savage, slowinski - 1992 - the colour at ion of the venomous coral snakes (family elapidae) and...

8/9/2019 Savage, Slowinski - 1992 - The Colour at Ion of the Venomous Coral Snakes (Family Elapidae) and Their Mimics (Fa

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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 (familiesAniliidae and Colubridae)JAY M . SAVAGE, F.L.S. AND JOSEPH B. SLOWINSKIDepartment 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 (familyElapid ae) and a series of harmless or mildly toxic mimics form a n im po rtan t compone nt of the snakefauna of the Americas. Coral snak e patterns are defined as any dorsal pa ttern found in a ny species ofvenomous coral snake and/ or any dorsal pattern containing a substantial amou nt of red, pink ororange distributed so as to resemble that of some species of venomous coral snake. Th e com ponen tsof coral snake colouration a re described and fou r principal dorsal patterns are recognized: unicolour,bicolour, tricolour and quadrico lour. Th e tricolour patterns may be further clustered based on thenum ber of black bands or rings separating the red ones as: monads, dyads, triads, tetrads o r pentads.A detailed classification of all coral snake colour patterns is presented a nd each p atte rn is illustrated.The taxonomic distribution of these patterns is surveyed for mimics and the 56 species of highlyvenomous coral snakes. Among the latter, the most frequent encountered patterns are tricolourmonads, tricolour triads and bicolour rings, in that order. No venomous coral snakes have atr icolour dyad , tr icolour te trad o r quadricolour pattern .As many as I15 species of harmless or mildly toxic species, c . 18% of all American snakes, areregarded as coral snake mimics. The colouration and behavioural traits of venomous coral snakescombine to form a significant an tipr eda tor defence of an ap osematic type. T h e mimics in turnrereive protection from predators th at innately o r through learn ing avoid coral snak e colourpatterns. The precise resemblances in colouration between sympatric non-coral snakes andvenomous coral snakes and the concordant geographic variation between the two strongly supportthis view. Batesian mimicry with the highly venomous coral snakes as the models and the otherforms as the mimics is the favoured explanation for this situation. It is further concluded that anumber of species in the genera Elaphc, Farancia, Nerodia an d Thamnophis, although having red intheir colouration, should not be included in the coral snake mimic guild.KEY WORDS:-Coral snakes ~ colouration ~ mimicry.

C O N T E N T SIntroduction . . . . . . . . . . . . . . .Definition of coral snake colouratio n . . . . . . . . .Components of the colour patte rn . . . . . . . . . .A classification of coral snake colour patterns . . . . . . .Taxonomic distribution in American species . . . . . . .Non-venomous or mildly venomous presumptive coral snake mimics.

Venomous coral snakes . . . . . . . . . . .References . . . . . . . . . . . . . . .Colouration and mimicry . . . . . . . . . . . .

. . . . 23 6. . . . 23 6. . . . 23 7. . . . 24 0. . . . 24 5. . . . 245

. . . . 248. . . . 250. . . . 25 323 5002+4066/92/030235 +20 S03.00/0 0 992 T he L innean Society of London


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236 J. M . SAVAGE AND J . B. SLOWINSKIINTRODUCTION

During a course of studies on the New World venomous coral snakes (familyElapidae) and their presumed aglyphous and opisthoglyphous mimics we werestruck by the absence of consistent terminology to describe major aspects oftheir colour patterns. Since these patterns are often utilized to distinguishbetween allied taxa and may be of significance in establishing relationships, thisinconsistency hampers systematic studies of both the highly venomous speciesand the guild of coral snake mimics. In addition, the lack of a uniformterminology inhibits attem pts to establish congru ence in colouration between th esupposed 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 amuch more detailed analysis is developed and we address the problem in depthby: ( 1 ) identifying and defining the major components of colour pattern in thesegroups; ( 2 ) establishing a consistent terminology to describe variation in thepatterns and; (3) summarizing the taxonomic occurrence of the various patterns.In the following sections the term venomous coral snakes refers toproteroglyphous elapids of the genera Leptomicrurus, Micrurus an d Micruroides.The term mimic is used to denote aniliid and colubrid snakes that resemblevenomous coral snakes an d which a re non-venomous o r mildly toxic and lack theadvanced venom delivery system (rigid canaliculate anteriorly placed fangs onthe upper jaw and venom gland compressor muscles) found in elapids.

