Ritz Et Al 2011 Ch4 - Wo - Cover 2

C H A P T E R F O U R
Social Aggregation in the Pelagic

Zone with Special Reference to Fish
and Invertebrates
David A. Ritz*,1, Alistair J. Hobday, John C. Montgomery
and Ashley J.W. Wardy
Contents
1. Introduction
2. Aggregation Principles and Features in Pelagic Ecosystems
2.1. Origins of sociality
2.2. Significance and benefits of social aggregation
2.3. Structure and functions of social aggregations
2.4. Association patterns within aggregations
2.5. Sensing the behaviour of neighbours
2.6. Social networks
3. Technology Breakthroughs in Experimental and Observational
Methods
3.1. Video and motion analysis software
3.2. Optical plankton counters and holography
3.3. Acoustic technology
3.4. Electronic tags
3.5. Future technology challenges
4. Theoretical Developments in Social Aggregation
5. Social Aggregation, Climate Change and Ocean Management
6. Conclusion
6.1. Do reviews stimulate new work?
6.2. Future needs and synthesis
Acknowledgements
References
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School of Zoology, University of Tasmania, Hobart, Australia

Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Hobart, Tasmania, Australia
Leigh Marine Laboratory, University of Auckland, New Zealand

y
School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia
1
Corresponding author: Email: David.Ritz@utas.edu.au
Advances in Marine Biology, Volume 60

ISSN: 0065-2881, DOI: 10.1016/B978-0-12-385529-9.00004-4
2011 Elsevier Ltd

All rights reserved.
161
162
David A. Ritz et al.
Abstract
Aggregations of organisms, ranging from zooplankton to whales, are an
extremely common phenomenon in the pelagic zone; perhaps the best known
are fish schools. Social aggregation is a special category that refers to
groups that self-organize and maintain cohesion to exploit benefits such as
protection from predators, and location and capture of resources more effectively and with greater energy efficiency than could a solitary individual. In
this review we explore general aggregation principles, with specific reference
to pelagic organisms; describe a range of new technologies either designed
for studying aggregations or that could potentially be exploited for this purpose; report on the insights gained from theoretical modelling; discuss the
relationship between social aggregation and ocean management; and speculate on the impact of climate change. Examples of aggregation occur in all
animal phyla. Among pelagic organisms, it is possible that repeated cooccurrence of stable pairs of individuals, which has been established for
some schooling fish, is the likely precursor leading to networks of social
interaction and more complex social behaviour. Social network analysis has
added new insights into social behaviour and allows us to dissect aggregations and to examine how the constituent individuals interact with each
other. This type of analysis is well advanced in pinnipeds and cetaceans, and
work on fish is progressing. Detailed three-dimensional analysis of schools
has proved to be difficult, especially at sea, but there has been some progress recently. The technological aids for studying social aggregation include
video and acoustics, and have benefited from advances in digitization, miniaturization, motion analysis and computing power. New techniques permit
three-dimensional tracking of thousands of individual animals within a single
group which has allowed novel insights to within-group interactions.
Approaches using theoretical modelling of aggregations have a long history
but only recently have hypotheses been tested empirically. The lack of synchrony between models and empirical data, and lack of a common framework
to schooling models have hitherto hampered progress; however, recent
developments in this field offer considerable promise. Further, we speculate
that climate change, already having effects on ecosystems, could have dramatic effects on aggregations through its influence on species composition
by altering distribution ranges, migration patterns, vertical migration, and
oceanic acidity. Because most major commercial fishing targets schooling
species, these changes could have important consequences for the dependent businesses.
Key Words: social aggregation; pelagic zone; marine; association; social
networks; technology; climate change; modelling
Social Aggregation in the Pelagic Zone with Special Reference to Fish and Invertebrates
163
1. Introduction
The marine pelagic zone is defined as the water column, usually in the
open sea. Further divisions of the water column into epipelagic and mesopelagic can be made; however, here we use the term generally. It differs from
the coastal marine domains with regard to ecological patterns; high alpha
diversity, low beta diversity; apparent lack of keystone predators; few examples of trophic cascades; and little apparent competition for space. The
marine pelagic environment represents 99% of the biosphere volume (Angel,
1993). In addition to supplying more than 80% of the fish consumed by
humans (Pauly et al., 2002), pelagic ecosystems account for almost half of the
photosynthesis on Earth (Field et al., 1998). Just as productivity in the pelagic
ocean is not uniform, individuals are not distributed evenly, and clustering is
the norm. Because of the lack of geological substrate, as in coastal regions,
many pelagic species are highly mobile as individuals or populations. In this
review, we focus on examples from species living in the upper 200 m, which
is also known as the euphotic zone.
Animals need to eat to survive, and in mobile pelagic ecosystems this
means finding prey. However, the average concentration of resources in the
worlds oceans is insufficient for growth and survival of a variety of marine
species, ranging from planktonic larvae to top predators (Steele, 1980; Levin,
1992; Genin et al., 2005). Therefore, their survival depends on encountering
dense patches of prey that, in the case of zooplankton, form aggregations
that vary in size along a continuum of spatial scales from 107 to 101 m
(Fig. 4.1) (Haury et al., 1978; Mackas et al., 1985, Nicol, 2006).
Steeles (1980) analysis showed that the patchiness resulting from aggregation increases with trophic level (Fig. 4.2). This seems to be a consequence
of the fact that the higher the trophic level, the less the response to the
detailed structure of the local environment, and a greater ability to use largescale ocean features such as currents or fronts. The higher the trophic level,
the less are the organisms dependent on short-term events such as storms,
which markedly affect phytoplankton production, and active behaviour plays
a more dominant role in generating patchiness.
This prey aggregation, in turn, aggregates their predators at the same
locations. But why is phytoplankton, the base of the food chain, patchy?
The main limitations on primary production are physical and chemical (i.e.
light and nutrient concentrations). Variations in the distribution of light
and nutrients occur both temporally and spatially in the ocean. The higher
the trophic level, the lower the physical environment plays in driving
spatial variability of standing stock, and the more behavioural processes
assume importance (Steele, 1980; Folt and Burns, 1999). A challenge for the
predators then is first to locate these patchy prey aggregations and to remain
164
Figure 4.1 The Stommel diagram, overlain to show the scales that can be sampled with
various platforms, and features such as fronts. From Kaiser et al. (2005), with permission from
Oxford University Press.
within them until it is no longer profitable to continue feeding. Arearestricted search patterns for food are widespread phenomena among pelagic
predators from copepods to whales indicating that many predators are
adapted to find and exploit aggregated prey (Steele, 1980; Leising and
Franks, 2000; Leising, 2001; De Robertis, 2002). While aggregation is ubiquitous at all scales in pelagic ecosystems, it is not simply a passive process
where individuals gather together to exploit a food source and separate once
the food has been eaten. The numerous additional benefits of group living
ensure that groups of many different species remain cohesive for non-feeding
periods though membership may change. These benefits are usually reported
as protection from predators, facilitation of foraging and feeding, access to
centralized information, energy saving and facilitation of mate finding and
reproduction (Wilson, 1975; Ritz, 1994; Hamner and Parrish, 1997;
Heppner, 1997; Krause and Ruxton, 2002).
Persistent animal aggregation has been called a central problem in ecological and evolutionary theory (Levin, 1997; Flierl et al., 1999) because of
the apparently conflicting requirements of short-term selfishness and longerterm group benefits. It may be that the study of the social histories of
genetic aggregations and organelle symbioses can resolve this dilemma
(Frank, 2007). We contribute to the analysis of social aggregation by
165
Figure 4.2 Patchiness resulting from aggregation increases with trophic level. Modified
from Steele (1980).
reviewing the social behaviour of invertebrates and fish living in the upper
200 m of the pelagic environment, but where appropriate, we use examples
from marine birds and mammals. This review builds on Ritz (1994), and
thus we restricted the present review to post-1994 discoveries except where
reference to earlier papers is necessary for clarity or because of previous
omission. Because the scope of this review has been expanded to include
fish and, where appropriate, other vertebrates, relevant pre-1994 papers are
also included for these groups. We explore general aggregation principles
(Section 2), describe a range of new technologies and provide examples of
the insights gained from their use (Section 3), and from theoretical modelling
(Section 4). In Section 5 we discuss the relationship between social aggregation and ocean management and speculate on the possible impact of climate
change. Since this review complements Ritz (1994), we also examine
whether the post-1994 literature on the subject of social aggregation indicates if the earlier review stimulated research in directions identified as being
particularly worthy of further study. We did this by using search terms associated with the previously identified gaps for the subsequent period. We conclude with areas ripe for further research to advance understanding of social
aggregation (Section 6).
We note that review papers offer an opportunity for synthesis, comparison, gap analysis and identification of new areas for attention. Explicit
guidelines to achieve these objectives in a repeatable and transparent
fashion have been codified for medical reviews by Roberts et al. (2006),
who also note that ecological reviews often fail to measure up to these
criteria. Many of these criteria helped to shape this review, but in particular, identification of the sources of evidence and how they were obtained
allows assessment as to whether the material included is likely to be
comprehensive with respect to a topic of interest. Depending on the
166
presentation of this material, this allows repeatability in future. We performed

a comprehensive search for relevant material using several search engines: ISI
Web of Science, Google Scholar, Science Daily using the following terms:
Social aggregation in pelagic environments; group dynamics; three-dimensional analysis
of pelagic aggregations; modelling pelagic aggregations; pelagic aggregations and ocean
management; pelagic aggregations and climate change, and the contractions of these
words. We did not to restrict our literature search to specific journals, as we
were concerned we might miss important insights and contributions in
journals covering alternative disciplines. Additional materials were obtained
from reference lists in papers located using our search procedure, our
personal reference collections, and from discussion with expert colleagues. In
this way we accessed relevant breakthroughs in the study of social insects and
humans. Grey literature is difficult to access with traditional search tools (e.g.
Biological Abstracts), but increasing use of the Internet allows searching using
the same keywords for posted grey literature.
2. Aggregation Principles and Features in

Pelagic Ecosystems
Before concentrating on social aggregation, some general points
about aggregation are relevant. For example, the importance of aggregation
for energy transfer is often ignored. This energy transfer can be trophic, or
spatial, connecting habitats and allowing biological processes to be enhanced
in non-productive areas. Hydrodynamic patterns can concentrate resources
(Alldredge and Hamner, 1980) while migrating animals cause cross-habitat
redistribution of carbon and nutrients (Young et al., 1996). Furthermore it
has been shown that schooling animals, by their swimming actions, are an
important source of fine-scale turbulence in the ocean (Huntley and Zhou,
2004). They found that estimated rates of kinetic energy production by animal schools are all of the same order, i.e. 1025 W kg 21, irrespective of size
(see Table 4.1).
Based on these data it appears that animal-induced turbulence is comparable in magnitude to energy dissipation resulting from major storms. In fact,
according to Dewar et al. (2006), the biosphere generates enough power to
stir the ocean. More recent work by Katija and Dabiri (2009) shows that
such fine-scale turbulence is primarily dissipated as heat. These authors highlight an alternative mechanism of mixing originally suggested by Darwin
(1953), which depends on animal shape and drift volume, i.e. the volume
of fluid that migrates with the animal as it swims. Importantly, the drift volume of adjacent animals in an aggregation may increase the effective size of
their combined boundary layers, enhancing the possibility of vertical mixing.
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Table 4.1 Kinetic energy production (Ep(W kg 21)) by a range of schooling species
Species
Mass (kg) Abundance Speed

(no. m 23) (m s 21)
Euphausia superba
Engraulis japonicus
Engraulis mordax
Sardinops saqax
Clupea harengus
Pollachius virens
Thunnus albacares
Tursiops truncatus
Thunnus thynnus
Orcin us orca
Physeter macrocephalus
0.0002
0.002
0.010
0.033
0.30
2.30
77
21.5
318
1645
19850
30000
1294
115
29.4
4.7
0.25
0.0035
0.0010
6.5 3 1024
8.9 3 1025
4.5 3 1026
0.05
0.09
0.14
0.19
0.35
1.05b
1.59
3.35c
1.30
3.95c
2.08d
0.11a
0.22
0.24
0.26
0.30
0.39
0.44
0.85c
0.48
0.87c
0.83e
Ep (W kg 21)
2.6431025
1.4131025
1.0631025
1.3131025
3.9031025
2.7031025
4.4931025
2.803l025
5.3631025
4.0331025
6.7731025
from Torres (1984).

