With a Summary of Batesian Mimicry in Marine Fishes

Home , Meiacanthus, Petroscirtes, Pomadasys

aqua, Journal of Ichthyology and Aquatic Biology

Juvenile grunt (Haemulidae) mimicking a venomous leatherjacket (Carangidae), with a summary of Batesian mimicry in marine fishes

Ivan Sazima

Departamento de Zoologia and Museu de História Natural, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil. E-mail: [email protected] - Fax: +55 (19) 3289 3124

Accepted: 16.10.2002

Keywords Brasilien. Beim Durchschwimmen offener Gebiete Protective resemblance, mimicry, Oligoplites verhalten sich junge Pomadasys ramosus (Haemuli- palometa, Pomadasys ramosus, venomous model, dae), genau so wie das mutmaßliche Model, junge juveniles, tidal streams, western Atlantic Oligoplites palometa (Carangidae) , eine Art mit Gift- drüsen in der Rücken- und Afterflosse, und sie ähneln Abstract diesem auch sehr. Eine Zusammenfassung von 24 A presumed example of facultative Batesian mimicry veröffentlichten Beispielen Betesscher Mimikry unter between a grunt and a leatherjacket is described from Meeresfischen zeigt an, dass die meisten Arten (83,3 tidal streams and mangrove zones in south-eastern %) giftige Modelle, drei Arten (12,5 %) toxische Mod- Brazil. While moving over open areas or when threat- elle, und ein Modell dass weder giftig noch toxisch ist, ened, juvenile Pomadasys ramosus (Haemulidae) nachahmen. closely resemble, and behave like, their presumed venomous model, juvenile Oligoplites palometa Résumé (Carangidae), a species with venom glands in its dor- Est décrit un exemple présumé de mimétisme sal and anal spines. A summary of 24 published batésien facultatif entre un Grogneur et un Carange examples of Batesian mimicry in marine fishes shows originaires de fleuves soumis aux marées et de zones that most species (83.3%) mimic venomous models, de mangrove au sud-est du Brésil. Lorsqu'ils se meu- three species (12.5%) imitate poisonous models and vent en zones découvertes ou qu'ils sont menacés, only one species (4.1%) mimics a model which is nei- les Pomadasys ramosus (Haemulidae) juvéniles ther venomous nor poisonous. ressemblent fort à et se comportent comme leur mod- èle venimeux présumé, l'Oligoplites palometa Resumo (Carangidae) juvénile, une espèce à glandes Um presumível exemplo de mimetismo Batesiano vénéneuses dans ses épines dorsales et anales. Un facultativo, entre uma espécie de corcoroca e uma résumé de 24 exemples publiés de mimétisme espécie de guaivira, é descrito de manguezais no batésien chez les poissons de mer montre que la plu- sudeste do Brasil. O juvenil de Pomadasys ramosus part des espèces (83,3%) imitent des modèles ven- (Haemulidae), quando se desloca por áreas abertas imeux, trois espèces (12,5%) s'inspirent de modèles ou quando ameaçado, apresenta grande semelhança toxiques et une seule espèce (4,1%) imite un modèle de colorido e comportamento com o seu presumido qui n'est ni venimeux ni toxique. modelo peçonhento, o juvenil de Oligoplites palometa (Carangidae), uma espécie com glândulas de Sommario peçonha em seus acúleos dorsais e anais. Um Viene descritto un esempio di presunto mimetismo sumário de 24 casos publicados sobre mimetismo facoltativo batesiano tra un grugnitore e un carangide, Batesiano entre peixes marinhos mostra que a maio- osservato presso le correnti di marea e le zone a man- ria das espécies (83.3%) imita modelos peçonhentos, grovie del Brasile sudorientale. Quando si muovono in três espécies (12.5%) imitam modelos venenosos e aree aperte oppure si sentono minacciati, i giovani di apenas uma espécie (4.1%) imita um modelo que não Pomadasys ramosus (Haemulidae) prendono le sem- é peçonhento nem venenoso. bianze e il comportamento del loro presunto modello velenoso rappresentato dall’individuo giovane di Oligo- Zusammenfassung plites palometa (Carangidae), una specie provvista di Hier wird ein mutmaßliches Beispiel von fakultativer, ghiandole velenifere nei raggi spinosi dorsali e anali. Betesscher Mimikry beschrieben, zwischen einem Esaminando 24 esempi di mimetismo batesiano in Grunzer und einer Stachelmakrele, in einem Gehzeit- pesci marini si osserva che la maggior parte delle enfluss sowie in Mangrovenzonen, im südöstlichen specie (83.3%) ha come modello specie velenose per

