Received: 10 February 2019 | Revised: 20 May 2019 | Accepted: 22 May 2019

DOI: 10.1111/faf.12384

ORIGINAL ARTICLE

Towards an ultimate explanation for mixed‐species shoaling

Kai C. Paijmans1 | David J. Booth2 | Marian Y. L. Wong1

1
Centre for Sustainable Ecosystems
Solutions, School of Earth, Atmospheric and
Life Sciences, University of Wollongong,
Wollongong, New South Wales, Australia
2 species, with differences in group compositions resulting in a range of fitness out‐
Fish Ecology Lab, University of Technology
Sydney, Sydney, New South Wales, Australia
Correspondence
Kai C. Paijmans, Centre for Sustainable
Ecosystems Solutions, School of Biological
Sciences, University of Wollongong,
Wollongong, NSW 2522, Australia.
Email: kp094@uowmail.edu.au
Funding information
Australian Government Research Training
Program
Abstract
The formation of social groups has important impacts on fitness for many animal
comes for individuals. Recent interest in mixed‐species grouping, which extends from
a large body of literature invested in understanding single‐species grouping, high‐
lights novel complexities of group formation which relate to phenotypic, behavioural
and physiological differences that naturally exist between species. Among fishes,
mixed‐species shoaling is a common form of social grouping behaviour displayed
across a range of marine and freshwater ecosystems. Research explaining mixed‐
species shoaling shows some overlap with explanations for single‐species shoaling;
however, it also demonstrates that distinct differences between species give rise to
unique cost‐benefit trade‐offs which need to be incorporated into conceptual mod‐
els of mixed‐species shoaling behaviour. Unique predation related trade‐offs may
arise from inefficiency of the confusion effect, variation in vigilance between species
and unequal species‐preferences shown by predators, whilst unique foraging‐related
trade‐offs may arise from diet partitioning, variations in foraging behaviour and dif‐
ferences in competitive abilities between species. We review the literature on fit‐
ness outcomes associated with mixed‐species shoaling and present a new theoretical
framework to explain the cost‐benefit trade‐offs for individuals within mixed‐spe‐
cies shoals. The framework incorporates both trade‐offs arising from differences
between species and those arising from group size, the former having been largely
ignored due to a focus on single‐species shoaling. Our framework is designed to in‐
form future research striving to explain mixed‐species shoaling behaviour.

KEYWORDS
fish, fitness trade‐off, group living, heterospecific, school, social groups

1 | I NTRO D U C TI O N
Social grouping behaviour is widespread across the animal kingdom,
and its fitness costs and benefits have been well studied (Alexander,
1974; Krause & Ruxton, 2002; Ward & Webster, 2016). Key benefits
of social grouping include reduced predation risk (due to collective
vigilance (e.g. Boland, 2003), predator encounter dilution (Santos et
al., 2016) and predator confusion (Tosh, Jackson, & Ruxton, 2006),
enhanced foraging efficiency (due to collective effort searching for
food (e.g. Cvikel et al., 2014) or increased ability to overcome com‐
petitors (Foster, 1985) and efficient aerodynamic or hydrodynamic
movement (e.g. Portugal et al., 2014). However, these key benefits
must outweigh important costs, such as within‐group competition
(e.g. Cresswell, 1998) and increased detectability by predators (Uetz
& Hieber, 1994), if individuals are to experience net fitness benefits.
The multiple trade‐offs operating within social groups are complex;
therefore, intensive research using suitable model systems is re‐
quired to synthesize an understanding of the ultimate explanations

Fish and Fisheries. 2019;20:921–933. wileyonlinelibrary.com/journal/faf

© 2019 John Wiley & Sons Ltd | 921
922 | PAIJMANS et al.

for social grouping behaviour. Social grouping behaviour displayed

by fishes (termed shoaling) provides an important model system for
1. INTRODUCTION 921
investigating the ultimate explanations for social grouping behaviour
2. THE COSTS AND BENEFITS OF SHOALING 922
because there is wide range of group forms and functions available
BEHAVIOUR
to research.
2.1 Predation on Shoals 923
Shoaling is common among both marine and freshwater fishes
2.2 Foraging efficiency 925
from a variety of aquatic ecosystems (Shaw, 1978), ranging from
3. WITHIN‐SPECIES DIFFERENCES 925
relatively small shoals in freshwater streams and lakes (e.g., Croft
et al., 2003; Krause, Hoare, et al., 2000) to highly structured pe‐ 4. MIXED‐SPECIES SHOALING 926

