards any other animal was performed by F1, that affiliated
(grooming, close swimming, echelon swimming, infant swimming and pushing up) a total
of 35.9 times per hour with other animals. The lowest rate of affiliative interactions with
any other animal was seen in M1, which did not perform any affiliative behaviour at all
during the study. It should be emphasized that data was collected during 10 different days,
so the lack of affiliative behaviour in M1 is really remarkable. Aggressive behaviour
reached its highest value in F1, which was aggressive towards all the other animals on
average 6.6 times/hour. The lowest levels was 1 interaction per hour, observed from F2
towards the other animals (Figure 1).

67
 Interactions were mostly observed to occur in couples. Three (in Kerteminde and
Harderwijk) and up to four (in Harderwijk) animals were also observed to interact at the
same time. During interactions of more than two animals it was not possible to asses
which animal or animals the affiliation was directed towards. In such interactions all the
pair wise combinations were counted. Aggression and grooming were only observed in
pairs.
The frequency of affiliative behaviours that pairs were involved in is shown in
Figure 2, including the animals of Harderwijk and Kerteminde. Significant differences can
been seen in the amount (or lack) of affiliative behaviours in all the possible pair
combinations in Kerteminde (X52= 1141; p<0.05) and Harderwijk (X142= 487; p<0.05).
Hence, harbour porpoises, do not randomly affiliate with one another, but a specific
partner is chosen. The results of pair-wise comparisons among couples interacting can be
seen in Figure 2.

Frequency of affiliative Frequency of affiliative interactions in H

interactions in K
30
A 30

25 echelon sw 25
pushing up
Interactions/hour
Interactions/hour

close sw
20
infant sw 20
close sw grooming
grooming 15
15

10 10
B
A
5 5 AB
AB B B
B
0 0
F1 F1 F2 F1 F2 F3 F1 F1 F2 F1 F1 F1 F2 F2 F2 F3 F3 F3 M1 M1 M2
F2 F3 F3 M1 M1 M1 F2 F3 F3 M1 M2 M3 M1 M2 M3 M1 M2 M3 M2 M3 M3
Ker teminde Harderwijk
Pairs of animals interacting Pairs of animals interacting

Figure 2. Frequency of affiliative interactions of pairs of harbour porpoises in (left) Kerteminde and (right)
Harderwijk. Individuals from Kerteminde (observed 10 hours) and Harderwijk (observed 14 hours) are
statistically tested with the animals from the same facility. The contribution of each behaviour to the total
frequency of affiliations is shown. Lack of bars means no interaction observed between the pairs. Pairs with no
uppercase letters (e.g. A) in common differ significantly in the total amount of affiliative interactions. The pairs
lacking letters are not used in the statistical test, as they contained very few interactions (less than 5 times in 14
hours).

The highest frequency of affiliative interactions was seen between F3 and F1 in

Kerteminde (in total 29.2 affiliative interactions/hour), corresponding to the mother calf
pair, that differ significantly (pair-wise comparisons, results shown in Fig.2) from the
frequency of interactions seen between F1 and F2, the two adult females (in total 6.7
affiliative interactions/hour).

68
 The frequencies of behavioural interactions in the data from Harderwijk are
probably underestimated, but the relatively differences between the animals can still be
compared within the facility (see Material and Methods).
Figure 3 shows the total duration of the affiliative interactions (i.e. the affiliative
behaviours ones except pushing up, see Material and Methods) from all the hours
observed (Harderwijk duration was standardized to 10 hours to be able to make
comparisons with Kerteminde), per pairs of animals.

Total duration of affiliative behaviours in K and H

4500 echelon sw
infant sw
4000
close sw
3500 grooming
3000
Seconds

2500
2000
1500
1000
500
0
F1 F1 F2 F1 F2 F3 F1 F1 F2 F1 F1 F1 F2 F2 F2 F3 F3 F3 M1 M1 M2
F2 F3 F3 M1 M1 M1 F2 F3 F3 M1 M2 M3 M1 M2 M3 M1 M2 M3 M2 M3 M3

Kerteminde Harderwijk
Pairs of animals interacting

Figure 3. Total duration of affiliative interactions (during all the observed period) in Kerteminde
and Harderwijk by couples of animals. The total duration of each behaviour, and its contribution of the
total bond per couple is shown.

Affiliations per pairs if considering only frequency (Figure 2) show different

couples having stronger bonds than if considering the total time the pairs were maintaining
affiliative interactions (Figure 3). This is because the duration of affiliative behaviours is
variable and therefore needs to be considered for better describing affiliation. The total
duration of interactions is therefore the best description of the affiliative bonds among
pairs (Figure 3). Note that the total duration of affiliative interactions in Harderwijk will
be underestimated, just as the frequencies of occurrences (see Materials and Methods).

The mean duration of affiliative interactions (see Material and Methods) can be
compared among facilities and are shown in Figure 4. The average durations of affiliative
interactions per pairs of animals are significantly different among facilities (two-sample t
test for unequal variances= 15.3; p<0.05). The mean durations of affiliations in
Kerteminde were shorter than the ones in Harderwijk.

69
 M ean duration of affiliative interactions by couples in H-K

A
210
AB
180
150
Seconds

120
AB
90 B AB
B
60
30 C C

0
F1 F1 F2 F1 F2 F3 F1 F1 F2 F1 F1 F1 F2 F2 F2 F3 F3 F3 M1 M1 M2
F3 F2 F3 M1 M1 M1 F2 F3 F3 M1 M2 M3 M1 M2 M3 M1 M2 M3 M2 M3 M3
Kerteminde Harderwijk
Pairs of animals interacting

Figure 4. Mean duration of affiliative interactions (mean ± S.E.M., N =16-202). The mean duration of
affiliative interactions (i.e. grooming, close swimming and infant swimming) is tested between of all the
pairs of animals in Harderwijk and Kerteminde. The durations shown in blue (pairs F1-F3 F1-M3, F3-
M3) were not statistically tested because N is smaller than 3. Average durations with no upper case
letters (e.g. A) in common are significantly different.