61 aqua vol. 6 no. 2 - 2002 Juvenile grunt mimicking a venomous leatherjacket, with a summary of Batesian mimicry in marine fishes contatto, mentre tre (12.5%) imitano specie che sono count. In addition, I seined a stretch of about 100 m in velenose per ingestione e solo una (4.1%) imita un another stream. modello non velenoso. Voucher specimens of both species were deposited in the fish collection of the Museu de História Natural, Introduction Universidade Estadual de Campinas (ZUEC). Colour Batesian mimicry involves a harmless species, the transparencies taken both in the habitat and in field mimic, which resembles a harmful or unpalatable one, aquaria were scanned and deposited in the ZUEC fish the model (Wickler, 1968; Edmunds, 1974). Several photo file (numbers as for specimens). cases of presumed protective mimicry between Measurements used throughout are total length (TL) marine fishes have been proposed, some of them dis- for both species, standard length (SL) for the grunt, and puted and others generally accepted (summaries in fork length (FL) for the leatherjacket. Microscopic sec- Randall & Randall, 1960; Randall & Kuyter, 1989; tions of anal and dorsal spines of Oligoplites were pre- Smith-Vaniz et al., 2001). Perhaps one of the best- pared using routine histological methods, and stained known examples is the blenny Ecsenius bicolor (Day, with haematoxylin/eosin to demarcate the venom 1888), which mimics Meiacanthus atrodorsalis (Gün- glands (Halstead et al., 1972; Sazima & Uieda, 1979). ther, 1877) a fangblenny able to deliver a toxic bite The summary of recorded cases of Batesian mim- (Losey, 1972; Springer & Smith-Vaniz, 1972; Smith- icry is drawn from the literature, with one additional Vaniz et al., 2001). Toxic (venomous or poisonous) example based on field observations. Species names models include species in fish families as diverse as follow Eschmeyer (1998, updated 2000 in Froese & the Blenniidae, Scorpaenidae, Trachinidae, and Pauly, 2001). Tetraodontidae (Randall & Randall 1960; Randall & Kuiter, 1989). Among jacks (Carangidae), species of leatherjackets of the genera Scomberoides Lacepède, 1801 and Oligoplites Gill, 1863 have dorsal and anal spines with venomous glands and are able to inflict a painful wound (Halstead et al., 1972; Sazima & Uieda, 1979; pers. obs.). However, no species of leatherjacket has hitherto been proposed as a venomous model in any case of protective resemblance. During studies on the natural history of mangrove-dwelling fishes in south- eastern Brazil, I came upon what I regard as an example of facultative Batesian mimicry involving the grunt Pomadasys ramosus (Poey, 1860) as the mimic and the leatherjacket Oligoplites palometa (Cuvier, 1832) as the model. The morphological and behavioural similarities between the two species are described herein. In addition, a summary of Batesian mimicry in marine fishes is provided, with comments.

Methods Juvenile grunts (P. ramosus) and leatherjackets (O. palometa) were opportunistically recorded from Feb- ruary to December 2001 in several tidal streams and mangrove zones in the region of Ubatuba (23° 23- 30'S), São Paulo, south-eastern Brazil. The behaviour of the fishes was recorded during daylight in the course of 11 surface and 3 underwater snorkelling session (Sazima 1986), using “local animal” and “all occurrences” samplings (Lehner 1979): a total of about 13 hours of field observations. Observations were focused on particular behaviours (e.g., foraging, flight) and associated colour changes related to the Fig. 1. Pomadasys ramosus juveniles: above, an individ- bottom type and potentially camouflaging back- ual about 15 mm TL drifting slowly close to the bottom in ground. In one tidal stream I counted the numbers of its mangrove habitat; below, a larger juvenile (22.4 mm individuals of both species on two occasions by slowly SL, ZUEC 5537) showing the dark, camouflaged, colour wading for one hour through clear, shallow water at pattern while hovering close to plant debris (pho- ebb tide, covering approximately 300 m during each tographed in field aquarium). Photos by I. Sazima. aqua vol. 6 no. 2 - 2002 62 Ivan Sazima