lagic schools containing multiple thousands of individuals in marine 4.1 Predation on mixed‐species shoals 926
systems (e.g. Weber, Peña, & Jech, 2009). As such, shoaling has in‐ 4.2 Foraging in mixed‐species shoals 927
spired questions of why social grouping occurs in such a variety of 4.3 Protective and aggressive mimicry 928
forms and what role it plays in the growth, survival and reproduction 4.4 Future research 928
of social fishes. Stemming from this key question is a large body of 5. CONCLUSIONS 929
literature invested in identifying and quantifying the multiple costs ACKNOWLEDGEMENTS 930
and benefits associated with shoaling behaviour, costs and benefits
REFERENCES 930
which theoretically trade‐off to produce net benefits for individu‐
SUPPORTING INFORMATION 933
als and the subsequent propagation of shoaling behaviour through
generations. One key outcome identified from this literature is the
importance of phenotypic, behavioural and physiological similar‐
ity among shoal members as a central component of shoal forma‐
tion and one which is correlated with multiple important benefits
for individuals. The third section applies this framework to under‐
(Krause, Butlin, Peuhkuri, & Pritchard, 2000; Krause, Hoare, et al.,
standing mixed‐species shoaling behaviour, highlighting where our
2000; Ward, Hart, & Krause, 2004; Ward, Webster, & Hart, 2007;
understanding of single‐species shoaling can be applied and where
Webster, Goldsmith, Ward, & Hart, 2007).
novel costs and benefits need to be considered. Finally, we provide
This then raises questions surrounding mixed‐species shoaling.
a theoretical framework designed to enhance understanding of the
Mixed‐species shoaling behaviour has been described across a range
cost‐benefit trade‐offs for individuals within mixed‐species shoals
of aquatic systems (Appendix S1), in some cases being as common
and act as a simple yet comprehensive platform on which future in‐
or more common than single‐species shoaling (e.g. temperate lake
vestigations of the significance of mixed‐species shoaling behaviour
fishes [Krause, Godin, & Brown, 1998], and small pelagic fishes
can be based.
[Louw, Fréon, Huse, Lipiński, & Coetzee, 2014]), however, inherently
contradicts the view that similarity in phenotype, behaviour and
physiology among shoal members is a central contributor to fitness.
2 | TH E COS T S A N D B E N E FIT S O F
Unsurprisingly, the body of research from which our understanding
S H OA LI N G B E H AV I O U R
of shoaling behaviour is derived has historically centred on single‐
species shoals (Breder, 1959; Pitcher, 1993; Shaw, 1978; Sridhar
Behaviours displayed by animals, like any traits, are subject to
& Guttal, 2018), with a relatively small number of publications in‐
natural selection to enhance an individual's growth, survival and
vested in understanding the significance of mixed‐species shoaling
(Figure 1). From those publications that do consider mixed‐species 250
shoaling, it is evident that there are overlaps between the functions
of single‐ and mixed‐species shoaling behaviour. However, what is 200
Number of publications

particularly noteworthy is that this research also identifies key cost‐

150
benefit trade‐offs specific to mixed‐species shoaling that arise di‐
rectly from differences between species. 100
In this review, we provide a synthesis of costs and benefits as‐
sociated with shoaling behaviour and discuss the extent to which 50

identified fitness outcomes derived from the single‐species shoal‐

0
ing literature may be applied to explain mixed‐species shoaling. The 1971–1980 1981–1990 1991–2000 2001–2010 2011–2018
first section is structured so that key drivers of shoaling behaviour,
F I G U R E 1 Approximate number of articles published per
predation threat and foraging efficiency, are synthesized and the ev‐
decade on shoaling behaviour in fishes (light grey) and on mixed‐
idence for costs and benefits of shoaling in relation to each is given.
species shoaling behaviour specifically (dark grey). Numbers
The second section synthesizes the influences of within‐species presented are approximations only as search parameters are not
differences between shoal members and the associated trade‐offs exhaustive. Search parameters are available in Appendix S2
PAIJMANS et al. | 923

F I G U R E 2 The multiple trade‐offs

Benefit
between predation risk (orange) and
foraging efficiency (blue) related functions
are considered the key mechanisms

Inc. circumvenon of territorial food competors

underlying the formation and size of fish

Inc. collecve effort searching for food/prey

Increasing predator encounter dilution

Decreasing me allocated to vigilance

Decreasing predator assessment risk

Increasing cooperave hunng

Increasing detecon of predators
Decreasing conspicuousness
shoals. Benefits associated with increasing

Increasing predator confusion

group size are shown on the y‐axis and
costs on the x‐axis [Colour figure can be
viewed at wileyonlinelibrary.com]

Solitary behaviour

Increasing compeon for food

Cost Increasing detecon by prey Benefit
Increasing detecon by predators

reproduction (Tinbergen, 1963). Social grouping is one such be‐

2.1 | Predation on shoals
haviour that has evolved in many fishes, the evolution of which
can be attributed to net benefits experienced by social individuals Central to our understanding of shoaling is the hypothesis that indi‐
(Krebs & Davies, 2009; Seghers, 1974; Wright, Rimmer, Pritchard, viduals within larger shoals experience a reduced risk of predation
Butlin, & Krause, 2003). Although multiple costs and benefits of relative to individuals that remain solitary or in smaller shoals (Neill &
social grouping have been identified and discussed across many Cullen, 1974; Pitcher, 1993; Sibly, 1983) (Figure 2). Early evidence for
taxa (Pitcher, 1993; Ward & Webster, 2016), the trade‐offs be‐ this key hypothesis comes from a comparison of shoaling behaviour
tween foraging efficiency and predation risk are considered key between populations of guppies (Poecilia reticulata, Poeciliidae) with
mechanisms underlying the formation and maintenance of most naturally different levels of predation. Guppies from streams with
social groups. Broadly, individuals benefit from reduced predation high predation displayed well‐developed shoaling behaviour com‐
risk and need for vigilance by grouping with others, whilst forag‐ pared to an absence of shoaling in guppies from streams with low
ing in groups is variously a trade‐off between enhanced food com‐ predation. These shoaling tendencies persisted over multiple gen‐
petition and increased efficiency searching for food (Godin, 1986; erations, providing strong evidence for the development of shoaling
Janson & Goldsmith, 1995; Kie, 1999; Pitcher, 1993; Powell, 1974) behaviour as an evolutionary response to predation threat (Seghers,
(Figure 2). 1974).
Although generally not considered as important as predation The anti‐predation benefits of shoaling have been attributed to
and foraging, reproduction and reduction in parasitism have also multiple mechanisms. The most obvious being “predator encounter
been identified as possible ultimate explanations for shoaling be‐ dilution”, whereby the chance of an individual encountering a pred‐
haviour, in some cases. Shoaling may provide fitness benefits in ator is reduced when surrounded by other individuals (Morgan &
terms of enhanced reproduction via the opportunity for individuals Godin, 1985). However, additional mechanisms have been identi‐
to choose the fittest partner from a large selection of candidates fied, those being reduced “conspicuousness” (Ioannou, Bartumeus,
(Ward & Webster, 2016) and spawning aggregations may act as a Krause, & Ruxton, 2011), collective vigilance and information
mechanism to ensure genetic variation among offspring (Coleman, transfer (Magurran & Higham, 1988; Magurran, Oulton, & Pitcher,
Koenig, & Collins, 1996; Domeier & Colin, 1997). Because the intri‐ 1985; Ward, Herbert‐Read, Sumpter, & Krause, 2011), predator as‐
cacies of reproduction do not apply to interactions between spe‐ sessment and inhibition (Licht, 1989; Magurran, 1990; Magurran &
cies within mixed‐species shoals (Morse, 1977), we will not provide Girling, 1986) and the confusion effect (Landeau & Terborgh, 1986;
a detailed discussion here. However, in saying that, the inability of Larsson, 2012; Neill & Cullen, 1974) (Table 1). Theoretically, this
individuals to breed with heterospecifics should be considered as series of mechanisms affords shoaling prey protection via initial
a potentially influential cost associated with mixed‐species shoal‐ avoidance of predators through to the mitigation of successful pre‐
ing. In addition, parasitism has been associated with both costs and dation once a predator attacks (Pitcher, 1993: table 12.1). Shoaling
benefits for shoaling fish (Table 1) but this has received less atten‐ prey may be less conspicuous to predators when in larger shoals
tion and is generally considered less influential than predation and because populations are finite; therefore, the formation of larger
foraging as an ultimate explanation for shoaling behaviour (Pitcher, shoals equates to less shoals overall. Indeed, three‐spined stickle‐
1986, 1993). backs (Gasterosteus aculeatus, Gasterosteidae) had lower detection
924 | PAIJMANS et al.