average swimming speed of free-swimming saithe schools (Pedersen, 2001).
c
direct measurement of cruising speed and propulsive efficiency (Fish, 1998).
d
from Rice (1989).
e
approximated from measurements on the white whale Delphinapterous leucas (Fish, 1998).
Reproduced with permission from Huntley and Zhou (2004).
b
The disadvantage of group living includes predator attraction, local depletion of food resources, competition for food and spread of disease (Parrish
and Edelstein-Keshet, 1999; Hoare and Krause, 2003) and the trade-offs have
been examined using a range of evolutionary models. These studies often
advocate greater integration between empirical work, theoretical and modelling approaches (see Parrish and Edelstein-Keshet, 1999).
Aggregations in the pelagic ecosystem may occur as a result of several
processes:
1. Passive aggregation including the concentrating effects of circulation
such as fronts from river plumes, Langmuir circulation and internal waves
(Flierl et al., 1999; Banas et al., 2004), and over abrupt topographies,
such as the shelf break and seamounts (Boehlert and Genin, 1987), and
coral reefs (Genin et al., 1988, 1994).
2. Active and non-social aggregation including independent attraction of
conspecific individuals to a food resource (e.g. copepods, Poulet and
Ouellet, 1982); or to a light source (Yen and Bundock, 1997); predators
may gather at the same natural features (Klimley et al., 2003; Hobday
and Campbell, 2009) as well as artificial structures such as fish aggregation devices (FADs) (Freon and Dagorn, 2000).
3. Active and social aggregation that includes groups that self-organize
and maintain cohesion because of the many derived benefits (Ritz,
1994; Krause and Ruxton, 2002). Parrish and Edelstein-Keshet (1999)
168
Figure 4.3 Examples of aggregations of invertebrates, fish and marine mammals. (A)
Schooling krill, Nyctiphanes australis; (B) mysids, Paramesopodopsis rufa; (C) squid, Sepioteuthis
sepiodea; (D) school of Real Bastard Trumpeter, Mendosoma lineatum; (E) school of northern
bluefin tuna, Thunnus thynnus; (F) pod of dolphins, Tursiops truncatus. (A) Photo by Rudi
Kuiter; (B) photo by Jon Bryan; (C) photo by Ruth Byrne; (D) photo by Ron Mawbey; (E) photo
by Bill Pearcy; (F) photo by Simon Talbot.
define social animal aggregations as those that self-organize as

opposed to aggregations that form in response to external cues e.g.
light or food.
It is this active social aggregation that is the focus of this review. This
subset of aggregation is sometimes termed congregation (Turchin, 1997)
and occurs in a range of invertebrates and vertebrates as shown in Fig. 4.3.
169
Ritz (1994) presented many examples of aggregations of pelagic

invertebrates (his Table 1) with their spatial and temporal attributes.
Figure 4.4 shows the spatial and temporal scales of aggregation of
Antarctic krill (Euphausia superba) and illustrates the range of descriptive
terms applied to groups of this species (see also Box 4.1).
Temporal
scale
Spatial
scale
Concentration
Mths
Patches
Wks
Hrs
Macro
>1000 km
Super-swarms
: few 1000 g m3
t:100-250mm
l: up to several km
Swarms
: few 10 to several
100gm3
t: 1-20 m
l: several 10s m
Cohesive
aggregations
Meso 10
1000 km
Layers and
Scattered forms
:10gm3 (approx):
t: large
l: many km
Irregular forms
: few 100s g
m3
t: 10 cm
Dispersed
aggregations
Non-aggregate
forms
: <0.1 g m3
Micro <10
km
Non-aggregated
forms
Figure 4.4 Nomenclature of aggregations of Antarctic krill, Euphausia superba. 5 density;

t 5 thickness; l 5 length. Reproduced with permission from Miller and Hampton (1989).
Box 4.1
Terms used to define aquatic invertebrate groups (after Ritz, 1994, and
Folt and Burns, 1999) and social groups of aquatic vertebrates (after
Pitcher and Parrish, 1993; Shane et al., 1986) as used in this review.
Swarm: used here to mean a discrete integrated social group with members evenly spaced, but not polarized (aligned in the same direction).
School: discrete integrated social group in which members are polarized
and displaying synchrony of movement. A school need not always imply
that all individuals are facing the same direction; social squid can swim
both backwards and forward.
Shoal: a (usually) larger grouping within which are contained subgroups
conforming to the definitions of swarm and school.
Pod (primary group): term confined to smallest social groupings of cetaceans that remain intact for days or weeks.
Herd (secondary group): temporary (minutes or hours) aggregations of
primary groups of cetaceans.
170
In the rest of this review we will concentrate on social aggregation.

Sociality means living in groups which, in turn, creates and intensifies two
opposing forces: on the one hand cooperation with conspecific neighbours,
and on the other competition for local resources (Frank, 2007). The former
can increase efficiency and aid in competition with other groups; the latter
may promote conflict. This antagonism between cooperation and competition is a recurring theme in studies of social aggregation. The title of Franks
(2007) paper, All of life is social, reflects the fact that multicellularity arose
through genetic aggregations and cellular symbioses. But what factors make
social aggregation, as exemplified by fish or krill schools, such a conspicuous
feature of the pelagic zone? Before addressing this question we consider how
sociality may have arisen.
2.1. Origins of sociality

Aggregation occurs in all phyla but where does sociality begin? In one sense
all of life is social (Frank, 2007), in that multicellularity owes its existence to
amalgamation and symbiotic cooperation of single-celled organisms.
According to the argument outlined below, animals (or cells) must be able to
recognize conspecifics to the extent that stable networks develop. How do
animals recognize each other? Recognition of self versus non-self must have
arisen early in the evolution of multicellularity, perhaps to protect these cellular aggregations against invasion by competing neighbours (Frank, 2007).
There is evidence that olfactory cues discriminated by the major histocompatibility complex are important in vertebrates (Krause and Ruxton, 2002;
Villinger and Waldman, 2008). It has been reported recently that there is an
analogous system in invertebrates (Cadavid et al., 2004).
Recent work on social insects has led to the postulation that development of complex societies arose initially through natural group dynamics,
i.e. not a genetic selection for particular traits favouring social behaviour but
a tendency towards network development within groups (Fewell, 2003).
Relatively simple connections between individuals in a group can create
patterns of behaviour of increasing complexity in the same way as simple
decision rules create complex behaviour in computer-generated aggregations. If true, this suggests that networks are an essential precursor to social
behaviour.
It has been suggested that the repeated co-occurrence of stable pairs
may have been an important prerequisite for the evolution of cooperative
behaviour and reciprocal altruism (Milinski, 1987; Croft et al., 2005).
Relatively simple connections between individuals in a group can create
patterns of behaviour of increasing complexity. Organized societies occurring within many different taxa may have arisen through the agency of
these simple local interactions self-organizing into global networks
(Glance and Huberman, 1994; Fewell, 2003). It has long been recognized
171
that inclusive fitness operates within groups whose members share genes
(Hamilton, 1964). However, it is now suggested that multilevel selection
operates not just because members of groups are related but that densely
connected networks exist within aggregations (Fewell, 2003). This permits rapid and efficient information transfer and flexible responses. It is
important to explain that multilevel selection does not imply that some
groups are more successful (fitter) than others and contribute more groups
to the next generation. Instead group-level selection implies that the fittest groups contribute the most individuals to the next generation.
Behavioural traits possessed by individuals need to influence the behaviour of others in the group to be relevant to group selection (Krause and
Ruxton, 2002).
Behavioural characteristics leading to social networks are not necessarily
restricted to vertebrates. According to Webster and Fiorito (2001), socially
guided behaviour, conforming to a framework developed for social vertebrates, can be found in a wide range of non-insect invertebrate phyla.
However, among marine taxa, only Crustacea, Gastropoda and Cephalopoda
displayed behaviour typical of social learning, i.e. the acquisition of novel
behaviour due to observation of, or interaction with, a conspecific. This
might indicate more sophisticated social behaviour in these groups compared
to lower invertebrate animals.
2.2. Significance and benefits of social aggregation

The commonly stated benefits of group living are facilitation of foraging
and feeding; reproductive facilitation (including sharing parental care in
the case of some cetaceans), protection from predators and energy saving
(Wilson, 1975; Ritz, 2000; Krause and Ruxton, 2002). Other authors
add maintenance of position in the environment (Clutter, 1969), habitat
defence (Hurley, 1977) and access to centralized information (Parrish
et al., 2002). Benefits of synchronous breeding and release of young
within aggregations of mysids are described by Johnston and Ritz (2001).
The benefits listed above are not divorced from one another; in fact an
ultimate advantage of aggregation may be energy saving in the broadest
sense, i.e. efficiency in foraging, food capture, locomotion, protection
from predators, etc. It is likely that any adaptation that conserves energy
will be favored by selection and fixed into the genetic blueprint (Ritz and
Swadling, 2006). Thus if energy can be conserved at the same time as
efficient food gathering and escape from predation, this will ultimately be
advantageous for the species. Cohen and Ritz (2003) found that mysids
in small uncohesive groups were more likely to expend energy (tailflips)
when exposed to a threat in the form of a fish kairomone than those in
swarms. A kairomone is a chemical substance released externally that benefits the recipient without benefitting the emitter. The energy saving
172
benefits of swarm membership by mysids were confirmed by Ritz et al.