DEFINITION O F CORAL SNAKE COLOURATIONAn initial consideration in undertaking this review was the need to delimitthose elements of pattern that constitute coral snake colouration since thevenomous coral snakes (th e nom inal gen era Leptomicrurus, Micruroides a n dMicrurus) an d their harmless to mildly toxic mimics display a sub stantial rang e ofvariation in colouration. Thro ug ho ut the Americas snakes having a considerableam ou nt of red, pink o r orange in their colouration are called coral snakes, corales(Spanish) o r cobras-coraes (Portuguese) and almost all venomous coral snakes andtheir mimics are known by these names. Consequently we have taken our cuefrom the vernacular names a nd define as a coral snake patte rn any one having asubstantial amo un t of red, pink or orange in the dorsal colouration and/or foundin some species of coral snake.The patterns usually consist of alternating bands or rings of black (or darkbrown) and red, pink or orange, but some coral snakes have a uniform red dorsal(a nd ventral) colouration an d a few others may only be spotted o r blotched withblack. In add ition, while most venomous coral snakes have the bod y encircled byblack and red rings and usually by yellow or white rings as well, a few specieshave bicolour black and yellow or black and white ringed patterns. For thisreason we have included in this survey all kinds of bicolour snakes havingalternating black and light rings around the body. Essentially bicolouredharmless and mildly toxic snakes having dark brown or black blotches or bandsrestricted to the dorsal an d lateral areas of the bod y (e.g. Leptodeira nigrofasciata)

are not considered to be mimics of bicolour coral snakes an d ar e not in cluded inthis review. Also excluded from ou r definition of coral snake patterns, since they


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T H E C O L O U R A TI O N OF T HE V E N OM O U S C OR A L S N A KES 237occur 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, pinkor orange venters and nuchal collars (e.g. Diadophis) or the dorsum suffused withone of these bright colours (e.g. Coluberjagellum).In view of the above discussion any definition of coral snake colouration mustinclude two components, one emphasizing the presence of red, pink or orangecolours and the second including all patterns found in the venomous coralsnakes. Consequently our definition is inclusive and takes into account bothcolour and taxonomic parameters. Simply stated, coral snake colouration isdefined as: any dorsal pattern fo un d in a species of venomous coral snake andlor any dorsalpattern containing a substantial amount of red, pink or orange distributed in a fashion thatresembles a pattern found in some species of venomous coral snake.

C OM P ON E N T S OF T HE C OL OU R P A T T E RNThe 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 dorsalpattern, the characteristics of other pattern components are often useful indiscriminating among taxa and in evaluating mimicry. The principal elements ofthe colour pattern in these snakes are described below:

1 . snout patern-if different from or discontinuous from the pattern on moreposterior 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 theshields may be light and edged with dark or the reverse (Fig. 1D);2. black head cap-the uniform black area variously covering the enlargedhead shields (rostral, internasals, prefrontals, parietals, nasals, loreal,supralabials and circumocular series) on the top and sides of the head; the headcap may be continuous from the snout posteriorly (Fig. 1A) but in other casesthe snout may be light in colour with the head cap restricted to the moreposterior shields or i t may be entirely lacking; in some cases the black snoutcolouration is separated from the head cap by a light bar across the prefrontaland/or interorbital area (Fig. 1B);3. light prefrontal band-the light band running transversely across theprefrontal region in some forms that separates the dark (usually black) snoutfrom the black head cap (Fig. 1B);4. light prefrontal-interocular band-a light band running transverselyacross the head in some mimics that separates the dark snout colour from thedark head cap;5 . light interocular band-a light band running transversely across the headin 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 posteriorhead shields on the upper surface of the head and continuing a short distanceonto the neck in most cases (Fig. 1A-C);7. light nuchal collar-a light coloured collar around the neck that may crossthe posterior portions of the parietals (Fig. 1D);8. dark nuchal collar-a dark coloured band or ring across neck, posterior to


