3597_book.fm Page 455 Friday, May 20, 2005 6:26 PM Oceanography and Marine Biology: An Annual Review, 2005, 43, 455-482 © R N Gibson, R J A Atkinson, and J D M Gordon, Editors Taylor & Francis ECOLOGY AND EVOLUTION OF MIMICRY IN CORAL REEF FISHES EVEN 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.au Address 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 the prevalence of mimicry in different taxa, its ecological consequences and postulated modes of evolution Mimicry appears to be a widespread and common phenomenon in coral reef fishes, with approximately 60 reported cases Although many are largely anecdotal accounts based on colour resemblance, recent quantitative comparisons and experimental manipulations have confirmed that many represent mimic-model relationships The distribution of mimics and models among reef fish 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, although imperfect forms of mimicry are likely to have been underestimated Mimicry appears to be particularly important during juvenile stages, with 28% of mimic species losing their mimic colouration when they outgrow their models All cases of mimicry support predictions that mimics are rare relative to their models Furthermore, the abundance of mimics in different areas may increase in proportion to model abundance The spatial distribution of mimics appears to be limited by that of their model species, although some change models in different habitats or in different parts of their range Many mimics live in close association with their models, and both foraging advantages and predator avoidance have been experimentally demonstrated Aggressive mimicry appears to be the most 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 be rare, although it may contribute to the mimetic complexes involving members of the blenniid tribe Nemophini However, these traditional classifications are too simplistic for reef fishes because both foraging advantages and predator avoidance can apply in a single mimetic relationship, and their relative importance has not been evaluated Preliminary data suggest a high degree of phenotypic plasticity in mimetic colouration and little genetic differentiation among different mimics of the same 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 coral reef fishes Introduction The phenomenon of mimicry, where one species evolves to closely resemble another, has arisen many 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 455 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 456 Friday, May 20, 2005 6:26 PM EVEN MOLAND, JANELLE V EAGLE & GEOFFREY P JONES pressures favouring individuals that are able to disguise their identity by masquerading as another species The study of mimicry began in the mid-1800s, with most of the theory developed from field studies on terrestrial animal groups, most notably butterflies Despite this long history of interest, the prevalence of mimicry, its ecological significance and mechanisms of evolution have yet to be evaluated for many animal groups The proposed fitness advantage of mimicry depends upon who is being deceived Four different types of mimicry have been traditionally recognised In Batesian mimicry, harmless and palatable species closely resemble unpalatable or venomous species usually avoided by predators (Bates 1862) In Müllerian mimicry, two unpalatable species share similar colour patterns and thus reinforce their predator deterrence (Müller 1879) In aggressive mimicry, a predatory species resembles 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 by Moynihan (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, the underlying bases of many mimic-model relationships are poorly understood Mimic-model systems are thought to share a number of defining ecological characteristics that should apply if mimicry is to provide a fitness advantage Mimic species must be rare compared with their model species because the deception will not work if the predators or prey that are being deceived encounter too many mimics and learn from these experiences (Bates 1862) Mimics should also 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 untested for most presumed cases of mimicry If such relationships hold, the distribution and abundance of mimics will be closely tied to that of their models An understanding of the ecological relationships between mimics and models is critical to assessing its ecological significance and underlying evolutionary 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 Many additional cases have been reported over the last four decades, suggesting that mimicry may be a relatively 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 have been relatively few studies specifically addressing the causes and consequences of mimicry in reef fishes 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 more rigorous observational studies addressing the criteria necessary to establish mimicry (e.g., Snyder 1999, Eagle & Jones 2004) and experimental studies establishing cause-effect links between mimic and 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 of mimicry 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 evidence for different types of mimicry in coral reef fishes Early reviews of the ecology of reef fishes argued that mimicry could have important implications (Ehrlich 1975, Sale 1980) but in recent texts this topic has received virtually no attention (Sale 1991, 2002) The prevalence of mimicry within a community can be difficult to assess Descriptions of mimicry usually focus on the more spectacular and specialized mimics that are striking to the observer, which may lead to an underestimate of its importance (Russell et al 1976) Three clear 456 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 457 Friday, May 20, 2005 6:26 PM 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 insert following page 278), the similarity of the monocanthid Paraluteres prionurus to the unpalatable tetraodontid Canthigaster valentini (Tyler 1966, Caley & Schluter 2003) (Figure 1C,D, see colour insert) 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 colour insert) Few would dispute that these are mimic-model pairs The problem begins when the colour similarities are not so striking to the observer Theory predicts that both good and poor mimics can evolve in different situations (Lindström et al 1997, Edmunds 2000, Sherratt 2002); however, distinguishing poor mimics from fortuitous resemblance can be a challenge Recent experimental studies (Munday et al 2003) suggest that there can be a strong association between similarly coloured reef fishes that would not be considered obvious cases of mimicry In addition, what the human 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 classified according to one of the four established evolutionary mechanisms For example, cleaner wrasse mimics may be unique among all known cases of mimicry They are primarily thought to be aggressive 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-predation mechanism Cleaner wrasses are afforded an ‘amnesty’ from predators because of the parasite removal service they provide Cleaner wrasse mimics may also benefit from this amnesty, thus gaining the dual advantages of both an increase in feeding and a decrease in predation (Kuwamura 1983) The overall aims of this review are to examine the current literature on the prevalence of mimicry 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 fishes critically assessed Specific questions that are addressed include: How prevalent is mimicry in coral reef fishes? Which families of coral reef fishes are involved in mimetic relationships, what is the prevalence of mimicry within these families, and within species, what life history stages are involved? 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 models and mimics and models influence each other’s abundance? What is the evidence for the four widely recognised types of mimicry (Batesian, Müllerian, aggressive and social) in reef fishes? Do reef fishes conform to this classification, which type of mimicry is most important, or is the evidence inadequate to reach this conclusion? Finally, which research directions must be taken to complete our 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 disproportionately represented, 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 is usually quite low (