TA B L E 1 A summary of identified costs and benefits associated with shoaling behaviour along with fundamental references

Costs References Description

Food competition Milinski (1984, 1986) Sticklebacks (Gasterosteus aculeatus) distributed themselves between
resource patches at a ratio proportional to patch profitability
Metcalfe and Thomson (1995) Minnows (Phoxinus phoxinus) showed preference for shoals of competi‐
tively inferior conspecifics over shoals of superior conspecifics
Parasite transfer Dugatkin, FitzGerald, and Lavoie (1994) and Uninfected sticklebacks (Gasterosteus aculeatus) showed preference for
Barber, Downey, and Braithwaite (1998) shoals of uninfected conspecifics
Richards, Oosterhout, and Cable (2010) Female guppies (Poecilia reticulata) shoaled more often and had higher
rates of infection compared to males
Increased predation Botham et al. (2005) Predators preferentially attacked shoaling guppies (Poecilia reticulata)
Benefits
Reduced predation risk due to
Attack dilution Brock and Riffenburgh (1960) Mathematical modelling suggests increasing shoal size is inversely related
to predator‐prey encounters
Increased vigilance Magurran et al. (1985) Minnows (Phoxinus phoxinus) in larger shoals collectively identified a
predation threat earlier
Predator confusion Landeau and Terborgh (1986) The success of largemouth bass (Micropterus salmoides) in preying
upon minnows (Hybognathus nuchalis) decreased as minnow shoal size
increased
Increased foraging efficiency due to
Forage area Pitcher et al. (1982) Individual foraging rate increased due to group effort searching for food in
copying minnows (Phoxinus phoxinus) and goldfish (Carassius auratus)
Decreased ag‐ Robertson, Sweatman, Fletcher, and Cleland Shoaling parrot fish (Scarus croicenus) received less aggression from ter‐
gression from (1976) ritorial damselfish (Eupomacentrus planifrons) (a food competitor) than
competitors solitary individuals
Social learning Lachlan et al. (1998) Guppies (Poecilia reticulata) showed preference for shoals containing con‐
specifics that had previously been fed within the test aquarium
Chapman, Ward, and Krause (2008) Guppies (Poecilia reticulata) where able to locate food faster when shoaling
with trained demonstrators
Reduction in indi‐ Magurran and Pitcher (1983) Goldfish (Carassius auratus) in larger groups spent more time on exposed
vidual vigilance food patches
Reduced risk of Poulin and FitzGerald (1989) Infection risk reduced with increasing shoal size in sticklebacks
parasitism (Gasterosteus aculeatus and G. wheatlandi)
Stumbo, James, Goater, and Wisenden Minnows (Pimephales promelas) in the centre of shoals experienced re‐
(2012) duced parasitism

