Animal Behaviour 79 (2010) 1025—1030

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Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Colour change and assortment in the western rainbowfishGwendolen M. Rodgers a,* Jennifer L Kelley b,1 Lesley J. Morrell a

a Institute of Integrative and Comparative Biology, University of LeedsbSchool of Animal Biology, The University of Western Australia

ARTICLE INFO

Article history:Received 7 October 2009Initial acceptance 2 November 2009Final acceptance 25 January 2010Available online 3 March 2010MS. number: 09-00660R

Keywords:colourcolour changeMelanotaenia australisoddityrainbowflshshoalingsocial behaviour

Grouping behaviour is widespread across the animal kingdom, and is known to reduce an individual’srisk of predation, for example through predator confusion, Theory predicts that individuals that aredifferent in appearance to the rest of the group are at a greater risk of predation because they are moreconspicuous to predators (the oddity’ effect). Thus, animals should choose group mates that are the mostsimilar in appearance to themselves. Another common antipredator tactic is crypsis (camouflage). Fishesare capable of changing colour to match their visual background, but few studies have examined howthis might influence shoaling decisions, particularly in the context of the oddity effect. We inducedcolour pattern changes in a colourful species of freshwater fish, the western rainbowflsh, Melanotaeniaaustralis, by maintaining fish in dark and pale aquaria for 2 weeks. Analysis of the proportion of blackbody pigmentation confirmed that rainbowfish in dark environments developed darker colour patternsthan those held in pale environments. We then conducted behavioural observations to determinewhether fish subsequently based their shoaling decisions on body coloration. We found that rainbowfishpreferred to shoal with similar individuals; fish that had been held in dark aquaria preferred to shoalwith other dark fish and fish from pale aquaria preferred other pale fish. Our findings are consistent withthe predictions of the oddity effect and demonstrate how morphological colour pattern changes andbehavioural decisions interact to mediate antipredator tactics in fish.© 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Animals that live in groups benefit through a reduction inpredation risk, via a variety of mechanisms (Krause & Ruxton 2002).Two of these, the ‘oddity’ (Theodorakis 1989) and ‘confusion’(Landeau & Terborgh 1986; Krakauer 1995) effects rely at leastpartially on individuals within a group having similar phenotypiccharacteristics. The oddity effect describes the preferential targeting of individuals that are phenotypically or spatially distinct fromothers in the group (Ohguchi 1978), while the confusion effectresults from attempts by predators to track multiple moving individuals within a group, and is reduced if some individuals differfrom others (Landeau & Terborgh 1986). Phenotypically distinctindividuals, therefore, are at enhanced risk of capture by predators,and predator preferences for odd phenotypes should result inselection for behaviours that lead to assortment on the basis ofphenotypic characteristics. As a result, group-living animals assort

* Correspondence: G. M. Rodgers, Genetics, Ecology and Evolution Group,Institute of Integrative and Comparative Biology, Miall Building, University of Leeds,Leeds LS2 9JT, U.K.

E-mail address: bsgmr@leeds.ac.uk (G.M. Rodgers).J. L Kelley is at the Centre for Evolutionary Biology, Zoology Building, School of

Animal Biology (Mo92), The University of Western Australia, Nedlands, WA 6009,Australia,

into nonrandom groups. This has been particularly well studied inshoaling fishes, where assortment by species (Ward et al. 2002),body size (Theodorakis 1989), parasite load (Krause & Godin 1996)and colour pattern is common.

Studies that have investigated the role of colour patterns ingrouping decisions in fishes have found preferences for shoalmateswith similar coloration. For example, black and white morphs ofsailfin mollies, Poecilia latipinna, and black and golden morphs offreshwater angelfish, Pterophyllum scalare, prefer to associate withmembers of the same colour morph (McRobert & Bradner 1998;Gómez-Laplaza 2009). Similarly, shoal choice trials with differentstrains of zebrafish, Danio rerio, have revealed preferences forshoalmates most similar to their own phenotype (Engeszer et al.2004; Rosenthal & Ryan 2005). However, these studies, and thoseexamining predation risk in relation to colour patterns, have usedeither dyed prey (Landeau & Terborgh 1986), domestic morphs(McRobert & Bradner 1998; Gómez-Laplaza 2009) or artificiallyselected laboratory strains (Rosenthal & Ryan 2005; Engeszer et al,2007), rather than drawing on natural variation in body coloration,on which predators must base their choice of prey.

