The colouration of the venomous coral snakes. Aniliidae and Colubridae) (family Elapidae) and their mimics (families

colouration mimicry. Biological Journal of the Linncon Socie& (1992), 45: 235-254. With 6 figures The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Colubridae) JAY M. SAVAGE, F.L.S. AND JOSEPH B. SLOWINSKI Department of Biology, University of Miami, P.O. Box 249118, Coral Gables, FL 33124, U.S.A. Received 7 August 1990, accepted for publication 30 October 1990 The bright coloured, highly venomous coral snakes, Lcptominurus, Micrurus and Mimroidcs (family Elapidae) and a series of harmless or mildly toxic mimics form an important component of the snake fauna of the Americas. Coral snake patterns are defined as any dorsal pattern found in any species of venomous coral snake and/or any dorsal pattern containing a substantial amount of red, pink or orange distributed so as to resemble that of some species of venomous coral snake. The components of coral snake colouration are described and four principal dorsal patterns are recognized: unicolour, bicolour, tricolour and quadricolour. The tricolour patterns may be further clustered based on the number of black bands or rings separating the red ones as: monads, dyads, triads, tetrads or pentads. A detailed classification of all coral snake colour patterns is presented and each pattern is illustrated. The taxonomic distribution of these patterns is surveyed for mimics and the 56 species of highly venomous coral snakes. Among the latter, the most frequent encountered patterns are tricolour monads, tricolour triads and bicolour rings, in that order. No venomous coral snakes have a tricolour dyad, tricolour tetrad or quadricolour pattern. As many as I15 species of harmless or mildly toxic species, c. 18% of all American snakes, are regarded as coral snake mimics. The colouration and behavioural traits of venomous coral snakes combine to form a significant antipredator defence of an aposematic type. The mimics in turn rereive protection from predators that innately or through learning avoid coral snake colour patterns. The precise resemblances in colouration between sympatric non-coral snakes and venomous coral snakes and the concordant geographic variation between the two strongly support this view. Batesian mimicry with the highly venomous coral snakes as the models and the other forms as the mimics is the favoured explanation for this situation. It is further concluded that a number of species in the genera Elaphc, Farancia, Nerodia and Thamnophis, although having red in their colouration, should not be included in the coral snake mimic guild. KEY WORDS:-Coral snakes ~ ~ CONTENTS Introduction............... Definition of coral snake colouration......... Components of the colour pattern.......... A classification of coral snake colour patterns....... Taxonomic distribution in American species....... Non-venomous or mildly venomous presumptive coral snake mimics. Venomous coral snakes........... Colouration and mimicry............ References................... 236.... 236.... 237.... 240.... 245.... 245.... 248.... 250.... 253 235 002+4066/92/030235 + 20 S03.00/0 0 1992 The Linnean Society of London

236 J. M. SAVAGE AND J. B. SLOWINSKI INTRODUCTION During a course of studies on the New World venomous coral snakes (family Elapidae) and their presumed aglyphous and opisthoglyphous mimics we were struck by the absence of consistent terminology to describe major aspects of their colour patterns. Since these patterns are often utilized to distinguish between allied taxa and may be of significance in establishing relationships, this inconsistency hampers systematic studies of both the highly venomous species and the guild of coral snake mimics. In addition, the lack of a uniform terminology inhibits attempts to establish congruence in colouration between the supposed mimics and their models. We have previously published a preliminary paper (Savage & Slowinski, 1990) outlining broad categories of coral snake patterns. In the present paper a much more detailed analysis is developed and we address the problem in depth by: (1) identifying and defining the major components of colour pattern in these groups; (2) establishing a consistent terminology to describe variation in the patterns and; (3) summarizing the taxonomic occurrence of the various patterns. In the following sections the term venomous coral snakes refers to proteroglyphous elapids of the genera Leptomicrurus, Micrurus and Micruroides. The term mimic is used to denote aniliid and colubrid snakes that resemble venomous coral snakes and which are non-venomous or mildly toxic and lack the advanced venom delivery system (rigid canaliculate anteriorly placed fangs on the upper jaw and venom gland compressor muscles) found in elapids. DEFINITION OF CORAL SNAKE COLOURATION An initial consideration in undertaking this review was the need to delimit those elements of pattern that constitute coral snake colouration since the venomous coral snakes (the nominal genera Leptomicrurus, Micruroides and Micrurus) and their harmless to mildly toxic mimics display a substantial range of variation in colouration. Throughout the Americas snakes having a considerable amount of red, pink or orange in their colouration are called coral snakes, corales (Spanish) or cobras-coraes (Portuguese) and almost all venomous coral snakes and their mimics are known by these names. Consequently we have taken our cue from the vernacular names and define as a coral snake pattern any one having a substantial amount of red, pink or orange in the dorsal colouration and/or found in some species of coral snake. The patterns usually consist of alternating bands or rings of black (or dark brown) and red, pink or orange, but some coral snakes have a uniform red dorsal (and ventral) colouration and a few others may only be spotted or blotched with black. In addition, while most venomous coral snakes have the body encircled by black and red rings and usually by yellow or white rings as well, a few species have bicolour black and yellow or black and white ringed patterns. For this reason we have included in this survey all kinds of bicolour snakes having alternating black and light rings around the body. Essentially bicoloured harmless and mildly toxic snakes having dark brown or black blotches or bands restricted to the dorsal and lateral areas of the body (e.g. Leptodeira nigrofasciata) are not considered to be mimics of bicolour coral snakes and are not included in this review. Also excluded from our definition of coral snake patterns, since they