(2001) who found that larger swarms expended less energy than smaller
ones, which, in turn, saved more energy than un-aggregated individuals
(Ritz, 2000). The conversion of these energy savings into enhanced fitness is assumed to follow, but empirical evidence is lacking to date.
The foregoing discussion raises some important questions, e.g. do different forces promoting patchiness and social aggregation dominate at different scales (Flierl et al., 1999)? Patterns apparent at large scale are not
independent of those at small scale and vice versa. Large populations of
individuals can self-organize into pattern-generating aggregations (Parrish
and Edelstein-Keshet, 1999; Parrish et al., 2002; Viscido et al., 2004).
Many of the patterns seen in real-life schools and swarms are apparent in
computer generated models based on a few simple rules (see Boids: http://
www.red3d.com/cwr/boids/ and Efloys: http://arieldolan.com/ofiles/
eFloys.html). An unresolved question is are all of these emergent patterns
evolutionarily advantageous? Can we reconcile the short-term selfishness
of individuals with the maximum group benefit of maintaining a cohesive
unit? There is potential for great complexity of trade-offs and constant tension determining decision-making. Examples can be found among krill in
the decision to migrate vertically, and whether it is advantageous to school
while doing so (De Robertis, 2002; Burrows and Tarling, 2004).
Silversides (Menidia menidia) changed their schooling behaviour according
to light levels during periods of twilight, which appeared to be associated
with predation threat and availability of food (Major, 1977). Vertically
migrating mesopelagic fish may apparently elect to form schools when
light levels at night are high enough to favour visual predators but not otherwise (Kaartvedt et al., 1996; see Fig. 4.5 reproduced from their paper).
This suggests there are some disadvantages to schooling, e.g. increased visibility to and attraction of the attention of predators; also decreased per
capita share of food resources.
Active and social groups are those that self-organize (characteristic
group patterns that arise from decentralized behaviour), and maintain
cohesion because the derived benefits outweigh the costs (Ritz, 1994;
Krause and Ruxton, 2002). As defined in Box 4.1, social aggregations
include swarms, schools, shoals, pods and herds. Regardless of the terminology, social aggregations can be recognized by their coordinated movement, persistence in time, reactions of individuals to the group and by the
fitness benefits provided by mutual attraction.
Animal aggregations occur where large numbers of individuals are to
be found gathered in close spatial and temporal proximity. Examples of
aggregations can be found in virtually all animal phyla (Parrish and
Edelstein-Keshet, 1999; Parrish et al., 2002). Such aggregations may consist entirely of conspecifics; however, there are also many examples of
multispecies aggregations, e.g. in fish (Allan, 1986), and crustaceans
173
Figure 4.5 Echogram showing abrupt changes in vertical distribution of krill, planktivorous (Norway Pout) and piscivorous (Pearlside) fish in response to changes in light penetration. Reproduced from Kaartvedt et al. (1996).
(Ohtsuka et al., 1995), and even mixtures of the two taxa (McFarland
and Kotchian, 1982). Aggregations may form in response simply to the
distribution of resources in the habitat, but the term social aggregation
refers specifically to groups of individuals that are brought together, either
wholly or in part, by social attraction.
Social aggregations are an extremely common phenomenon with considerable ecological and economic importance. For example, well over half
the worlds fishes, including the overwhelming majority of the commercially harvested species, form social aggregations at some stage during their
lives (Shaw, 1978). Theoretically, a social aggregation could consist at a
minimum of two individuals (e.g. spawning cuttlefish); however, most
marine social aggregations are substantially larger than this, indeed some
may often encompass billions of individuals (e.g. krill). The scale of such
aggregations can be dramatic ! DeBlois and Rose (1996) reported shoals
of cod (Gadus morhua) of over 10 km in length, migrating groups of mullet
(Liza aurata and L. saliens) stretch for over 100 km (Probatov, 1953), while
Radakov (1973) estimated the volume of some Atlantic herring (Clupea
harengus) shoals at up to 5 km3. The concept of the optimal group size has
been the subject of considerable theoretical debate (see Sibly, 1983;
174
Giraldeau and Gillis, 1985; Giraldeau and Caraco, 2000); however, few
empirical data exist to test theoretical predictions (Willis, 2008). In marine
environments, many of the larger aggregations that may be observed are
so-called free-entry systems, where group members have little or no ability
(and indeed little incentive) to control group membership. In these cases,
group sizes are highly dynamic and groups frequently split and reform
according to the context, a property which has led to them being described
as fission!fusion societies (Couzin, 2006). Restricted-entry groups are
far less common in the marine environment, and the examples that exist
are all of vertebrates, perhaps most notably the small aggregations of coral
reef fishes (Sale, 1971; Forrester, 1991; Whiteman and Cote, 2004) and
social groups of cetaceans (Gowans et al., 2001; Lusseau 2003; Hartman
et al., 2008).
There exists considerable variation, both within and between species, in
sociality. Some authors draw a distinction between facultative and obligate
sociality; however, such distinctions are somewhat arbitrary since the extent
to which any individual manifests social attraction is likely to vary with
ontogenetic stage and with context (Ritz, 1994). Nonetheless, some animals exhibit considerable stress if separated from conspecifics: Atlantic herring that have been experimentally isolated from conspecifics have been
reported to die as a result (Gerasimov, 1962). While this is an extreme
example, many social species do manifest stress-related changes in behaviour
and/or physiology if isolated. For example, Ritz et al. (2003) showed that
heart rate of an individual Antarctic krill was high when isolated but slowed
significantly when it was tethered at normal schooling distance from a conspecific and was presumably able to access social cues. The extent to which
marine animals form social aggregations may also be highly dependent
upon the environment. For example, in heterogeneous environments, shoal
cohesion often decreases (Mochek, 1987). Many fish, amongst them cod
(Gadus morhua), sergeant majors (Abudefduf saxatilis) and grey snappers
(Lutjanus griseus), exhibit shoaling behaviour when in mid-water, but the
shoals break up towards the bottom of the water column or when in nearshore areas (Pavlov and Kasumyan, 2000). Furthermore, shoals of fish
characteristically break up at night as light intensity decreases (Higgs and
Fuiman, 1996).
While some species consistently form aggregations throughout their
lives, many others are more social during some stages of their life history
than others. The larvae of many pelagic fish typically do not begin to
shoal until metamorphosis (Fuiman and Magurran, 1994). The importance
of the development of the central nervous system in relation to schooling
behaviour in larval and juvenile striped jack (Pseudocaranx dentex) was
highlighted by Masuda and Tsukamoto (1999), who reported the emergence of mutual social attraction among individuals at around 12 mm in
length. Interestingly, Antarctic krill first begin to show social attraction at
175
around the same length (Hamner et al., 1989), even though final size is
very different. The expression of strong social attraction towards conspecifics during the juvenile phase is a common pattern in fishes before becoming increasingly solitary as they grow (Pavlov and Kasumyan, 2000).
Indeed, many marine species form aggregations during vulnerable early life
stages, since grouping behaviour is often suggested to confer valuable antipredator benefits upon group members (Ritz, 1994). The opposite trend is
manifest in spiny lobsters where juveniles are typically solitary and adults
very often live in groups (Ratchford and Eggleston, 1998). Butler et al.
(1999) demonstrated that attraction to conspecific chemical cues in spiny
lobsters only occurs once individuals reach a given size.
The larvae (and indeed the adults) of many marine species aggregate as
plankton; however, it is arguable whether this is to any great extent due
to social attraction. Banas et al. (2004) consider that the interaction
between individuals in many zooplankton swarms (as opposed to schools)
is of secondary importance. For example, Leising and Yen (1997) contend
that density of copepod swarms in their experiments was controlled by
avoidance reactions to chance close-range encounters. The same authors
found five species of copepod to be insensitive to proximity of conspecifics except at very close range. Extrapolating this view, in their modelling
studies, Banas et al. (2004) regard a swarm not as an interaction between
individuals, but between each animal and its local stimulus field. Of
course, this interpretation does not necessarily reduce the importance of
social attraction. Swarms can be social and density-dependent or nonsocial and density-independent. Most modelling studies of swarming/
schooling behaviour are based on a resolution of forces of attraction,
repulsion and alignment (Couzin, 2006). The degree to which individuals
respond to each other and over what distance is probably a function of
sensory capability but also the need to maintain a hydrodynamic territory (or flow field) that is an essential part of the feeding current, and by
distortion of which an individual gains information about approaches by
other animals.
Social aggregation in general is less well studied in pelagic invertebrates, despite their amenable sizes for experimental laboratory work. The
label plankton, with its connotations of passivity, has probably seriously
hindered the study of social behaviour of true zooplankton and micronekton (Ritz, 1994). The term plankton is not a taxonomic unit and
encompasses a huge diversity of species and forms. It seems likely that a
spectrum of capacity to manifest social behaviour exists in which most
copepods would occupy one end, and live in swarms, with little social
interaction between individuals except to ensure that empty space around
themselves is maintained. On the other end, mysids and euphausiids
exhibit a full range of social interaction with neighbours. Unfortunately,
many authors still group the larger more active constituents, e.g. krill and
176
mysids, with the smaller ones, e.g. up to the size of most copepods, and
ascribe little in the way of social interaction. Alldredge et al. (1984)
claimed that zooplankton swarms with a nearest neighbour distance
(NND) of more than a few body lengths were rare in nature. Later results
(Jiang et al., 2002) explain why this is true for copepods. Larger interindividual distances of 7!14 body lengths ensure that hydrodynamic
interactions between neighbours are minimized so that feeding currents
and detection of nearby individuals are not compromised. Jiang et al.
(2002) showed that copepods gain no energetic benefits when in close
proximity to conspecifics. In contrast, OBrien (1989) showed that mysid
and euphausiid NNDs were on average 1!2 body lengths, and energetic
benefits of swimming close to neighbours were demonstrated by Ritz
(2000) and Patria and Wiese (2004), and communication benefits by
Wiese (1996).
The characteristics of aggregations of zooplankton are sometimes suggested to vary considerably between different species (Banas et al., 2004).
Despite these assertions, there exist many similarities between the aggregation behaviour of many different marine species. For example, Hamner
(1985) and OBrien and Ritz (1988) describe behaviour of swarms and
schools of krill and mysids as being strongly reminiscent of fish schools.
Escape manoeuvres of groups of the two taxa require a high degree of synchrony between individuals, probably requiring a combination of vision,
chemoreception and mechanoreception. Furthermore, the possibility of any
clear distinction between the aggregation behaviour of copepods and that
of mysids and krill seems unlikely since even copepods (Labidocera pavo) can
be found forming schools (Omori and Hamner, 1982) which surely
requires some inter-individual coordination. Differences in NNDs between
aggregations of copepods and krill/mysids may be due to the different
feeding methods, lack of any energetic benefit in close alignment in the former and/or the differences in the reliance on vision. The eyes of most
copepods and other non-Malacostracan crustacean zooplankters do not
have lenses and do not have an image-forming capacity (Eloffson, 1966).
However, it is perhaps significant to note that Labidocera have remarkable
eyes (Omori and Hamner, 1982) that have a dorsal pair of spherical lenses
serving a single mobile eyecup (Land, 1988). Land suggests that scanning
movements of the rhabdoms in the eyecup are concerned with visual detection of conspecifics.
2.3. Structure and functions of social aggregations

From an evolutionary point of view, it is predicted that for aggregations
to persist, the benefits of group membership must, on average, outweigh
the costs. The benefits and costs of grouping generally are dealt with
extensively in other texts (Krause and Ruxton, 2002) and so here we
177
provide only limited pelagic examples to illustrate the commonality with

non-pelagic taxa and to emphasize social benefits and costs.
According to Flierl et al. (1999), many groups in marine pelagic systems, with the exception of marine mammals, seem to be large, relatively
transient and loosely knit. This is not necessarily the case for fish schools
or schools of mysids and euphausiids, where the aggregation can be longlived even if membership changes over time (OBrien, 1988; Parrish and
Edelstein-Keshet, 1999). Social grouping implies some appreciation by
individuals of their membership of the group and its consequences. In
other words, individuals respond to conspecifics in a density-dependent
manner (Flierl et al., 1999; Burrows and Tarling, 2004; Hensor et al.,
2005; Grunbaum, 2006). A group formed initially by random encounters
may grow by density-dependent interactions between members with
eventual size being determined by mean payoff to individuals in the
group (Parrish and Edelstein-Keshet, 1999). An example might be in
food acquisition whereby all group members are disadvantaged if the
group outgrows the food resource and individual rations decrease. Social
organization then is an emergent property (group characteristic arising
from decentralized interactions) that develops from the network structure
(see below).
Research on the influence of the social group on metabolic processes
including growth, feeding efficiency and energy use has been neglected
(Ritz, 2002). Ritz (2000) predicted that growth rate in schools or swarms
of krill and mysids was likely to be much greater than in isolated individuals or small groups; however, it was some years before evidence was
forthcoming. Atkinson et al. (2006) showed that when growth of freshly
caught krill is recorded by the instantaneous rate method, a technique
that allows insight into the recent social behaviour, the maximum values
were much higher than most of the previously published rates. These
high rates are likely due to the benefits of feeding within a school immediately before capture. Analysis by Ritz (1997) showed that food capture
rate by mysid swarms of different sizes varied significantly when per capita
food availability was constant and inhomogeneous. Furthermore Ritz
(2000) noted that ingestion rates of Antarctic krill measured in freshly
caught animals by faecal egestion were 3 times higher than those fed in
laboratory tanks (Pakhomov et al., 1997). He suggested that the difference
was due to the former having fed within aggregations immediately before
capture, whereas the krill in laboratory tanks rarely form aggregations
(Kawaguchi et al., 2010). It appears that krill (and mysids) not only save
energy in social groups but may also feed more efficiently (see also Ritz,
1997). The latter is a well-established principle in fish. For example, fish
are known to forage more successfully on spatially variable food patches
when searching in social groups (Ryer and Olla, 1992). The issue of food
competition in aggregations may be more acute for vertebrates than for
178
Figure 4.6 (A) Time series of body outlines of trout superimposed on vorticity and
velocity vector plots of the wake produced by a cylinder located in the flow (left to right).
(B) Midlines for seven consecutive tailbeats. (C) Phase between body and vortices where
180" represents slaloming in between vortices and 0" and 360" represent vortex interception. After Liao et al. (2003a,b).
invertebrates. Ritz (2000) made the point that fish in schools in the sea
are more likely to be food limited than particle-feeding coastal mysids.
Many animals that aggregate socially have been demonstrated to save
energy while aggregated. Birds (pelicans) in V-formation showed a significant decrease in heart rate and the energy saving may have been because
they were able to spend more time gliding and less flapping (Weimerskirch
et al., 2001). Fish (trout) have been shown to slalom between experimentally generated vortices (Karman gait) using only their anterior axial muscles. By synchronizing their body kinematics in this way, they may use
very little energy and gain a hydrodynamic advantage beyond that gained
by simple drafting (Fig. 4.6). Thus it is possible that any favourable hydrodynamic consequences generated by the aggregation itself or its interaction
with surfaces (ground effect) could be exploited to save energy.
2.3.1. Patchiness in zooplankton
Many authors have documented the uneven or patchy distribution of
zooplankton in marine and freshwater (Hardy and Gunther, 1935; Steele
and Henderson, 1981; Folt and Burns, 1999). It has taken several decades
for the contribution of plankton behaviour in generating this patchiness
179
to be fully appreciated (Ritz, 1994; Folt and Burns, 1999). These authors
describe general principles of invertebrate aggregations, and both papers
highlight the importance of biological factors in creating and maintaining
planktonic aggregations. By contrast, Siegel and Kalinowski (1994) provide Table 4.2 listing suggested causes of aggregation by Antarctic krill. It
is particularly noteworthy for how few authors credit behaviour as a primary contributor to aggregation.
Nonetheless, the conclusion that social behaviour is the main driver of
variability in small-scale density distribution of Antarctic krill is strongly
supported by a comparison of variance spectra of phytoplankton, temperature and krill (Weber et al., 1986; Verdy and Flierl, 2009). At small scales,
the krill spectrum is flatter than the others indicating that factors other
than environmental ones are generating the observed patchiness in density
distribution (Fig. 4.7).
Folt and Burns (1999) list four behavioural mechanisms that can result
in zooplankton patchiness: (1) diel vertical migration, (2) predator avoidance, (3) food finding and (4) mating behaviour. Genin (2004) gives five
further mechanisms contributing to patchiness by which plankton, micronekton and fish can become aggregated above abrupt topographic features, all driven by (1) ocean currents where long residence upwelled
water enriches primary production which propagates up the food web;
(2) daily accumulations where topography blocks morning descent of
zooplankton, e.g. over seamounts; (3) behavioural response of zooplankton to upwelling currents; (4) behavioural response to downwelling currents; (5) enhanced population growth by residents due to current
amplification driven by abrupt topographies. These mechanisms do not
necessarily imply any social interaction between individuals but may provide opportunities for closer attraction. Hamner (1988) observed that
almost any animal behaviour can generate patchiness, but more sophisticated behaviour is required for social aggregation.
Recent work by Genin et al. (2005), using sophisticated multibeam
acoustic equipment, has demonstrated that zooplankters,5 mm actively
swim against upwelling and downwelling currents in an effort to maintain
depth. In this way, they aggregate at fronts. The value of maintaining depth
in this way is not yet clear, but may serve to keep them within food-rich
zones and prevent them straying into less favourable depths. Any behaviour
that actively or passively leads to individual distributions becoming clumped
could result in a tendency to remain in a group once the many benefits are
manifested. Swimming against currents of up to 1 cm s 21 at rates of .10
body lengths s 21 (Genin et al., 2005) is energetically expensive but
might be less so if the individuals formed aggregations. Ritz (2000) and
Ritz unpublished observation have shown that mysid swarms expend
between 3 and 7 times less energy than small groups of individuals swimming uncohesively. A possible explanation is that swimming action by
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Table 4.2 Suggested causes of aggregation in Antarctic krill, Euphausia superba

Author
Main causes and environmental

limits
Region
Marr (1962)
Inflow of the current branches

from the Weddell Sea
Presence of system currents
flowing in opposite direction
Occurrence of eddies
South Georgia
No elements of environmental
limits directly influence
distribution
Environmental parameters and
social behaviour
Oxygen limits
West Atlantic
Maslennikov (1972)
Wolnomicjski et al.
(1978)
Rukusa-Suszczewski
(1978)
Mauchline (1980)
Kils (1979)
Wilek et al. (1981)
Stein and RakusaSuszczewski (1984)

Kalinowski and Witek
(1985b); Witek et al.
(1988)
Hydrodynamic forces, thermocline