Some animals, in particular fishes, reptiles, amphibians andcephalopods, are able to change their body colour by controlling thedispersion of colour pigments in their skin (Parker 1948; Waring

0003-3472/$38.O0 © 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.doi: 10.1016/j.anbehav.2010.01.017

1026 G.M. Rodgers et at / Animal Behaviour 79 (2010) 1025—1030

1963; Bagnara & Hadley 1973). These colour changes can be used

for social signalling (Bradbury & Vehrencamp 1998) but are more

often associated with predator defence and, in particular, camou

flage through background matching, where the animal’s body

coloration matches the visual background (Edmunds 1974; Endler

1978). For example, several species of octopus demonstrate

dynamic background matching when moving slowly over changing

substrates (Hanlon et al. 1999) and mimic various venomous

animals when moving more quickly or encountering specific

predatory threats (Hanlon et al. 1999; Norman et al, 2001). Specific

predators have been seen to elicit different colour change

responses in other species too. For example in the neotropical

treefrog, Dendropsophus ebraccatus, colour pattern changes that

enhance warning, misleading or cryptic coloration are all possible

(Touchon & Warkentin 2008). In juvenile pumpkinseed sunfish,

Lepomis gibbosus, the opercular tab marking faded when presented

with the image of a predator (largemouth bass, Micropterus sal

moides; Rowland 1999).Colour change according to background is particularly well

known for fishes and has been studied since the 1930s. These early

experiments showed that mosquitofish, Gambusia patruelis (now

G. affinis) changed their body colour (becoming darker or lighter) to

match their background environment after being kept in black or

white tanks for 72 days (Sumner 1935a, b). Furthermore, Sumner

(1935a, b) demonstrated a survival benefit from this colour

change as predators (green sunfish, Apomotis cyanellus, now

Lepomis cyanellus) were more likely to target light-coloured

mosquitofish than dark ones when trials were conducted in

a black tank. Sumner (1935b) noted that colour differences

between the two treatment groups were visibly reduced after

several hours but remained discernable (to the human eye) over

several days when the fish were placed on a common background.

These morphological colour changes are under hormonal control

(Sugimoto 2002) and last a considerable period of time, during

which the fish may have entered a different habitat where its

coloration no longer matches the visual background. However

colour change is just one of a suite of antipredator tactics and fishes

may also display behavioural responses such as habitat avoidance,

shoaling, hiding and predator inspection (Godin 1997; Kelley

2008). An effective overall antipredator response therefore

involves the integration of morphological and behavioural

defences, yet few studies have taken this approach.

We investigated the relationship between colour pattern change

and grouping (shoaling) decisions in a colourful species of fresh

water fish, the western rainbowflsh, Melanotaenia australis. First,

we induced changes in fish colour patterns by exposing individuals

to differently coloured environments (dark or pale aquaria) for

2 weeks. Second, we used image analysis to compare the photo

graphs of individuals taken before and after they were placed in the

dark/pale treatment tanks to confirm that colour pattern changes

(i.e. background matching) have occurred. Third, we performed

shoal choice trials to determine whether shoaling decisions are

based on environment-induced colour changes and, in particular,

whether individuals show a preference for shoalmates with similar

colour patterns (as predicted by the oddity effect).

METHODS

Study System

The western rainbowfish is a small freshwater fish, widespread

across northwestern Australia, and is a particularly small member

of one of the most common genera in the country (Melanotaenia

spp.). Rainbowflsh live in small, dynamic shoals, are amenable to

handling by humans, and have received attention as a suitable

study system for behavioural experiments (e.g. Brown & Warburton

1997; Brown 2002). Rainbowfish are brightly coloured and their

body coloration varies within and between populations (Allen et al.