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 237 occur in no venomous coral snakes, are patterns of snakes having narrow red, pink or orange dorsal and lateral stripes (e.g. some lhamnophis and Liophis), others with uniform or striped dorsums that have red, pink or orange venters (e.g. some species of Coniophanes, Rhadinaea, Trimetopon and Urotheca) or red, pink or orange venters and nuchal collars (e.g. Diadophis) or the dorsum suffused with one of these bright colours (e.g. Coluberjagellum). In view of the above discussion any definition of coral snake colouration must include two components, one emphasizing the presence of red, pink or orange colours and the second including all patterns found in the venomous coral snakes. Consequently our definition is inclusive and takes into account both colour and taxonomic parameters. Simply stated, coral snake colouration is defined as: any dorsal pattern found in a species of venomous coral snake andlor any dorsal pattern containing a substantial amount of red, pink or orange distributed in a fashion that resembles a pattern found in some species of venomous coral snake. COMPONENTS OF THE COLOUR PATTERN The following paragraphs are designed to identify and define major components of the colour pattern in coral snakes (venomous and otherwise). Although emphasis in the remaining sections of this paper will be on the dorsal pattern, the characteristics of other pattern components are often useful in discriminating among taxa and in evaluating mimicry. The principal elements of the colour pattern in these snakes are described below: 1. snout patern-if different from or discontinuous from the pattern on more posterior head shields, the snout region is most often uniform black (Fig. la, B) in the venomous coral snakes but it may be red, white or yellow (Fig. 1C) or the shields may be light and edged with dark or the reverse (Fig. 1D); 2. black head cap-the uniform black area variously covering the enlarged head shields (rostral, internasals, prefrontals, parietals, nasals, loreal, supralabials and circumocular series) on the top and sides of the head; the head cap may be continuous from the snout posteriorly (Fig. 1A) but in other cases the snout may be light in colour with the head cap restricted to the more posterior shields or it may be entirely lacking; in some cases the black snout colouration is separated from the head cap by a light bar across the prefrontal and/or interorbital area (Fig. 1B); 3. light prefrontal band-the light band running transversely across the prefrontal region in some forms that separates the dark (usually black) snout from the black head cap (Fig. 1B); 4. light prefrontal-interocular band-a light band running transversely across the head in some mimics that separates the dark snout colour from the dark head cap; 5. light interocular band-a light band running transversely across the head in some mimics that separates the dark snout from the dark head cap; 6. light head band-a red, orange, yellow or white area crossing the posterior head shields on the upper surface of the head and continuing a short distance onto the neck in most cases (Fig. 1A-C); 7. light nuchal collar-a light coloured collar around the neck that may cross the posterior portions of the parietals (Fig. 1D); 8. dark nuchal collar-a dark coloured band or ring across neck, posterior to

238 J. M. SAVAGE AND J. B. SLOWINSKI A C B D Figure I. Characteristic patterns of the head and nuchal regions in coral snakes. Stippled areas represent red; white areas yellow or white; black areas black. See text for explanation of components. the light head band or light nuchal collar when one of these is present (Fig. 1 A-D) ; 9. postnuchal light collar-a contrasting light collar located on the body posterior to the dark nuchal collar (Fig. 1A-D); 10. dorsal pattern-uniform or variously marked with dark or light; 11. tail pattern-uniform or variously marked with dark or light; similar to or different from dorsal pattern;