No physical and chemical
variability
Phytoplankton (2!20 km spatial
scale)
Kalinowski and Witek Presence of daylight for patch
(1985a)
formation
Loeb and Shulenberger Temperature (infusion of cold
(1987)
water) and wind direction
Everson and Murphy Hydrodynamic processes (passive
(1987)
current-borne movement)
El-Sayed (1988)
Phytoplankton at scales 2!20 km
Priddle et al. (1988)
South Georgia
Theoretical
consideration
Laboratory
experiments
West Atlantic
No elements of environmental
parameters T, S, O2, nutrients,
phytoplankton
Bransfield
Topography of bottom, which
Strait
influences direction of water
masses and hydrodynamic process
Hydrodynamic processes and social West Atlantic
behaviour
Hampton (1985)
Weber and El-Sayed
(1985)
Weber et al. (1986)
Murphy et al. (1988)
South Georgia
Environmental phenomena and

food availability
Environmental phenomena and
active reaction for
disadvantageous environmental
conditions
Indian sector
Indian sector
West Atlantic
Elephant
Island
King George
Island
Southern
Ocean
Southern
Ocean
South Georgia
Bransfield
Strait
(continued)
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Table 4.2 (continued )

Author
Main causes and environmental

limits
Region
Maslennikov and
Solyankin (1988)
Makarov et al. (1988)
Variability of hydrological
conditions
Stable eddies and influence of
water masses
West Atlantic
West Atlantic
Reproduced with permission from Siegel and Kalinowski (1994).
Figure 4.7 Mean spectral plots for krill, fluorescence and temperature. . After Weber et al.
(1986); http://plankt.oxfordjournals.org/content/14/10/1397.full.pdf
cohesive groups generates favourable currents that could be exploited by

members to reduce the cost of forward propulsion and/or to minimize the
rate of sinking by relatively dense crustaceans. Patria and Wiese (2004)
showed that swimming krill (Meganyctiphanes norvegica) generated vortex
182
rings behind the tail that could be exploited by following krill for this purpose. Note that this benefit would only make sense if the krill were in
school formation, i.e. individuals polarized and neighbours sufficiently close
to perceive and take advantage of currents moving in the same direction as
themselves. Ritz (2000) showed that energetic benefit accrued in mysid
swarms, i.e individuals, was not polarized. In this case it may have been the
powerful downdraft generated collectively by the group that induced an
updraft at the margins of the swarm. This could have been used to counteract sinking. Buskey (1998) reported that mysids frequently changed vertical
position in the school while maintaining their horizontal position in a current. Energetic benefit may derive from specific relative positions of individuals in groups (Parrish and Edelstein-Keshet, 1999; Svendsen et al., 2003).
Thus it would be logical for individuals not to adopt fixed positions within
the group but to continually make excursions in order to maximize whatever benefits accrued at any given moment (Ritz, 1997).
2.3.2. Diel vertical migration
Diel vertical migration (DVM) is generally held to represent a trade-off
between the functions of food gathering and avoiding predators
(Kaartvedt et al., 1996). The typical pattern is a dawn descent into deeper,
darker levels during the day and an ascent towards the surface beginning
around dusk. Ritz (1994) was the first to suggest that since social aggregation serves the same purposes, species that form swarms or schools may
find DVM redundant. This could account for the confusing and sometimes contradictory evidence for vertical migration in Antarctic krill
(Miller and Hampton, 1989). It appears from work by De Robertis
(2002) that there are situations in which the normally social euphausiid
Euphausia pacifica performs DVM but does not form social aggregations,
i.e. one is redundant in the presence of the other. De Robertis suggests
that DVM may be favoured over social behaviour in open-water zooplankton because of well-developed vertical gradients in predation risk.
However, Antarctic krill are strongly social in open-water situations and
exhibit variable DVM (OBrien, 1987; Daly and Macaulay, 1991). Further
evidence is supplied by Kaartvedt et al. (1996). The DVM behaviour of
fish and krill (mainly Thysanoessa inermis) varied according to the light
conditions in upper shelf waters and the predation risk. In brief intervals
at dawn and dusk, known as anti-predation windows, there is sufficient
light for planktivorous fish to locate prey, but not enough to render these
fish vulnerable to piscivores. Anti-predation windows may occur at other
times due to the passage of fronts bringing water of higher turbidity. At
these times planktivorous Norway Pout may migrate vertically to forage
on krill, whereas when the light penetration through overlying waters is
greater, the planktivores remain in safer, deeper layers but out of contact
with their prey. It is unclear whether the planktivores migrate in schools.
183
These examples serve to illustrate the great flexibility of behavioural strategies and the fitness benefits they may confer.
2.4. Association patterns within aggregations

Association patterns within and between groups of marine animals are seldom entirely random. At a very basic level, multispecies aggregations are
very often dominated by a small number of species (Krause et al., 1996;
2005), suggesting either species-level recognition and an association preference for conspecifics, or that this emerges passively from similarities in
activity patterns within but not between species (Conradt and Roper,
2000). Beyond this, group membership may be structured by phenotype;
fish shoals for example frequently assort by body length, species, colour and
parasite load (Krause et al., 2000). The fact that invertebrate aggregations
commonly consist of a narrow individual size range (Watkins et al., 1992)
suggest that they too possess a certain level of cognitive ability permitting
pairing with other morphologically similar individuals (Wilson and
Dugatkin, 1997). Watkins and Murray (1998) reported that biological characteristics between adjacent swarms of Antarctic krill (Euphausia superba)
vary in individual size, maturity stage, moult and feeding state. Young et al.
(1994) show that Daphnia clones have differing swarm-forming tendencies
and suggest that clone-mates can recognize each other probably by chemical cues. This appears to be a fruitful subject for further research.
Any advantages of group fidelity may be partly related to the fact that
individuals associate with others of similar phenotype. In addition to this,
research has shown that individuals manifest social association preferences
for some conspecifics over others, in the absence of any clear phenotypic
differences (Milinski et al., 1990; Ward and Hart, 2003). Familiarity, as
this subgrouping phenomenon is known, acts to enhance the benefits of
shoaling, further reducing the per capita risk of predation (Chivers et al.,
1995) and improving foraging performance (Ward and Hart, 2005). In consequence, it might be expected that this would act in concert with other
mechanisms (Conradt and Roper, 2000) to stabilize association patterns
over time. Yet the data gathered from field studies on this topic are equivocal; it appears that there is no general rule regarding shoal fidelity among
free-ranging schooling fish. Evidence exists for shoal fidelity in three-spine
sticklebacks, Gasterosteus aculeatus (Ward et al., 2002), and Klimley and
Holloway (1999) reported the co-occurrence of individual yellowfin tuna
in time and space. By contrast, banded killifish (Fundulus diaphanus)
appeared to show no consistent shoal fidelity (Hoare et al., 2000) despite
showing a strong tendency to assort with fish of similar phenotypic characteristics. Of the few other studies in which the movement of marked fish
among and between shoals have been followed, Helfman (1984) found low
shoal fidelity among yellow perch (Perca flavescens), and Hilborn (1991)
184
showed that schools of skipjack tuna (Katsuwonus pelamis) mixed rapidly and
were not composed of the same individuals for more than a few weeks (see
also Willis and Hobday, 2007). There are even fewer examples of experiments testing shoal fidelity in invertebrate aggregations, although Twining
et al. (2000) demonstrated homing behaviour and shoal fidelity in a mysid
(Mysidium gracile).
On a larger scale, studies of migrating fish populations do suggest a tendency for stable association patterns to develop (McKinnell et al., 1997; Hay
and McKinnell, 2002). McKinnell et al. (1997) reported that steelhead trout
(Oncorhynchus mykiss) form long-term associations at sea throughout their
migration. Furthermore, Hay and McKinnells (2002) remarkable study of
the movements of more than half a million Pacific herring (Clupea pallasii)
over a period of 14 years concluded that individuals formed stable temporal
and spatial associations. Nonetheless, it would be difficult to conclude that
familiarity alone is entirely responsible for the observed patterns. Group
fidelity in fish migrations may be influenced by any of several different
mechanisms, including kin- or population-specific recognition (Quinn and
Tolson, 1986), activity synchronization (Conradt and Roper, 2001), population-specific migration traditions (Warner, 1988) or pheromonal attraction
(Baker and Montgomery, 2001). Alternatively, because migrating fish tend to
remain in large, temporally stable shoals, as opposed to the smaller and looser
aggregations characteristic of many of the shallow water species studied by
behavioural ecologists, patterns of association in migrating fish may be
explained simply by long-term shoal cohesion.
2.5. Sensing the behaviour of neighbours

The sensory dimensions of social aggregation include the sensory basis of
group formation (about which little is known), and the behaviour of individuals, and hence the group, under different contexts such as feeding and
predation threat. Understanding the sensory basis of behaviour is one of
the first steps to understanding the underlying neural algorithms driving
the behaviour in individuals and hence the behaviour of the aggregation.
The focus of this section will be to review the sensory basis of fish schooling, as one of the most important, and highly coordinated, examples of
social aggregation. This discussion will then be extended to consider the
similarities and differences between fish schooling, and invertebrate aggregations, and briefly the sensory communication within marine mammal
aggregations.
The sensory basis of fish behaviour has been reviewed in Montgomery
and Carton (2008). Vision, lateral line and hearing are the strongest candidates for schooling coordination although olfaction may also play an
important role. Olfaction is certainly implicated in schooling coordination
for group spawning. Pheromones play a role in maturation timing, and
185
spawning synchrony by ensuring that male spawning readiness is linked to

female maturation and spawning. Observations of spawning behaviour in
the sparid (Pagrus auratus) also describe males following females prior to
and during their vertical spawning run (JM, personal observation).
However, for the more demanding expressions of schooling coordination,
the high temporal and spatial resolution characteristics of visual and
mechanosensory (lateral line and acoustic) senses are required. The sensory basis of schooling behaviour during feeding will first be considered,
followed by the more challenging context of tight schooling coordination
in response to predator threat. Both examples provide interesting case
studies in the conflicting demands of mid-water camouflage and schooling
communication and coordination.
In most coral and temperate reef habitats, schools of plankton-feeding
fish form over reefs. The reefs provide hydrodynamic conditions that can
concentrate and transport plankton to the schools, and in some cases the
reef also provides shelter from predators of the fish. This discussion concentrates on those species such as mackerel (Trachurus? sp.) that are often
reef associated, but that depend more on schooling rather than reef shelter
for predator defence (a parallel example exists for mysids; see Flynn and
Ritz, 1999). These species also depend on the strategy of reflective camouflage to reduce their visibility to predators in open water (Denton,
1970, 1980; Johnsen and Sosik, 2003). Clearly camouflage and visual
communication are conflicting requirements; visual communication signals must to some extent undermine effective camouflage. Reflective
camouflage also only operates effectively within strict physical constraints,
including fish orientation. When the camouflage is compromised by
change in orientation, or a sudden turn, the resulting visual stimulus can
provide a basis for visual communication.
A mirror in the water column will be difficult to see, only if it is vertical
and far enough away from the surface to be in a vertically symmetrical
light field. Only under these conditions will the reflected light match the
background space light and reduce the contrast between target and space
light and hence the effective visual range of detection. The reflective camouflage of pelagic fishes operates on a similar principle (Denton, 1970,
1980). Reflective platelets in the skin and the scales of the fish are oriented
parallel to the dorso-ventral axis of the fish so that when the fish is in its
normal orientation they form an array of vertical mirrors. This reflective
camouflage works best when the fish is horizontal in the anterio-posterior
axis, with its dorsal surface pointing to the most intense downwelling light.
Deviations from this position increase the target contrast against background space light for an observer (Dare, 2008). The relevance of these
considerations for social aggregation is that the demands for effective foraging can over-ride camouflage and provide schooling conspecifics with
visual signals that convey information on feeding opportunity and success.
186
Reflective camouflage is a strategy used by many larger mobile (hence