2002).The rainbowfish used in this experiment were captured from

Wittenoom Gorge, a tributary of the Fortescue River, in the Pilbara

region of northwestern Australia in May 2006. This population is

subjected to moderate predation risk from fish predators such as

spangled perch, Leiopotherapon unicolor, and flathead gobies,

Glossogobius giuris (M. Young, personal communication). Fish were

captured as juveniles or young adults with a seine net and trans

ported to the University of Western Australia (see Ethical note for

more information). The population was maintained in mixed-sex

groups in stock tanks (85 x 45 cm, and filled to a water depth of

30 cm) until taking part in the experiments. Stock aquaria were

maintained at 26 ± 1 C with a light cycle of 12:12 h; this is

comparable to their conditions in the wild, where at the time of

capture, the water was 50 cm deep, and at 23 °C. In the wild, rainfall

and water temperature fluctuate seasonally, being moderate in

May, highest in january—February and lowest in August—September.

Stock conditions, therefore, approximated late spring or early

autumn field conditions. We used male test fish in all of our

experiments because they are larger and more brightly coloured

than females and may therefore be at greater risk from visual

predators (Brown 1999). Although male-only shoals may not

represent the situation in the wild (where female-dominated

shoals are more likely, Brown 2002), we wanted to avoid the

potential confounding effect of courtship in our trials. Furthermore,

male rainbowfish have previously been used in dichotomous choice

trials and have shown shoaling preferences for other males (Arnold

2000). After experiments all fish were returned to mixed-sex stock

tanks for breeding purposes.

Colour Change Experiment

Forty-eight male rainbowfish of between 42 and 55 mm

(mean ± SD = 49.50 ± 2.68 mm) standard body length were

anaesthetized using clove oil (dose of 80 mg/litre as for the product

AQUI-S; see Young 2009) and photographed in standard lighting

conditions with a Kodak EasyShare V1003 digital camera, set to

standard settings, before being placed in an aerated recovery tank

for a minimum of 20 mm. After recovery, these fish were allocated

to either ‘dark’ or ‘pale’ experimental treatments (N = 24 fish per

treatment), We set up six tanks (24.5 x 29 cm and 21 cm high, filled

to a depth of 17 cm) for each experimental treatment. Each tank

contained an airstone and was covered with a fine mesh to

prevent the fish from jumping between tanks. The dark and pale

environments were created by adding coloured back and side walls,

coloured gravel and a coloured artificial plant made from wool to

each aquarium. ‘Dark’ treatment tanks had black side walls and

gravel, and a dark brown back wall and artificial plant. ‘Pale’

treatments had white gravel and walls, and a cream-coloured

artificial plant. One wall was not coloured to allow monitoring of

the condition of the fish. Natural rainbowfish habitats contain

substrates (gravel, boulders, silt, plant and algal material) of various

colours and shades. These colour treatments represent the

extremes of natural colours of different microhabitats.

All aquaria were maintained at 26 ± 1 C under identical

lighting conditions, with a light cycle of 12:12 h light:dark. Fish

were fed flake food daily. Four males were placed into each

experimental tank and we ensured that each fish could be indi

vidually identified by size. All males in each experimental aquarium

had previously been housed in the same stock tank as each other

and hence were potentially familiar with one another. As we

observed some male—male aggression during the experiment, we

G.M. Rodgers et at / Animal Behaviour 79 (2010) 1025—1030 1027

also added four (nonfocal) females to each aquarium to create morenatural social conditions. These females played no further part inthe experiments. Some aggressive males were removed during theexperiment (see Ethical note), leaving 21 for the pale treatment and17 for the dark treatment. Experimental fish were photographedagain (following the procedure above) after they had spent 1 weekin the pale or dark treatment tanks.