of grouped prey (chironomid larvae) when groups were larger and
less numerous compared to smaller and more numerous (Ioannou et
al., 2011). Vigilance and early predator detection are key if prey are
to avoid capture (Pitcher, 1986). Common minnows (Phoxinus phox‐
inus, Cyprinidae) in larger shoals reduced feeding rate sooner than
those in smaller shoals when threatened by a model predator, sug‐
gesting that they collectively identified the predation threat earlier
(Magurran et al., 1985). Once a potential threat has been detected,
predator assessment allows prey to ascertain whether they are in
danger. However, there are obvious risks associated with approach‐
ing a potential predator, risks which may be minimized by shoaling
behaviour (Pitcher, 1991). Guppies from areas with naturally high
predator densities inspected an approaching model predator in
larger shoals than those from areas with low predator densities,
suggesting benefits associated with group inspection (Magurran &
Seghers, 1994). Once a predator attacks, the predator confusion
effect may limit predation success upon grouped prey. Predatory
largemouth bass (Micropterus salmoides, Centrarchidae) quickly and
effectively captured solitary silvery minnows (Hybognathus nuchalis,
Cyprinidae), however as minnow shoal size increased bass took lon‐
ger to capture minnows and performed more unsuccessful attacks.
These findings were attributed to the predator being “stymied” by
shoaling prey (Landeau & Terborgh, 1986), a phenomenon that has
further been attributed to the intricacies of evasion tactics displayed
by phenotypically similar grouped prey and the neurological func‐
tion of predators (Krakauer, 1995; Ruxton, Jackson, & Tosh, 2007).
Conversely, increased detectability of larger shoals by predators
may be an important cost (Figure 2). When given the choice between
shoaling and solitary guppies, predatory cichlids (Aequidens pulcher
and Crenicichla frenata, Cichlidae) and wolf‐fish (Hoplias malabaricus,
Eruthrinidae) all preferentially attacked shoals (Botham, Kerfoot,
Louca, & Krause, 2005).
PAIJMANS et al.
2.2 | Foraging efficiency
Alongside predation avoidance, foraging efficiency is a fundamental
determinant of individual fitness and foraging‐related benefits can
promote the formation of shoals (Olson, Haley, Dyer, & Adami, 2015;
Ward & Webster, 2016). Shoaling may benefit individual foraging
success via group vigilance, which reduces the need for individual
vigilance and therefore increases time allotted to foraging (i.e. the
many eyes hypothesis [Pulliam, 1973]). This phenomenon has been
described often and across a range of taxa including fish (Elgar, 1989;
Lima, 1995; Quenette, 1990; Ward et al., 2011). Secondly, a collec‐
tive effort in searching for food within shoals may increase foraging
efficiency. Both goldfish (Carassius auratus, Cyprinidae) and common
minnows located food patches faster when in larger shoals (Pitcher,
Magurran, & Winfield, 1982). Thirdly, an increased ability to over‐
whelm competitors due to large shoal size may allow for the circum‐
vention of food competitors (Heinrich & Marzluff, 1995). Bite rates of
individual blue tang (Acanthurus coeruleus, Acanthuridae) increased
as shoal size increased, with the correlation attributed to decreased
territorial aggression by a food competitor (the dusky damselfish
[Stegastes dorsopunicans, Pomacentridae]) (Foster, 1985). However,
there are also foraging‐related costs associated with shoaling includ‐
ing within‐shoal food competition (Hensor, Godin, Hoare, & Krause,
2003; Milinski, 1979; Robinson, 1994; Ward, Webster, & Hart, 2006).
When given the choice between multiple food patches, three‐spined
sticklebacks grouped together with shoal sizes proportional to food
patch quality, suggesting that food competition drives the sorting of
individuals into shoals (Milinski, 1979).
Shoaling not only occurs among prey, but also among predatory
species, a phenomenon which has again been attributed to forag‐
ing‐related cost‐benefit trade‐offs (Stephens, Brown, & Ydenberg,
2014: chapter 10). Individuals hunting in larger shoals may be more
likely to encounter prey due to collective vigilance and coverage of
a larger volume of space (Pitcher et al., 1982). Although this has not
been demonstrated for shoaling fish, bats (Rhinopoma microphyllum,
Rhinopomatidae) actively aggregated whilst hunting suggesting ben‐
efits associated with collective vigilance and eavesdropping (Cvikel et
al., 2014). Further, cooperative hunting may provide individual ben‐
efits via access to larger prey (Creel & Creel, 1995), increased prey
capture success (Herbert‐Read et al., 2016), or via suppression of the
confusion effect when hunting grouped prey. For group‐hunting sail‐
fish (Istiophorus platypterus, Istiophoridae), prey capture success was
improved for individuals which attacked schooling prey (Sardinella
aurita, Clupeidae) after conspecifics due to an increasing number
of injured prey with successive attacks (Herbert‐Read et al., 2016).
Blue‐green Chromis (Chromis viridis, Pomacentridae) in shoals had
higher feeding rates and greater prey capture success when preying
upon swarms of brine shrimp with results attributed to suppression
of the confusion effect (Smith & Warburton, 1992). Finally, increased
hydrodynamic efficiency may reduce the energy requirements asso‐
ciated with hunting (Partridge, Johansson, & Kalish, 1983). On the
other hand, possible costs associated with hunting in groups include
an increased probability of being detected by prey and susceptibility
| 925
to “scrounges” (i.e. group members that do not contribute to hunting
but which take food once it has been captured) (Vickery, Giraldeau,
Templeton, Kramer, & Chapman, 1991).
3 | W ITH I N ‐S PEC I E S D I FFE R E N C E S
In addition to the cost‐benefit trade‐offs associated with shoal size,
variations among shoal members may be an important determinant
of individual fitness. Shoals in which conspecifics are phenotypi‐
cally, behaviourally and physiologically similar are generally under‐
stood to provide the greatest benefit to individuals due to efficiency
of the confusion effect (Krause & Godin, 1994; Wong & Rosenthal,
2005), the maintenance of shoal structure (Krause, Godin, & Brown,
1996) or the aquisation of information about habitats (Ward et al.,
2004, 2007; Webster et al., 2007). Indeed, predation success by lar‐
gemouth bass was greater upon shoals of phenotypically different
silvery minnows (1 or 2 blue died minnows in shoals of 8) compared
to shoals of phenotypically similar minnows (Landeau & Terborgh,
1986). However, a growing body of research is showing that subtle
variations in the phenotype, familiarity, experience, state or person‐
ality of conspecific group members can benefit individuals in some
cases (Magnhagen, 2012; Ward & Webster, 2016). An important ex‐
ample is seen in shoals where dominance hierarchies or leader–fol‐
lower dynamics operate. In such cases, shoal function is dependent
upon within‐shoal variation in, for example, body size (e.g. Matthews
& Wong, 2015) or swimming speed (e.g. Jolles, Boogert, Sridhar,
Couzin, & Manica, 2017). Faster three‐spined sticklebacks occupied
the peripheries of shoals and were more likely to be leaders in the
collective movement of shoals containing both fast and slow indi‐
viduals (Jolles et al., 2017). Such organization may drive efficient col‐
lective movement and therefore benefit individuals due to predator
confusion and collective vigilance (Katz, Tunstrøm, Ioannou, Huepe,
& Couzin, 2011).
Shoals containing more experienced members may benefit naive
individuals via social learning about food locations and predation