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 239 12. ventral pattern-uniform or variously marked with dark or light; 13. subcaudal pattern-uniform or variously marked with dark or light; similar to or different from ventral pattern. Components 3, 4 and 5 are essentially the same feature differing only in how far forward the dark head cap extends. Similarly, components 6 and 7, differ only in the degree to which the black nuchal collar extends anteriorly; if far anteriorly a light head band is produced (Fig. 1 A-C), if not a light nuchal collar is present (Fig. 1D). Much of the confusion regarding the concordance or lack thereof between presumed mimics and venomous coral snake models derives from the absence of a standardized system for categorizing the variation in dorsal colour patterns. In the system adopted in this paper emphasis is placed upon the nature of the black (sometimes dark brown) portion of the pattern for establishing a consistent terminology. The kinds of black markings found in snakes included in this review are defined as follows: spots-small regular or irregular markings covering a portion of a single scale, a single scale or several scales; blotches-regular or irregular figures covering many scales; saddles-saddle-shaped blotches extending only a short distance onto flanks; bands-continuous transverse markings that extend across the dorsum well onto the flanks or to the margin of the ventrals; rings-regular transverse markings that completely encircle the body; stripes-continuous longitudinal lines. A common cause of difficulty in studying colour pattern is the failure of many authors to discriminate between bands and rings. Because this difference is crucial for identification in many cases, the term band should only be used for markings restricted to and crossing the upper and lateral body surfaces. When the body pattern consists of bands or rings the several distinctive patterns may be defined based on the number of black components per light interspace or ring. For example in the simplest case (bicolour) the pattern is one of alternating black bands or rings and light (red, orange, yellow or white) bands or rings (one dark marking, one light). In tricolour and quadricolour banded or ringed snakes there are a variety of patterns. A classification of these elements for banded and ringed snakes follows: (I) Bicolour-alternating bands or rings of black and light (red, pink, orange, yellow or white; frequently red in the venomous coral snakes); one black component for each light component (1 black: 1 light). (11) Tricolour-alternating bands or rings of black, red and light (usually yellow, sometimes white): (a) tricolour monads-red bands or rings separated from one another by a sequence of alternating bands or rings of light-black-light; one black component between two red components (1 black: 1 red); (b) tricolour dyads-red bands or rings separated from one another by a sequence of alternating bands or rings of black-light-black; two black components between two red components (2 black: 1 red); (c) tricolour triads-red bands or rings separated from one another by a sequence of alternating bands or rings of black-light-black-light-black; three black components between two red components (3 black: 1 red); (d) tricolour tetrads-red bands or rings separated from one another by a

240 J. M. SAVAGE AND J. B. SLOWINSKI sequence of alternating bands or rings of black-light-black-light-black-lightblack; four black components between two red components (4 black: 1 red); (e) tricolour pentads-red bands or rings separated from one another by a sequence of alternating bands or rings of black-light-black-light-black-lightblack-light-black; five black components between two red components (5 black: 1 red). (111) Tricolour lacking black bands or rings-red rings separated from one another by an alternating sequence of white, yellow, white rings (0 black: 1 yellow: 1 red); (IV) Quadricolour-red or orange centred dyads (black-red-black or blackorange-black) outlined by white on a grey ground colour (2 black: 1 grey in terspace). Some authors (Taylor & Smith, 1943; Smith & Fitzgerald, 1986, for Scaphiodontophis) have called condition 11( b) above a triad because it consists of three elements (2 black and 1 light). Others (Klauber, 1943; Tanner, 1953, 1983; Zweifel, 1952, 1974, for some Lampropeltis) have taken the opposite tack for this pattern, calling the red ring plus the bordering black ring on each side a triad and assuming that the light ring separating the black rings is an interspace. We believe that these usages are inappropriate and confusing since the term triad has long been used for condition II(c) above (at least since Schmidt & Schmidt, 1925), especially to describe the pattern of many venomous coral snakes. Consequently, the terms dyad (for pairs of black bands or rings: II(b)) and triad (for trios of black bands or rings: II(c)) are adopted here to provide a consistent and logical terminology for these aspects of colour pattern. It should be noted that a few taxa with coral snake patterns (particularly some Lampropeltis) have the black body bands continuing irregularly onto the ventrals but these usually do not form complete rings. In these cases both white (or yellow) and/or red rings may be present. In the system adopted below these patterns are considered to be ringed and the light ring colour(s) will be mentioned. A CLASSIFICA TION OF CORAL SNAKE COLOUR PATTERNS The following outline indicates the principal colour patterns found in coral snakes. Each pattern type is denoted by a letter code that will be used in the taxonomic survey to follow (Figs 2-6) I. UNICOLOUR (U) A. Dorsum and venter red 1. unmarked (U) 2. nuchal black collar (Uc) B. Only dorsum red 1. unmarked (Ud) 2. nuchal black collar (Ucd) 11. BICOLOUR (BI) A. Spots or blotches 1. black a. spots (BIS) b. blotches (BIL)

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 24 1 Figure 2. Diagrammatic representations of spotted, blotched and striped coral snake patterns. 2. red blotches on light ground colour (BIr) 3. red blotches on black ground colour (Brb) B. Black bands 1. alternating (BIB) 2. fused dorsally (BIFb) C. Rings 1. black rings alternating with light () 2. black rings fused dorsally (BIF) 3. red bands on light (RB) D. Secondarily bicolour-black rings 1. suffused tricolour monads (BIM) 2. suffused tricolour dyads (BID) Figure 3. Diagrammatic representations of bicolour coral snake patterns. Colours as indicated in Fig. 2.