‘Before’ and ‘after’ colour treatment photographs were identifled for the same individuals based on size differences between thefish in each treatment tank. Photographs were then analysed usingtwo image analysis software programs: lmageTool Uthscsa version3.0 (http://ddsdx.uthscsa.edu/dig/itdesc.html) for converting togreyscale and counting black and white pixels, and lmageJ 1.38x(http://rsbweb.nih.gov/ij/index.htrnl) for measuring sizes, standardizing white balance, selecting relevant image sections andpixels darker than standard ‘black’. Neither program could performall of these operations, so both were necessary. Images were firststandardized for white balance, and then converted to greyscale.The percentage of body colour that was darker than a standard‘black’ (a value of 70 on a 0—255 scale where 0 is ‘true’ black) wasmeasured (hereafter referred to as ‘black coloration’). Digital imageanalysis has previously been used for analysing colour patterns inanimals (e.g. Touchon & Warkentin 2008) and this method providesa simple way of summarizing changes in lightness without focusingon a particular animal’s visual system (Bennett et al. 1994; Stevenset al. 2007). Black was chosen after initial observations (of fishassigned to the ‘dark’ treatment tanks) indicated that body coloration became darker, and the extent of black pigmentationincreased. Indeed, changes in the dispersion of melanin (responsible for dark pigmentation) is a typical response of fishes tochanges in background coloration; on a light background melaninis aggregated within the chromatophores, making the colourpatterns appear paler whereas on a dark background the melanin isdispersed, giving the fish darker pigmentation (Sugimoto 2002).

Shoal Choice Experiment

Fish were returned to their experimental aquaria (in theirprevious colour treatment tanks) where they remained for a furtherweek. After these 2 weeks in the dark and pale experimental tanks,the male fish were used in binary choice trials (females played nofurther part in the experiment and were returned to stock aquaria).We did not notice any further colour change as a result of thesecond week spent in the dark/pale experimental treatment tanks.Individual fish from both colour treatments (dark: N = 17; pale:N = 16) were presented with a choice between two shoals of threefish: one shoal from the dark treatment and one shoal from the paletreatment, in a standard binary choice arena (Brown 2002) adaptedfrom Wright & Krause (2006). Fish used in these experiments hada mean body depth (measured at the deepest part of thebody) ± SD of 1.49 ± 0.129 cm, The choice tank measured85x45 cm, and was filled with conditioned water to a depth of10 cm above the gravel substrate, allowing test fish adequate spaceto swim, Each tank contained brown gravel identical to that in thestock tanks, to a depth of 5 cm, and two transparent stimulus shoalcylinders (10 cm diameter). The stimulus shoal cylinders wereperforated to allow chemical cues from the stimulus shoals to passinto the rest of the water, and positioned at opposite ends of thechoice tank, so that their centres were 20 cm from the tank end.Each cylinder was surrounded by a 10 cm preference zone (equivalent to two standard body lengths) which results in a conservativeestimate of shoaling tendency (Pitcher & Parrish 1993). The preference zones were marked with depressions in the gravel.

In each trial, a dark stimulus shoal was placed into one of thecylinders and a pale stimulus shoal in the other. Within a shoal, the

three fish were taken from a single experimental tank, and weensured that the fish in the two stimulus shoals had originally beensourced from the same stock tank. Thus, all fish within a stimulusshoal would have potentially been familiar with one another, andmay also have been familiar with the opposite-coloured stimulusshoal. The test fish had not been housed in the same experimentalor source tank as any of the fish in stimulus shoals, and was thusunfamiliar with both shoals. After the stimulus shoals had beenadded to the cylinders, and given 5 mm to acclimatize, the test fishwas introduced in a net to the centre of the choice tank.

Each trial began after the test fish had visited both stimulusshoals (swum inside each preference zone) and returned to theneutral zone. Trials lasted 10 mm. Cumulative time in each preference zone was measured using stopwatches, and one observer madeall recordings. Half of the water in the binary choice tank waschanged after each trial, to reduce the build up of olfactory cues.After the trial, fish were returned to their experimental tank. Fishthat had previously been used as stimulus fish were not later reusedas test fish, but test fish could later be reused as stimulus fish. Malesappeared to retain their dark/pale colour patterns (according to theirexperimental treatment) for the duration of the experiment.