Results both fishes occasionally darted at prey, which they Juvenile grunts, Pomadasys ramosus, bear a close engulfed before resuming their hovering. resemblance to juvenile leatherjackets, Oligoplites While close to decaying plant fragments and other palometa, both in colour pattern and behaviour, and dark debris, both species often adopted a dark colour were found together in tidal streams and mangrove pattern, which camouflaged them against the back- zones. The two counts produced similar proportions of ground (Fig. 1, see Sazima & Uieda, 1979 for a figure models to mimics: three leatherjackets and two grunts of O. palometa). When camouflaged in this dark attire, in one count and three leatherjackets and one grunt in both species moved slowly close to the bottom and the other. The seine catch yielded five leatherjackets their swimming resembled the movement of water- and two grunts. logged plant debris drifting in the water current. How- Both fish species may hover in a head-down, oblique ever, while moving over open, detritus-free, light- and curved posture (Fig. 1), although the leatherjacket coloured sandy bottom, both the leatherjacket and the was observed to hover both close to the bottom and to grunt promptly adopted a contrasting, bicoloured (yel- the water’s surface, whereas the grunt hovered close lowish and dark) pattern (Figs. 2-3). While in this to the bottom only. This difference appears related to bicoloured attire, both species no longer behaved like foraging tactics, as the grunt feeds mainly on bottom- “waterlogged debris” and swam in a normal fish-like dwelling invertebrates, whereas the leatherjacket manner instead (see also Sazima & Uieda, 1979). The preys on both benthic and pelagic invertebrates, bicoloured pattern was also adopted when the fishes besides picking scales from other fishes (Sazima & were chased or otherwise threatened, regardless of Uieda, 1980; pers. obs.). From this hovering posture, the bottom type and the presence of dark debris.

Fig. 2. Oligoplites palometa juvenile and venom glands: Fig. 3. Mimetic pair: above, Oligoplites palometa juvenile above, an individual 14.4 mm FL (ZUEC 5197) showing 22.1 mm FL (ZUEC unnumbered); below, Pomadasys the contrasting bicoloured pattern (photographed in field ramosus juvenile 22.4 mm SL (ZUEC 5537) while mov- aquarium); below, cross-section of the dorsal spine of a ing over an area of open, light-coloured sandy bottom in juvenile 26 mm FL showing venom cells (dark red) their tidal stream habitat. Photos by I. Sazima. packed in the anterior grooves. Photos by I. Sazima (upper) and V. S. Uieda (lower).

63 aqua vol. 6 no. 2 - 2002 Juvenile grunt mimicking a venomous leatherjacket, with a summary of Batesian mimicry in marine fishes

Table I. Species of fishes reported as Batesian mimics and their putative models, with the type of noxiousness of each model species, and sources. The sequence of families for mimics follows Nelson (1994); genera and species are in alphabetical order.