242 J. M. SAVAGE AND J. B. SLOWINSKI Figure 4. Diagrammatic representations of non-ringed tricoiour coral snake patterns. Colours as indicated in Fig. 2. E. Longitudinal pattern 1. dorsal area red, dark stripe(s) (LS) 2. dorsal area red, lateroventral area light (RL) 3. dorsum dark, lateral red stripe (S) 111. TRICOLOUR (T) A. Non-ringed patterns 1. black dorsal blotches and/or bands a. interspaces red dorsally (Tb) b. interspaces red ventrally (Tbx) c. interspaces yellow, red, yellow (Tbi) 2. black dorsal and lateroventral bands with red saddles on light ground colour (TYv) 3. black bands and lateroventral spots, with red bands above a. solid black bands (TXa) b. central red area in black bands (TX) 4. red bands (outlined by black) on light (TSR) 5. alternating black and red blotches (TBr) 6. saddles a. yellow or white (outlined in black) on red (Tsy) b. black (outlined in yellow) on red (Tsb) c. red (outlined in black) on yellow (Tsr) 7. tricolour monads: one black band per red band separated from one another by yellow (TMb)

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 243 Figure 5. Diagrammatic representations of tricolour banded and ringed coral snake patterns. Colours as indicated in Fig. 2. 8. tricolour dyads: two black bands per red band, black bands in contact with red separated from one another by yellow or white (TDb) 9. tricolour triads: three black bands per red band, outer black bands Figure 6. Diagrammatic representations of tricolour and quadricolour banded and ringed coral snake patterns. Colours as indicated in Fig. 2.

244 J. M. SAVAGE AND J. B. SLOWINSKI in contact with red, separated from inner black band by yellow or white (TTb) 10. tricolour striped (TS) B. Ringed in black, red and usually yellow (or white) 1. black rings, interspaces red above yellow or white below a. interspaces with red saddles (TZs) b. interspaces uniform red dorsally (TZ) 2. tricolour monads: one black ring per red ring, separated from one another by yellow rings (TM) 3. tricolour monads with accessory black elements (spots, bands, saddles or rings): one black ring per red ring with each red ring split by an accessory black element (TMa) 4. tricolour monads: black and/or yellow rings incomplete dorsally (TMi) 5. tricolour monads with incomplete white (or yellow) rings partially splitting black rings dorsally; red rings completely separated from black rings by complete yellow (or white) rings (TMs) 6. tricolour dyads: two black rings per red ring, black rings in contact with red rings and separated from one another by yellow (or white) rings (TD) 7. tricolour dyads with incomplete yellow (or white) rings partially splitting black rings dorsally a. red rings contact black rings on both sides (Td) b. red ring contacts black ring on one side, a yellow (or white) ring contacts black ring on other side (tdte) 8. tricolour dyads with red rings incomplete ventrally and venter mostly black (tdv) 9. tricolour dyads with incomplete red rings partially splitting black rings lateroventrally; black rings separated by yellow or white rings (td) 10. tricolour dyads with accessory yellow rings separating black from red rings (Tda) 11. tricolour triads: three black rings for each red ring; outer black rings in contact with red rings, separated from inner black ring by yellow or white rings (TT) 12. tricolour tetrads: four black rings for each red ring; outer black rings in contact with red rings, other black rings separated from one another by yellow (or white) rings (TTE) 13. tricolour pentads: five black rings per red ring; outer black rings in contact with red rings, other black rings separated from one another by yellow (or white) rings (TP) C. Ringed in white, yellow and red (NBR) IV. QUADRICOLOUR A. Saddles of red or orange outlined by black with a light margin on a grey ground colour (Qs) B. Banded with light-outlined red or orange centred dyads on a grey ground colour (QDb) C. Ringed by light-outlined red or orange centred dyads on a grey ground colour (QD)