Statistical Analysis

Data were analysed using the statistical analysis programR version 2.6.0 (R Core Development Team, Vienna, Austria).Changes in fish colour patterns were analysed with a general linearmixed-effects model (LME) with ‘before’ treatment colour patterns,colour treatment (dark/pale) and standard body length as explanatory variables. Fish identity (ID) nested in tank ID were randomfactors, controlling for the use of multiple fish from the same tank.Two-tailed t tests were used to test for differences in the colourpatterns of fish both before and after their allocation to the dark/pale treatment tanks. For the shoal choice trials, we calculated theproportion of time spent with each colour shoal, which was thenangular transformed to meet the assumptions of normality. Thiswas also analysed using a general linear mixed-effects model withstandard body length and change in body colour as explanatoryvariables, and fish ID nested in tank ID as a random factor.

Ethical Note

This work was approved by the University of Western AustraliaAnimals Ethics Committee. We ensured minimal stress to the fishduring transport by using fish transport bags (approximately20 x 30 cm) that come lined with clove oil, which is an effectivesedative for these fish (Young 2009). Up to 12 fish were placed ineach bag which was filled with one-third water (containinga conditioning treatment, Armour Coat, Aristopet, Eagle Farm, QLD,Australia) before being placed in an insulated polystyrene box, andtransported to the University by vehicle.

During the experiments, we observed no mortality or otheradverse effects as a result of the anaesthesia and photographyprocedures. During the colour change experiment, tanks weremonitored four times daily for signs of ill health or aggression.Male—male aggression was observed in four of the 12 treatmenttanks. In these cases, any victims of the aggression (identified bydamage to tail and fins; torn fins as a result of ‘nipping’) wereremoved as soon as any damage was noted, and housed singly intanks with water containing Armour Coat, until recovered. Finsdamaged in this way grow back in a matter of weeks with no lastingdamage to the fish. Three fish were removed from the ‘pale’treatment tanks and seven from the ‘dark’ treatment tanks. Three ofthese seven males were from a single ‘dark’ treatment tank inwhich high levels of aggression were observed. In this case all four

1028 G.M. Rodgers et al. /Animal Behaviour 79(2010) 1025-1030

male fish were removed and isolated to allow recovery of the

victims. All victims of aggression recovered after removal from the

treatment tanks and no mortality occurred.

RESULTS

Colour Patterns

Before we placed test males in experimental colour tanks, fish

that had been allocated to the pale treatment did not differ in

percentage black body colour from those allocated to dark treat

ments (t355 —0.575, P= 0.569; Fig. 1). Males showed consider

able variation in the percentage of black pigmentation on the body

(range 1.83—50.06%; mean ± SD 16.46 ± 13,58%, N 48). These

data were positively skewed, with the majority of males having

<20% black pigmentation (median = 11.38%).

Following the week housed in experimental colour tanks, there

were significant effects on colour pattern change of colour treat

ment (LME: F10 192.777, P < 0.0001), but not of standard body

length (LME: F24 = 3.736, P 0.065). Fish that had been in dark

treatment tanks had increased their black coloration (t31,8 —7.173,

P < 0.0001), and those in pale tanks had reduced it (t3o0 3.502,

P = 0.002; Fig. 1). Overall, fish that had been kept in dark treat-

merits now had significantly more black pigmentation than those

kept in pale treatments (t254 12.1201, P < 0.0001). Examples of

this colour pattern change can be seen in Fig. 2.

Shoal Chofce

We found that fish from both the dark and pale treatments

showed a significant preference for shoalmates displaying similar

colour patterns (i.e. levels of black pigmentation). Fish from dark

treatments preferred to shoal with others from the dark treatment

(LME: F12 = 10.729, P = 0.007), and those from the pale treatments

preferred to shoal with others from the pale treatment (LME:

F11 =8.304, P= 0.015; Fig. 3). Change in body colour was not

a significant predictor of social preference.

DISCUSSION

We have demonstrated that changes in the visual background

influence the colour patterns and shoaling behaviour of the

western rainbowfish. Rainbowfish exposed to dark aquaria dis

played a higher proportion of black pigmentation in their colour

patterns and preferred to associate with other darkened fish.

Likewise, fish exposed to pale aquaria reduced the level of black

pigmentation in their colour patterns and showed a preference for

shoalmates with lighter colour patterns. This is consistent with

classic work on colour pattern changes according to background

(e.g. Parker 1948) and the predictions of the oddity effect in

showing that individuals prefer shoalmates with colour patterns

similar to their own (McRobert & Bradner 1998; Engeszer et al.