Mimics Models Noxiousness Sources

Cheilodipterus nigrotaeniatus (Apogonidae) Meiacanthus grammistes (Blenniidae) venomous Smith-Vaniz et al. (2001) Cheilodipterus parazonatus (Apogonidae) Meiacanthus vittatus (Blenniidae) venomous Allen et al. (1975), Smith-Vaniz et al. (2001) Cheilodipterus zonatus (Apogonidae) Meiacanthus geminatus, M. vittatus venomous Gon, 1993, (Blenniidae) Smith-Vaniz et al. (2001) Fowleria vaiulae (Apogonidae) Scorpaenodes guamensis venomous Goren & Karplus (1983) (Scorpaenidae) Fowleria sp. (?= F. variegata) (Apogonidae) Scorpaenodes guamensis venomous Siegel & Adamson (1983) (Scorpaenidae) Plectropomus laevis (Serranidae) - juvenile Canthigaster valentini poisonous Randall & Hoese (1986) (Tetraodontidae) Calloplesiops altivelis (Plesiopidae) Gymnothorax meleagris powerful bite McCosker (1977) (Muraenidae) Centrogenys vaigiensis (Centrogeniidae) Scorpaena picta (Scorpaenidae) venomous Whitley (1935) Pomadasys ramosus (Haemulidae) - juvenile Oligoplites palometa (Carangidae) venomous This paper juvenile Pentapodus trivittatus (Nemipteridae) Meiacanthus crinitus (Blenniidae) venomous Smith-Vaniz et al. (2001) juvenile Scolopsis bilineatus (Nemipteridae) Meiacanthus atrodorsalis venomous Russell et al. (1976), juvenile M. lineatus, M. smithi (Blenniidae) Smith-Vaniz et al. (2001) Scolopsis margaritifer (Nemipteridae) Meiacanthus geminatus, venomous Russell et al. (1976), juvenile M. lineatus, M. vittatus (Blenniidae) Smith-Vaniz et al. (2001) Ecsenius bicolor (Blenniidae) Meiacanthus atrodorsalis (Blenniidae) venomous Losey (1972), Smith-Vaniz et al. (2001) Ecsenius gravieri (Blenniidae) Meiacanthus nigrolineatus, venomous Smith-Vaniz et al. (2001) (Blenniidae) Petroscirtes breviceps (Blenniidae) Meiacanthus grammistes, venomous Springer & M. kamoharai, M. vittatus Smith-Vaniz (1972), (Blenniidae) Smith-Vaniz et al. (2001) Petroscirtes fallax (Blenniidae) Meiacanthus lineatus (Blenniidae) venomous Russell et al. (1976), Lieske & Myers (1994) Plagiotremus laudandus (Blenniidae) Meiacanthus atrodorsalis (Blenniidae) venomous Losey (1972), Smith-Vaniz et al. (2001) Plagiotremus phenax (Blenniidae) Meiacanthus smithi (Blenniidae) venomous Springer & Smith-Vaniz (1972), Smith-Vaniz et al. (2001) Plagiotremus townsendi (Blenniidae) Meiacanthus nigrolineatus (Blenniidae) venomous Lieske & Myers (1994), Smith-Vaniz et al. (2001) Amblygobius linki (Gobiidae) Meiacanthus anema (Blenniidae) venomous Springer & Smith-Vaniz (1972) Valenciennea helsdingenii (Gobiidae) Meiacanthus anema (Blenniidae) venomous Springer & Smith-Vaniz (1972) Solea solea (Soleidae) Echiichthys vipera, Trachinus draco venomous Masterman (1908) (Trachinidae) Paraluteres arqat (Monacanthidae) Canthigaster margaritata poisonous Randall & Randall (1960) (Tetraodontidae) Paraluteres prionurus (Monacanthidae) Canthigaster valentini (Tetraodontidae) poisonous Tyler (1966)