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 245 It should be noted that in many species of coral snakes and their mimics the scales in the red areas have black tips. In certain cases the amount of black pigment increases ontogenetically and suffuses the red areas, sometimes obliterating the red entirely (e.g. bicolour Micrurus alleni). We have referred to these patterns as secondarily bicolour patterns (IID above). TAXONOMIC DISTRIBUTION IN AMERICAN SPECIES Non-venomous or mildly venomous presumptive coral snake mimics The following list is based on published reports and photographs and our own observations on living or recently killed specimens. Principal literature sources include, but are not restricted to: Campbell & Lamar (1989); Cei (1986); Conant (1975); Dixon & Soini (1986); do Amaral (1976); Duellman (1978); Freiberg (1982); Hecht & Marien (1956); Lancini (1979); Mehrtens (1987); Mertens (1956); Moonen, Eriks & Deursen (1979); Perez-Santos & Moreno ( 1988); Pough ( 1988) ; Roze ( 1966); and Stebbins ( 1966). Brattstrom (1955) and Pough (1988) provided lists of snakes having coral snake patterns. We have found that their surveys are rather incomplete and Pough's ( 1988; table 1 ) regional comparisons are consequently misleading. The number of American species (1 15; exclusive of the venomous coral snakes) potentially involved in this complex is really quite astonishing and approaches 18% of the total number of snake species found in the Americas. Of these about 90% have red in the colour pattern. We believe that we have included in this list all authentic records of New World snakes having a coral snake pattern as defined above. However, a number of species within the genera Apostolepis, Atractus, and Elapomorphus that have not been described or illustrated from life may prove to have substantial amounts of red in their colouration and might be added to this listing. An asterisk (*) indicates no red, orange or pink in the dorsal colouration. Light areas other than the red ones in the tricolour patterns are usually yellow or white. If some other light colour is involved it is noted. For species in which the dorsal pattern does not continue onto the venter, the ventral colouration is indicated. Codes separated by a comma indicate patterns found as variants on different individuals of the same species (e.g. TM, TT). Codes separated by a slash indicate variant patterns found on different parts of the body of one individual (e.g. TM/Ttb). Anilius scytale- Apostolepis (black nuchal collar variably present in some striped forms) ambiniger-ucd; venter cream ussimilis-ucd; venter white bum'oi-ls; venter cream cearensis-ucd; venter cream dorbignyi-ucd; venter white erythronota--1s; venter cream with paired lateral black spots fluvitorquata-ls, Ucd (rarely); yellow venter ventrimaculatus--1s; venter cream with black crossbands villaricae-ls; venter cream Atructus elaps-, TD, TT, TTE

246 J. M. SAVAGE AND J. B. SLOWINSKI etyfhromelas-bib, BIS; venter red with black spots guenfheri-bib; venter cream latifrons-td, TT, TTE obesus-td poeppingi-bif reticulatus-u; venter cream Cemophora coccinea-tdb, Tsr; venter white Chilomeniscus cinch-tb; venter cream Chionactis occipitalis-tbr, TZs; often no red; venter cream or white palarostris-tbr, TZs; venter cream Clelia juveniles of all species-ucd; venter white Dipsas articulata-tm bicolor-tzs breuifacies- gaigeae-tb gracilis- pauonina BIB* anteriorly; venter tan femporalis- fenuissima-b I R uiguieri- Drepanoides anomalus-ucd; venter cream Elaphe guffafa-bir, Tsr (rarely); venter blotched Javirufa-Tsr Elapomorphus (black nuchal collar variably present in striped forms) lemniscafus-ls; ventrals black with light edges lefiidur-ucd, LS; venter white rnerfmi-ucd; venter white puncfatw-ls, Ucd; venter white tticolor-ucd; venter white Erythrolamprus aesculapii-, TD, Tsy, TTE, Tda buupnfhuisiz-tdltdte, TTE bizona-td gumtheri-bid above/ below, TM mimus-tm, TMs pseudocorallw-tm Farancia abacura-bif, BIFb adults BIB, BIF, BIFb juveniles cryfrogramma-ts Geophis brachycephalw-brb, S; venter white to grey, usually banded with dark cancellafur-bib; venter cream duellman-bib (red or white); venter red or white luficincfw-bib; venter blackish russafus-bib; venter cream scmidoliafus-bib (white)/bib(red); venter immaculate (whitelred) or mottled zcledoni--s; venter uniform black Gyalopion quadranguluris-tbi; venter yellowish Helicofis angulata-tbx (tan)

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 247 HydrodFtes bicinctu-tx, TXa Hydrops martii-tm triangulum-; venter red Lampropeltis getulw-bib*, * (some) mexicanur-tsr, QS, QDb, QD, BID* pyromclunu-td; red and sometimes white rings triangulum-tsr, TSR, TDb, tdv, td, TD,, BID (red rings only) zonutu-bid*, TD, td Lcptodciru rubric&-bib; venter red Liophis unomulur-tb (some individuals), othen with lateral black blotches as well; venter yellow cpincphalur-bib; venter with dark markings frenata-bif poccilogyrus-tdb; venter with dark markings Lystrophis dorbigny-tsb, TYv, BIF, TbR; most of venter red histricus-tmb; venter red smicinctus-tdb; venter mostly black Nerodia fyciah-u, RB, TSR (some individuals); venter blotched Nma sebue-tmb, BIS, Ucd, BIS/UcD; venter cream Oryrhopus formosus-u (adults), BIB; venter cream leucomela-tz; venter cream mclunogcnys-ttb; venter cream occipitulis-ucd; venter cream pctolurius-bib (most individuals), TZs; venter cream rhombifcr-tbx, Tsb; venter cream trigeminur-ttb; venter cream vmezuclanur-tmb; venter cream Pseudo boa coronuta-ucd in juveniles; venter cream huai-rl, sometimes with a mid-dorsal stripe; venter cream ncuwiedii-ucd in juveniles and some adults; venter cream Rhinobothryum bovullii-tm lmtiginosum-tm Rhinochcilus lecontci-bib, TMb, Tsb; venter cream or white Scuphiodontophis annulutur-tdb; venter cream vmwtissimur-tmb; venter cream Scolecophis atrocinctur-tz; venter yellow Sibon anthracops-tm, TZ, TZs (no red on venter) unnulutur-, TD/TSR Sirnophis rhinostom-tt, TP, TP/TT rohdei-tt Siphlophis ccrvinur-tb, blotches often separated on mid-line; venter yellow Sonoru ucmulu-uc, TZs, TM/TD/TT

