Oceanography and Marine Biology: An Annual Review (Volume 43) - Chapter 9 pot

Aggressive mimicry appears to be themost prevalent type of mimicry overall in coral reef fishes, constituting 48% of all cases reported to date, followed by Batesian 40% and social mimic

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Oceanography and Marine Biology: An Annual Review, 2005, 43, 455-482

Taylor & Francis

ECOLOGY AND EVOLUTION OF MIMICRY

IN CORAL REEF FISHESEVEN MOLAND,* JANELLE V EAGLE & GEOFFREY P JONES

School of Marine Biology and Aquaculture, James Cook University,

Townsville, 4811 Queensland, Australia

*E-mail: even.moland@graduates.jcu.edu.auAddress correspondence to: Even Moland, Carsten Ankersgt 11, N-1524 Moss, Norway

Abstract This review examines the literature on mimicry in coral reef fishes and evaluates theprevalence of mimicry in different taxa, its ecological consequences and postulated modes ofevolution Mimicry appears to be a widespread and common phenomenon in coral reef fishes, withapproximately 60 reported cases Although many are largely anecdotal accounts based on colourresemblance, recent quantitative comparisons and experimental manipulations have confirmed thatmany do represent mimic-model relationships The distribution of mimics and models among reeffish families appears largely serendipitous Mimics are most common in the families Blenniidae,Serranidae and Apogonidae and models in the families Pomacentridae, Blenniidae and Labridae.Mimics and model species usually represent less than 10% of species within families, althoughimperfect forms of mimicry are likely to have been underestimated Mimicry appears to be partic-ularly important during juvenile stages, with 28% of mimic species losing their mimic colourationwhen they outgrow their models All cases of mimicry support predictions that mimics are rarerelative to their models Furthermore, the abundance of mimics in different areas may increase inproportion to model abundance The spatial distribution of mimics appears to be limited by that oftheir model species, although some change models in different habitats or in different parts of theirrange Many mimics live in close association with their models, and both foraging advantages andpredator avoidance have been experimentally demonstrated Aggressive mimicry appears to be themost prevalent type of mimicry overall in coral reef fishes, constituting 48% of all cases reported

to date, followed by Batesian (40%) and social mimicry (12%) Müllerian mimicry seems to berare, although it may contribute to the mimetic complexes involving members of the blenniid tribeNemophini However, these traditional classifications are too simplistic for reef fishes because bothforaging advantages and predator avoidance can apply in a single mimetic relationship, and theirrelative importance has not been evaluated Preliminary data suggest a high degree of phenotypicplasticity in mimetic colouration and little genetic differentiation among different mimics of thesame species Overall, the review highlights the many significant steps that need to be taken towards

a more complete understanding of the ecological and evolutionary significance of mimicry in coralreef fishes

Introduction

The phenomenon of mimicry, where one species evolves to closely resemble another, has arisenmany times throughout the plant and animal kingdoms (Wickler 1965, Turner 1977, Gilbert 1983,Malcolm 1990, Mallet & Joron 1999) The evolution of mimicry occurs in response to selective

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EVEN MOLAND, JANELLE V EAGLE & GEOFFREY P JONES

pressures favouring individuals that are able to disguise their identity by masquerading as anotherspecies The study of mimicry began in the mid-1800s, with most of the theory developed fromfield studies on terrestrial animal groups, most notably butterflies Despite this long history ofinterest, the prevalence of mimicry, its ecological significance and mechanisms of evolution haveyet to be evaluated for many animal groups

The proposed fitness advantage of mimicry depends upon who is being deceived Four differenttypes of mimicry have been traditionally recognised In Batesian mimicry, harmless and palatablespecies closely resemble unpalatable or venomous species usually avoided by predators (Bates1862) In Müllerian mimicry, two unpalatable species share similar colour patterns and thusreinforce their predator deterrence (Müller 1879) In aggressive mimicry, a predatory speciesresembles a harmless or beneficial species and thus achieves increased opportunities for foraging

by deceiving prey (Wickler 1965, 1968, Malcolm 1990) Social mimicry, proposed for birds byMoynihan (1968), refers to examples of mimics that associate with similarly coloured individuals

in order to escape the attention of predators Despite these relatively well-defined categories, theunderlying bases of many mimic-model relationships are poorly understood

Mimic-model systems are thought to share a number of defining ecological characteristics thatshould apply if mimicry is to provide a fitness advantage Mimic species must be rare comparedwith their model species because the deception will not work if the predators or prey that are beingdeceived encounter too many mimics and learn from these experiences (Bates 1862) Mimics shouldalso occupy the same habitat (Randall & Randall 1960) and geographic range as the model (Turner

1977, Thresher 1978) so that signal receivers are able to recognise them Across this range, variation

in the mimic should match any geographic variation in the model (Turner 1977, Thresher 1978)

or change to other model species with complementary ranges (Gilbert 1983, Mallet & Joron 1999).Mimetic species should also alter their behaviour from that characteristic of their taxonomic group

to enhance resemblance to their models (Snyder 1999) These basic ecological patterns are untestedfor most presumed cases of mimicry If such relationships hold, the distribution and abundance ofmimics will be closely tied to that of their models An understanding of the ecological relationshipsbetween mimics and models is critical to assessing its ecological significance and underlyingevolutionary mechanisms