aqua vol. 6 no. 2 - 2002 64 Ivan Sazima

Both species change their colours and habits when 1966; Wickler, 1968; Edmunds, 1974). Although they reach about 30-40 mm TL. The grunt changes to leatherjackets are venomous throughout life, small dusky yellow above (with sinuous darker lines on the individuals are presumably more vulnerable to preda- flanks) shading to whitish below, adopts a demersal tion than larger ones, due not only to their smaller size lifestyle, and no longer swims in a head-down or but also to their solitary habits – larger individuals curved posture. The leatherjacket changes to dusky school (pers. obs.). Hence more effective defensive green above, shading to silvery white below, and tactics are to be expected among juveniles, and this is adopts a pelagic lifestyle similar to that recorded for indeed the case for a number of marine fish species, two other sympatric leatherjacket species, Oligoplites be this camouflage, Batesian mimicry, or association saurus and O. saliens (Sazima & Uieda, 1980; Ran- with larger and/or dangerous organisms (e.g. Randall dall, 1996; Carvalho-Filho, 1999). The venom glands & Randall, 1970; Heck & Weinstein, 1978; Mansuetti, of O. palometa are retained throughout life, albeit the 1963). The combination of well-developed venom venom cells (Fig. 2) occupy much less space (up to glands on dorsal and anal spines (Fig. 2, see also about 50%, pers. obs.) in the spine grooves of adults Sazima & Uieda, 1979) and a warning colour pattern than in those of juveniles. renders the juvenile O. palometa a suitable Batesian Published records of 24 examples of Batesian mim- model. ics in marine fishes are summarised here (Table I), The colour pattern adopted by P. ramosus is remark- together with their presumed models and their type of ably similar to that of its presumed model O. noxiousness. For reference, the scientific names of palometa, as both fishes may change their colour the species concerned (except for the four already according to the bottom type (with or without dark detailed in the text), including author and date, are debris) and circumstances such as flight and fright listed here in alphabetical order: Amblygobius linki reaction. While the dark pattern is an example of cam- Herre, 1927; Calloplesiops altivelis (Steindachner, ouflage (Sazima & Uieda, 1979), the contrasting pat- 1903); Canthigaster margaritata (Rüppell, 1829); Can- tern may best be viewed as an example of Batesian thigaster valentini (Bleeker, 1853); Centrogenys mimicry, in which the bicoloured P. ramosus juvenile is vaigiensis (Quoy & Gaimard, 1824); Cheilodipterus a mimic of O. palometa, a well-armed model (Sazima nigrotaeniatus Smith & Radcliffe, 1912; Cheilodipterus & Uieda, 1979). I regard this as an example of facul- zonatus Smith & Radcliffe, 1912; Echiichthys vipera tative mimicry, not only because it is adopted in the (Cuvier, 1829); Ecsenius gravieri (Pellegrin, 1906); juvenile phase only (Russell et al., 1976), but also Fowleria vaiulae (Jordan & Seale, 1906); Fowleria var- because the grunt is already afforded some degree of iegata (Valenciennes, 1832); Gymnothorax meleagris protection by its dark camouflaging pattern while (Shaw, 1795); Meiacanthus anema (Bleeker, 1852); close to dark debris. The mimetic, bicoloured pattern Meiacanthus crinitus Smith-Vaniz, 1987; Meiacanthus is adopted while the fish is particularly exposed (mov- geminatus Smith-Vaniz, 1976; Meiacanthus gram- ing over open areas), or when chased or otherwise mistes (Valenciennes, 1836); Meiacanthus kamoharai frightened. The fact that both species rely on camou- Tomiyama, 1956; Meiacanthus lineatus (De Vis, flage as a first-line defence, and on warning coloration 1884); Meiacanthus nigrolineatus Smith-Vaniz, 1969; (and mimicry) as a second-line defence, is notewor- Meiacanthus oualanensis (Günther, 1880); Meiacan- thy, and probably related to the small size and solitary thus smithi Klausewitz, 1962; Meiacanthus vittatus habits of the juveniles. Smith-Vaniz, 1976; Paraluteres arqat Clark & Gohar, It may be argued that P. ramosus and O. palometa 1953; Paraluteres prionurus (Bleeker, 1851); Pentapo- together represent a case of defensive convergence in dus trivittatus (Bloch, 1791); Petroscirtes breviceps which both species use a dark attire while close to (Valenciennes, 1836); Petroscirtes fallax Smith-Vaniz, dark debris and a bicoloured one while over open 1976; Plagiotremus laudandus (Whitley, 1961); Pla- sandy bottom (contrasting colours may be regarded as giotremus phenax Smith-Vaniz, 1976; Plagiotremus a disruptive pattern, see below). However, when in the townsendi (Regan, 1905); Scolopsis bilineatus (Bloch, open, both species could instead simply adopt plain, 1793); Scolopsis margaritifer (Cuvier, 1830); Scor- pale attire, which, in principle, would be more difficult paena picta Cuvier, 1829; Scorpaenodes guamensis for a visually-guided predator, foraging over a sandy (Quoy & Gaimard, 1824); Solea solea (Linnaeus, background, to perceive. Juveniles of Trachinotus fal- 1758); Trachinus draco Linnaeus, 1758, Valenciennea catus (Linnaeus, 1758), also a carangid, adopt a heldingenii (Bleeker, 1858). curved posture and a dark pattern (Randall & Randall, 1960) while among decaying vegetation, and change Discussion to pale greyish or yellowish and silvery while over an The contrasting colours of O. palometa may be open sandy bottom (pers. obs.). Pale colours without regarded as an example of a warning pattern, since any obviously visible markings are widespread among the combination of black and yellow or white is one of fishes dwelling over sandy areas (e.g. Hobson & the most widespread colour patterns among animals Chess, 1986; Humann & DeLoach, 2000; pers obs.). which advertise their noxious properties (e.g. Cott, Contrasting colours are often found among reef