248 J. M. SAVAGE AND J. B. SLOWINSKI michoacanensis-uc,, TD, TD/td semiannulata-tb, TZ Stenorrhim fminvillii-ud, LS (rarely); dark ventral markings Tantilla rubra-ucd supracinch-tdb; venter red Thamnophis Couchi-TbR sirtalis-tbr Tripanurgos compressus-bil, BIB Tropidodipsas annulifera- fasciata-*, BIB* Jlscheri-*, BIB* philippii-* sartorii-, BIB zweifcli-* Urotheca elapoides-uc,, BIS, BIL, TM, TT, TTb, TMb, TMi euryrom-tz (no red on venter), *, Xenopholis scalari-bib; venter cream Among these genera Apostolepis, Clelia, Drepanoides, Elapomorphus, Oxyrhopus, Pseudoboa, Rhinobothpm, Siphlophis, Sonora, Stenorrhina, Tantilla, Tripanurgos and Xenopholis have grooved rear-fangs and a venom gland (Duvernoy s gland). Urotheca contains one striped species with grooved fangs, but the forms listed above lack them although their bites are known to cause definite toxic effects in human beings (Dunn, 1954; Seib, 1980). The putative coral snake mimics listed for these genera are regarded as mildly toxic and not dangerous to human beings, but their venoms are doubtless used to subdue prey. The listed species of the genera Clelia and Erythrolamprus, like the venomous coral snakes, are principally ophiophagous and Lampropeltis often consumes other snakes. Venomous coral snakes This review includes all species and putative subspecies listed by Roze (1983, 1987, 1989) and Campbell & Lamar (1989). When all subspecies have the same pattern only the inclusive species name is listed. A double asterisk (**) indicates that some representatives of that taxon have a tricolour monad pattern; a triple asterisk (***) indicates that some have a bicolour ringed (, BIM) or banded (BIMb) pattern. Unless otherwise noted bicolour species have a black and red pattern. UNIFORM (U) Micrurus diastcma alicnus (U, Uc)** BICOLOUR (BI) BLOTCHES BIL Micrurus bdi*** BIL Micruw limbatus (some)*** RINGS BIF Leptomirmrus collaris BIF Lcptomicrurus narduccii BIF Lcptomicrurus scutiuentfir

THE COLOURATION OF THE VENOMOUS CORAL SNAKES 249 BANDS BIB Micrurus bernadi Micrurus ephippijier ephippijier (black and yellow above, TM below) BIM BIM BIM BIF RINGS Micrurus alleni yatesi adult (black and yellow above, TM below) ** Micrurus annellatus annellatus adult (black and white or red)** Micrurus annellatus balzani adult (black and white or red)** Micrurus diastema apiatus Micrurus langsdorfi langsdorfi** (black and white above, TM below; some TM/) Micrurus langsdorfi omtissimus (black and white above, TM below)** Micrurus limbatus (some) Micrurus margaritijierus (black and white; white discontinuous; venter black and white or black, white and brown) Micrurus mipartitus (black and white, or ye 11 ow ) Micrurus multijiasciatus (black and white, red or yellow) Micrurus multkcutatus Micrurus nigrocinctus divaricatus* * Micrurus nigrocinctus zunilmis* * Micrurus peruvianus (black and yellow) * * Micrurus petersi (black and yellow) * Micrurus psyches psyches (black and white or yellow) Micrurus psyches donosoi Micrurus psyches medemi (black and yellow) * * Micrurus putumaynrris (black and yellow) Micrurus rwtanus Micrurus spurrelli (black and white) Micrurus stewarti TRICOLOUR MONADS (TM) RINGS Micruroides euryxanthus Micrurus alleni alleni Micrurus alleni yatesi juvenile* * * Micrurus annellatus annellatus juvenile* ** Micrurus annellatus balzani juvenile* ** Micrurus annellatus bolivianus Micrurus averyi Micrurus bogcrti Micrurus browni Micrurus clarki Micrurus corallinus Micrurus diastema @nis Micrurus diastema aglaeope (TMa) Micrurus diastema alienus Micrurus diastema diastema (some TMb) Micrurus diastema macdougalli Micrurus diastema sappm' Micrurus distm Micrurus dumm'lii antioguiensis Micrurus dumm'lii carinicauda Micrurus dumm'lii transandinus Micrurus dumm'lii venezuelmu