The potential significance of mimicry in coral reef fishes was first recognized by Randall &Randall (1960) who drew attention to many of the examples that are well known today Manyadditional cases have been reported over the last four decades, suggesting that mimicry may be arelatively widespread phenomenon on coral reefs (Russell et al 1976, Siegel & Adamson 1983,Kuiter 1995, Snyder 1999, Snyder et al 2001) However, despite the increasing records, there havebeen relatively few studies specifically addressing the causes and consequences of mimicry in reeffishes Much of the evidence for mimicry in the early literature on coral reef fishes was anecdotal,based on colour resemblance and observer intuition This is gradually being superseded by morerigorous observational studies addressing the criteria necessary to establish mimicry (e.g., Snyder

1999, Eagle & Jones 2004) and experimental studies establishing cause-effect links between mimicand model species (e.g., Springer & Smith-Vaniz 1972, Caley & Schluter 2003, Munday et al

2003, Moland & Jones 2004) Although there have been a number of reviews of different kinds ofmimicry in fishes that include coral reef species (Randall & Kuiter 1989, Randall & McCosker

1993, Sazima 2002a,b) there have been no recent reviews evaluating the prevalence of and evidencefor different types of mimicry in coral reef fishes Early reviews of the ecology of reef fishes arguedthat mimicry could have important implications (Ehrlich 1975, Sale 1980) but in recent texts thistopic has received virtually no attention (Sale 1991, 2002)

The prevalence of mimicry within a community can be difficult to assess Descriptions ofmimicry usually focus on the more spectacular and specialized mimics that are striking to theobserver, which may lead to an underestimate of its importance (Russell et al 1976) Three clear

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MIMICRY IN CORAL REEF FISHES

examples are the similarity of the blenny Aspidontus taeniatus to the cleaning labrid Labroides dimidiatus (Eibl-Eibesfeldt 1959, Randall & Randall 1960) (see Figure 1A,B, in the colour insertfollowing page 278), the similarity of the monocanthid Paraluteres prionurus to the unpalatabletetraodontid Canthigaster valentini (Tyler 1966, Caley & Schluter 2003) (Figure 1C,D, see colourinsert) and the similarity of the harmless blenny Petroscirtes breviceps to the blenny Meiacanthus grammistes which possesses a venomous bite (Smith-Vaniz et al 2001) (Figure 1E, see colourinsert) Few would dispute that these are mimic-model pairs The problem begins when the coloursimilarities are not so striking to the observer Theory predicts that both good and poor mimics canevolve in different situations (Lindström et al 1997, Edmunds 2000, Sherratt 2002); however,distinguishing poor mimics from fortuitous resemblance can be a challenge Recent experimentalstudies (Munday et al 2003) suggest that there can be a strong association between similarlycoloured reef fishes that would not be considered obvious cases of mimicry In addition, what thehuman eye records as identical may be very different from what the fishes actually perceive(Marshall 2000)

Coral reef fishes may provide a challenge to the assumption that mimicry can be neatly classifiedaccording to one of the four established evolutionary mechanisms For example, cleaner wrassemimics may be unique among all known cases of mimicry They are primarily thought to beaggressive mimics, increasing their feeding opportunities when, masquerading as cleaner wrasses,they remove scales or chunks of flesh rather than parasites from the bodies of their ‘customers’(Randall & Randall 1960) However, they may also benefit from a special type of anti-predationmechanism Cleaner wrasses are afforded an ‘amnesty’ from predators because of the parasiteremoval service they provide Cleaner wrasse mimics may also benefit from this amnesty, thusgaining the dual advantages of both an increase in feeding and a decrease in predation (Kuwamura1983)

The overall aims of this review are to examine the current literature on the prevalence ofmimicry in coral reef fishes and to evaluate its ecological and evolutionary significance In particular,the degree to which reef fishes conform to a body of theory largely developed to explain mimicry

in terrestrial animals is evaluated and the evidence for different types of mimicry in coral reef fishescritically assessed Specific questions that are addressed include: How prevalent is mimicry in coralreef fishes? Which families of coral reef fishes are involved in mimetic relationships, what is theprevalence of mimicry within these families, and within species, what life history stages areinvolved? What is the relationship between the distribution and abundance of mimics and models?

Do the geographic ranges of mimics and models coincide, are mimics rare relative to their modelsand do mimics and models influence each other’s abundance? What is the evidence for the fourwidely recognised types of mimicry (Batesian, Müllerian, aggressive and social) in reef fishes? Doreef fishes conform to this classification, which type of mimicry is most important, or is the evidenceinadequate to reach this conclusion? Finally, which research directions must be taken to completeour understanding of the ecology and evolution of mimicry in reef fish communities?