threats in novel situations (Pitcher & House, 1987). Guppies showed
preference for shoals containing conspecifics that had previous ex‐
perience with food in a test aquarium over naive shoals, suggesting
that individual guppies perceived benefits associated with the ability
to learn foraging information from shoal members (Lachlan, Crooks,
& Laland, 1998). Variation in individual state or hunger may influ‐
ence shoaling propensity as costs associated with food competition
outweigh other benefits of social grouping for hungry individuals.
Multiple examples show decreased shoal cohesion and increased
time spent solitary with increasing hunger (Barber, Huntingford, &
Crompton, 1995; Hensor et al., 2003; Metcalfe & Thomson, 1995;
Robinson, 1994). Variations in consistent behavioural differences
(i.e. personality traits) among conspecific shoal members may influ‐
ence individual fitness. Both bold and shy three‐spined sticklebacks
preferred to associate with conspecific shoals composed of bold
individuals over shoals composed of shy individuals, with results
been attributed to bold shoals being more active and therefore likely
926 | PAIJMANS et al.
providing greater benefits in terms of foraging efficiency (Harcourt,
Sweetman, Johnstone, & Manica, 2009).
In summary, differences between individual shoal members may
mediate the fitness outcomes associated with increasing shoal size.
Theoretically, the combined effects of the multiple costs and benefits
discussed above influence an individual's perception of net benefit,
and hence choice of social grouping behaviour (Figure 2). However,
this theoretical understanding comes overwhelmingly from studies
of single‐species shoals (Figure 1). To understand the significance
of mixed‐species shoals, critical consideration of the distinct phe‐
notypic, behavioural and physiological differences between species
need to be incorporated into the conceptual framework.
4 | M I X E D ‐S PEC I E S S H OA LI N G
The formation of shoals containing multiple species is a commonly
observed phenomenon among both marine and freshwater fishes
and is likely to be of considerable consequence for the growth, sur‐
vival and reproduction of shoaling individuals, and therefore the
function of fish communities and their surrounding ecosystems. Our
aim here is to progress our understanding of the ultimate reasons
why fishes form mixed‐species shoals. In saying this, the evolution
of mixed‐species shoaling has not been strictly demonstrated. That
is, there are no publications that show, by forming mixed‐species
shoals, individuals of a species were less likely to be eaten or gained
more food and therefore left more offspring, therefore making the
trait more common in the population. Indeed, it may be that indi‐
viduals associate with heterospecifics due to constraints in cognition
and therefore the inability to distinguish heterospecifics from con‐
specifics. Research has also shown that passive mechanisms such as
variation in swimming speeds can play an important role in structur‐
ing the composition of mixed‐species shoals (Krause et al., 2005).
Further, the formation of mixed‐species shoals may be driven by a
lack of available conspecifics. Mixed‐species shoal formation could
theoretically result from a solitary individual choosing to join the
only available shoal, comprised of heterospecifics, over starting its
own shoal (i.e. remaining solitary until joined by others) (Sibly, 1983).
Given our current understanding of mixed‐species shoal‐
ing, there is no clear consensus as to the relative influence of
constraint verses adaptive explanations and it is likely that both
operate to varying extents in different systems. Another im‐
portant consideration is the influence of social learning, with re‐
search demonstrating that learning can shape both conspecific
(Lachlan et al., 1998; Pitcher & House, 1987) and heterospecific
(Warburton & Lees, 1996) association preferences. If a species
preference for mixed‐species shoaling behaviour is learned rather
than innate, it may be that selection acts upon between‐species
information transfer and learning ability rather than mixed‐spe‐
cies shoaling behaviour itself. Rapidly progressing research into
the cognitive ability of fishes and the ability of fish to communi‐
cate within‐ and between species is providing important insight in
this field, with the evidence demonstrating that fish are capable
of recognizing, communicating with, and learning from hetero‐
specifics (Warburton & Lees, 1996; Ward, Holbrook, Krause, &
Hart, 2005; Ward et al., 2018; Ward & Webster, 2016; Webster,
Ward, & Hart, 2008). Irrespective of how selection may act upon
mixed‐species shoaling behaviour, shoal choice experiments and
investigations of resource use demonstrate that there are unique
costs and benefits associated with the formation of mixed‐species
shoals relative to single‐species shoals. This insight, which relates
to “once‐removed” fitness such as survivorship and growth rather
than true fitness, provides evidence for the evolution of mixed‐
species shoaling as a response to environmental drivers. In the
following sections, we provide a synthesis of the multiple unique
costs and benefits likely to be operating in mixed‐species shoals
and discuss where research effort is required to produce a better
understanding of the ultimate reasons why fishes form mixed‐spe‐
cies shoals.
From a relatively small number of publications offering insight
into mixed‐species shoaling behaviour (Figure 1, Appendix S1) and
other literature concerning the formation of mixed‐species social
groups in birds and mammals (Goodale, Beauchamp, & Ruxton,
2017), it is evident that the functions of single‐species shoaling are
also characteristic of mixed‐species shoaling, but only to a limited
extent. Generally, the key drivers of single‐species shoaling, those
being predation avoidance and foraging efficiency, can also explain
mixed‐species shoaling. Further, fitness outcomes associated with
increasing shoal size (Figure 2) can apply to mixed‐species shoals.
However, unique cost‐benefit trade‐offs arising from differences
in phenotype, behaviour and physiology between species within
mixed‐species shoals (Figure 3) highlight the need for a theoretical
framework developed specifically for investigations of the fitness
outcomes of mixed‐species shoaling behaviour.
Goodale et al. (2017) provide a theoretical framework of fitness
outcomes arising from an individual's association with either sin‐
gle‐ or mixed‐species groups. This framework highlights the need
to consider payoffs associated with mixed‐species grouping for each
species individually, as the direction and magnitude of fitness out‐
comes are not necessarily equal for each species involved (for fur‐
ther information see Table 4.1 in Goodale et al. (2017)). With this in
mind, the following sections synthesizing costs and benefits asso‐
ciated with mixed‐species shoaling have been structured from the
perspective of one “focal” species.
4.1 | Predation on mixed‐species shoals
The formation of mixed‐species shoals may incur a variety of costs
and benefits for individuals regarding predation susceptibility, with
the payoffs likely driven by differences between species (Figure 3)
as well as fitness outcomes associated with increasing shoal size
(Figure 2). Benefits unique to mixed‐species shoaling may arise from
a higher vigilance of heterospecifics (Semeniuk & Dill, 2006) or a
predator's preference for heterospecifics (Mathis & Chivers, 2003;
McKaye, Mughogho, & Lovullo, 1992). On the other hand, inherent
phenotypic oddity within mixed‐species shoals means individuals
PAIJMANS et al. | 927