muscular) fish, but zooplankton (including ichthyoplankton) typically
employ an alternate strategy based on transparency. Transparent prey are by
definition hard to see; however, sighting of transparent prey can be
improved by viewing them just beyond angles in Snells window (Janssen,
1981). Snells window is a phenomenon by which an underwater viewer
sees everything above the surface through a cone of light of width of about
96" . This phenomenon is caused by refraction of light entering water and
is governed by Snells law. The area outside Snells window will either be
completely dark or will show a reflection of underwater objects (Janssen,
1981). Tilting up by approximately 40" to achieve this forward sighting
line improves feeding success, but necessarily increases the predator fish
contrast against the background and hence visibility to conspecifics and
predators. Moreover, the slight flaring of the gills and opening of the
mouth associated with suction feeding also provides a clear visual signal, or
light flash, to other school members conveying feeding success. In essence,
by attending to visual contrast and flashes, members of a school can gain
information on which parts of the school are feeding and how successfully.
It is debatable as to whether this represents a signal in the sense of being
purposely sent, but if one was looking for a benefit to the sender, the shift
of the school towards favourable feeding areas may provide some safety in
numbers advantage for them. Finally, from a sensory perspective this
behaviour is almost exclusively visually mediated. The polarization of the
school facing into the current (positive rheotaxis) would likely be visually
mediated, though maybe with a lateral line component (Montgomery
et al., 1997), but the dynamics of schooling coordination in relation to targeting food patches would be exclusively mediated by visual signals. By
contrast, the tight coordination of schools under predation threat requires
more complex multimodal sensory communication.
Under the threat of predation, observations and studies of complex
schooling behaviour (Pitcher, 1993; Pitcher and Parrish, 1993) tend to
evoke descriptions of the school as a super organism. Discrete behaviours of the school are observable such as splits, vacuoles and flash
expansion. The sensory basis of these school behaviours is extremely
hard to study, but is almost certainly due to the sensory detection of an
attack by the fish on the front line via the visual looming stimulus of the
predator, and/or the associated pressure pulse of a lunging strike. The
behaviour of the school will result from the way in which this information propagates into the school, both directly, and as a result of the avoidance response of the front line fish. Thus, communication between
neighbours is likely central to the schooling response to attack, but it is
also key to understanding the schooling coordination under the threat of
predation. For this latter case, there is good experimental evidence and
theoretical reasoning to support the active involvement of both vision and
187
the octavolateralis sensory systems (lateral line and hearing) (Partridge and
Pitcher, 1980; Gray and Denton, 1991; Montgomery et al., 1995;
Faucher et al., 2010).
The main sensory requirements for coordination relate to initiating and
maintaining the close association of individuals, combined with highly effective collision avoidance. We know rather little about the sensory mechanisms
underpinning initiation of tight schooling formations. The perception of
threat by individual members of the school and the communication of that
threat may simply be a function of an abrupt change in direction of those fish
aware of the threat and a reduction in NND in that part of the group. An
abrupt change in behaviour in one part of the school could propagate
through the school visually, but it is also feasible that acoustic communication
is involved. This could be both passive on the part of the signaller, resulting
simply from the abrupt turn or acceleration (Gray and Denton, 1991;
Denton and Gray, 1993), but could also include active acoustic communication. Some schooling fish such as mackerel and tuna produce sound through
stridulation of the gill rakers; however, the behavioural context of this sound
production is not known (Allen and Demer, 2003). Once initiated, the
maintenance of close NND is mediated by both visual and lateral line stimuli.
Partridge and Pitcher (1980) have shown that blinded fish can still swim in
formation and Faucher et al. (2010) have shown that in some fish the lateral
line may be necessary for tightly coordinated schooling behaviour. Liao
(2007) also provides an excellent discussion of the theoretical rationale for a
hydrodynamic basis to school structure. The prediction is that a fish located
behind and in between two preceding members of the school can take
advantage of the average reduced velocity associated with the thrust wakes of
those ahead. In effect, fish in schools can benefit from flow refuging (exploiting regions of reduced flow) and vortex capture (harnessing the energy of
environmental vortices). Direct experimental determination of vortex capture, associated energetic benefits and its sensory basis have not been done for
schooling fish. However, individual fish swimming in a flume have been
shown to use lateral line information to position themselves in an energetically favourable position behind a cylinder (Montgomery et al., 2003), and to
entrain to shed vortices from a bluff object in the flow (Liao et al., 2003a,b).
Figure 4.6 reproduced from Liao et al.s paper illustrates this.
Visual communication in schooling has been extensively studied by
Rowe and Denton (1997) and Denton and Rowe (1994, 1998). Their analysis is that the same substrate of reflective surfaces that provides for midwater camouflage, supplemented by additional reflective and non-reflective
surfaces (such as the double yellow reflective dots on the tail: see Fig. 4.9),
can provide strong communication signals to nearest neighbours.
Additional reflective and non-reflective surfaces include highly silvered
patches on the tail, the dorsal lateral line which is a non-sensory reflective
open canal (Rowe and Denton, 1997) and the bands of reflection that
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Figure 4.8 School of Trachurus novaezelandiae showing double yellow reflective dots on
tail. Photo by John Montgomery.
can mask underlying black stripes (Denton and Rowe, 1998). The combination of light reflection and colour changes can provide large changes
in appearance for relatively small changes in roll, pitch and yaw. These
changes could in theory signal a fishs movement and/or position relative
to its neighbours. These visual communication signals are thought to
combine with hydrodynamic and acoustic stimuli to provide for the
impressive collision avoidance capability of schooling fish.
Crustacean species such as Antarctic krill (Euphausia superba) and mysids
also undertake coordinated swimming in formation (OBrien, 1988; Patria
and Wiese, 2004; Kawaguchi et al., 2010). Wiese (1996) has reviewed the
available information on the role of vision and mechanoreception in the
control of schooling in krill. He concludes that the evidence strongly supports a mechanosensory basis for control of this behaviour. Even though
blinded krill were unable to school (Strand and Hamner, 1990), this seems
to be simply a result of the inability to orient the body to a fixed vertical
axis in space i.e. to the axis of light from the surface. In contrast, fish can
continue to school with loss of either vision or lateral line but not when
deprived of both (Partridge and Pitcher, 1980). Yen et al. (2003) and Patria
and Wiese (2004) have also described the vortex wake behind a tethered
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Figure 4.9 (A) Communities and subcommunities in a dolphin social network. Vertices
shaded in black are all part of one community, while all other vertices are part of the second community. The second community is subdivided into three subcommunities represented by white, light grey and dark grey shading. (B) Social network of a population of
guppies. All guppies from two interconnected pools were collected, marked and released.
Over the next 2 weeks approximately 20 shoals were captured daily and fish that belonged
to the same shoal were connected in the network. (A) After Lusseau and Newman (2004);
(B) after Couzin et al. (2006).
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krill and the latter authors demonstrated the ability of antennular sensors to
detect these oscillations at normal schooling distances and entrain a synchronous pleopod beat in a following animal. From these and other studies
(e.g. Wiese and Ebina, 1995), it appears that the vortex wake generated by
swimming krill could be used by followers both as a source of information,
both hydromechanical and chemical, about the neighbour ahead, and also
as a means of reducing their energy expenditure.
Acoustic signals travel much better than visual ones in the ocean, so it
is not surprising that highly mobile marine mammals have exploited this
communication channel for social purposes (Tyack, 2000). Social communication within and between groups of delphinid cetaceans includes
not only vision and tactile stimulation, but also sound production in the
form of narrow-band, frequency-modulated signals (whistles) (Dudzinski
et al., 2002). These types of signals are relatively easily localized, with
directional characteristics which, together with their variability and
power, make them particularly suited to contact calls, the pod-specific
dialects of resident Orcas or the signature whistle of bottlenose dolphins
(Tyack, 2000). Echolocation by clicks, on the other hand, is thought to
be used more for foraging and navigation (Dudzinski et al., 2002).
Communication among groups of Spinner dolphins, which feed mainly
at night, may differ from this general pattern. Apparently these dolphins
do not use whistles while hunting for prey (Benoit-Bird and Whitlow,
2009). Instead they used a series of clicks with the highest click rates just
prior to foraging. The authors suggested that this may be a strategy to
limit communication only within the group and to avoid betraying the
location of rich food resources to other predators (e.g. tuna) which can
also hear whistles but not clicks.
2.6. Social networks

Recent application of social networks analysis to the study of animal behaviour and ecology has allowed novel and intriguing insights into populations
of aggregating animals (Croft et al., 2008). As Croft et al. (2005) note
Social network theory can help bridge the gap between interactions at the
local and global level and provides a framework for the study of sociality.
In a social network analysis a graph is often used to describe the interactions
between individuals. These individuals are represented as nodes in the
graph, and the lines joining them represent social ties. Most nodes are connected by at least one short path, and nodes in the network with a high
number of connections are known as hubs. One class of social network, the
so-called small-world network, is characterized by a comparatively short
average path length between nodes and a large number of hubs or cliques
of interacting individuals. These qualities are important in facilitating the
spread of such things as information, genes or even disease across
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population. Such small-world networks (Watts and Strogatz, 1998) exist

within large fish aggregations (Croft et al., 2005; Couzin et al., 2007), birds
(Ballerini et al., 2008) and in dolphin pods (Lusseau, 2003; Lusseau and
Newman, 2004) (Fig. 4.9). The implications of these small-world networks,
in information transfer and speed of spreading of disease, are now starting
to be seriously studied at a range of levels of biological organization, from
the individual to the population, in marine mammals.
Arguably the main strength of this method is to examine how individual
interactions scale to structure population-level processes, which allows us to
examine self-organization, and potentially the transmission of genes, information and disease (Watts and Strogatz, 1998; Latora and Marchiori, 2001;
Cross et al., 2004). In the context of the present review, social network analysis allows us to dissect aggregations to look at the structures within, particularly how the constituents of an aggregation interact with one another.
Many of the aggregations discussed here are examples of fission!fusion
groups (Couzin et al., 2006) where, as the name suggests, aggregations split
into smaller groups at certain times before later coalescing into larger aggregations once more (Pearson, 2009). Aggregations, therefore, are very often
made up of a mosaic of smaller functional subgroups, a phenomenon that
may be elucidated using social network analysis. For example, a study of
social networks in bottlenose dolphins (Tursiops truncatus) reported that the
population of these animals off the east coast of Scotland was composed of
two largely separate social units (Wiszniewski et al., 2009).
Indeed, most of the work carried out on social networks in the marine
environment has focused on pinnipeds (Wolf et al., 2007) and cetaceans
(Slooten et al., 1993; Chilvers and Corkeron, 2002; Ottensmeyer and
Whitehead, 2003; Lusseau, 2003). This may be easier in these species as
the individuals are large, and can be recognized via photo studies. Such
work has greatly extended our knowledge of the function of cetacean
social groups in particular. For example, a study by Lusseau and Newman
(2004) identified different sex and age-structured social patterns in a New
Zealand dolphin population, and perhaps most interestingly, reported the
existence of key individuals (brokers) within the population that linked
separate subgroups (Fig. 4.9A). Such findings are important not only for
our understanding of the social dynamics of these animals, but behavioural studies of association patterns and social networks in these animals offer
insights that may be used to inform key management and conservation
decisions in marine animals (Williams and Lusseau, 2006; Higham et al.,
2009; Williams et al., 2009). In the coming years, it is hoped that social
network analysis will enable us to gain greater understanding of the social
dynamics of a broader range of marine animals.
Complex biological structures such as social groups consistently show
attributes of networks that have non-random systems of connectivity.
Several authors point to the fact that emergent properties are common to
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groups of simple, identical units even non-biological ones, e.g. molecules

and spin magnets, and caution that appearance of pattern may not necessarily signify adaptive behaviour (Parrish and Edelstein-Keshet, 1999:
Parrish et al., 2002). Others stress that an acceptance of social groups as
networks is an important preliminary to an understanding of fitness of
individuals and groups (Fewell, 2003). Wilson and Dugatkin (1997) show
that assortative interactions within or among groups can create conditions
of highly non-random variation providing material for group selection.
The idea of group selection was an unthinkable and heretical concept
until just a few decades ago (Wilson and Dugatkin, 1997). A more modern view is that selection operates on a nested hierarchy of units (see
Wilson and Sober, 1994, for a review of this concept). As noted in
Section 1, group selection implies that the fittest groups contribute not
more groups to the next generation, but more individuals which are themselves predisposed to form successful groups.
3. Technology Breakthroughs in Experimental

and Observational Methods
Aggregative behaviour is of profound importance to both the ecology
and economical exploitation of the pelagic environment, but the remoteness and opacity of the environment has limited the observations that
can inform behavioural understanding. With regard to exploitation these
limitations may have, in fact, prevented the complete over-exploitation of
important commercial fish species such as tuna (Sibert et al., 2006), and
near elimination of other species such as great whales (Clapham and Baker,
2003; Roman and Palumbi, 2003). However, technology currently available considerably improves our observational abilities, so due caution to
avoid continued non-sustainable exploitation needs to be considered. In
the following subsections we review insights on social aggregation that
have been generated using modern technology including (i) video and
motion analysis software, (ii) optical plankton counters, (iii) acoustics and
(iv) electronic tagging.
3.1. Video and motion analysis software

3.1.1. Historical use
In earlier sections we argue that aggregative behaviour is of profound
importance to the ecology and economy of the pelagic environment.
Aquatic animals aggregate for a variety of reasons including reproduction,
defence against predators, food finding and energy savings (Ritz 1994,
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2000). Classically, research has focused on the attributes of a group as a

whole, with little consideration given to individuals within the group.
Recent studies highlight the fact that it is the behaviour of individuals
that collectively determine the behavioural trajectory of the aggregation.
Detailed analysis of behaviour of individuals and small groups can thus
illuminate the behaviour of the much less tractable larger aggregations
(Parrish and Edelstein-Keshet, 1999; Banas et al., 2004). Within any
aggregation relative positions of individual members are not static, but
usually change constantly, moving from the centre to the edge and back
again (Hamner and Parrish, 1997). Until recently studying individuals
within the context of the entire swarm or school was difficult, particularly
for small planktonic animals, and researchers generally concentrated either
on analysing behaviour in the two-dimensional plane or examining
swarming/schooling individuals under artificial, laboratory conditions.
The common first step in studies of social behaviour in aggregations
is to capture images of the aggregation. Video and motion analytical
tools were first tested in the laboratory, with isolated individuals in
controlled situations. Behaviour of pelagic crustaceans has been recorded
in three dimensions using a variety of photographic and video methods
to examine mating (Doall, 1998; Strickler, 1998), escape responses
(Buskey et al., 2002) and attack volume (Doall et al., 2002). However,
these were usually measured in detail under laboratory conditions where
small groups or individuals were isolated from the rest of the aggregation often in a small volume of water. Group attributes in the form of
NNDs, bearings and angles of elevation have been measured using still
photographs (OBrien et al., 1986), but these methods provided only
approximations of parameters such as velocity. Obtaining threedimensional trajectories of specific individuals for extended periods was
also difficult, with data typically generated under highly artificial conditions (Parrish et al., 2002).
In the past, most analysis of objects in three-dimensional space
(photogrammetry) employed film cameras because only these cameras
could provide sufficiently high image quality and geometric reliability.
However, digital still cameras and digital video cameras now offer image
resolution approaching that of film and, more importantly, provide an
imaging geometry that is sufficiently stable for photogrammetric purposes. Modern digital video cameras offer the possibility of capturing
stereo-video and obtaining accurate three-dimensional measurements of
moving targets (Osborn, 1997). These early studies also tracked a limited number of individuals, with individuals identified by eye in sequential images. Thus, while a focus has been on the spatial and temporal
description of aggregations, these early studies have also shown that
energetic benefits to individuals in aggregations often cannot be inferred
from analysis of isolated individuals.
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3.1.2. Technological developments in video and image analysis