Prevalence among reef fishes

Taxonomic distribution

Approximately 60 species in 16 families have been reported to mimic other coral reef fish species(Figure 2A) Three speciose families (Blenniidae, Serranidae and Apogonidae) are disproportionatelyrepresented, accounting for about two-thirds of the reported cases Nine families are represented

by only a single mimetic species The proportion of species in each family that are mimics isusually quite low (<10%) The exception appears to be the Nemipteridae, where 27% of speciesare mimetic at some stage in their life history Mimicry is least prevalent in the two of the most

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speciose of coral reef fish families, the Pomacentridae and Labridae, with one and three mimicsrepresenting 0.3% and 0.8% of their total species diversity, respectively Many reef fish familiesthat are characteristic of coral reefs (e.g., Chaetodontidae, Pomacanthidae and Scaridae) are notablyabsent from the list of mimics The taxonomic distribution of mimicry appears largely serendipitousand it has evolved independently on numerous occasions

The models for mimetic species are also found in a wide range of reef fish families (Figure 2B).However, the taxonomic distribution of mimics and models is quite different, with approximately

Figure 2 (A) Prevalence of mimicry in coral reef fish families involved in mimetic relationships, (B) lence of species functioning as models in the same families Percentages represent proportion of mimics and/or models within each family Number of mimics and models are drawn from the literature Percentages were calculated using information on species diversity derived from Bellwood (1997) and Munday & Jones (1998).

Po

m a

a nthidae Chaetodontidae Scorpaeni

dae

Atherinidae Muraen idae

Mona

canthidae Chaenopsi dae

Po

m ace

ntridae Mullidae Carang idae

Malacanthidae Plesiopidae Pseudoc

hr omidae Acanthuridae Gob

iidae Lab rid ae

Lutjanidae Nemipteridae Apogonidae Serr ani dae Blenniidae

P omacanth

idae

Chaetodontidae Sco

rpaenidae

A therinidae Muraenidae Monacanthid

ae

Chaenopsidae

P omacentr

idae Mullidae Car angidae Malacanthidae Plesiopidae Pseudoc

hr omidae Acanthuridae Gobii

dae Labrid ae

Lutjanida e

Nem

ipteridae Apogonidae Serranidae Blenniidae

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three-quarters of model species found in the families Pomacentridae, Blenniidae and Labridae Theproportion of species in these families that serve as models is also low (<10%) and for nine familiesthere is only one species that is a model Only the families Blenniidae and Serranidae includerelatively high numbers of both mimics and models

Around three-quarters of mimetic relationships involve one mimic and one model species.However, there are cases where a model has more than one mimic (Figure 3A) and cases where amimic has more than one model across its geographic range (Figure 3B) There are several cases

of mimetic species having four or more models For example, juvenile Lutjanus bohar mimic fourdifferent Chromis species (Russell et al 1976, Moyer 1977) and the two labrids Oxycheilinus diagrammus and Epibulus insidiator (Ormond 1980) Some model species appear to be soughtafter, such as the cleaner wrasse Labroides dimidiatus, which is mimicked by three blennies, Aspidontus taeniatus, A filamentosus and Plagiotremus rhinorhynchos (Randall & Randall 1960,Wickler 1961, Springer & Smith-Vaniz 1972, Kuwamura 1983) Other cases of several mimics to

a single model include the mimetic complex (‘mimicry rings’) centred on each of the fangblennies

Meiacanthus nigrolineatus, M oualanensis and M vittatus (Smith-Vaniz et al.2001)

Body size and ontogenetic patterns

Mimicry appears to be particularly important in small coral reef fishes and for larger fishes, mimicry

is confined to the juvenile stage Of the 60 mimetic species reported to date, 17 (28%) are mimetic

Figure 3 (A) Number of mimic species per model and (B) number of model species per mimic Percentages represent the prevalence of the different relationships.

0 5 10 15 20 25 30 35 40 45 50

Number of model species per mimic

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only as juveniles (Figure 4) These species appear to lose mimetic colouration when they grow to

a larger size than their model species (Sazima 2002a, Eagle & Jones 2004, Moland & Jones 2004)

In the family Serranidae, the seven species mimetic throughout ontogeny are the small hamlets,

Hypoplectrus spp (Randall & Randall 1960, Thresher 1978), which grow to a maximum size of

13 cm (Lieske & Myers 1996) In contrast, the seven species that are mimetic only as juvenilesare all epinepheline groupers (Russell et al 1976, Randall & Kuiter 1989, Kuiter 1995, Snyder

1999, Snyder et al 2001) that reach a much larger body size ranging from 52–110 cm depending

on the species (Lieske & Myers 1996)

The blenniid Meiacanthus nigrolineatus is interesting because it starts life first as a mimic,then itself becomes a model It is a social mimic of several Cheilodipterus spp (Apogonidae) as

a juvenile (Dafini & Diamant 1984) As an adult, it serves as a model in Batesian and aggressivemimicry for the blenniids Ecsenius bicolor and Plagiotremus townsendi, respectively (Springer &Smith-Vaniz 1972, Smith-Vaniz et al 2001)