Mean durations of affiliative behaviours of animal pairs were tested for

differences among facilities and among couples. Differences among couples (comparing
pairs of both facilities) were also found to be significant (F7,298=33.63; p<0.05) in
Harderwijk. In Figure 4 the data is shown. In Kerteminde, the mean duration of affiliative
behaviours do not differ in the two pairs of interacting animals.

Kerteminde

Figure 5 shows the affiliative interactions

(total duration of affiliative interactions)
of the pairs of animals in Kerteminde as
reported in Figure 3.
The strength of affiliative interactions in
Kerteminde can be compared by means of
the frequency of affiliation among the
animals in the same facility because the

Figure 5. Flow chart showing the affiliative bond

mean duration of affiliative interactions
between animals in Kerteminde. The bond showing does not differ significantly between the
the total duration of affiliative interactions including:
echelon sw, infant sw, close sw and grooming, among two pairs of animals interacting (see
pairs of animals. Dashed lines indicate no interaction.
Arrows are based on N=67-292 (N= number of Figure 4).
affiliative interaction per pair). The thickness of the
arrows is proportional to the strength of affiliative
interactions per pair.
70
 Significant differences are seen in the strength of affiliation among pairs (i.e.
frequency of interactions per pairs are significantly different as described in Figure 2).

If the frequency of all the affiliative and neutral interactions as well as the non-
categorized swimming behind behaviour are added totgether (Figure 6), significant
differences are also found among couples of interacting animals (X52= 1362; p<0.05). In
Figure 6, the statistical differences found in pair-wise comparison among couples
considering affiliative, neutral and other interactions can be observed.

Frequency of affiliative, neutral interactions (and swimming

behind)
45 A close resting
40 sw behind
echelon sw
Interactions/hour

35
pushing up
30
close sw
25 grooming
20 infant sw
15
B
10
5 C C
D D
0
F1 F3 F1 F2 F2 F3 F1 M1 F2 M1 F3 M1
Pairs of animals interacting

Figure 6. The frequency of affiliative interactions (infant swimming, grooming, close

swimming, pushing up and echelon swimming), neutral interactions (close resting) and swimming
behind. It is showed the contribution of each behaviour to the bond but pair interactions are tested
together. Frequency of interactions among pairs with no upper case letters (e.g. A) in common are
significantly different.

Nursing (defined as the calf F3 attaching its mouth to the mammaries of her mother
F1) has probably also an affiliative function. It was observed 162 times in the ten hours,
i.e. and average of 16.2 events per hour.

The direction of aggressive behaviours (i.e. which animal is aggressive towards

which other animal) is shown in Figure 7. Differences were also found in the amount of
aggressions directed from one animal to another. This shows that aggression was not
directed randomly but towards specific individuals. F1 showed significantly different
amounts of aggression towards the other animals (X22= 23.5; p<0.05). This was also true
for M1 (X22= 35.3; p<0.05). F3 and F2 were only aggressive towards the male. The
statistical results of the pair-wise comparisons of the quantity of aggressions that F1 and
M1 directed towards the others are shown in Figure 7.

71
 Frequency of aggressive interactions
4.5 A
a
4
3.5
Agressions/hour 3 Reciver F3
Reciver F1
2.5
B Reciver F2
2 b
Reciver M1
1.5
B
1
0.5 c
0
F3 F1 F2 M1

Actor

Figure 7. The frequency of aggressive behaviours of the four animals directed towards
other individuals. The amount of aggressive interactions that an actor directed to a receiver with
no upper case letters (actor F1) or lower case letters (actor M1) in common are significantly
different. Lack of bars means lack of aggression.

The average frequency of aggression for all animals in Kerteminde was 1.7
aggressions/hour. The highest level of aggression was observed in F1, directing it towards
M1 with a frequency of 4 aggressions/hour. The lowest level of aggression was absence of
aggression between e.g. F3 towards the other two females, as seen in Figure7

Harderwijk

Considering only the frequency of interactions (Figure 2), this is not a good
method to describe the bonds among animals whose affiliative interaction have different
durations as seen in the pairs in Harderwijk (Figure 4). Thus, the total duration of
affiliative interactions is the best reflection of the pairwise affiliative bonds, presented in
Figures 4 and 8.
There were some porpoises interacting more than others, while some pairs that
never interacted, but statistical differences cannot be tested on the total amount of time
interacting (because of being a unique measure form all the time observed). If we
considered only the frequency of affiliative interactions (Figure 2), M1-M2 had a
significantly different strongest affiliation than F2-M2, F2-M3 and M2-M3. If we
considered the mean duration (Figure 4), F2-F3 had a significantly longest mean duration
of affiliative behaviours than F2-M1 and M2-M3. If frequency and mean duration are both
considered the pairs of animals appearing to have the strongest affiliation are F2-F3
followed by M1-M2. F2-M1 and F2-M2 come next, and the weakest of all the pairs
showing consistent affiliations seem to be F2-M3 and M2-M3. However, all this bonds

72
seem strong as no clear statistical differences among all of them were obtained neither by
means of frequency or mean duration.

Figure 8. Sociogram showing the strength of affiliative interactions among pairs of animals in
Harderwijk (i.e. total duration of affiliative interactions including: close swimming and grooming).
The numbers are the durations of affiliative interactions are indicated in seconds. Absence of lines
means no interactions, these lines have not been drawn for clarity. Dashed lines indicate N<6, arrows
indicate N= 23-74 (N= numbers of affiliative interactions per pair). The thickness of the arrows is
proportional to the strength of affiliative interactions per pairs.

The frequency of aggressive behaviours have been presented for every individual
in Figure 1. In Figure 10, the data is split into the different receptors for each aggressive
event.