65 aqua vol. 6 no. 2 - 2002 Juvenile grunt mimicking a venomous leatherjacket, with a summary of Batesian mimicry in marine fishes fishes and may sometimes be regarded as disruptive and dangerous bite (Halstead, 1970). camouflaging patterns, in addition to their generally Five species (20.8%) of the mimics, including the accepted functions of warning, territorial, and sexual grunt P. r a m o s u s , resemble their presumed models signalling (e.g. Wickler, 1968; Lowe-McConnell, only as juveniles. Four of these cases involve juveniles 1987). Among fishes dwelling over sandy or muddy of species that outgrow their model, and thus the pro- bottoms, contrasting colours are generally related to tective resemblance is lost as the mimic grows (the only social signals or sexual displays (certainly not the example in which both the mimic and the model lose case in a solitary juvenile) or to warning colours plus their similarity as they grow is the pair P. r a m o s u s and Batesian mimicry (e.g. the pairs Trachinus draco- O. palometa). Fish species which act as mimics only as Solea solea or Meiacanthus anema-Amblygobius juveniles are classified as facultative mimics, whereas linki). Moreover, contrasting colours employed as a the remaining examples summarised here are disruptive pattern are generally found over complex regarded as obligatory mimics (Russell et al., 1976). types of background (e.g. coral reef, forest floor), not Except for the pairs Amblygobius linki-Meiacanthus over plain backgrounds such as sand or mud (Cott, anema and Pomadasys ramosus-O. palometa, both of 1966; Edmunds, 1974; Wickler, 1968). Thus, it seems which occur in tidal streams, mangrove zones, and more plausible (and parsimonious) to follow the work- estuaries (Springer & Smith-Vaniz, 1972; Sazima & ing hypothesis that the bicoloured, contrasting pattern Uieda, 1979; Menezes & Figueiredo, 1980), the of the leatherjacket is a warning signal and that the remaining mimetic associates come mostly from coral resemblance of the grunt involves a Batesian mimetic reefs, the most species-rich marine habitat, especially relationship, albeit facultative and restricted to partic- in the Indo-Pacific (e.g. Thresher, 1991). I suspect that ular situations. examples of mimicry among brackish water fishes, In both the counts and the seine catch the leather- besides being less numerous than those on coral jacket model outnumbered (albeit only slightly) its pre- reefs, are also less likely to be detected due to factors sumed grunt mimic, one of the postulated require- such as poorer visibility (compared to coral reef ments for Batesian mimicry (e.g. Wickler 1968; Losey waters), and also to a scarcity of underwater or other 1972; Edmunds, 1974; Russell et al., 1976). However, studies of live fishes (i.e. in their habitual colours) in even if the leatherjacket did not outnumber its mimic, mangrove zones and estuaries. Moreover, these latter Batesian mimicry cannot be disregarded since the environments harbour fewer fish species and are less mimic would still enjoy some degree of protection stable than the rich tropical coral reefs (e.g. Sale, (Springer & Smith-Vaniz, 1972; Edmunds, 1974). 1991; Moyle, 1995) and thus possibly offer fewer A glance at Table I reveals that most mimics (83.3%) opportunities for the development of evolutionarily imitate venomous models, three species (12.5%) complex processes such as mimicry. These factors mimic poisonous models, and only one mimic (4.1%) notwithstanding, examples of aggressive mimicry imitates a model which is neither venomous nor poi- among fish species dwelling in brackish water have sonous. In more than half (62.5%) of the cases the been reported recently (Sazima, 2002). venomous models are fangblennies of the genus Given the large number of known venomous, poiso- Meiacanthus, a model involved in several mimicry nous, or otherwise noxious fish species (Halstead, complexes (Springer & Smith-Vaniz, 1972), including 1970) which might act as models, the number of a few cases of aggressive mimicry (Russell et al,. reported Batesian mimics is surprisingly low and 1976). For instance, the blenny Plagiotremus laudan- based on few models. One possible explanation is that dus, a Batesian mimic of M. atrodorsalis (Losey, the focus on protective mimicry in marine fishes is 1972), is an aggressive mimic of both the latter and scarce and/or inadequate (see comments above on the blenny Ecsenius bicolor (see Sazima, 2002 for a brackish waters) or, more probably, that these fishes summary of aggressive mimicry in fishes). Blenniids rely mostly on defensive tactics other than mimicry dominate the cases of Batesian mimicry (Table I), and (e.g. schooling, sheltering, camouflage). It should be are similar to serranids in numbers of aggressive mim- noted that defence types other than mimicry may be icry examples (Sazima, 2002). This richness of mim- simpler and perhaps less costly from an evolutionary icry examples among blenniids is probably due both viewpoint (e.g. Wickler, 1968; Edmunds, 1974). to the large number of species within the family (Nel- Although mimicry in marine fishes is sometimes a son, 1994), and to the fact that the nemophine fang- controversial issue (e.g. Domeier, 1994), the cases blennies are very suitable as noxious models for mim- summarised here may be taken as at least good work- icry complexes due to their efficient venom-delivering ing hypotheses. There are examples in which the apparatus plus the warning colours in some species mimics display habits strikingly divergent from most (see recent review in Smith-Vaniz et al., 2001). The other species within a given family, as in the case of few reported poisonous Batesian models among three diurnal Cheilodipterus species (Apogonidae) in marine fishes are puffers of the genus Canthigaster, an otherwise nocturnal family (Smith-Vaniz et al., and the only case of a model that is neither venomous 2001). In such and other similar cases, mimicry still nor poisonous is a moray, a fish able to inflict a painful represents the most plausible (and parsimonious) aqua vol. 6 no. 2 - 2002 66 Ivan Sazima explanation until better interpretations are presented. tionships between tropical burrfishes and opisto- Limited but nevertheless convincing demonstrations branchs. Biotropica, 10 (1): 78-79. of the value of Batesian mimicry among blennies have Hobson, E. S. & J. R. Chess. 