Increased computing power, digital storage capability and modern digital
cameras have allowed an order of magnitude increase in analytical power
and offer new insights into the spatial and temporal mechanistics of
aggregation. A selection of technological aids used in studying zooplankton aggregations was provided by Folt and Burns (1999). Here we update
this list and focus on technology that is particularly applicable to, or was
developed for the purpose of, recording social aggregative behaviour.
A second challenge has been to develop technology to allow observations of aggregations at sea. Kils (1992) described a small, free-drifting
system for recording in situ predator!prey interactions between juvenile
herring schools and copepod swarms. One particular objective of the
study was to determine how herring schools search and encounter prey
under the reduced visibility conditions in the Baltic caused inter alia by
recent enhancement of phytoplankton blooms. The hardware, known as
ecoSCOPE, consists of two optical endoscopes mounted on a remotely
operated vehicle. Microlayers containing the herring schools are located
from 40 m away using a scanning sonar also mounted on the ROV.
Images of the predators are collected by one charge coupled device array
and prey by a second one. The field system is accompanied by a software
package dynIMAGE that allows the user to process images in a way that
compensates for system swaying caused by microturbulence. Using this
system, Kils (1992) was able to provide one of the first recordings of fish
schools capturing prey in the field, describing copepod captures at a rate
of 2.4 s 21 by herring feeding within layers containing high (up to
850 l 21) concentrations of copepods.
Recent advances in digital video and its miniaturization and low cost
have resulted in a range of new equipment for in situ and laboratory observations. Kawaguchi et al. (2010) present a method that combines footage
captured with dual digital stereo-video cameras with a commercially available motion analysis system, WinAnalyse (Intec), which enables sophisticated studies of the movement of aquatic animals, including the analysis of
complex interactions among individuals in an aggregation. An introduction
to the basic stereophotogrammetry, including specifics on calibration and
precision of the hardware and software, is provided. They demonstrate the
capability of this equipment by describing qualitative behaviour of laboratory schools of Antarctic krill and testing hypotheses about the effects of
light and food. For example, the method allows a comparison of NNDs
and swimming speeds in different regions of the swarm. Krill swam in
polarized groups and responded cohesively to objects that produced a sharp
contrast but not to those that were less distinct. Schools broke up when
they encountered dense phytoplankton patches but aggregated more tightly
when kept in a white featureless background. Viscido et al. (2004) used
similar equipment to compare behaviour of real and simulated fish schools.
195
Some parallels with krill schools are apparent, e.g. there was a clear relationship between group speed and polarity; in both cases polarized groups
swam faster than non-polarized ones.
This equipment would permit researchers to test in situ, e.g. whether
individuals at the edge of a swarm are likely to be travelling predominantly in vertical trajectories compared to those in the centre that are
hypothesized to be travelling predominantly in a more horizontal direction. This would enable those at the edges to exploit favourable currents
generated by the swimming movements of swarm members (Ritz, 2000).
A breakthrough in the three-dimensional analysis of thousands of individuals in a group was reported by Cavagna et al. (2008a,b). These authors
studied flocks of starlings and devised computerized techniques to identify
corresponding images of individuals from stereoscopic pairs of pictures taken
by cameras placed 25 m apart and about 100 m from the birds (Fig. 4.10).
This analysis yielded several important conclusions, among them:
i. Each bird interacts with a fixed number of neighbours irrespective of
their distance. In other words, the birds interacted with neighbours
according to topological distance are not metric. One of the consequences seems to be that birds under attack from predators do not lose
cohesion when the flock rapidly changes shape, density and direction.
ii. Each bird interacted with a maximum of seven neighbours. This may
represent a cognitive limit for starlings although there is some evidence that it may be a more widespread limit for other social species.
The techniques described by Cavagna et al. (2008a,b) lend themselves
to the study of aggregations of other social species with the promise of
more robust estimates of behavioural characteristics. They also report
methods for removing bias due to individuals at the borders of the aggregation. Neglect of this factor can cause erroneous conclusions especially
in small groups which, hitherto, have necessarily been the subject of
three-dimensional analysis.
A new approach in visualization of aggregations was recently introduced by Myriax Pty Ltd. (http://eonfusion.myriax.com/). It is called
Eonfusion and permits aggregations to be readily displayed in four dimensions, x, y, z coordinates and time. An example of a krill school is shown
in Fig. 4.11, and other examples can be found at http://www.youtube.
com/watch?v 5 CF8pb1a9gvA&feature 5 player_embedded.
Recent developments include the video plankton recorder (VPR)
(Fig. 4.12) that is essentially a towed underwater video microscope that
images, identifies, counts and sizes plankton, and other particles in the
size range 100 m!5 cm (IGBP Science 5).
Some of the newest VPR platforms permit high-speed towing (10
knots) out of the wake of the ship, a moored autonomous profiler to obtain
high-resolution time series of water column plankton, and autonomous
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Figure 4.10 Upper panels are actual photos of a flock of starlings taken by a pair of stereoscopic cameras placed 25 m apart and about 100 m from the birds. Square boxes indicate corresponding birds in the two pictures. Lower panels are three-dimensional
reconstructions of the flock from four different perspectives. After Cavagna and Giardina
(2008).
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Figure 4.11 (A) Visualization of a school of Antarctic krill (Euphausia superba) using
Eonfusion. The positions (x,y,z) were used to derive metrics, e.g. swimming speed, direction, acceleration and nearest neighbour data. These were used to explore behaviour of
individuals over time. (B) Krill connected to their nearest neighbour (for distances
,50 mm). Reproduced with permission from Eonfusion: Tim Pauly; Australian Antarctic
Division: Rob King, So Kawaguchi; University of Tasmania: Jon Osborn; Georgia Tech: David
Murphy, Jeanette Yen, Donald Webster.
underwater vehicles to provide remote spatial sampling of plankton and

environmental variables (IGBP Science, 2003). Together these image capture systems offer a wide range of potential approaches to gather the primary data on aggregations.
3.2. Optical plankton counters and holography

Since its first appearance in 1992 (Checkley et al., 1997), use of the optical plankton counter has increased exponentially to provide quantitative
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Figure 4.12 The housing for a VPR, with a very streamlined shape, sits ready for deployment off the back of a research vessel (Gulf of Maine Area Program ! GoMA). . http://
www.coml.org/investigating/observing/vprs.
measurements of abundance and sizes of meso-zooplankton. In addition

it has evolved to become an important piece of equipment in multidisciplinary studies for acquiring and displaying data from a range of sensors
(Cass-Calay, 2003). Spatial and temporal zooplankton distributions can be
recorded by instruments mounted on a range of underwater towed frames
(Zhou and Tande, 2002). At present, however, OPCs have limited value
in the study of social aggregations because of issues of avoidance, coincidences in measurements, image resolution and depth of field.
A submersible holographic system has been used to visualize the
instantaneous in situ three-dimensional distribution of copepods and particles .10 m in a 1 l volume (Fig. 4.13; Malkiel et al., 1999). Results
show clear evidence of clustering at almost all depths sampled. One great
advantage of holographic imaging systems over other optical systems is
their ability to resolve small particles, e.g. plankters over a much larger
sample volume. The authors give as an example the comparison between
a planar imaging system that can resolve a 20 m object with a depth of
field of 0.6 mm at a given wavelength, whereas a holographic system
under similar conditions would resolve the same object with a depth of
field over 100 times larger. This potentially makes holography a valuable
tool for in situ studies of pelagic aggregations.
3.3. Acoustic technology

Traditional acoustics involves the detection of sound waves reflected
from a target (active) or emitted from a target imbedded with an acoustic
Sam
pling
or
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volum
irr
o
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Exp
an
len ding
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ses
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Figure 4.13 Holocamera: optical setup of in-line holography. Redrawn from Malkiel
et al. (1999).
transmitter. Detection of natural sound from a target (passive acoustics)

has also shown promise for detection of large objects, and we discuss it
briefly with regard to pelagic species in a following subsection.
Verifying the species or individual represented by the acoustic signal
has been a primary challenge and as a result there have been several
attempts to combine optical and acoustic sensors for the purpose of identifying and quantifying zooplankton in situ. For example, Jaffe et al.
(1998) introduced the optical!acoustical submersible imaging system in
which a digital still camera was mounted on their FISH-TV sonar array.
The camera is triggered to capture an image within the sonar beams
when the target strength exceeds 290 dB. Using this equipment, the
authors reported imaging 375,000 individual zooplankters, many as small
as 1 mm (Genin et al., 2005). In a variation on a theme, Warren et al.
(2001) used an analogue video camera to aim their acoustic array,
mounted on an ROV, at individual zooplankters, i.e. siphonophores,
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euphausiids or other taxa. These images of individuals can then be used

as for conventional optics to derive measures of in situ school parameters
related to social aggregation such as NND.
Traditional acoustics have been limited to resolving pelagic
zooplankton and fish at distances of 10s to 100s of metres from the vessel. A further limitation is that single-beam downward-looking echosounders sample only a narrow cone of water beneath the vessel (Cox
et al., 2009). Thus they may undersample activity just outside this cone,
e.g. predators interacting with target schools. Increasingly, multibeam
echosounders (MBEs) have been used that not only broaden the
width of the swath sampled but also enable direct observation of
volume and surface area of aggregations leading to more accurate threedimensional estimates of individuals (Cox et al., 2009). This equipment
is well suited to resolving pelagic aggregations in situ, and has been used
to analyse three-dimensional structure of anchovy and sardine schools
(Gerlotto and Paramo, 2003; Gerlotto et al., 2004), and also to study
predator!prey interactions between Atlantic puffins and herring
(Axelsen et al., 2001). Cox et al. (2009) used an MBE to study interactions between swarms of Antarctic krill and penguins and fur seals.
Kaartvedt et al. (2009) showed that detailed in situ behaviour of individual mesopelagic fish could be resolved by multibeam acoustics deployed
from a stationary vessel (Fig. 4.14). This study revealed a variety of
DVM behaviour amongst myctophid fish including normal, reverse
migration and non-migration of some individuals. Techniques using
submerged echosounders offer exciting prospects for studying deep-living aggregations non-intrusively, assuming that the target species are not
themselves responding to the echoes.
The GLOBECs Southern Ocean programme employs a Bio-Optical
Multi-frequency Acoustical and Physical Environmental Recorder
(BIOMAPER-II) to map abundance and distribution of Antarctic phytoplankton, zooplankton and especially krill (Wiebe et al., 2002).
BIOMAPER can record data from 500 m or more of the water column at
a time. It is towed at speeds up to 10 knots and data are fed continuously
to the surface via conducting cable. The instrument uses a five-frequency
sonar system, a VPR and an environmental sensor system that measures
water temperature, salinity, oxygen, chlorophyll and light levels.
The most astounding breakthrough in recent years is that of continental shelf-scale imaging (Makris et al., 2006), that has revealed huge
fish shoals covering many square kilometres and containing tens of millions of fish. An example of the trace from the ocean acoustic waveguide
remote sensing (OAWRS) system is shown in Fig. 4.15. This technique
relies on the continental shelf environment acting as an acoustic waveguide, making it possible to survey areas roughly one million times
greater than conventional fish-finding methods. The technology utilizes
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Figure 4.14 (A) Echo traces of individual mesopelagic fish. Graduated scale at right of
picture refers to backscattering strength (dB). (B) Example of three-dimensional movement and swimming speed of a target ascribed to Benthosema glaciale (framed in A) at
380 m depth. Graduated scale at right of picture refers to swimming speed (m s 21).
Reprinted with permission from Kaartvedt et al. (2009).
a moored acoustic source and a towed receiving array. Sound propagates

over long ranges via trapped modes that suffer only cylindrical spreading
loss rather than spherical loss suffered by more conventional sonar. Using
this technique, unprecedented imaging of fish shoals is possible providing
details of behaviour such as school formation, fragmentation and movement. Once species can be discriminated, this technology offers exciting
potential to look at the interaction between schools as a basic unit of
analysis, perhaps using the density within a school as a measure of behavioral response.
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(A)
(B)
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Figure 4.15 (A!D) Comparison of OAWRS with conventional fish-finding sonar (CFFS).
A sequence of areal density (fish m 22) images taken roughly 10 min apart is shown. The corresponding CFFS is overlain in light blue (see colour plate). CFFS position for the given
OAWRS image is indicated by a circle. (E) Range-depth profile of fish volumetric density
(fish m 23) measured along the transect in (A!D). After Makris et al. (2006).
Traditional optical visualization is compromised by poor visibility,

which acoustics can also overcome, although acoustic methods can also
be compromised when the water contains many particles. A promising
new instrument for use in turbid water is the acoustic camera
(DIDSONt ! Dual Frequency Identification Sonar, i.e. either 1.8 and
1.1 MHz or 0.70 and 1.2 MHz) that has been used to count and identify
fish, and to reveal schooling behaviour of salmon in hatchery ponds
(Belcher et al., 2002). Depending on the frequencies, it can image objects
from 1 out to 80 m range. The near video quality of the image allows
observation of fish behaviour in turbid water and at night near natural
and manmade structures. Furthermore, the equipment can be used close
to the banks of rivers or streams where deployment of other acoustic
instruments is problematic. Since the sonar beam is emitted perpendicular
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to the flow, fish can be counted and sized as they pass through the field of
view. DIDSONt is small and portable requiring only 30 W of power.
3.4. Electronic tags