Frequency of agressive interactions

0.7
Receiver F1
0.6 Receiver F2
Interactionn/hour

0.5 Receiver F3
0.4 Receiver M1

0.3 Receiver M2
Receiver M3
0.2
0.1
0
F1 F2 F3 M1 M2 M3

Actor

Figure 10. The frequency of aggressive behaviours of the six animals directed towards the others.

73
 The animals F1 (X42= 78; p<0.05), F2 (X42= 80; p<0.05), F3 (X42= 13; p<0.05),
M1(X42= 58; p<0.05), M2 (X42= 47; p<0.05), and M3 (X42= 10; p<0.05) showed different
amounts of aggression towards the other animals, but pair-wise comparisons did not allow
to find any differences, due to the small amount of aggressive data. F1 and F2 direct
aggression towards all the individuals in contrast with the other animals that direct it only
to some of the others.

Sexual interactions were observed to be heterosexual and homosexual. Males

attempted to, and some times mated with, females. Mating attempts were also observed
among males. Data is shown in Figure 11, divided into the pairs of animals interacting.

Frequency of heterosexual interactions

4.5
4
intromission
3.5
mating at (erection)
Interaction/hour

3 mating at (no erection)

A
2.5
2 A
1.5 B A
1 B a B
0.5 a
a a a a a a
0 a
M1-F1 M1-F2 M1-F3 M2-F1 M2-F2 M2-F3 M3-F1 M3-F2 M3-F3
Pairs of animals interacting (male-female)

Figure 11. Frequency of heterosexual interactions among the animals in Harderwijk. The
contribution of each behaviour to the total frequency of interactions is shown. The two behaviours are
tested separately. Intromission (white): pairs with no uppercase letters in common differ significantly
in the amount of copulations (e.g. A). Mating attempts (purple): animals with no lowercase letters in
common differ significantly in the amount of mating attempts (e.g. a).

Pair-wise comparisons among amounts of intromissions and mating attempts are

shown in Figure 11. Mating attempts were performed by all the males at equal amounts
(Figure 11), i.e. any significantly differences was found among pairs of animals (X82=
15.1; p<0.05). In contrast, significant differences (X82=228; p<0.05) were found in the
intromission (copulation) amounts. See Figure 11 for statistical individual differences
(pair-wise comparisons).

Figure 12 shows the distribution of homosexual activities among individuals. The

actor of the sexual interaction performed the same movement patterns as during a mating
attempt with females, but directed towards a male, with our without erection.

74
 Mating attempt without no erection were only observed in male-male interactions,
except with M3 (the youngest immature male) towards F3 (once). The frequency at which
the animals displayed the homosexual interactions is shown in Figure 12 by pairs of
animals interacting.

Frequency of homosexual interactions among males

0.8
0.7 mating at (erection)
Interactions/hour

0.6 mating at (no erection)

0.5
0.4
0.3
0.2
0.1
0
M1 M2 M1 M3 M2 M1 M2 M3 M3 M1 M3 M2
Pairs of males interacting (actor receiver)

Figure 12. Frequency of homosexual interactions among male harbour porpoises in

Harderwijk. The direction of arrow show who is the actor of the sexual behaviour. The contribution
of each behaviour to the total frequency of interaction is shown.

Significant differences were found in the frequency of interactions directed

towards different individuals (X52= 18.8; p<0.05), however the reduced amount of this
kind of interactions (in 14 hours of observations the maximum frequency of interactions
was 7.2) did not provide any significant result in the pair wise comparisons.

DISCUSSION

The female F1 in Harderwijk behaved significantly different from all the other
females both in Harderwijk and in Kerteminde (Figure 1), showing significantly lower
affiliative behaviour and relative high levels of aggression. This pattern also differs from
the one observed in the Harderwijk males, but resembles the behaviour of the male in
Kerteminde (observed during another time of the year). Due to her cardiac problems the
behaviour of F1 may not be representative of healthy harbour porpoises. Therefore the
data on her behaviour is excluded from the discussion of affiliative and aggressive
interactions below. However, concerning sexual interactions, F1 behaved similarly to F2

75
(who was of similar age) from Harderwijk. Therefore, in the discussion of sexual
behaviour below F1 is considered.

Aggression

The average frequency of aggressive interactions in all animals (in Kerteminde)

was 1.7 (± SEM 0,79) aggressions/hour. Compared to the frequency of aggressions in
bottlenose dolphins (Tursiops truncatus), Samuels & Gifford (1997) report from a captive
situation 1.08 aggressions/hour (calculated as the average of aggressions seen between
male-male, male-female and female-female interactions). However, aggression observed
in dolphins is of a much more intense nature than all the aggressive types of behaviours
observed in harbour porpoises. Bottlenose dolphins have been seen to inflict physical pain
to conspecifics, such as bites leaving tooth marks or even leading to death (McBride &
Hebb, 1948); In harbour porpoise, aggressive interactions have never been reported to
leave similar observable marks in the receptor; it has mostly been characterized as a
distant signalling (Andersen & Dziedzic 1964; Amundin & Amundin 1971; this thesis).
However, the use of burst pulses during aggressive interactions in harbour porpoises have
the potential of inflicting hearing pain and damage due to the high received levels
(Clausen et al. in prep).
In this study, the highest average cumulative duration of aggressive behaviours
from a harbour porpoise towards another animal was 0,1% of the time the animal was
observed (i.e. 4 aggressions/hour, for F1 in Kerteminde). In agreement with values seen in
other studies of harbour porpoises, Benhan (1999) reported an average level of 2.7
aggressions/hour (sideward turnings and chases) directed from the same F1 to M1 (at 3
and 4 years respectively during the mating season); Wilson (1999) reported aggression
levels from M1 towards a one-year old female on average 2.5 chases/hour in Kerteminde
during the same period as the study made by Benham (1999). In Nakamura (1998) a
maximum frequency of aggression (calculated from the plots) of around 18
aggressions/hour from an immature female towards the male was reported. The second
highest level of aggression was directed from the male towards an adult female (length
150cm) and was around 160 chases and 30 sideward turnings (extracted from the plots),
i.e. 8.8 aggressions/hour. The average aggression levels of the most aggressive
interactions of this study do not seem to differ with the levels reported in other studies in
Kerteminde.