250 J. M. SAVAGE AND J. B. SLOWINSKI RINGS Mimrus ephippifcr zapotecus (TMa, black spots, bands or saddles in red rings) Micrurus fulvius Micrurus hippocrepis TM/TMi Micrurus langsdo@ langsdorfz (some TM/)*** Micrurus langsdorfz omatissimus* * Micrurus 1atiJiiciatus Mimrus mcrtm Micrurus ncbularis Micrurus nigrocinctw nigrocinctus Micrurus nigrocinctus babaspul Micrurus nicrocinctus coibmris Micrurus nigrocinctus divaricatuss * * Micrurus nigrocinctus mosguilmfis Micrurus nigrocinctus zunilm s* * Mimrus pmvianus*** Micrurus petcrsi*** Mimrus proximans Micrurus psychs circinalis Micrurus psyches mcdcmi* * Micrurus psyches paraensis Micrurus psyches remotus Micrurus stdndachncri Micrurus stuarti TRICOLOUR DYADS (None) TRICOLOUR TRIADS (TT) RINGS Micrurus bocourti RINGS M imcrus catamayenu M icrurus decoratus M icrurus dissolnccus M icrurus dumm lii dumcrilii M icrurus dumm lii colombianus M icrurus jlifomis M imrus fronhjkwiatus M icrurus fronhlis M icrurus hcmprichii M icrurus ibiboboca M imrus isozonus M ~imrus laticollaris Mimrus lcmniscatus Micrurus sangilmis Micrurus spixii Micrurus surinammis Micrurus tschudii TRICOLOUR TETRADS (TTE) (None) TRICOLOUR PENTADS (TP) RINGS Micrurus elcgans (black blotches in some orange rings) TRICOLOUR WHITE, YELLOW AND RED (NBR) RINGS Micrurus langsdorfi langsdorfz**. * * *, Significantly, the head pattern and colouration in tricolour venomous coral snakes generally corresponds to that on the body. In most species having the tricolour monad pattern, the white or yellow head band or nuchal collar, black nuchal collar and postnuchal light collar represent the first monad. Micruroides euryxanthus is an exception for although it has a white nuchal collar it lacks a black one and the first monad is located several head lengths posterior to the nuchal region. In typical tricolour triad forms the black nuchal collar is the anterior black element in the first triad and the light head band or nuchal collar is usually red. Micrurus dissoleucus, Micrurus laticollaris and some Micrurus spixii are unusual in lacking red on the dorsum of the head. COLOURATION AND MIMICRY The 56 species of venomous coral snakes are essentially restricted to the Neotropics in distribution, although one species (Micrurus fuluius) occurs in the south-eastern United States and another (Micruroides euryxanthus) is found in the southern arid regions of New Mexico and Arizona and in adjacent Mexico. Members of this lineage are active at night and during the day under conditions of low illumination (i.e. inside forests). They tend to be secretive and feed primarily on other snakes (including their own species), although several South American forms (Micrurus lemniscatus and Micrurus surinamensis) also eat