Ecological patterns and consequences

Rarity and local abundance

There is surprisingly little published data on the relative abundance of mimic and model species(Figure 5) Generally, reef fishes conform to the prediction that mimetic species must be rare relative

to their model species (Bates 1862) However, while mimic species are usually less abundant thantheir models, the percentage of mean abundance per site ranges from 1–78% of the abundance oftheir model species (mean 29.3% ± 7.3%)

Recent quantitative studies suggest that the abundance of mimics is influenced by the abundance

of their models Eagle & Jones (2004) showed that the densities of Acanthurus pyroferus, a mimicduring its juvenile stage, are promoted by the abundance of one of its models, Centropyge vroliki.The abundance of mimics (juveniles) increased in proportion to increased abundances of the model

at spatial scales both within and among reefs Similarly, Moland & Jones (2004) found a positiverelationship between the mimic Plagiotremus rhinorhynchos and its model Labroides dimidiatus

Figure 4 Frequency of mimicry in juveniles vs mimicry throughout life history for all coral reef fish families with mimetic species.

0 2 4 6 8 10 12 14 16 18 20

Bl e n iidae Serranidae A pog onidae Nem

ipteridae Lutjanidae LabridaeGo

b ii

d a

A canth urid ae

Pseudoc

h ro

m idae Plesiopidae

M ala

canthidae

C arangidae Mu llidae

Po

m acentridae Chaeno

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If this proves to be a trend for a number of mimetic relationships, especially those involving juvenilemimics, then mimicry could be of vital importance for survival of some species through the morevulnerable ontogenetic stages

Geographic range and local distribution

Reef fishes also conform to the prediction that mimetic species should occupy the same habitatand geographic range as their model species, or change to other model species in other habitats or

Figure 5 Relative abundance of coral reef fish species in proposed model-mimic relationships White bars = model species Black bars = mimic species N = number of sites Percentages represent average mimic to model ratio per site References at top of each panel refer to the study in which each example of relative abundance between model and proposed mimic was reported.

Moland & Jones 2004 N=10

8 7 6 5 4 3 2 1 0

Seigel & Adamson 1983

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parts of their range (Thresher 1978, Gilbert 1983) Spatial concordance between mimics and theirmodels appears to apply across a range of spatial scales including: (1) regional geographic ranges;(2) local ranges within regions and (3) depth and microhabitat ranges within locations A goodexample of multiscale spatial relations can be seen in the mimic surgeonfishes In the Indian Ocean

Acanthurus tristis juveniles are mimics of the pygmy angelfish Centropyge eibli (Kuiter & Debelius1994) In the Indo-Pacific, juveniles of the sister species Acanthurus pyroferus mimic three different

Centropyge species, C vroliki, C heraldi and C flavissima (Randall & Randall 1960, Myers 1989,Kuiter 1996)(Figure 6, see colour insert) In general C vroliki is found in the central Indo-Pacific,

C flavissima is most abundant on coral atolls of the far Eastern Pacific and C heraldi is in between.There is, however, a very large area where the ranges of all three Centropyge model species for

Acanthurus pyroferus overlap (Allen et al.1998) It is unclear what determines the model speciesthat A pyroferus mimics in the area of overlap but it may be separation among the species at localscales within this region For example, whereas all three model species are reported from the GreatBarrier Reef, Centropyge vroliki is widespread but most abundant in inshore areas (Eagle, unpub-lished data), C flavissima is commonly seen in northern offshore areas and C heraldi is uncommon,occurring only occasionally on outer reefs and in the Coral Sea (Australian Institute of MarineScience Monitoring Team, unpublished data)

The adopted model species may also reflect the depth distributions of potential model species.There are many sympatric Centropyge species found across the geographic range of Acanthurus pyroferus that are not mimicked The four model Centropyge species are closely related sister taxa,known to hybridise where their boundaries overlap (Allen et al 1998, Debelius et al 2003).Furthermore, they are all shallow water species, found at their highest abundance closest to thereef crest relative to their congeners (Allen et al 1998, Eagle et al 2001) Eagle & Jones (2004)propose that this case of mimicry has evolved in part so that Acanthurus pyroferus juveniles candeceive aggressive territorial herbivorous fishes and gain access to algal food resources on the reefcrest If this is the case, mimicking Centropyge species that inhabit deeper microhabitats on thereef would be of no benefit

Mimics appear to be able to expand their distributions by changing to different model species

in different habitats For example, juvenile Anyperodon leucogrammicus are aggressive mimics ofcongeners Halichoeres biocellatus, H purpurascens and H melanurus (Russell et al 1976,Randall & Kuiter 1989) These three wrasses have disjunctive distributions along both depth andexposure gradients (Jones et al unpublished data) Hence, by mimicking all three species, Anyperodon leucogrammicus may increase the habitat and area that it is able to utilise Similarly, Pseudochromis fuscus is an aggressive mimic of Pomacentrus adelus, P amboinensis, P chrysurus and