76
 Considering the different environments (pens) where the animals where kept in
these studies, and the number of animals interacting, the levels of aggression found in the
our study is comparable in magnitude with previous studies. Thus, it can probably be
generalized that these levels of aggressions may be characteristic for the species.
However, stress caused by the way the animals are kept may cause biases in the data. The
slightly lower (maximum) aggression level observed in Benham (1999) and Wilson
(1999), in comparison with the levels observed in this study, could be due that during this
study the animal density was increased beyond what the animals were used to (se
Materials and Methods). This is supported by the density-aggregation model observed in
many mammals (Videan & Fritz 2007), which predicts that with increased spatial density
aggression will increase as a short term response. The same but in a greater level, may
apply for the higher maximum observed in Nakamura et al. (1998), as 5 animals were
enclosed in a concrete pool of 42.4m3, i.e. 8m3 per animal. For a comparison of space
availability, animals in Harderwijk had an average of 48,2m3 per animal, and in the pen
where animals were enclosed for the observations in Kerteminde the average volume per
porpoise was down to 77m3 per animal during the lowest tide.
The aggression levels reported here provide some basis for further studies to
compare different conditions and times, and to assess animal welfare. When dealing with
social interactions in captive animals, the density and group structure of the animals are
used to must be considered. Short term changes in aggression will probably occur if such
parameters are changed, until adaptation to the new situation is achieved.

Affiliative behaviour

9 of the 10 harbour porpoises studied - all except M1 in Kerteminde - showed

affiliative behaviours. As observations were made in two different facilities, and at
different times of the year, we can possibly generalize these observations. Which are very
different from the notion of harbour porpoises not being very social and mostly solitary
(e.g. Evans 1980). Affiliative interactions were more frequent than aggressive ones for all
animals, except for F1 in Harderwijk (se above) and M1 in Kerteminde (discussed below).
The highest frequency of affiliative interactions among pairs was between F1 and
F3 (the mother-calf pair) in Kerteminde, with average values of 29.2 interactions/hour.
When compared with other studies of harbour porpoises Wilson (1999) reported an
average of 12.6, 8.5, and 3.8 grooming events/hour, split up into different types of

77
behavioural subcategories, which in total is 25 events/hour. These observations were made
on the pair that interacted the most, F1 in Kerteminde, 3y old at the time, and a 1y old
female. In Nakamura et al. (1998) the pair interacting the most was a male and the oldest
pregnant female, showing an average frequency of affiliative interactions around 28
interactions/hour (calculated from the Figures 5 and 6, summing in rubbing and close
swimming from N1 to N2 and from N2 to N1, divided by 21.4 hours of study). In these
former two studies and in the present study, the frequency of affiliative events seems
similar in the animals interacting the most.
Above, only frequency of occurrence is compared, as this is the only data available
from other studies. Frequency of occurence is a good measure of an interaction if the
duration of a behaviour is constant. Therefore, frequency is a good measure of sexual
interactions, and aggressive interactions in harbour porpoises, but not for affiliative
interactions which have a variable duration. Thus, for studying affiliative bonds the
duration needs to be considered to reflect the intensity of a bond. This is demonstrated by
the fact that the affiliative bonds vary between pairs when considering only the frequency
(Figure 2), but when also considering the duration (total duration of affiliative interactions,
Figure 3), being the total amount of time interacting the best description of the affiliative
bond.

Sexual behaviour

Sexual behaviour was observed at the end of April until the beginning of May in
Harderwijk but was not observed in Kerteminde in December and January. This is in
agreement with harbour porpoises expected to have a breeding season, predominantly
taking place during August in Danish waters as stated by Lockyer & Kinze (2003);
However, previous studies on the sexual behaviour on captive harbour porpoises in
Kerteminde have shown more variability than this. The mating season has been observed
from mid-July to mid-August in 1998 (copulation attempts, in Kristensen (1999) reviewed
by Desportes et al. 2003), during July to mid-August in 1999 (copulation attempts and
presence of spermatozoa in vaginal smears in (Benham 1999)), during July and August in
2000 (the majority of copulation attempts and presence of spermatozoa in vaginal smears
(Jepsen 2002)), and from mid-July to early October in 2001 (presence of spermatozoa in
vaginal smears (Jepsen 2002)). However, in the only longitudinal behavioural study not
only performed in the summer months (Jepsen 2002) sexual behaviour was observed from

78
April to mid-November, with the greatest activity in July and August. This extended
period of sexual activity might be caused by different reasons. It may be an artefact caused
by keeping males and females together all year around in captivity, or it could be that the
mating season is more extended than previously estimated, but that conceptions is
restrained by the female receptivity. Thus, sexual interactions may also have an important
social function. If sexual activity is always initiated by males outside the peak mating
season, it could be that male “mating season” is broader than the time females are
receptive. This hypothesis would be confirmed testing if females to allow copulation
during a more extended period of the year. This is unlikely as Jepsen (2002) did found
spermatozoa in vaginal smears only in July and August. And as reviewed by Desportes et
al (2003) males initiate sexual activities but females decide the outcome. Thus, males
might have a broader mating predisposition than previously thought.
In this study, copulations with mature females were observed in Harderwijk in
May, probably explained by an earlier mating season in Holland than in Denamrk. In
Dutch waters, spermatogenetic activity and sperm has been reported in March, and the
breeding season has been reported to start earlier and finish later than in Denmark (Addink
et al 1995). Therefore, the sexual activities observed in this study in Harderwijk are
expected to be occurring in the mating season. However, it should be considered that a
male harbour porpoise (actually, M1 in Kerteminde), when immature (1997), was
observed to perform sexual activities towards F1 (from Kerteminde) during all the winter
(Desportes et al. 2003). In this study both F3 and M3 (in Harderwijk) were sexually
immature. But the other animals were probably mature –females become mature around 3-
4 years, at a length of 138-147 cm (Lockyer 2003), and males at around 3-4 years, length
of 127-135 cm (Lockyer 2003) – and therefore, the sexual activity of at least the certainly
mature males should be observed because of being the mating season.
Further studies of the seasonality of sexual behaviour in captive harbour porpoises
may confirm or reject these ideas. And care must be taken when inferring the results
derived from captive animals to animals in the field. However, in bottlenose dolphins
(Tursiops truncatus) with a more variable seasonality of reproduction than porpoises, there
is a correlation between the origin of the population and the seasonality of reproduction in
the wild and in captivity (Urian et al. 1996). This strongly suggests that the breeding
seasonality in harbour porpoises derived from studies made in captivity will reflect the
breeding pattern in the wild (probably the pattern observed in captive animals will be the
one belonging to the population that the animals came from).