F I G U R E 3 Multiple predation risk

(orange) and foraging efficiency (blue) Benefit
related trade‐offs arising from the
differences in phenotype, behaviour and

oning
Predator preference for heterospecifics

Circumven on of territorial compe tors

physiology between species within mixed‐

Access to unaccusable food sources

High vigilance of heterospecifics
species shoals. Benefits associated with

Increasing Protec ve mimicry

Decreasing detec on by prey

Diet or feeding me or spa al par
the formation of mixed‐species shoals
are shown on the y‐axis and costs on the
x‐axis [Colour figure can be viewed at
wileyonlinelibrary.com]

Single-species shoal

Increasing between-species food compe on

Cost Benefit
Increasing oddity

may experience increased predation susceptibility relative to indi‐ a reduced likelihood of being selected by a predator by joining shoals
viduals within single‐species shoals due to inefficiency of the confu‐ of minnows (Mathis & Chivers, 2003).
sion effect. Indeed, the tendency for a focal chub (Leuciscus cephalus, In summary, individuals within mixed‐species shoals may incur
Cyprinidae) to associate with a mixed‐species shoal containing com‐ both costs and benefits, due to differences between species in‐
mon minnows became progressively less with a decreasing number fluencing predation threat. A key cost is inefficiency of the confu‐
of conspecifics in the shoal (i.e. increasing oddity of the focal fish) sion effect within mixed‐species shoals compared to single‐species
(Ward, Axford, & Krause, 2002). shoals, whilst potential benefits include the relatively high vigilance
Group vigilance may provide greater benefits for individuals of heterospecifics and predator's preference for heterospecifics
within mixed‐species shoals, relative to those within single‐spe‐ (Figure 3). These concepts are not well understood for shoaling fish,
cies shoals, if heterospecifics are more vigilant than conspecifics. or any other socially grouping animals, therefore require further
Although not conclusively demonstrated for shoaling fish, an ex‐ investigation.
ample is seen in two species of marine elasmobranch (the cowtail
stingray [Pastinachus sephen, Dasyatidae] and reticulate whipray
4.2 | Foraging in mixed‐species shoals
[Himantura uarnak, Dasyatidae]) that form mixed‐species groups
whilst resting. Stingrays preferred to rest alongside whiprays and Foraging in mixed‐species shoals may incur unique cost‐benefit
when in mixed‐species groups, whiprays responded earlier than trade‐offs for individuals (Figure 3) in addition to those associ‐
stingrays to an approaching mock predator, suggesting that the whip‐ ated with shoal size (Figure 2). Diet partitioning between species
rays benefit disproportionally more from the association (Semeniuk may minimize within‐shoal food competition, but in contrast un‐
& Dill, 2006). There is evidence to show that fish recognize and re‐ equal competitive ability between species may be costly for infe‐
spond to heterospecific alarm cues (e.g. Chivers, Mirza, & Johnston, rior competitors. Diet analysis of tuna from mixed‐species schools
2002) and that information transfer between species does occur revealed significant differences in both diet and feeding times be‐
with respect to directional movement in mixed‐species shoals (Ward tween yellowfin tuna (Thunnus albacares, Scombridae) and skipjack
et al., 2018). These examples provide support for multi‐species vigi‐ tuna (Katsuwonus pelamis, Scombridae) (Alatorre‐Ramirez, Galván‐
lance in fishes; however, further research is required to conclusively Magaña, Torres‐Rojas, & Olson, 2017), with partitioning of food
demonstrate the rapid transmission of accurate information about between the two species possibly minimizing within‐shoal food com‐
predation threats between species within mixed‐species shoals. If petition. Additionally, within‐shoal segregation of species, whereby
a predator prefers one species over another, the less‐preferred spe‐ different species occupy different areas within a single shoal, may
cies may benefit more from the formation of a mixed‐species shoal facilitate food partitioning, so minimizing competition (Allan, 1986;
relative to a single‐species shoal. Both flathead minnows (Pimephales Krause, 1993; Parrish, 1989). However, if diet partitioning does
promelas, Cyprinidae) and brook sticklebacks (Culaea inconstans, not occur, unequal competitive ability between species may incur
Gasterosteidae) preferred single‐species shoals when unthreatened; higher costs for inferior species in mixed‐species shoals relative to
however, sticklebacks switched their preference to shoals of min‐ single‐species shoals (Stier, Geange, & Bolker, 2013). Food compe‐
nows when threatened by a predator. The results are attributed to tition occurred within mixed‐species shoals of brook sticklebacks
sticklebacks being heavily armoured and therefore less vulnerable and flathead minnows with minnows being competitively superior.
to predation than minnows, meaning that sticklebacks benefit from However, when under predation threat, sticklebacks still preferred
928 | PAIJMANS et al.
mixed‐species shoals, likely exemplifying the trade‐off between pre‐
dation avoidance and shoaling with a competitively superior species
(Mathis & Chivers, 2003).
In addition to benefits associated with diet partitioning, for‐
aging associations are known to be an important driver of the for‐
mation of mixed‐species shoals (Lukoschek & McCormick, 2002).
Wrasse (Halichoeres garnoti, Labridae) associating with goatfish
(Pseudupeneus maculatus and Mulloides martinicus, Mullidae) made
more bites on sand substrata than solitary wrasse, suggesting that
wrasse gain access to an otherwise un‐accessible food source by
forming shoals with goatfish (Aronson & Sanderson, 1987). Foraging
associations may also provide benefits via the circumvention of