1986. Relationships been presented and commented upon by Losey among fishes and their prey in a nearshore commu- (1972), Springer & Smith-Vaniz (1972), and Smith- nity of southern California. Environmental Biology of Vaniz et al. (2001). Fishes, 17 (3): 201-226. Humann, P. & N. DeLoach. 2000. Reef fish identifi- Acknowledgements cation: Florida, Caribbean, Bahamas. 3rd ed. New I thank Marlies Sazima, Virgínia S. Uieda, and Wil- World Publications, Jacksonville, 481 pp. son Uieda for helping during the field work (MS also Lehner, P. N. 1979. Handbook of ethological helped with field and aquarium photographs); José L. methods. Garland STPM Press, New York. Figueiredo for checking the identity of the mimic; Losey, G. S. 1972. Predation protection in the Jansen S. Zuanon for critically reading the manu- poison-fang blenny, Meiacanthus atrodorsalis, script; John E. Randall and William F. Smith-Vaniz for and its mimics, Ecsenius bicolor and Runula laudan- providing copies of their inspiring papers; the Instituto dus (Blenniidae). Pacific Science, 26 (2): 129-139. Florestal (Núcleo Picinguaba) for logistical support on Lowe-McConnell, R. H. 1987. Ecological studies in the northern tip of the São Paulo coast; the IBAMA for tropical communities. Cambridge University Press, permits to study and collect fishes along the Brazilian Cambridge, 382 pp. coast; the CNPq, FAEP-Unicamp, and FAPESP for Mansuetti, R. 1963. Symbiotic behavior between essential financial support. This paper is dedicated to small fishes and jellyfishes, with new data on that John E. Randall, William F. Smith-Vaniz, and Barry C. between the stromateid, Peprilus alepidotus, and the Russell, for their inspiring insights on mimicry in scyphomedusa, Chrysaora quinquecirrha. Copeia, marine fishes. 1963 (1): 40-80. Masterman, A. T. 1908. On a possible case of mimicry References in the common sole. Journal of the Linnaean Society Allen, G. R., Russell, B. C., Carlson, B. A., & W. A. (Zoology), 30: 239-244. Starck, II. 1975. Mimicry in marine fishes. Tropical McCosker, J. E. 1977. Fright posture of the plesiopid Fish Hobbyist, 24 (1): 47-56. fish Calloplesiops altivelis: an example of Batesian Carvalho-Filho, A. 1999. Peixes: costa brasileira. 3rd mimicry. Science, 197: 400-401. ed. Ed. Melro, São Paulo, 320 pp. Menezes, N. A. & J. L. Figueiredo. 1980. Manual de Cott, H. B. 1966. Adaptive coloration in animals. peixes marinhos do sudeste do Brasil. IV. Teleostei Methuen, London, 508 pp. (3). Museu de Zoologia Universidade de São Paulo, Domeier, M. L. 1994. Speciation in the serranid fish São Paulo, 105 pp. Hypoplectrus. Bulletin of Marine Science, 54 (1): Moyle, P. B. Fish: an enthusiast’s guide. University of 103-141. California Press, Berkeley, 272 pp. Edmunds, M. 1974. Defence in animals: a survey of Nelson, J. S. 1994. Fishes of the world. 3rd ed. John anti-predator defences. Longman, Harlow, 357 pp. Wiley & Sons, New York, 600 pp. Eschmeyer, W. N. (ed.) 1998. Catalog of fishes. Cali- Randall, J. E. 1996. Caribbean reef fishes. T. F. H. fornia Academy of Sciences, San Francisco. Publications, Neptune City, 386 pp. Froese, R. & D. Pauly., (Eds.) 2001. FishBase. World Randall, J. E. & D. F. Hoese, 1986. Revision of the Wide Web electronic publication. www.fishbase.org. groupers of the Indo-Pacific genus Plectropomus (Per- Gon, O., 1993. Revision of the cardinalfish genus ciformes: Serranidae). Indo-Pacific Fishes, 13: 1-31. Cheilodipterus (Perciformes: Apogonidae), with Randall, J. E. & R. H. Kuiter. 1989. The juvenile Indo- description of five new species. Indo-Pacific Fishes, Pacific grouper Anyperodon leucogrammicus, a 22: 1-59. mimic of the wrasse Halichoeres purpurescens and Goren, M. & I. Karplus. 1983. Preliminary observa- allied species, with a review of the recent literature tions on the scorpion fish Scorpaenodes guamensis on mimicry in fishes. Revue Française d’Aquariolo- and its possible mimic the cardinal fish Fowleria abo- gie, 16 (2): 51-56. cellata. Development in Ecology and Environmental Randall, J. E. & H. A. Randall. 1960. Examples of Quality, 2: 327-336. mimicry and protective resemblance in tropical Halstead, B. W. 1970. Poisonous and venomous marine fishes. Bulletin of Marine Sciences Gulf & marine animals of the world. Vol. 3. U.S. Government Caribbean 10 (4): 444-480. Printing Office, Washington, D.C., 1006 pp. Russell, B. C., Allen G. R. & H. R. Lubbock. 1976. Halstead, B. W., D. D. Danielson, W. J. Baldwin & P. New cases of mimicry in marine fishes. Journal of C. Engen. 1972. Morphology of the venom appara- Zoology, London. 180: 407-423. tus of the leatherback fish Scomberoides sanctipetri Sale, P. F. (Ed.) 1991. The ecology of fishes on coral (Cuvier). Toxicon, 10: 249-258. reefs. Academic Press, San Diego. 754 pp. Heck, K. L., Jr. & M. P. Weinstein. 1978. Mimetic rela- Sazima, I. 1986. Similarities in feeding behaviour