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 In Figure 1 it is observed that the potentially mature females (F1 and F2 in
Harderwijk) have significantly lower levels of sexual activity than the immature female
(F3). Supporting that immature animals seems to practice sexual activities more often,
probably for training (Desportes et al 2003; observed it in a young male). F3, allowed
significantly more copulations than F1 and F2 (Figure 11), which supports the theory
suggested by Desportes et al. (2003) of females deciding the end of the sexual encounter,
as the immature female allowed copulation in a greater level than mature females. This
may possibly be because at this immature stages there might be no hormonal constrains to
control the fitness implications of having an offspring. These two theories are also
supported in the observations of the immature male M3, who attempted to mate with all
the females (Figure 11) but he only achieved copulation with the immature female F3 but
never with the probably mature females.
This study provides new insights in the mating structure, with three males and
three females observed together in Harderwijk. All the males attempted to mate equally
(no significant differences) with the different females, mature as well as immature (Figure
11). Thus there is not specific mate choice made by the males. This also shows that males
do not form any specific coalition or alliance that would allow them to achieve more
copulations than otherwise, as observed in dolphins (e.g. Connor 2007). Neither did we
observe any absolute dominance among males, where a specific male controls the other
males’ mating attempts. This supports that male-male competition is not evolutionary
selected for in harbour porpoises.
Our study gives the first empirical data that shows that harbour porpoises probably
have a promiscuous mating system. In such a system the males do not compete for
females. In harbour porpoises it is in accordance with the theoretical expected mating
structure based on morphological data: the great testes size (predicting sperm competition
Aguilar & Monzon 1992), the reverse sexual dimorphism (females being larger than
males) and the absence of males’ secondary characters (Jefferson 1989; Connor et al.
2000). Observations of other groups of animals are needed to confirm that this is the
general mating structure in this species.

Homosexual interactions: Dominance and hierarchy?

Homosexual behaviour in harbour porpoises have previously been reported by

Amundin & Amundin (1971) among 3 one-year-old male porpoises observed from April

80
to September. It has also been seen among 2 three-year-old males (month of observation
unknown; Amundin 1974c), and between a mature male and a three-month old calf
(Kastelein & Staal, 1997) in September an October. In this study homosexual interactions
were observed in Harderwijk, in the spring, at the same time as heterosexual interactions
were observed. Therefore, there is no available data to show if homosexual interactions
are also seen outside the mating season.
Homosexual behaviour, has been reported to be used as a way of establishing
hierarchy in dolphins (e.g. Tavolga 1996), and in harbour porpoises (Amundin 1974c).
Amundin (1974c) used a detailed protocol to define hierarchy, testing aggressive
responses together with copulation attempts. In our study, the differences in homosexual
mating attempts were significantly different among animals, but pair-wise comparisons
did not give significant results due to the reduced amount of data of this kind (Figure 12).
However, Amundin (1974c) did not find any absolute dominance among the three-year-
old males that were studied. In our study, the direction of aggressions, achievements of
copulations with mature females, and homosexual copulation attempts all suggest a (not
absolute) hierarchical order. In Harderwijk, M1, being the older and probably more
dominant male, achieves more copulations (5 per 14 hours) with both of the mature
females, in contrast with M2 (1) and M3(0). All the females directed aggression towards
M1, M2 and M3, but F3 (the younger female) did not direct aggression towards M1.
Homosexual copulation attempts, even if not significantly different in their frequency of
occurrence, showed a tendency to be higher in M1 towards M2 and M2 towards M3.
These tentative conclusions need to be tested with a larger data set.

Social behaviour

Interactions by gender of the animals

The male in Kerteminde (M1) did not show any affiliative interaction towards any
other animal (all being females) outside the mating season (absence of sexual behaviour)
in December and January (Figures 1, 2, 3, 4, 5). In contrast, in Kristensen’s (1999) study
(reviewed in Desportes et al. 2003), affiliative interactions (grooming) of M1 with F1
were observed from the end of June to the beginning of September 1998, including the
period where sexual behaviour was observed (July to mid August), also in the summer of
1999 affiliative interactions where observed among M1 and F1 and with another female

81
kept in Kerteminde at that time, from early July to mid-August, the mating season being
included in that period (Benham 1999; Wilson 1999 reviewed by Desportes et al 2003).
Jepsen (2002) reported social and sexual interactions in the Kerteminde M1 and F1 pair (5
and 4 years old, respectively, at that time), both increasing during the mating season and
decreasing outside it, and being absent (or less frequent) from December to April (in 8
observations in December, January and March, neither sexual nor social behaviour was
observed).
This correlation between mating and social behaviour was regarded as a general
tendency, but it must be emphasized that sexual behaviour was seen in 3 of the
observations where social behaviour was not observed, and social behaviour was also seen
in three observation without any occurrence of only affiliative interaction (in contrast with
the 25 observations with the presence of both). And this not absolute correlation between
sexual and social behaviour may explain why the close swimming (affiliative behaviour)
was described to occur among a male and a female in a semi-natural pen in Harderwijk in
May by Kastelein & Staal (1997), while sexual behaviour was reported to not have been
observed. Nakamura et al (1998) also observed affiliative interactions among male-
females in their study (observations done during three days at the end of April) but not
sexual interactions were reported.
In this study male-female associations were observed in Harderwijk during the
mating season (Figures 2, 3, 4 and 8) agreeing with the proposed male-female affiliative
association related to male-female sexual interactions. Therefore, this results suggest that
adult males do not affiliatively associate with females outside the sexual season (in a
period before and after it affiliative associations are probably seen), but males and females
show affiliative associations simultaneously with the occurrence of sexual activities.
Further studies of long term social interactions among males and females may confirm
these results.
If the male-female affiliative bond occurs only in relation to sexual activities, its
function will be linked to sexual activity. Being females those allowing mating to be
achieved (i.e. copulation) the male-female bond might have an influence in the female
decision. This last suggestion needs to be proved with a correlation among affiliative
interaction and copulation achieved with mature females. The 6 copulation’s observed
with mature females did not allow any correlation. This would outline the promiscuous
mating system by a need of an affiliative association.