territorial food competitors. This phenomenon has been described
multiple times for mixed‐species shoals containing surgeonfishes
as a core species on coral reefs. Various satellite species including
midnight parrotfish (Scarus coelestinus, Scaridae) (Alevizon, 1976),
tangs (Acanthurus sp., Acanthuridae) (Barlow, 1974) and multiple
other fishes (Itzkowitz, 1974, 1977) form mixed‐species shoals with
surgeonfishes (Acanthuridae) to gain access to algal mats which are
aggressively defended by territorial damselfishes (Pomacentridae).
In summary, foraging within mixed‐species shoals may provide
individuals with benefits due to diet partitioning, access to other‐
wise inaccessible food resources or the circumvention of territorial
food competitors. However, in some cases asymmetric food compe‐
tition can be an important cost for inferior species (Figure 3). This
series of trade‐offs are unique to mixed‐species shoaling because
they arise from differences between species and therefore provide
some possible explanations for mixed‐species shoaling.
4.3 | Protective and aggressive mimicry
Mimicry is well studied in fishes and overlaps in theory with mixed‐
species shoaling when individuals within mixed‐species shoals
benefit from phenotypic and behavioural similarity to heterospe‐
cifics. Protective mimicry, defined as situations in which individu‐
als gain predation avoidance benefits by mimicking another species,
can operate within mixed‐species shoals (Dafni & Diamant, 1984).
Mulloidichthys martinicus (Mullidae), Sparisoma axillare (Scaridae)
and Harengula clupeola (Clupeidae) appear to display protective
mimicry with multiple species of grunt (Haemulon sp., Haemulidae)
on Brazillian coral reefs. The three minority species (M. martinicus,
S. axillare and H. clupeola) were observed approaching and mimicing
the behaviour of numerically abundant grunts when threatened by
predators (Pereira, Feitosa, & Ferreira, 2011). Although this example
provides only anecdotal evidence, it may be that predation avoid‐
ance benefits associated with inclusion in a large phenotypically
similar shoal (Section 2, Figure 2) may be afforded individuals that
display protective mimicry, in addition to benefits associated with
differences between species, in, for example, diet or vigilance.
Aggressive mimicry, defined as situations in which a predatory
mimic gains foraging benefits via the ability to approach prey unde‐
tected, can also operate within mixed‐species shoals (Moland, Eagle,
& Jones, 2005). Although again not conclusively demonstrated,
observations of the hunting behaviour of seabass (Dermatolepis derma‐
tolepis, Serranidae) joining shoals of herbivores (Montgomery, 1975),
and predatory blennies (Runula azalea, Blenniidae) joining shoals of
unthreatening wrasse (Thalasoma lucasanum, Labridae) (Hobson, 1969)
provide some evidence. Further research comparing the predation rate
and foraging efficiency of individuals displaying mimicry in mixed‐spe‐
cies shoals, to solitary individuals or those within single‐species shoals
would provide important insight in this field. Theoretically, cases in
which mixed‐species shoaling incorporates protective‐ or aggres‐
sive mimicry could be considered as evolutionarily advanced cases of
mixed‐species shoaling because individuals potentially benefit from re‐
markable phenotypic similarity (to the extent where predators and prey
are unable to distinguish species) as well as between‐species variations
in other important traits such as diet or vigilance.
4.4 | Future research
No published research has demonstrated the evolution of mixed‐
species shoaling in response to environmental drivers which is an im‐
portant barrier to our understanding of the ultimate reasons fishes
form mixed‐species shoals. Studies of single‐species shoals have
demonstrated that shoaling behaviour more generally is a heritable
adaptation (Seghers, 1974; Wright et al., 2003). Further, research
suggests that fishes are capable of recognizing and communicating
with heterospecifics (Ward et al., 2018) and that there are unique
benefits associated with the formation of mixed‐species shoals (e.g.
Alatorre‐Ramirez et al., 2017; Alevizon, 1976; Mathis & Chivers,
2003). This insight suggests that species preference for associating
with heterospecifics is an adaptive behaviour rather than a result of
constraints in, for example, cognition or the availability of conspecif‐
ics. Multi‐generational experiments should be a central component
of future research into mixed‐species shoaling behaviour. Such ex‐
periments should expose populations to different levels of predation
threat or food availability and then quantify mixed‐species shoaling
propensity over multiple generations.
We cite multiple studies that quantify benefits for individuals in
terms of growth (e.g. Smith, Fox, Booth, & Donelson, 2018) and sur‐
vival (e.g. McKaye et al., 1992), via the formation of mixed‐species
shoals. However, most studies have only inferred costs and benefits
from choice experiments and measures of foraging (e.g. Mathis &
Chivers, 2003). Further, several of the mechanisms we propose as
drivers of mixed‐species shoaling (Figure 4) are not associated with
evidence from studies of shoaling fish but rather evidence taken
from studies of other mixed‐species groups. Those mechanisms,
including the increased vigilance of heterospecifics relative to con‐
specifics and diet partitioning between subgroups of conspecifics
within mixed‐species shoals, require further investigation in fish.
Future research which directly quantifies the costs and benefits
outlined in our theoretical framework (Figure 4), rather than infer‐
ring costs and benefits from choice experiments will be particularly
valuable contributions.
Underlying all the mechanisms, we propose as linked to mixed‐
species shoaling is the assumption that shoal members are capable of
PAIJMANS et al. | 929