Both visual and acoustic in situ observations of pelagic social aggregation
typically require the presence of the scientist or attending vessel. For
larger pelagic species, an alternative is to implant or attach data recorders
that can transmit data or be recovered at a later time. The primary goal of
most electronic tagging studies has been to understand the movements of
individual animals, which with sufficient sample size are assumed to be
representative of the population (Hobday et al., 2009). The study of individual behaviour has been a focus, aggregation behavior less often, and
social behavior rarely. Three types of tag are in common use: archival
tags, satellite transmitting tags and acoustic tags, all of which could provide information on social behaviors in aggregations.
Archival tags are usually internally implanted in an individual, and collect a variety of data (depth/pressure, internal/external temperature,
light), while the animal is at liberty (Gunn and Block, 2001). Following
recovery of the animal, data can be processed to determine daily position
(Welch and Eveson, 1999; Teo et al., 2004). Errors in calculated position
can still be in the order of hundreds of kilometers which has prevented
insights into group behaviors (Nielsen et al., 2009). Depth resolution is
more accurate, and so simultaneous movements in depth of tagged animals could be used to determine coherence in group behaviors.
A modification of the basic archival tag has been a range of satellite
archival tags which are externally attached and transmit data continuously
(e.g. SPLASH, SPOT; Weng et al., 2005) or detach from the animal after
a period of time and transmit summarized data to satellites (PSAT; Block
et al., 2001; Patterson et al., 2008). Position estimates are similarly coarse,
and these tags have been of little use for studies of social aggregation.
However, both types of archival tag have been widely used on a range of
pelagic species with social aggregations, including fishes, sharks, marine
mammals and birds, and even a few large invertebrates (Nomuru jellyfish)
and squid (Gilly et al., 2006), and so potential remains to use these tags
within their technological constraints to achieve breakthroughs in documenting social behaviors.
Acoustic tags transmit while attached to the animal, which can be
actively tracked by an attending researcher (Block et al., 1997; Davis and
Stanley 2002) or monitored using fixed acoustic receivers (Heupel et al.,
2006; Hobday et al., 2009). Advantages of using fixed receivers include the
increased time over which multiple individuals can be simultaneously monitored subsequent to the tagging event. Thus, there is increased likelihood of
detecting natural behaviors and recurrent grouping of individuals. The
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resolution of the position estimates (tens to hundreds of metres) also allows

greater certainty that individuals are clustering (Klimley and Holloway,
1999).
Aggregations of pelagic fishes are common, either with each other,
with floating objects, or with topographic features such as seamounts
(Holland et al., 2009). This behaviour is increasingly being exploited by
fishermen who each year release thousands of floating FADs throughout
the oceans (Hallier and Gaertner, 2008). These devices typically attract
tunas, but also a range of other species including sharks, billfish and sea
turtles (Dagorn and Freon, 1999; Gaertner et al., 2002; Hallier and
Gaertner, 2008). Ongoing research is aimed at a greater understanding of
the relationship between aggregation/association of fish at FADs and the
potential impact of fisheries (Hallier and Gaertner, 2008). Evolution of
electronic tags for this purpose has been rapid and there are plans to test
the feasibility of using acoustic data to determine whether the fish are,
indeed, schooling, or if they are responding to the floating structure
(Taquet et al., 2007; Soria et al., 2009).
Another recently developed device, the CHAT (Communicating
History Acoustic Transmitter) or Business Card tag, has the potential to
exchange data between fish and then remotely transfer archived data from
the fish to listening stations deployed on the seabed or on buoys (Holland
et al., 2009). Whether or not data on schooling behaviour could be logged
would depend on successful design of suitable sensors, but would be an
important innovation in monitoring aggregations at sea, as well as contributing vital information to ecologists and fisheries scientists (Holland and
Dagorn, 2009).
While most electronic tagging studies have a single-species focus,
Goni et al. (2009) acoustically tracked juvenile albacore in the Bay of
Biscay and simultaneously collected prey distribution data from echosounders. Although tuna depth distribution did not relate to prey distribution,
the combination of these technologies is suitable for developing fine-scale
understanding of tuna schooling and foraging behavior, and may yield
interesting results in future.
3.5. Future technology challenges

Traditional technologies based on visualization have provided most of the
insights regarding pelagic social aggregations to date, with increases in
usage of acoustic technology providing recent breakthroughs for a range
of species. The challenge for understanding pelagic social behavior is
developing systems that can be used in the open sea, often remote from
the observing researcher. Use of electronic tags is likely to be restricted to
the larger species for the foreseeable future, and so information on the
smaller taxa is likely to come from combining technologies, such as
205
camera systems with traditional acoustics. The resolution of the data in

time is sufficient in existing technologies, with millisecond reporting
commonplace. Spatial resolution can be considerably improved, and while
geolocation may have inherent limitations (Welch and Eveson, 1999;
Nielsen et al., 2009), alternative technologies that allow tags to communicate will overcome the uncertainty in individual position estimates, by
confirming co-location.
With regard to tags, a number of companies are supplying technology,
yet these are generally incompatible. Given the scale of the pelagic ocean,
and the infrequent encounters between independently tagged animals,
opportunities are likely to be missed if tags cannot communicate.
Commercial considerations are important and likely prevent complete
compatibility between technologies; however, a middle ground may to
use a common signal for chat between tags and maintain individual coding for the primary data collection (Grothues, 2009).
4. Theoretical Developments in Social

Aggregation
A key purpose of modelling is to distinguish behavioural cause from organizational
effect by studying the consequences of various hypothetical social interaction rules
Parrish et al. (2002)
We do not propose to give a comprehensive review of theoretical

modelling of aggregations here. Instead we will describe the kinds of
models that have been applied to the problem to date, outline the results
obtained and identify areas and directions where further work is warranted. Levin (1997) discussed conceptual issues posed by modelling
aggregations, particularly in relation to scale, and Parrish et al. (2002) provided a recent review of theoretical modelling approaches particularly as
they relate to fish schools. The current state of modelling animal aggregations and its relation to empirical data has been described with great clarity by Giardina (2008). In general, three major frameworks have been
used to model animal aggregations (Parrish and Edelstein-Keshet, 1999).
These three types differ in (i) spatial and temporal scale of the analysis, (ii)
the kind of information individuals use to aggregate and (iii) the mathematical complexity (Giardina, 2008).
First, individual-based models (IBMs or Lagrangian) are based on
individual trajectories with attributes such as location, genotype, phenotype,
physiological and behavioural status, and allow rule-based responses
to environmental data in order to explore the dynamics that lead to formation of groups. For example, fish joining a school would assume a particular
206
angular position with respect to another individual and a particular

direction that could be modified by the environment (e.g. current strength)
(Adioui et al., 2003). The individual unit could be an individual fish, or a
school of fishes. An aggregation has been shown to result when individuals
follow three simple rules: move in the same direction as neighbours, remain
close to them and avoid collisions (Giardina, 2008).
Second, Eulerian models deal with populations as the base unit. They
typically consider each unit at a geographically fixed location instead of
simulating each individual and, in the case of a school, predict emergent
group properties such as population density. Space is not georeferenced
and the number of individuals inside each cell is followed in time.
Environmental drivers can also be applied to each unit, which responds
according to a set of dynamical equations. This type of model is mostly
applied when investigating population evolution on long time scales or
over large spatial scales, and has made a strong contribution to fisheries
science.
A third approach relies on discrete simulations using a range of individual behavioural rules and motion (an example is the use of cellular
automata). This method, it is argued, gives a clear, visual prediction of
how individual behaviour contributes to that of the group. Rules that do
not lead to group formation can be modified or rejected, allowing some
form of hypothesis testing. Automatic selection of the rules based on
reproductive fitness occurs in models using genetic algorithms which
have been used to explore schooling behaviour (Giske et al., 1998).
Lagrangian and Eulerian concepts have been combined (Adioui et al.,
2003) and further refined to better forecast three-dimensional movement
patterns of individual salmon in the ELAM (Eulerian!Lagrangian!Agent
method) (Goodwin et al., 2006). These studies have shown that the
ELAM framework is well suited to describing large-scale patterns in
hydrodynamics and water quality at the same time as much smaller scales
at which individual fish make movement decisions. This ability to simultaneously handle dynamics at multiple scales allows ELAM models to realistically represent fish movements within aquatic systems. This method
seems to hold promise for future ecological modelling of fish schools.
An Eulerian approach has been used to model the effects of environmental conditions, krill fishery and natural predation on Antarctic krill
growth, distribution, vertical migration, feeding, etc. (Alonzo and
Mangel, 2001; Alonzo et al., 2003). These authors used a dynamic statevariable model to predict the effect of changes in predation risk on
behaviour and spatial distribution of Antarctic krill. However, these models did not incorporate the influence of schooling behaviour, which could
be a key factor affecting krill population abundance (Willis, 2007a). The
problem has been that, it has been impossible to reproduce schooling
behaviour of Antarctic krill in laboratory conditions and thus gather
207
reliable empirical data with which to paramaterize models. Recently,

however, routine generation of schooling behaviour in krill in aquarium
tanks has been achieved (Kawaguchi et al., 2010) which may allow progress in population modelling. Research on other social aquatic species
suggests that individual behaviour is so closely tied to that of the aggregation that data extrapolated from individuals isolated from their schools
will be misleading. A good example is metabolism, where it has been
demonstrated that individuals in aggregations consume far less energy per
unit mass than isolated individuals (Ritz, 2000; Ritz et al., 2001).
IBMs and computer-generated artificial life creatures (e.g. boids and
later offshoots such as efloys) have been successful in reproducing the selforganizing characteristics of aggregations of flocking birds and marine
species, particularly fishes. But are these emergent properties of the group
functionally important? Parrish and Edelstein-Keshet (1999) caution that,
although simple rules can generate lifelike behaviour, there is no guarantee that living systems follow simple rules. More experimental data gained
by tracking individuals in small groups is needed (Parrish and EdelsteinKeshet, 1999). In fact, one clear conclusion from this overview is that the
feedback between empirical observations and modelling, that is so important to scientific progress, has been seriously hampered by lack of data on
the former (Giardina, 2008).
The theoretical study of animal aggregations has a long history, but
attempts to characterize the relationships between individual-level behaviour
and group-level patterns have been hampered by lack of a common framework to schooling models (Parrish et al., 2002). They argue in favour of a
distinction between group- and population-level characteristics that are
inevitable consequences when many identical particles become aggregated
in space (epiphenomena or pattern), and true emergent properties, that
benefit members because of their membership of the group. Viscido et al.
(2007) continued this theme by analysing the factors contributing to fish
school formation and maintenance. In a simulation study they found that
several, mostly social, factors were important in giving rise to emergent
properties: notably a repulsion factor is necessary to prevent collisions, a
neutral zone must exist in which there is neither attraction nor repulsion, a
modest alignment impulse strong enough to induce polarity is necessary,
number and weighting of influential neighbours is critically important, as is
speed of motion. A topological response to neighbours, i.e. focal individual
interacting with a fixed number of neighbours irrespective of distance, has
also been shown in simulations of starling flocks (Ballerini et al., 2008) but
only recently demonstrated empirically (see Cavagna et al., 2010) (see also
Fig. 4.10). Bode et al. (2010) suggested an alternative interpretation of the
behavioural rules governing individuals moving in aggregations that is distance based rather than topological. They hypothesize that an individual
under threat must minimize its oddity by increasing the rate at which it
208
Figure 4.16 Simplified food web of the Great Australian Bight, Australia. In this ecosystem representation, southern bluefin tuna are represented in two separate boxes, lone tuna
and tuna in schools, illustrating the different trophic relationships related to school membership. With permission from Willis (2007b).
updates its position and orientation within the group, leading to an overall
increase in synchronization and uniformity. This is a subject rich with possibilities for future study.
Ecosystem modelling, such as trophic modelling via Ecopath, has also
ignored the implications of social aggregation. However, Willis (2007b) has
recently examined ways in which to incorporate social aggregation and
behaviour into an ecosystem model of southern bluefin tuna (Thunnus maccoyii) in the Great Australian Bight (see Fig. 4.16). This simple solution,
including a schooling and non-schooling category, may be suitable for discrete behaviours, but it unlikely to succeed when a continuum of states is
possible. Given that factors such as feeding success, predator vulnerability
and reproductive capacity differs across the spectrum of solitary to aggregated individuals, inclusion of aggregation state in ecosystem models, such
as ecopath is likely to influence ecosystem understanding.
5. Social Aggregation, Climate Change and