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 In contrast, females were observed to perform affiliative interactions with other
females outside the mating season in Kerteminde (Figures 2, 3, 4, and 5), and during the
mating season in Harderwijk (Figures 2, 3, 4, and 8). Female-female affiliative
interactions were also seen during periods of sexual activity by Wilson (1999) in
Kerteminde (F1 (3y old) with a younger female). Female-female associations were also
reported by Nakamura (1998) by the end of April. Thus, female associations probably
have a different function than sexual, as proposed to be the ultimate cause for close
affiliative association of male-female.

This study shows that males in Harderwijk associate with other males during the
mating season (Figures 2,3,4 and 8). This is supported by Amundin & Amnundin (1971)
that described grooming among three sub-adult males (around one year old) in
observations made from April to September. It is not known if this affiliation is also
maintained in periods when no sexual activity takes place, as seen among females.

Interactions compared between individual pairs of animals

Comparing interactions between facilities

If the levels of affiliative interactions are compared among facilities (Figure 3)
(considering that the interactions recorded in Harderwijk are probably an underestimation
(see Material and Methods), and affiliative interactions in Harderwijk are expected to be
stronger than shown) at least F2 F3 from Harderwijk have a stronger affiliative bond than
F1-F3, the mother calf pair in Kerteminde, and M1-M2, F2-M1 and F2-M2 from
Harderwijk have an stronger bond than F1-F2 in Harderwijk. Mean durations of affiliative
interactions per pairs can be compared among facilities (Figure 4), and all the pairs that
interacted showed significantly longer interactions in Harderwijk than in Kerteminde. The
higher levels of affiliation in Harderwijk than in Kerteminde may be due by the mating.
This is in accordance with Benham (1999) who showed that the frequency of proximity
patterns of F1 in Kerteminde to M1 and to a younger female decreased at the end of the
sexual season. In Wilson (1999) the affiliative behaviours of the younger female in
Kerteminde towards F1 and M1 decreased as well at the end of the sexual season. And the
mean duration of affiliative behaviour among a male-female (M1-F1) was significantly
higher during the mating season than in the rest of the year Benham (2002).

83
 However, the different sizes of the enclosures (in Harderwijk and Kerteminde)
might have some influence. The tension-reduction model has shown that under long-term
high spatial density, affiliative behaviours increase, resulting in decreased tension and less
aggression (de Waal, 1989, reviewed by Videan & Fritz 2007). And thus the higher
durations of affiliations in Harderwijk might be influenced by a higher density aggregation
than the one in Kerteminde. However further studies with density changes in the same
conditions need to be done to confirm the effects of this proposed density-aggregation
models.

Comparing interactions between pairs in Kerteminde

The strongest affiliative bond is seen among F1 and F3, a mother-calf pair, the
1y4m calf and still maintaining a close bond with her mother (Figure2). Nursing attempts
were observed on an average of 16.2 events per hour, which fall within the average
frequencies seen among the mother-calf in the first 8 months of life (Delgado et al. in
prep.). It is not know whether milk was obtained, or if nursing at this stage may fulfil an
affiliative function, as suggested by Brodie (1969). The affiliative bond among the mother
calf is three times stronger than the affiliation of F1 (12 years old) with F2, a younger
female (around 5 years old; Figure 3, 5). The lack of affiliative interactions among F3, the
calf, and F2 (5y) is striking.
When neutral-tolerant and swimming behind behaviours are also considered
(Figure 6), F2-F3 and F3-M1 show a proximity relation, and in contrast F1-M1 and F2-M1
show the strongest avoidance responses. Swimming behind could be interpreted as one of
the animals trying to interact in some manner but the other animal not responding. Close
resting has a strong affiliative function in the wild, but in captivity the lack of this
behaviour probably indicates avoidance.
Aggression among the Kerteminde animals (Figure 7) confirms the male-female
avoidances described above for the winter period, where all the females direct aggression
towards the male (in addition to the lack of affiliative behaviours among male-females).
Simultaneously the male directs aggression towards all the females. In contrast F1 also
shows aggression towards the younger females, but maintains strong affiliative bonds with
them as well (e.g. Figure 5). F2 and F3, being the youngest females, show only aggression
towards the male, but never towards F1 neither each other. F1 and M1, the older male and
female, direct their highest levels of aggression towards each other (Figure 7). These two
individuals also show the (individually) highest levels of aggression (Figure1).

84
 It can then be seen that M1 F2 avoid each other, not showing any affiliative bonds,
nor remaining close to each other (Figure 7) but showing low levels of aggression towards
each other (Figure 8); F3 and M1, in contrast, were seen to show proximity patterns
(Figure 7) but aggression is also shown (Figure 8). The strongest avoidance seen among
F1 and M1, were not affiliation or toleration is seen (Figure 7) and the highest levels of
aggression that each of them perform are directed towards each other (Figure 8).
In relation to dominance, F1 is probably dominant over F2, as F2 never directed
aggression towards F1. In contrast, F1 directed aggression towards F2 most of the times to
end an affiliative interaction. In agreement with these suggestions, Wilson (1999) showed
that the youngest animal (one year old female) was subdominant over the adult male and
the older female, and most of the interactions were initiated by them. Also in Nakamura et
al. (1998) the youngest (immature) female directs the lowest levels of aggression
(snouting, chasing and pecking) towards the other animals (all adults).