P moluccensis, four damselfishes that are found at different depths and in different microhabitatsbut in the same reef areas (Munday et al 2003)

Other mimics with more restricted geographic ranges, but which overlap broadly in depth andmicrohabitat, mimic a range of species from different families For example, the hamlets, Hypoplec- trus spp., are aggressive mimics found only in the Caribbean that mimic species of angelfishes,wrasse and damselfishes The subset of microhabitats used by each species closely mirrors that oftheir respective models (Thresher 1978)

Overall, the nature of the spatial relationship between mimics and models is likely to depend

on many factors including the type of mimicry and the geographic range size and habitat specificity

of both mimic and model species

Dispersion and behaviour

Recent quantitative studies have found a closespatial association between mimics and their models.Eagle & Jones (2004) found that juvenile Acanthurus pyroferus were found in local scale areas of

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reef (30 m2) inhabited by one or more fish of the model species Centropyge vroliki, more often

than would be expected if mimics were distributed at random Within this scale, mimic Acanthurus

pyroferus were never observed >2 m away from an individual of the model species Centropyge

vroliki, and 10% of the time that they were observed they were actually located at a distance of

less than 10 cm from a model fish Similarly, Moland & Jones (2004) found that Plagiotremus

rhinorhynchos mimics of the cleaner wrasse Labroides dimidiatus were often found less than 1 m

from a model fish Many published anecdotes of mimetic relationships include observations of

behavioural associations between mimics and models (e.g., Barlow 1975, Caley & Schluter 2003)

and it is likely that more in-depth studies of other model-mimic pairs may uncover similarly close

patterns of spatial dispersion This pattern suggests that just being located in a region or locality

where the model is found may not be enough to deceive most species, and that constant

reinforce-ment of the mimicry through interactions of the signal receivers with models is required

For mimicry to work, it may not even be enough to look like and be found in close proximity

to models, mimics may also need to alter their behaviour (Snyder 1999) It has been observed in

at least two cases of mimicry in coral reef fishes that mimics alter their swimming behaviour to

enhance their resemblance to their model The fins and swimming motion used for propulsion are

features that make it easy to distinguish different families of coral reef fishes underwater Eagle &

Jones (2004) have observed that when foraging as a pair with a model (Centropyge vroliki), mimic

surgeonfish juveniles (Acanthurus pyroferus) do not swim with the pectoral fin propulsion

charac-teristic of other surgeonfishes, but instead adopt the ‘wiggling’ swimming motion of angelfishes

Similarly, instead of using caudal propulsion, the juveniles of the grouper Plectropomus laevis have

been observed to fold their caudal fin, erect the front section of their dorsal spines and use their

pectoral fins in a sculling motion for propulsion in the style of the distinct posture and swimming

motion of the pufferfish Canthigaster valentini (A.M Ayling, personal communication) Further

observations of the swimming motion and behavioural characteristics of other mimics may bring

to light similar modifications for enhancing model resemblance

Types of mimicry and the evidence

There has been considerable variation in the types of evidence used to establish mimicry and

distinguish among the different types Most early published studies provide only anecdotal

obser-vations of colour similarities and speculation about the basis of the mimicry Only a few studies

quantify the ecological relationships between pairs of species (Springer & Smith-Vaniz 1972,

Kuwamura 1983, Côté & Cheney 2004, Eagle & Jones 2004) and even fewer provide experimental

evidence of the ecological advantages resulting from the mimetic relationship (Caley & Schluter

2003, Munday et al 2003, Moland & Jones 2004) No studies provide all the evidence required to

establish mimicry and at present there is no clear guide to distinguish among the different types

Here a set of criteria is established that can be used as ‘minimum evidence’ as an initial step to

identify the potential fitness advantages of mimicry and distinguish among the four recognised

types in each case observed (Table 1)

Batesian mimicry

In Batesian mimicry, harmless and palatable species closely resemble unpalatable or venomous

species usually avoided by predators (Bates 1862) Batesian mimicry has been reported for 25

species from 10 families of coral reef fishes It is most prevalent in the families Apogonidae and

Blenniidae, with five and six species, respectively (Table 2)

Batesian mimicry has been recognized on the basis of six criteria (Rettenmeyer 1970 in

McCosker 1977): “(i) a species, the model, is undesirable to predators; (ii) a second species, the

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mimic, is desirable to predators but has evolved from its ancestral appearance until it resembles

the model so closely that potential predators are deceived and leave it alone; (iii) the mimics are

less abundant than the models; (iv) the mimics are found at the same place and time as the models;

(v) both model and mimic are conspicuous or readily seen by potential predators and (vi) the

predators learn or associate undesirability with the appearance of the model” However, although

this list is comprehensive, some of the criteria are common to other forms of mimicry (Table 1)