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238

A

B

J. M . SAVAGE AND J . B. SLOWINSKI

C

D

Figure I . Characteristic patterns of the head and nuchal regions in coral snakes. Stippled areasrepresent red; white areas yellow or white; black areas black. See text for explanation ofcomponents.

the light head band or light nuchal collar when one of these is present (Fig.9. postnuchal light collar-a contrasting light collar located on the body10. dorsal pattern-uniform or variously marked with dark or light;1 1. tail pattern-uniform or variously marked with dark or light; similar to or

1A-D) ;posterior to the dark nuchal collar (Fig. 1A-D);

different from dorsal pattern;


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THE COLOURATION OF THE VENOM OUS CORAL SNAKES 23912. 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 howfar 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 faranteriorly a light head band is produced (Fig. 1A-C), if not a light nuchal collaris present (Fig. 1D).Much of the confusion regarding the concordance or lack thereof betweenpresumed mimics and venomous coral snake models derives from the absence ofa standardized system for categorizing the variation in dorsal colour patterns. Inthe system adopted in this paper emphasis is placed upon the nature of the black(sometimes dark brown) portion of the pattern for establishing a consistentterminology. The kinds of black markings found in snakes included in this revieware 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 wellrings-regular transverse markings that completely encircle the body;stripes-continuous longitudinal lines.

onto the flanks or to the margin of the ventrals;

A common cause of difficulty in studying colour pattern is the failure of manyauthors to discriminate between bands and rings. Because this difference iscrucial for identification in many cases, the term band should only be used formarkings restricted to and crossing the upper and lateral body surfaces.When the body pattern consists of bands or rings the several distinctivepatterns may be defined based on the number of black components per lightinterspace or ring. For example in the simplest case (bicolour) the pattern is oneof alternating black bands or rings and light (red, orange, yellow or white) bandsor rings (one dark marking, one light). In tricolour and quadricolour banded orringed snakes there are a variety of patterns. A classification of these elements forbanded 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 blackcomponent for each light component ( 1 black: 1 light).(11) Tricolour-alternating bands or rings of black, red and light (usuallyyellow, sometimes white):(a) tricolour monads-red bands or rings separated from one another by asequence of alternating bands or rings of light-black-light; one black componentbetween two red components ( 1 black: 1 red);(b ) tricolour dyads-red bands or rings separated from one another by asequence of alternating bands or rings of black-light-black; two blackcomponents between two red components (2 black: 1 red);(c) tricolour triads-red bands or rings separated from one another by asequence of alternating bands or rings of black-light-black-light-black; threeblack components between two red components (3 black: 1 red);(d) tricolour tetrads-red bands or rings separated from one another by a


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240 J. M . SAVAGE AND J . B. SLOWINSKIsequence of alternating bands or rings of black-light-black-light-black-light-black; four black components between two red components (4 black: 1 red);(e) tricolour pentads-red bands or rings separated from one another by asequence of alternating bands or rings of black-light-black-light-black-light-black-light-black; five black components between two red components (5 black:1 red).(111) Tricolour lacking black bands or rings-red rings separated from oneanother by an alternating sequence of white, yellow, white rings (0 black: 1yellow: 1 red);(IV) Quadricolour-red or orange centred dyads (black-red-black or black-orange-black) outlined by white on a grey ground colour (2 black: 1 greyin terspace).Some authors (Taylor & Smith, 1943; Smith & Fitzgerald, 1986, forScaphiodontophis) have called condition 11(b) above a triad because it consists ofthree elements (2 black and 1 light). Others (Klauber, 1943; Tanner, 1953,1983; Zweifel, 1952, 1974, for some Lampropeltis) have taken the opposite tack forthis pattern, calling the red ring plus the bordering black ring on each side atriad and assuming that the light ring separating the black rings is aninterspace. We believe that these usages are inappropriate and confusing sincethe term triad has long been used for condition II(c) above (at least sinceSchmidt & Schmidt, 1925), especially to describe the pattern of many venomouscoral snakes. Consequently, the terms dyad (for pairs of black bands or rings:II(b)) and triad (for trios of black bands or rings: I I( c) ) are adopted here toprovide a consistent and logical terminology for these aspects of colour pattern.It should be noted that a few taxa with coral snake patterns (particularly someLampropeltis) have the black body bands continuing irregularly onto the ventralsbut these usually do not form complete rings. In these cases both white (oryellow) and/or red rings may be present. In the system adopted below thesepatterns are considered to be ringed and the light ring colour(s) will bementioned.