2004; Rosenthal & Ryan 2005; Gómez-Laplaza 2009). Our experi

ments combine two antipredator strategies and show that

morphological colour pattern changes can have an important

bearing on subsequent behavioural (shoaling) decisions.

Changing colour patterns is one way in which prey fishes can

allow their coloration to serve multiple functions, for example

increasing colour pattern conspicuousness to communicate with

mates and competitors and enhancing crypsis to avoid detection by

predators. However, behaviour plays a critical role in determining

how colour patterns are perceived by both conspecifics and pred

ators. Morphological colour pattern changes, which occur over

a relatively long period of time (cf. physiological colour changes),

may be disadvantageous if prey move between different visual

backgrounds faster than they can change colour. Furthermore, even

if the background environment is homogeneous, changes in the

light environment (e.g. diurnal fluctuations) will alter the visual

properties of the prey’s colour pattern and its background, poten

tially reducing the level of background matching (Ruxton et al.

2004). In these situations, prey may either need to adopt other

antipredator strategies to reduce their level of predation risk, or

they may achieve ‘behavioural background matching’ by choosing

a substrate that is most similar to their own coloration.

Endler (1978) noted that an animal’s visual background can

comprise not only the habitat (substrate, open water, etc.) but also

an individual’s group mates when animals form a dense group,

such as a shoal of fish. In the current study, rainbowfish may have

achieved behavioural background matching by selecting a back

ground of shoalmates similar to their own coloration. This would

effectively increase their level of crypsis (when viewed against

a background of shoalmates) and reduce their risk of oddity (where

odd prey animals within a group are more likely to be targeted by

predators, Theodorakis 1989). We acknowledge that this change

able aspect of body coloration could also reveal an aspect of recent

habitat to conspecifics. This may be used as a cue to familiarity in

a similar way to the olfactory diet and habitat cues seen in three

spined sticklebacks, Gasterosteus aculeatus (Webster et al. 2007).

Changing colour to background match group mates and reduce

the oddity effect is an interesting idea which has received limited

attention from researchers. Cheney et al. (2008) showed that blue-

striped fangblennies, Plagiotremus rhinorhynchos, rapidly changed

colour (within 30 mm) to mimic juvenile cleaner fish, Labroides

dimidiatus, allowing them to attack reef fish (feeding off dermal

tissue and scales) that visit cleaner stations. However, the nonmi

metic coloration of the fangblennies resembled the colour patterns

of other species, for example blue-green chromis, Chromis viridis,

which often occur in the same shoal. Crook (1999) observed the

shoaling decisions of juvenile bullethead parrotflsh, Chlorurus sor

didus, which are able to change their colour patterns within

seconds or minutes. Solitary fish typically chose shoals containing

other juvenile parrotfish with similar colour patterns and only 4% of

fish were observed to change colour after joining a shoal (Crook

1999). These studies suggest an interesting trade-off between

behavioural and physiological background matching.

The nature of this trade-off has been investigated in two closely

related species of salamander that differ in their ability to change

C

C

‘CC

U

***.

Ij

Before After

Figure 1. Percentage ‘black’ body coloration before and after being housed for I week

in pale- (white bars) and dark-coloured habitats (grey bars). < 0.001: <0.01.

Error bars indicate ±1 SE.

GM. Rodgers et at / Animal Behaviour 79 (2010) 1025—1030 1029

‘ 600,

50,0,0

40

5)

5)