Ocean Management
The direct impacts of climate change on species and populations
include changes in distribution, abundance, phenology and physiology.
The pelagic ocean is well buffered from some of the impacts of climate
209
change; however, some secondary processes, including aggregation, will

likely be affected. Climate impacts will also be expressed indirectly via
changes in the habitats where aggregation can occur, as well as directly on
the aggregating species. For example, changes in CO2 concentration that
change acidity of the ocean, or changes in ocean circulation that control
oxygen concentrations, may limit the waters where aggregation can
occur. Given the many instances of change in distributions of marine species (Occhipinti-Ambrogi, 2007; Last et al., 2011), species composition is
changing regionally. A change in local water temperature could change
the competitive advantages of one species over another. If one species
lived in schools and the other did not, this could have a profound influence not only on the food web but also potentially on commercial
fisheries.
While climate change has already begun to impact waters around the
world (Harley et al., 2006; Cao and Caldeira, 2008), the variation in
future predictions and the spatial and temporal resolution of predictions
make forecasting biological change difficult. The response to historical
climate variability is a window to the future, and so we first describe
some of the documented responses of aggregations to climate variability
at a range of scales. We explore the implication of these changes for
pelagic trophic linkages (e.g. changes in energy that pass from aggregations of zooplankton to fish/seals/whales).
Disruption to physiological abilities, such as smell, has been shown to
affect homing, predator and conspecific detection in larval fishes (Munday
et al., 2009). If senses important to establishing aggregations are disrupted,
then benefits to populations discussed in earlier sections will be reduced,
with possible ecosystem impacts.
One outcome of global warming is that warmer seawater will have
markedly decreased viscosity. For example, a rise in temperature from
0" C to 5" C decreases viscosity of seawater by about 15%. This could possibly lead to aggregation at a smaller size if, as Ritz (2000) suggests, currents generated by the group serve to offset the tendency to sink in
heavier than water animals, i.e. crustaceans. Antarctic krill only begin to
aggregate when they reach late furcilia stage at a length of around 10 mm
(Hamner et al., 1989). Ritz (2000) suggests that this is the size at which
the cost of resisting sinking becomes too great to remain solitary. On the
other hand, increasing acidity of oceanic waters could result in crustaceans
and molluscs (e.g. pteropods) precipitating less calcium carbonate in their
cuticles and shells and becoming less dense, which may offset the decreasing viscosity.
Polar marine ecosystems are particularly vulnerable to climate change
because of the effects that small increases in temperature can have on the
critical interfacial habitat between ice and water (Smetacek and Nicol,
2005). The atmosphere around the Antarctic Peninsula region has been
210
warming faster than any other part of the planet and a concomitant
decrease in sea ice extent and krill population has been documented
(Atkinson et al., 2004). However, the effect of climate warming in this
region could be more subtle and complex than described by these authors
given the influence of ocean/atmosphere interactions such as El Nino
Southern Oscillation (Loeb et al., 2009).
Overall, the impact of climate change on social aggregation is unknown
but may deliver ecosystem surprises. What effects might climate variability
have on social species? In the first place, warming might change species distributions, but it is not clear whether warming per se would affect aggregative behaviour directly. However, there is a range of indirect consequences
of warmer oceans. For example, it seems inconceivable that DVM would
not be affected. If DVM is traded for aggregation in certain circumstances,
could climate change push it in a particular direction?
One serious consequence of climate change for social aggregatuons
might be through an affect on seasonal migrations. Barbaro et al. (2009)
have modelled the migration of the Icelandic Capelin stock, an important
commercial resource. The most significant factor in determining the
route of migration was oceanic temperature and the way the fish schools
responded to it. In a warming ocean, the migration routes and aggregation tendency of fishes may change.
The possible effects of both predator and climate-change-induced alterations in schooling behaviour of krill need to be considered for sustainable
management. Predation risk is commonly held to be an important stimulus
for aggregation in krill (Ritz, 1994; Kaartvedt et al., 1996; Folt and Burns,
1999; De Robertis, 2002), but the urgency for aggregation can be overridden, e.g. if predation risk is low, if light levels are low enough to frustrate
visual predators or possibly if energetic considerations dictate that vertical
migration is a more economical option. The urge to aggregate with similar
individuals is very strong (Bakun and Cury, 1999), but clearly there is great
flexibility in this behaviour (Bertrand et al., 2006) and possibilities for tradeoffs are many. Willis (2007a) proposes that decimation of whales in the
Southern Ocean has led not to widely predicted large increases in krill
stocks but to a change of vertical migratory behaviour that resulted in lower
krill abundance. If the disappearance of a large proportion of the whale
population had been the direct result of climate change rather than man
induced, this would have profound implications for our strategies to prepare
for the effects of a changing climate.
A second and more immediate threat for pelagic systems comes from
commercial fisheries which are already inducing profound changes in fish
populations (Heino and Dieckmann, 2009). Since the majority of commercially important fish are those living in schools (Pauly et al., 2005),
evolutionary changes induced by fishing will also affect the food web
dynamics. Fisheries management can benefit from including information
211
on social behaviour to better manage fisheries. The basin hypothesis, that

fish stocks collapse to a core area of habitat as population declines
(MacCall, 1990), is in part due to social interactions between aggregations. Mixed-species or mixed age-class aggregations provide information
on population status. Effective closed area management is dependent on
identifying the vulnerable stages of an animals life, and social theory can
identify these stages.
Introduction of exotic species into new regions could disrupt competitive interactions and predator!prey relationships. The net result of such
introductions could be complicated by aggregative behaviour of the newcomer or the ousted competitor, making prey availability more problematic. This could extend to human fisheries activities which are highly
dependent on schooling behaviour of prey species (Quinn and Deriso,
1999; Cury et al., 2000).
6. Conclusion
6.1. Do reviews stimulate new work?
In his earlier review of social aggregation in pelagic invertebrates, Ritz
(1994) suggested that several topics deserved particular attention, including:
1. General behavioural studies regarding individuals in aggregations.
2. Determining genetic relatedness among individuals in aggregations.
3. Evaluating whether particle capture is more successful by aggregated
than by solitary individuals. This was considered to be challenging, as
rigorous assessment requires experimental reproduction of patchy food
distribution instead of the more common homogeneous distribution
used in laboratory containers.
4. Effectiveness of aggregations with regard to successful mate finding
and reproduction.
5. Experimental studies of decision-making, e.g. trade-offs between
aggregation or other behavioral choices.
Evaluating if this earlier review was successful in promoting research
in specific areas is worthwhile before suggesting additional areas for future
study, as such insight can help modify the way such suggestions can be
made. This type of analysis is rare in review papers (Roberts et al., 2006)
but in our view is a worthy consideration. Using the search tools available
in ISI (http://apps.isiknowledge.com), publication trends for these topics
were analysed. Comparing pre-1995 and post-1995 is difficult as the electronic indexing of publications was incomplete in the early period, so
here we consider the effort against the suggested areas in Ritz (1994). We
212
also do not claim a direct influence, only that these topics did receive
attention in the subsequent years, and although we concede that the
results are somewhat inconclusive, they do suggest that for some topic
areas a different approach to the one suggested by Ritz (1994) might lead
to breakthroughs. Since 1994 a total of 76 papers have been published
with a focus on pelagic invertebrates (search term: pelagic SAME invertebrates); of these 8 (11%) had a behavioural component (topic 1), four
(5%) a genetic component (topic 2), although none focused on the relationship between individuals in an aggregation, and 16 (21%) considered
feeding aspects, again few compared aggregated against solitary individuals
(topic 3). Papers focusing on reproductive advantages as a consequence of
aggregation (topic 4) and trade-offs in decision-making (topic 5) have not
received any experimental attention, according to our search approach
(but see the example described below). Thus, some of these topics are still
worthy of attention some 15 years on.
By way of example, one suggestion made by Ritz (1994) has acted as a
catalyst for further research. Ritz (1994) suggested that because schooling
behaviour sub-served predator protection and facilitated foraging and feeding, social species might find vertical migration redundant since it too serves
the same functions. Although this work was not experimental in nature, it
can be regarded as an example under topic 5 (trade-offs). Observational
research by De Robertis (2002) and De Robertis et al. (2003) suggested
that Euphausia pacifica did not form subsurface social aggregations in certain
environments, instead relying on DVM for protection from fish predators.
The fact that E. pacifica forms schools in other environments (Mauchline,
1980; Hanamura et al., 1984) highlights the flexibility of the behavioural
repertoire, and indicates that flexibility in behavior can result from environmental differences. On a related theme, Kaartvedt et al. (1996) suggested
the significance of anti-predation windows that may encourage vertical
migration of the predators (Norway Pout) at times of low visibility, e.g.
dawn and dusk, when it is less risky to chase prey (krill) closer to the surface. At other times, vertical migration is suppressed and fish remain in deeper water. If social aggregation is a cost, e.g. if schools are more likely to
attract the attention of piscivorous predators, then it might be suggested
that schooling would be abandoned while migrating vertically. This argument could be negated if the energy saved by migrating in schools is more
than offset by the increased risk of predation.
6.2. Future needs and synthesis

Benefits of aggregation in a wide range of systems are well known, and it is
no surprise that aggregation is also commonly found amongst pelagic species. There are many aspects of aggregations in the ocean still in need of
research, e.g. energy saving: larger swarms expended less energy than smaller
213
ones, which, in turn, saved more energy than un-aggregated individuals

(Ritz, 2000). The conversion of these energy savings into enhanced fitness
is assumed to follow, but empirical evidence is lacking to date.
Network analysis is a relatively new field that should lead to more
breakthroughs in future, particularly for understanding social structure
and membership persistence. Social networks have been demonstrated in
aggregations of fish, birds and mammals. There is ample scope for extending this kind of analysis to other aggregations including invertebrates.
Understanding sensory processes, and their role in forming, maintaining and dispersal of groups is an area ripe for future research. Conflicts
between sensory inputs and processes (e.g. camouflage and communication) can occur, and the decision-making processes of individuals could
be studied empirically using the latest optical or acoustic technology. Or
it might lend itself to analysis by simulation or modelling.
Technologies for the study of aggregation have progressed markedly in
recent decades, and offer insights in the future, using tools such as simultaneous acoustic imaging of individuals (Kaartvedt et al., 2009) and electronic communicating tags (Holland et al., 2009). We expect threedimensional analysis to extend to thousands of individuals within marine
aggregations to occur soon, as has been reported for terrestrial birds
(Cavagna et al., 2008a,b).
Membership of aggregations is often claimed to be an effective strategy
in successful mate finding and reproduction (topic 4 in Section 6.1). We
could find no evidence of progress since Ritz (1994) suggested that more
experimental evidence was needed. This is perhaps an area that might be
advanced through modelling studies, to examine the benefit in terms of
fitness, and help refine experimental design. Ultimately, tests on real species would be desirable.
Modelling studies (topic 5 in Section 6.1) are the basis of a suggestion
that predatory risk-induced changes in behaviour could lead to major
changes in population abundance (Alonzo and Mangel, 2001; Alonzo
et al., 2003; Willis, 2007a). Using a dynamic state-variable model, Alonzo
and Mangel (2001) predict that, in the face of extreme temperatures and/
or predation risk, Antarctic krill will shrink in size and spatial distribution
may change. In Alonzo et al. (2003) they use the same approach to try to
understand the relationship between krill fisheries and penguin foraging
success in the Antarctic. The model suggests that a change in krill behaviour is likely to cause stronger effects of the fishery on penguins than can
be explained solely by the percentage of biomass removed. This is
because, as offshore krill are depleted by fishing, the deeper location of
inshore krill near penguins, which are land based for reproduction, will
make them less accessible to diving penguins. Note, though, that the
absence of the influence of schooling behaviour in these models might
alter the predator!prey dynamics (Ritz, 2002).
214
Experimental studies of decision-making in the face of conflicting signals also seem rare in recent decades, and perhaps modelling or simulation
studies might be timely to explore such trade-offs.
Impacts of climate change on aggregations are difficult to predict
though we do not anticipate direct effects. However, there are many possibilities for indirect consequences. These include the consequence of
likely changes in water viscosity with increasing temperature; decreased
acidity with increasing dissolved CO2; and distribution changes both geographical and vertical. With unprecedented rates of environmental
change, the ability of pelagic species to adapt is questionable, and so we
expect more attention to this area in the coming years.
Aggregation in the pelagic zone is common, and likely important in
the survival and well-being of many species, including humans who, via
fisheries, rely heavily on aggregation to efficiently catch food. In fact, the
average encounter rate of non-aggregated prey would lead to starvation
in many predators (e.g. whales). With many of the worlds commercial
target species already overfished, the importance of aggregation should
not be underestimated in a functioning pelagic zone.
ACKNOWLEDGEMENTS
The encouragement of the former editor for Advances in Marine Biology, David Sims, in
seeking this review and the comments of the editorial board in focusing the scope are
appreciated. We thank all of our colleagues who allowed us to reproduce their published
and unpublished figures.
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C H A P T E R F O U R

Social Aggregation in the Pelagic

School of Zoology, University of Tasmania, Hobart, Australia

Leigh Marine Laboratory, University of Auckland, New Zealand

Advances in Marine Biology, Volume 60

2011 Elsevier Ltd

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presentation of this material, this allows repeatability in future. We performed

2. Aggregation Principles and Features in

Mass (kg) Abundance Speed

from Torres (1984).

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define social animal aggregations as those that self-organize as

Ritz (1994) presented many examples of aggregations of pelagic

Figure 4.4 Nomenclature of aggregations of Antarctic krill, Euphausia superba. 5 density;

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In the rest of this review we will concentrate on social aggregation.

2.1. Origins of sociality

2.2. Significance and benefits of social aggregation

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benefits of swarm membership by mysids were confirmed by Ritz et al.

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2.3. Structure and functions of social aggregations

provide only limited pelagic examples to illustrate the commonality with

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Table 4.2 Suggested causes of aggregation in Antarctic krill, Euphausia superba

Main causes and environmental

Inflow of the current branches

Stein and RakusaSuszczewski (1984)

Hydrodynamic forces, thermocline

Priddle et al. (1988)

Murphy et al. (1988)

Environmental phenomena and

Table 4.2 (continued )

Main causes and environmental

Reproduced with permission from Siegel and Kalinowski (1994).

cohesive groups generates favourable currents that could be exploited by

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2.4. Association patterns within aggregations

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2.5. Sensing the behaviour of neighbours

spawning synchrony by ensuring that male spawning readiness is linked to

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Reflective camouflage is a strategy used by many larger mobile (hence

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2.6. Social networks

population. Such small-world networks (Watts and Strogatz, 1998) exist

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groups of simple, identical units even non-biological ones, e.g. molecules

3. Technology Breakthroughs in Experimental

3.1. Video and motion analysis software

2000). Classically, research has focused on the attributes of a group as a

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3.1.2. Technological developments in video and image analysis

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underwater vehicles to provide remote spatial sampling of plankton and

3.2. Optical plankton counters and holography

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