THE COLOURATION OF THE VENOMOUS CORAL SNAKES freshwater fishes and one (Micrurus hemprichii ortoni) prefers onychophorans (genus Periputus). Known predators on coral snakes are primarily birds (see Brugger, 1989) and snake-eating snakes. Available evidence indicates that envenomation by coral snakes may kill large raptors but there are recorded cases of successful avian predation on these snakes (Smith, 1969). Many species of coral snakes exhibit defensive behaviours that are keyed to reducing predation. Some or all of these behaviours may be used by a single individual and include hiding the head under the body coils, flattening the body, coiling the tail to expose the bright colours on the underside and waving the tail about. In addition the head may be withdrawn from hiding and swung from side to side with the mouth open and ready to bite any object that is contacted, the body may be snapped back and forth almost spasmodically, the tail may be used to strike aggressively or waved to divert attention from the head and the contents of the cloaca may be discharged with or without a series of loud popping sounds. The idea that the bright colouration typical of venomous coral snakes is also an antipredator defense that performs an aposematic (warning) function and that other similarly coloured snakes are mimics has been long and hotly debated (Dunn, 1954; Brattstrom, 1955; Hecht & Marien, 1956; Mertens, 1956; Wickler, 1968; Grobman, 1978), although A. R. Wallace (1867, 1870) long ago concluded that mimicry was involved. Contrasting patterns of alternating black and light bands or rings are found in many species of snakes (Brattstrom, 1955). In these forms, including the venomous coral snakes, the pattern serves a cryptic function serving to hide them from predators (Brattstrom, 1955; Jackson, Ingram & Campbell, 1976; Pough, 1976). However, there now seems to be little question that the bright coral snake colour patterns combined with the unusual behaviours described above are important antipredator defences that act through the vision of potential predators on venomous coral snakes to warn them that they may be subject to a serious venomous bite (Greene, 1988; Pough, 1988; Campbell & Lamar, 1989). In some cases, predator avoidance of coral snake colour patterns probably involves learning based upon an unpleasant experience with a coral snake bite. Because of their short fangs and the need to chew to ensure envenomation, coral snakes frequently inject only small and not necessarily deadly amounts of venom so that predators probably often survive bites (e.g. Smith, 1969). The carefully designed experiments of S. Smith (1975, 1977), however, demonstrate innate avoidance of a coral snake pattern by several potential avian predators, including motmots (Eumomota) and kiskadees (Pitunow). Smith s studies convincingly established the reality of aposematic colouration in coral snakes and their mimics. Both Batesian and Miillerian mimicry have been proposed as explanations for the coral snake mimicry guild. Additionally, Wickler (1968) popularized the concept that the highly venomous coral snakes and the harmless mimics were mimicking the mildly toxic, rear-fanged forms, a type of mimicry he called Mertensian. However, we agree with Greene & McDiarmid (1981) that the term is unnecessary since it represents a form of Batesian mimicry. That some kind of mimicry is involved is attested to by the precise resemblances in colouration between non-coral snakes and sympatric venomous coral snakes and the concordant geographic variation between the two (Savage & Vial, 1974; Greene & McDiarmid, 1981; Roze, 1983). We support the concept that Batesian 25 I

252 J. M. SAVAGE AND J. B. SLOWINSKI mimicry is involved with the venomous coral snakes being the models and the other forms the mimics. Nevertheless, it seems unlikely that all of the diverse colour patterns described in this paper actually evoke an avoidance response in predators. Consequently, we have attempted to identify those colour patterns that are most likely to be involved in coral snake mimicry and the taxa which may be regarded with some confidence to be members of the coral snake mimic guild. There can be little question that snakes having ringed tricolour patterns (IIIB) are mimics since these patterns are identical to, or closely resemble the most common colourations in venomous coral snakes. Similarly, tricolour forms having the black body bands arranged in monads, dyads or triads (IIA 8-10) resemble both tricolour ringed coral snakes and ringed mimics in their dorsal patterns and are almost certainly mimics as well. Most snakes exhibiting other non-ringed tricolour patterns are probably mimics. However, we are sceptical regarding the role of the colour patterns in Elaphe (Tsr, BIr) and Nerodia (U, TSR, RB) and do not consider the patterns in Thamnophis and Farancia erytrogramma (TS) to be involved in mimicry since they do not even superficially resemble the pattern of any venomous coral snake. The several quadricolour patterns (IVA-C) are essentially modifications of tricolour ones and snakes having them are considered mimics. Snakes having bicolour ringed or banded patterns (IIB-C) of black and red are doubtless mimics of similarly marked venomous coral snakes. The same may be said for bicolour black and white or yellow ringed forms since they have patterns typical of some bicolour venomous coral snakes. We are dubious as to whether all black and white or yellow banded snakes (BIB*) are mimics since this pattern has a cryptic function and is frequently found in arboreal forms or in species that do not co-occur geographically with venomous coral snakes. The mimetic role of all other bicolour black and red patterns is questionable although those with a substantial amount of red may sufficiently resemble banded or unicolour species to gain some protection. Although only one species (Micrurus diastema) of venomous coral snakes includes individuals that have a uniform red body, we believe that this colouration serves an aposematic function in these individuals and in a series of mildly toxic and harmless snakes. Consequently, we regard the latter as members of the mimic guild although the suspected role of the uniform, bright red colouration remains to be confirmed. According to this analysis the following genera contain species that may be regarded as coral snake mimics; an asterisk (*) means that all members of the genus may be so considered: Anilius*, Apostolepis, Atractus, Cemophora*, Elapomorphus, Erythrolamprus*, Farancia, Geophis, Gyalopion, Hydrops*, Lampropeltis, Leptodeira, Liophis, Lystrophis, Ninia, Oxyrhopus, Pseudoboa, Rhinobothryum*, Rhinocheilus*, Scaphiodontophis*, Scolecophis*, Sibon, Simophis*, Siphlophis, Sonora, Stenorrhina, Stilosoma*, Tantilla, Tripanurgos*, Tropidodipsas, Urotheca and Xenopholis*. Those individuals interested in further investigation of coral snake mimicry should concentrate their attention on these genera and co-occurring venomous coral snakes. More studies are certainly in order to determine how widespread innate avoidance of coral snakes by predators may be. In addition, although difficult to test, the role of empathetic learning in the origin and maintenance of

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