Batesian mimicry could be postulated on the basis of just three critical pieces of evidence,

although very few studies meet all these criteria (Table 2): (1) overall resemblance between model

and mimic in shape and colour, and known non-palatability of the model, (2) known palatability

in the mimic and (3) predator avoidance in the mimic (Table 2) The first requirement establishes

visual similarity and that the model has some feature that makes it less susceptible to predation

The second requirement is crucial in ruling out the possibility of dealing with Müllerian mimicry,

in which both mimic and model are unpalatable or possess means of predator deterrence The third

requirement is important in order to establish that the visual similarity has a realised adaptive

advantage As shown in Table 2 there are only five of 25 coral reef fish species that fulfil these

criteria

Although mentioned by Whitley (1935), Clark & Gohar (1953 in Randall & Randall 1960)

and others, the first proposed case of Batesian mimicry among coral reef fishes was the filefish

Paraluteres prionurus (Monacanthidae), which is strikingly similar to the pufferfish Canthigaster

valentini (Tetraodontidae) (Tyler 1966) Model and mimic are virtually indistinguishable when

observed in the field The evidence presented in the original article is anecdotal and does not contain

records of experiments testing the palatability of the mimic or to what degree the model is

unpalatable It is now known, however, that C valentini is likely to be avoided by predators

throughout its life history because the eggs and larvae are unpalatable (Gladstone 1987) and have

toxin in their skin and inner organs (Allen et al 1975)

Caley & Schluter (2003) described the adaptive advantage gained by a mimic species as a

‘protective umbrella’ that may vary in size and shape according to the extent the mimic is protected

by its resemblance to the unpalatable model They provide an excellent demonstration of a study

designed to measure the ‘protective umbrella’ that the pufferfish C valentini provides for its mimic

Paraluteres prionurus By exposing predators to plastic models with increasingly divergent colour

Table 1 Multiple criteria to distinguish among the four recognised types of

mimicry when reporting cases of mimicry in coral reef fishes

Record of foraging on other food source than model No No Yes No

* Referring to different trends suggested for species exhibiting aggressive mimicry; Yes = species that

feed on prey smaller than themselves tend to mimic and join species harmless to their prospective prey;

No = species that feed on prey larger than themselves tend to mimic mostly beneficial species (cleaners)

(modified from Sazima 2002a).

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Table 2 Coral reef fish species reported as Batesian mimics and their putative models, with

references and the kind of evidence presented for each species

Meiacanthus vittatus Blenniidae Smith-Vaniz et al 2001 AB

Cheilodipterus zonatus Meiacanthus geminatus Blenniidae Gon 1993 AB

Fowleria abocellata Scorpaenodes guamensis Scorpaenidae Goren & Karplus 1983 AB

Fowleria sp Scorpaenodes guamensis Scorpaenidae Seigel & Adamson 1983 AB

Haemulidae

Pomadasys ramosus* Oligoplites palometa* Carangidae Sazima 2002b AB

Nemipteridae

Pentapodus trivittatus Meiacanthus crinitus Blenniidae Smith-Vaniz et al 2001 AB

Scolopsis bilineatus* Meiacanthus lineatus,

M oualanensis,

M smithi

Blenniidae Blenniidae Blenniidae

Springer & Smith-Vaniz 1972 Russell et al 1976

Blenniidae Springer & Smith-Vaniz 1972 ABC

Petroscirtes brevipes Meiacanthus grammistes,

M kamoharai,

M vittatus

Blenniidae Blenniidae Blenniidae

Smith-Vaniz 1987 Smith-Vaniz et al 2001

A

Petroscirtes fallax Meiacanthus lineatus Blenniidae Springer & Smith-Vaniz 1972,

Russell et al 1976, Vaniz et al 2001

Paraluteres arqat Canthigaster margaritata Tetraodontidae Randall & Randall 1960 AB

Paraluteres prionurus Canthigaster valentini Tetraodontidae Tyler 1966, Caley & Schluter

2003

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patterns from the model Canthigaster valentini, they showed a relatively broad region of protection

surrounding the colour pattern of the model species Predators did not approach plastic models

even roughly similar in colouration to C valentini Their findings indicate that evolution of Batesian

mimicry may begin with only moderate resemblance of a mimic to a model species and that closeresemblance evolves gradually thereafter

The broad region of protection associated with a particular colour pattern may explain less than

perfect Batesian mimics For example, small juveniles (<12 cm total length) of Plectropomus laevis (Serranidae) also resemble Canthigaster valentini, but to a much lesser degree (Randall & Hoese

1986) Future studies focusing on the experimental approach used by Caley & Schluter (2003) forother proposed cases of Batesian mimicry are needed to attain a greater understanding of howBatesian mimicry evolves in coral reef fish species