Comparing interactions between pairs in Harderwijk

Not negligible affiliative bonds were seen among different pairs of animals in
Harderwijk, among F2-F3, M1-M2, F2-M1, F2-M2, F2-M3 and M2-M3 (Figures 4 and 8).
It can be seen that differential affiliative bonds are seen among males, females, and by
differently aged animals. No clear statistical differences among pairs were seen, varying if
considering frequency (Figure 2) or duration (Figure 4). This shows that male-female,
female-female and male-male interactions had a similar strength in Hardewijk, which is
quite different from the results from Kerteminde.
If frequencies of affiliation are considered, a clear difference among ages can be
seen (Figure 1), adults interacting significantly more frequently than younger animals (F2,
F3).
Analysing the direction of interactions (Figures 3 and 8) it can be seen that F3 and
M3, the youngest immature animals, did not interact in an affiliative manner towards each
other, and differences were seen between the male and the female in the relation with the
others. M3 (2y) affiliated with an adult male (M2) (9y and probably subdominant) and
with and adult female (F2, 4y). In contrast, F3, did not show any affiliative behaviour
towards males, but also interacted affiliatively with and adult female (F2) (the strongest
bond among pairs if considering the total duration of affiliative interactions). The pattern
observed in the younger female can be compared with the one observed in Wilson (1999)
which describes an strong affiliative interactions of a one year old female in Kerteminde

85
with F1 (Freja) (at that time 3years old), and very few affiliative interactions towards M1
(Eigil) (4 years old at that time) during the mating season, being affiliative interactions of
the same age females very concordant. In Nakamura et al. (1998) the strongest affiliation
of an immature female (128cm of length) was observed with a 148 cm female porpoise. If
lengths are compared with growth curves for the North Atlantic (Lockyer & Kinze 2003),
they should be around 2 and 5 respectively. The relation of the claf with two other adult
females was negligible. This is concordant which what was found in the present study.
It has been seen in belugas (Delphinapterus leucas) that younger animals,
sometimes affiliate together, and also tend to affiliate with older animals (some months-
years older), being subdominants in their relationship. This is believed to be a part of their
developmental learning: because of their lack of social experience they follow a slightly
older animal (Krasnova et al. 2009). Which coincides with the reported above, and with
M3 affiliating with M2 (9y) but not with M1 (12y).
F3 and M3 in Harderwijk, were only some months older than F3 in Kerteminde,
and thus F3 (in Kerteminde) might be expected to affiliate with F2 (5y), as seen in the
claves in Harderwijk but F3 in Kerteminde did not interact with the younger female F2.
This could be because the calf in Kerteminde stayed during all her developmental process
separated only with her mother. But the relations of F3 and M3 with F2 (4y) (Harderwijk)
could be a normal calf developmental processes (as seen in belugas), or the lack of a
mother might have influenced, additionally the developmental process of the Harderwijk
calves has not been observed (it is not know if they were kept with F2 since their arrival).
Therefore, alloparental care cannot be assessed in the observed situations.
However, whether or not alloparental care or “baby sitting” (a younger female
taking care of another female’s young) occurs in other Odontocete species is controversial.
It has been reported in dolphins (Tursiops truncatus; e.g. Tavolga 1996; Amundin 1986);
when the mothers performing their shows in the dolphinarium, a younger animal took care
of them, herding them far away from the show area. However, Mello et al. (2005) reported
to have never observed such cases, and that females with young calves tended to avoid
other animals’ company at least in the first two weeks post-partum; suggesting the “aunt”
concept to be overrated or even misconcepted. It has been seen that the strongest
avoidances from the cows to other conspecifics are seen during the first period post
partum, e.g. a cow-calf pair avoided conspecifics immediately after birth (Eastcott &
Dickinson 1987) and this behaviour decreased with the calf development. Additionally it
has been only observed in some very specific situations by some individuals (Tavolga

86
1996). It seems clear that it is not a basic biological need for the survival of the young of
the species as seen in other mammals (for instance in the painted hunting dog (Lycaon
pictus, Courchamp et al. 2002), but it may occur in specific situations. In this study we
have not observed any female-young relationship that could be specifically linked to
alloparental care.

All the males (ranging from 2 to 12 years) affiliated with F2, the oldest female 4
years old and probably mature (F1 not considered), in contrast males did not maintain
affiliative interactions with the younger (certainly immature) female F3 (Figures 4 and 8).
This agrees with the male-female affiliative relations linked to a sexual function. It is
supported by Nakamura et al. (1998) who also report affiliative interaction between a male
and the 3 adult females, and in contrast being the interactions with the immature female
almost negligible (1 interaction/hour in contrast with 25 affiliations/hour with the oldest
female, calculated from the plots).
The two adult mature males M1(12y) and M2 (9y) affiliated together (the second
pair in strength; Figures 3 or 8).

The pattern of affiliation of the adult female F2 (4 years old) in Harderwijk in this
study (Figures 4 and 8), slightly differs from the behaviour observed during the mating
season of F1 (3 years old) in Kerteminde (Benham 1999), showing an stronger affiliative
bond towards the younger female (1year old) than towards the adult male M1 (4 years
old), but both (male-female and female-female) bonds were observed.