How many species in the shoal?

1 >1

Single-species shoal Mixed-species shoal

Shoal members are similar in Shoal members are different in

terms of phenotype, behaviour terms of phenotype, behaviour
and/or physiology and/or physiology

Shoal formation due to net benefits Shoal formation due to net benefits afforded individuals from
afforded to individuals from the multiple the multiple trade-off’s of differences between species (Fig 3),
trade-off’s of increasing shoal size (Fig 2) along with those of increasing shoal size (Fig 2).

Benefit
(Fig 2) Benefit (Fig 3)
Inc. circumvention of territorial food competitors

Diet or feeding time or spatial partitioning

Inc. collective effort searching for food / prey

Circumvention of territorial competitors

Predator preference for heterospecifics
Increasing predator encounter dilution

Decreasing time allocated to vigilance

Decreasing predator assessment risk

Access to unaccusable food sources

Increasing cooperative hunting
Increasing detection of predators
Decreasing conspicuousness

High vigilance of heterospecifics

Increasing predator confusion

Increasing Protective mimicry

Decreasing detection by prey

Solitary behaviour

Single-species shoal
Increasing competition for food
Increasing between-species food competition
Cost Increasing detection by prey Benefit Cost Benefit
Increasing oddity
Increasing detection by predators

F I G U R E 4 A new conceptual framework for future research into the ultimate explanations for mixed‐species shoaling behaviour
incorporating possible fitness trade‐offs associated with shoal size and differences between species [Colour figure can be viewed at
wileyonlinelibrary.com]

efficiently transferring information among heterospecifics. Recent fitness outcomes associated with shoal size. However, this un‐
research has demonstrated that shoaling fish respond rapidly to the derstanding is derived from a body of literature focused on sin‐
movements of heterospecific shoal‐mates (Ward et al., 2018), are gle‐species shoaling. When considering mixed‐species shoaling,
capable of recognizing and responding to heterospecific alarm cues differences between species need to be considered as a central
(Chivers et al., 2002), and prefer to shoal with heterospecifics from determinant of individual fitness, not just as a modulator of the
familiar habitats (Ward et al., 2005; Webster et al., 2008) suggest‐ trade‐offs associated with shoal size. The small body of literature
ing benefits associated with habitat‐specific information transfer. invested in explaining mixed‐species shoaling by fishes, along with
However, further research across more mixed‐species shoaling sys‐ research into mixed‐species social grouping in other animals, in‐
tems and considering a variety of information (such as information dicates that predation threat and foraging efficiency are central
about the location and quality of food) should be undertaken to un‐ drivers of mixed‐species shoaling. Despite this commonality with
derstand the extent and limitations of between‐species information single‐species shoaling, fitness trade‐offs associated with spe‐
transfer as well as the role that social learning plays in mixed‐species cies‐specific responses to predation threat and food, and how
shoaling behaviour. they interact within mixed‐species shoals are not well under‐
stood. Evidence suggests that there are a series of unique preda‐
tion avoidance and foraging efficiency related costs and benefits
5 | CO N C LU S I O N S for individuals in mixed‐species shoals. Here, we have provided a
synthesis of those unique trade‐offs and a framework for future
Previously, differences in phenotype, behaviour and physiol‐ investigations of the evolutionary significance of mixed‐species
ogy among individuals within shoals have been seen to modulate shoaling (Figure 4).
930 | PAIJMANS et al.
AC K N OW L E D G E M E N T S
Thanks to Dr. Phil Byrne and Prof. Andy Davis for their comments
on an early version of this manuscript and to multiple anonymous
reviewers whose comments helped us greatly strengthen the
manuscript. Thanks to Abbey Dalton, Daniel Swadling and Kye
Adams for their support and comments on the manuscript. Thanks
to the Australian Government Research Training Program for fi‐
nancial support. Thanks to all the social fishes for their incredibly
intriguing behaviour.
ORCID
Kai C. Paijmans https://orcid.org/0000-0002-7243-3791
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section at the end of the article.
How to cite this article: Paijmans KC, Booth DJ, Wong MYL.
Towards an ultimate explanation for mixed‐species shoaling.
Fish Fish. 2019;20:921–933. https​://doi.org/10.1111/faf.12384​