Of particular interest for studies of Batesian mimicry is the evolution of prey avoidance.Predators must instantly recognize a particular morphology or behaviour as belonging to highlytoxic or unpalatable prey species (Springer & Smith-Vaniz 1972, Smith 1975, Greene & McDiarmid1981) This avoidance is likely to be genetically ‘hard-wired’ because there is little scope forlearning from mistakes Failure to recognise unpalatable species will be fatal if the species is highlytoxic The same argument may apply to the unusual case of Batesian-type mimicry where cleaner

wrasses, such as the species Labroides dimidiatus, are afforded a special predator ‘amnesty’ due

to the parasite removal service they provide (Kuwamura 1983) Various species of blennies thatmimic this species may also benefit from this predator ‘amnesty’ Presumably a predator would

not ‘learn’ to spare L dimidiatus from consumption, there being no repercussions from eating it,

but this species is somehow innately recognised as ‘not for consumption’ Whether or not predatorshave innate avoidance of certain species based on their colour patterns would help to determinewhy some species are mimicked and others are not

Müllerian mimicry

In Müllerian mimicry, two unpalatable species share similar colour patterns and thus reinforce theirpredator deterrence (Müller 1879) Although Bates (1862) commented on the occurrence of twocommon unpalatable species with similar phenotypes, it was Müller (1879) who proposed the

Table 2 (continued) Coral reef fish species reported as Batesian mimics and their putative models, with references and the kind of evidence presented for each species

Randall & Randall 1960 Randall et al 1997

A

Acanthurus tristis* Centropyge eibli Pomacanthidae Randall & Randall 1960,

Kuiter & Debelius 2001

Notes: A = overall resemblance plus information on means of predator avoidance in model; B = known palatability in

mimic; C = record of predator avoidance in mimic Sequence of mimic families follows Randall et al (1997); genera and species in alphabetical order Species denoted by * are only mimetic or act as models in the juvenile stages Format of table modified from Sazima (2002a).

† Referring to evidence reported in Smith-Vaniz et al (2001) suggesting Batesian mimicry with elements of i) Müllerian mimicry, because some predatory fishes ingest and then reject the mimic (both dead and alive individuals) and ii) aggressive

mimicry, because the Plagiotremus spp feeds on mucus and epidermis (including scales) of other fishes.

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benefits of mimicry for pairs of unpalatable species If a constant number of unpalatable individualsmust be sacrificed per unit time to teach local predators to avoid a given colour pattern, the fractionsuffering mortality in each species will be reduced if they share a colour pattern Müllerian mimicry

is a mutualism once attained, but can be sustained as an asymmetric mutualism with unequalbenefits (Mallet & Joron 1999) However, the rare species will gain far more from a mimeticrelationship than will the more common one (Müller 1879)

Müllerian mimicry has not been proposed as the single basis for any mimetic relationshipamong coral reef fishes However, Springer & Smith-Vaniz (1972) and Smith-Vaniz et al (2001)propose examples of mixed-type mimicry that include Müllerian mimicry in several interspecificmimetic complexes Mimetic complexes are also known as ‘mimicry rings’ and involve more thantwo species (e.g., Losey 1972, Springer & Smith-Vaniz 1972, Russell et al 1976, Smith-Vaniz

et al 2001) Many of the known cases of mimetic complexes in coral reef fishes involve one ormore species of the family Blenniidae, in particular from the tribe Nemophini, the ‘sabertoothed’blennies or ‘fangblennies’ This essentially Indo-Pacific tribe of blennies derives its common namefrom an impressive pair of dentary canines, which are used in territorial threat displays or for

defensive purposes One of the five nemophinine genera, Meiacanthus, possesses a toxic buccal

gland positioned near the base of a pair of deeply grooved canines Field and laboratory experiments

and observations have revealed that members of the genus Meiacanthus can use their fangs to inject

a noxious substance that causes some predatory fishes to avoid them as potential prey (Losey 1972,Springer & Smith-Vaniz 1972)

On the basis of this predator deterrence the members of the Meiacanthus genus are reported

as models in several cases of Batesian mimicry (Table 2). However, mimics of Meiacanthus include members of another genus of the Nemophini, Plagiotremus, which possess fangs but no toxic buccal

glands In light of the definition of unpalatability “any trait that acts on predators as punishment,and that causes learning leading to a reduction in attacks” (Mallet & Joron 1999), the fangs of

Plagiotremus may be sufficient to provide some degree of predator protection Furthermore, because

predatory fishes are known to ingest and then reject both live and dead individuals of Plagiotremus

townsendi, Smith-Vaniz et al (2001) proposed an element of Müllerian mimicry in the complexes

involving members of both genera Plagiotremus species feed on mucus, epidermis and the scales

of other fishes, in contrast to Meiacanthus species, which feed on benthic and planktonic

crusta-ceans Hence there may also be elements of aggressive mimicry in this relationship (Losey 1972,

Springer & Smith-Vaniz 1972) A future study extensively testing the unpalatability of the

Pla-giotremus species involved in mimetic relationships with Meiacanthus species may add strength

to the proposal that Müllerian mimicry is a partial explanation of colour similarities in thesecomplexes