67 aqua vol. 6 no. 2 - 2002 Juvenile grunt mimicking a venomous leatherjacket, with a summary of Batesian mimicry in marine fishes

between some marine and freshwater fishes in two tropical communities. Journal of Fish Biology, 29 (1): 53-65. Sazima, I. 2002. Juvenile snooks (Centropomidae) as mimics of mojarras (Gerreidae), with a review of aggressive mimicry in fishes. Environmental Biology of Fishes, 65 (1): 37-45. Sazima, I. & V. S. Uieda. 1979. Adaptações defensi- vas em jovens de Oligoplites palometa (Pisces, Carangidae). Revista Brasileira de Biologia, 39 (3): 687-694. Sazima, I. & V. S. Uieda. 1980. Comportamento lep- idofágico de Oligoplites saurus e registro de lepid- ofagia em O. palometa e O. saliens (Pisces, Carangi- dae). Revista Brasileira de Biologia, 40 (4): 701-710. Seigel, J. A. & T. A. Adamson. 1983. Batesian mimicry between a cardinalfish (Apogonidae) and a venomous scorpionfish (Scorpaenidae) from the Philip- pine Islands. Pacific Science, 37 (1): 75-79. Smith-Vaniz, W. F., Satapoomin, U. & G. R. Allen. 2001. Meiacanthus urostigma, with discussion and examples of mimicry in species of Meiacanthus (Teleostei: Blenniidae: Nemophini). aqua, Journal of Ichthyology and Aquatic Biology, 5 (1): 25-43. Springer, V. G. & W. F. Smith-Vaniz. 1972. Mimetic relationships involving fishes of the family Blenni- idae. Smithsonian Contributions in Zoology, 112: 1- 36. Thresher, R. E. 1991. Geographic variability in the ecology of coral reef fishes: evidence, evolution, and possible implications. In: The ecology of fishes on coral reefs. (Ed. P. F. Sale): 401-436. Academic Press, New York. Tyler, J. C. 1966. Mimicry between the plectognath fishes Canthigaster valentini (Canthigasteridae) and Paraluteres prionurus (Aluteridae). Notulae Naturae, 386: 1-13. Whitley, G. P. 1935. Fishes from Princess Charlotte Bay, North Queensland. Records of the South Aus- tralian Museum, 5 (3): 345-363. Wickler, W. 1968. Mimicry in plants and animals. McGraw-Hill, New York, 255 pp.

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