The pattern of aggressions in Harderwijk, shows that the adult female (F2) have
higher levels of aggression that the younger animals F3, M3 (Figure 1).
This is in agreement with the younger animals being subdominants. This varies in
Kerteminde because the high levels of interaction of the juvenile F3 (Figure 1) are directed
towards her mother (Figures 2, 3, and 5). Males (in Harderwijk) seem to show an
intermediate level of aggression, not statistically differing from the aggression in female
or juveniles (Figure 1). In Figure 10 it can be seen that the adult female (F2) directs
aggression but also maintains affiliative interactions with all other animals (Figures 4 and
8). In contrast, the other animals only direct aggression towards some individuals (Figure
10). Some tendencies can be seen in the differential levels of aggression. but no statistical
differences were found due to the low frequencies of occurrence.

87
 As affiliative interactions have been seen to be present in harbour porpoises’
budget, the presence of conspecifics should be considered as an important need in all
social animals for their welfare in captivity. Different interactions have been seen
depending on the age, gender and time of the year, which reflects harbour porpoises
complex social interactions, and should not be disregarded as a basic requirement for
welfare. Supporting this remark on sociality in its most fundamental form, Amundin
(1974b) showed that a harbour porpoises can develop strong stereotyped behaviours while
being kept isolated in a concrete pool; also, Kastelein & Staal (1997) showed that
stereotypic behaviour in isolated individuals could be stopped as a result of the presence of
another harbour porpoise. Therefore, when keeping animals in captivity, sociality needs to
be accounted for, in addition to available space, and enrichment of the environment. It is
also important to point out that a higher complexity of the social groups permits the
performance of natural social patterns, that the presence of different sexes and aged
animals allow (Galhardo et al 1996) (seen for example in the male-male affiliations
observed in Harderwijk, that were not possible for the only male in Kerteminde).

New behaviours have been observed during this study. Harbour porpoises in
Harderwijk were observed to slap with their tail during aggressive interactions, and the
receiving animal was observed to avoid the initiator. Therefore, tail slapping has an
aggressive function, as described in bottlenosed dolphins (Samuels & Gifford 1997).
Grooming was seen to occurs in bouts, (also reported by Wilson 1999) as seen in
other behaviours like for example nursing (Delgado et. al in prep.).
[0]Open or closed mouths giving during aggression, increasing the intensity of the
aggressive interaction (Amundin & Amundin 1971), and jerked nodding another
aggressive display, possible with open and closed mouth (Amundin & Amundin 1971),
were never observed in the present study, probably due to the position observations were
made, from above, that would have difficulted to observe an up down movement, but it
will have been probably counted as a sideward turn (aggression).
It was observed that the sideward turn with its synchronic specific sound was not
always directed towards the head of the receiving animal, as described by Amundin &
Amundin (1974) but also seen to be directed towards the trunk and the tailstock. The
sideward turns directed towards the trunk of the receiver were performed from a distance
(not pushing, Amundin & Amundin 1971); In all of the interactions the same type of
sound was emitted. F1 and M1 were observed to direct some of their sideward turns at the

88
tailstock of F3, the sound emitted appears equal to the aggressive buzz. F3 reacted
differently to those aggressions, and was seen escaping and avoiding the animal
performing it, not reacting and answering with aggression back. If F3 did not react to the
behaviour, it was usually prolonged and ended with the actor performing it touching the
tailstock (i.e. pushing) while the sound was being emitted. Aggression was seen directed
towards the tails stock, and it may have been directed towards the genital area (mainly
seen from M1 towards F3 in Kerteminde). Therefore it might have a sexual function,
which has been attributed to pecking (pushing another animal with the snout; Andersen
and Dziedzic 1964, and Nakamura et al. 1998). However, this hypothesis needs to be
tested with more data, as differences among these kinds of aggressions were all combined
because the observations of each subcategory could not be tested due to its reduced
frequency of occurrence.
Belly exposures were also observed in F3, M1 and M2 (in Harderwijk) however it
could not be assessed towards whom they where directed and were not quantified. Belly
exposure was also observed in F2 in Kerteminde, when no other animals were close an
always in a specific location, which reflects a probably stereotyped behaviour, from the
harbour porpoise repertory but with no sexual function in that circumstance.
Hover and roll described by Benham (1999) were also observed in the females in
Harderwijk. Hover – i.e. a female stays immobile while a male attempts to mate– was
constantly observed in F3. The tailstock of F3 was observed to be bent upwards some
times during copulation. F3 was also seen to lay vertically the head out of the surface, and
males responded to that behaviour attempting copulation, and thus should be considered as
another position eliciting mating behaviour. Rolls – the female turn as an avoidance
response of a copulation attempt – were, in contrast, observed in the mature females F2
and F1, as well as aggression as a response of mating attempts.

OVERALL CONCLUSIONS

This study quantified the affiliative, aggressive and sexual interactions in two groups of
captive harbour porpoises, providing insights into the mating strategy of this species. The
study provided data on affiliations between animals of different gender at different times
of the year, finding affiliation patterns to have a sexual function in male-female

89
interactions, and non-sexual related associations in female-female interactions were seen.
The data suggests a promiscuous mating system in harbour porpoises but with the females
making the final decision about copulation. A strong mother-calf association 1y 4m post-
birth was observed. No explicit alloparental care by younger females towards younger
animals was seen. Immature animals behaved different from adults in their sexual and
other behaviours. In this study new behaviours were described, and the description of
other previously defined behaviours were given more detail. The conclusions from the
study could be important both in animal husbandry and conservation of this species.

ACKNOWLEDGEMENTS

We thank the trainers at Fjord and Bælt and Harderwijk for their help during this study.
The animals were kept in Fjord and Bælt according to a permit from the Danish Forest and
Nature Agency, Danish Ministry of Environment, J.nr. SN343/FY-0014 and 1996-3446-
0021. Funds for this study were kindly supplied by the Siemens Foundation. We thank
Malene Agerled, for help and support specially during the stay in Harderwijk, and help
with translations from Danish. We also thank Tomoko Ishigami for translating
“Nakamura’s et al. 1998” article to use it for comparisons with our data.

90
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seasonality in the harbour porpoise from Dutch waters. In Whales, seals, fish & man. (Ed.
A.S. Blix, L. Walløe & Ø. Ulltang). pp. 459-464. Elsevier Science.

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