Most species of coral reef fishes have some form of predator evasion tactic and it can be arguedthat some cases of presumed Batesian or other mimicry could also have elements of Müllerian

mimicry In the case of the palatable filefish Paraluteres prionurus and toxic pufferfish Canthigaster

valentini, Paraluteres prionurus has some degree of predator protection through a set of retrorse

spines on the caudal peduncle and a semi-erectile first dorsal spine (Tyler 1966, Randall et al.1997) Similarly, when speculating about the adaptive advantage gained by the mimic surgeonfish

Acanthurus pyroferus and its model pygmy angelfishes from the genus Centropyge, Randall &

Randall (1960) cited the diagnostic spines of each family, caudal blades of the surgeonfish thuridae) and cheek spines of the angelfish (Pomacanthidae), as possible evidence of a Müllerian

(Acan-relationship However, given the high rates of mortality reported for a species of Centropyge

(Aldenhoven 1986) and the evidence in support of other types of mimicry for this example, it isunlikely that Müllerian mimicry is a significant factor in this relationship Experimental tests ofprey selection by predators comparing preferences for mimics, models and other species are required

to detect Müllerian mimicry in cases such as these

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Aggressive mimicry

In aggressive mimicry, a predatory species resembles a harmless or beneficial species and quently achieves increased opportunities for foraging by deceiving prey (Wickler 1965, 1968,Malcolm 1990) Wickler (1965) cites Poulton (1890) as the first to draw the distinction betweendefensive, or protective, mimicry by which the adaptive advantage decreases predation, and aggres-sive mimicry, which increases feeding opportunities Aggressive mimicry is reported for 32 speciesfrom 10 families of coral reef fishes, but is most prevalent in the families Serranidae and Blenniidae,with 13 and 8 species, respectively (Table 3) Wickler (1960, 1961, 1963, 1965, 1968) carried outpioneer work on aggressive mimicry in coral reef fishes in his studies of the relationship between

conse-the cleaning labrid Labroides dimidiatus and its aggressive mimic, conse-the blenniid Aspidontus

taenia-tus Larger fishes, expecting only to have their parasites removed, allow A taeniatus to approach

them and it uses this opportunity to bite off pieces of fins and epidermis (e.g., Eibl-Eibesfeldt 1959,Randall & Randall 1960, Wickler 1961, Kuwamura 1981, 1983)

However, even seemingly unequivocal cases of aggressive mimicry such as the cleaner wrasse

example are not straightforward Since some authors had observed A taeniatus also to feed on

demersal fish eggs (Randall & Randall 1960, Losey 1974, Smith-Vaniz 1976), Kuwamura (1983)

examined the gut contents of 11 specimens of A taeniatus According to this study, fish fins were

rarely found in the gut contents and, in fact, the mimic blenny fed mostly on demersal fish eggs

as well as polychaete tentacles Furthermore, during behavioural observations A taeniatus rarely

bit pieces from the fins of host fishes even when they were posing for cleaning (Kuwamura 1983).Kuwamura (1981, 1983) suggests that the low rate of exploitation of posing fish by the mimic is

a strategy to prevent fish visiting cleaning stations from learning its disguise It is possible that themain benefit of this mimicry is immunity from predation but mimics may rely on aggressive mimicrywhen other kinds of prey are rare (Losey 1978, Kuwamura 1983)

It is also possible that this relationship between A taeniatus and Labroides dimidiatus is a form

of Batesian-type mimicry, due to amnesty of models rather than non-palatability During tions of the same two species in Kimbe Bay, Papua New Guinea, carried out at the same time as

observa-another study (Moland & Jones 2004) we never observed any life history stage of Aspidontus

taeniatus strike fish However, small groups of two to three individuals were observed to feed on

demersal eggs in nests protected by various egg-caring pomacentrids on several occasions Thefierce aggression elicited from egg-caring individuals was ignored by the blennies Being a scav-enger of demersal fish eggs involves much travelling around in search for food and immunity frompredation in a Batesian-type relationship may facilitate this type of lifestyle However, aggressivemimicry could have an important role in the juvenile stage when the blenny does not yet have thebody size required to withstand attacks form egg-caring fishes protecting their nests In light of

these findings, it seems inappropriate to consider A taeniatus only as an aggressive mimic.

The above example illustrates why it is necessary to impose strict criteria to distinguish amongtypes of mimicry in order to assess cases of mimicry Sazima (2002a) reviewed the literature onaggressive mimicry in fishes and sorted the evidence into two categories: (1) evidence of overallresemblance plus information on diet and social behaviour and (2) a record of prey taken by themimic under the supposed disguise Category 2 evidence is vitally important in ruling out thepossibility of an element of social mimicry

These two categories are used in this review to assess the evidence given in cases of aggressivemimicry reported for coral reef fishes (Table 3) Of the 32 species reported as aggressive mimics,less than half (13) include reports of category 2 evidence

Cases of aggressive mimicry found in coral reef fishes can also be categorised into three trendsdescribed by Sazima (2002a) for fish species exhibiting aggressive mimicry in freshwater cichlids:(1) species that feed on prey smaller than themselves tend to mimic and join species harmless to

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