Figure 2. Examples of fish body colour after 1 week in (a) dark and (b) pale treatment tanks. Images not standardized for white balance,

colour (Garcia & Sih 2003). The species showing the greater experiments, the oddity effect did not persist in larger groups, thatcapacity for colour change (Ambystoma barbouri) did not alter its is, odd prey in shoal sizes of 15 fish were not more vulnerable thanbehaviour according to its colour patterns but showed a preference common prey types: however, work using computer simulationsfor dark substrates followed by a colour change (becoming darker). has found no evidence that the oddity effect is confined to smallerIn contrast, A. texanum (which has limited colour change ability) groups (Ruxton et al. 2007). The oddity effect operates in systemsdisplayed behavioural background matching and preferred where predators display a preference for rare prey (positivesubstrates that were most similar to its own coloration. Further- frequency-dependent selection). However, if predators are lessmore, use of a refuge under predation risk was dependent on body likely to detect and attack rare prey (for example because of lack ofcolour for A. texanum (which spent less time in a refuge when its experience), rare prey types have higher fitness (Ruxton et al.level of background matching was high) but not for A. barbouri 2004), In this case, rare prey may reduce their risk of predation(Garcia & Sih 2003). This demonstrates how antipredator behav- by remaining solitary rather than joining a group comprisingiours in prey are influenced by both immediate levels of coloration common prey types. Grouping decisions are therefore contingentand the potential for colour pattern change. on the proportion of odd prey in the population, which in the case

The relationship between predation risk and group composition of background matching may reflect the heterogeneity of the local(i.e. the proportion of odd prey) is also influenced by group size. habitat.Experiments with silvery minnows, Hybognathus nuchalis, and Morphological colour pattern changes may be important inlargemouth bass predators showed that solitary minnows were allowing individuals to adapt to seasonal changes in their lightalways captured by bass whereas attack success was reduced to 50% environment. In rainbowfish habitats, for example, changes in theif an odd individual was in a group of eight (Landeau & Terborgh light environment may be associated with increased water1986). However, shoals containing a few odd prey received more turbidity during the cyclone season. The resulting colour patternattacks than homogeneous shoals, suggesting that the other group changes could have implications for dispersal and mate choice, ifmembers incur a cost through accepting odd shoalmates. In these for example individuals become restricted to a particular habitat (in

which they are background matched) and become limited in theirchoice of mates. Although restrictions on dispersal are an important mechanism of speciation (Wilson & Hessler 1987), a recentstudy of coastrange sculpin, Cottus aleuticus, found that divergencein background matching coloration was due to morphologicalplasticity rather than genetic diversity (Whiteley et al. 2009).

Colour pattern changes also serve as important social and sexualsignals in many species of fish (Shibatta 2006; Korzan et al. 2008).For example, colour pattern changes are used as a signal of subordination during aggressive interactions in Atlantic salmon, Salmosolar (O’Connor et al. 1999). Assortment based on colour patternsmay therefore be complicated by the role that colour plays in othersocial interactions, leading to interesting trade-offs between theantipredator benefits of colour pattern matching, and the potentialadvantages associated with honest signals of social status (Keys &Rothstein 1991). Observations made during the current study

* suggest that black coloration may play a role in social dominance inDark Pale western rainbowflsh, possibly signalling dominance status, which

Colour treatment has an effect on group organization and composition in manyspecies. This would be consistent with findings from other specieswhere melanic forms are more aggressive (Price et al. 2008).

In summary, rainbowflsh displayed morphological backgroundmatching after being exposed to different light environments.

I30

20

Figure 3. Percentage time spent shoaling with the dark stimulus shoal, The dashedhorizontal line represents no preference, above the line represents a preference for thedark stimulus shoal and below the line represents a preference for the pale stimulusshoal, Error bars represent ±1 SE,

1030 G.M. Rodgers et aL / Animal Behaviour 79 (2010) 1025—1030

Subsequent shoaling decisions were based on these colour patternchanges with individuals showing a preference for similarly coloured, background-matched shoalmates. These combinedprocesses of morphological and behavioural background matchingamount to a sophisticated suite of colour-mediated antipredatordefences.

Acknowledgments

We thank Cameron Duggin for practical advice and assistancewith fish husbandry, Mike Young for useful information on thestudy species, Stuart l-lumphries for useful discussions, Jens Krause,Jolyon Faria, Steven Sait, Ben Chapman and Christos Ioannou forcomments on the manuscript, and Andy Beckerman for supportand encouragement. Comments from two anonymous refereesimproved the manuscript tremendously. This work was funded bythe Royal Society, Company of Biologists, British Ecological Society,NERC, BBSRC and the University of Western Australia.

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