A CLASSIFICATION OF C OR A L SN A KE C OLOU R PATTERNSThe following outline indicates the principal colour patterns found in coralsnakes. Each pattern type is denoted by a letter code that will be used in thetaxonomic survey to follow (Figs 2-6)I. UNICOLOUR (U)A. Dorsum and venter red1. unmarked (U)2. nuchal black collar (Uc)

1 . unmarked (Ud)2. nuchal black collar (Ucd)B. Only dorsum red

11 . BICOLOUR (BI)A. Spots or blotches1 . black

a. spots (BIS)b. blotches (BIL)


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THE COLOURATION OF THE VENO MOUS CORAL SNAKES 24 1

Figure 2. Diagramm atic representationsof spotted, blotched and striped coral snake patterns.

2. red blotches on light ground colour (BIr)3. red blotches on black ground colour (Brb)1 . alternating (BIB)2. fused dorsally (BIFb)1 . black rings alternating with light (BIR)2. black rings fused dorsally (BIF)3. red bands on light (RB)1. suffused tricolour monads (BIM)2. suffused tricolour dyads (BID)

B. Black bands

C. Rings

D. Secondarily bicolour-black rings

Figure 3. Diagrammatic representations of bicolour coral snake patterns. Colours as indicated inFig. 2.


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242 J. M. AVAGE AND . B. SLOWINSKI

Figure 4. Diagrammatic representations of non-ringed tricoiour coral snake patterns. Colours asindicated in Fig. 2.

E. Longitudinal pattern1. 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 patterns1. black dorsal blotches and/or bandsa. 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 lightground colour (TYv)3. black bands and lateroventral spots, with red bands abovea. 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. saddlesa. 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 oneanother by yellow (TMb)


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THE COLOURATION O F 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 white9 . tricolour triads: three black bands per red band, outer black bands( T D b )

Figure 6 . Diagrammatic representations of tricolour and quadricolour banded and ringed coralsnake patterns. Colours as indicated in Fig. 2.


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244 J. M . SAVAGE AND J. B.SLOWINSKIin contact with red, separated from inner black band by yellow orwhite (TTb)10. tricolour striped (TS)B. Ring ed in black, red an d usually yellow (o r white)1. black rings, interspaces red above yellow or white belowa. interspaces with red saddles (TZs)b. interspaces uniform red dorsally (TZ)2. tricolour monads: one black ring per red ring, separated from oneanother by yellow rings ( T M )3. tricolour monads with accessory black elements (spots, bands,saddles or rings): one black ring per red ring with each red ringsplit by an accessory black element (TMa)4. tricolour monads: black and/or yellow rings incomplete dorsally( T M i )5. tricolour m onads w ith incom plete white (o r yellow) rings partiallysplitting black rings dorsally; red rings completely separated fromblack rings by complete yellow (or white) rings (TMs)6. tricolour dyads: two black rings per red ring, black rings in contactwith red rings an d separated from on e an oth er by yellow (o r white)rings (TD)7. tricolour dyads with incomplete yellow (or white) rings partiallysplitting black rings dorsallya. red rings contact black rings on both sides (Td)b. red ring contacts black ring on on e side, a yellow ( o r white) ring

8. tricolour dyads with red rings incomplete ventrally and ventermostly black (tdv)9. tricolour dyads with incomplete red rings partially splitting blackrings lateroventrally; black rings separated by yellow or white rings

10. tricolour dyads with accessory yellow rings separating black fromred rings (Tda)11. tricolour triads: three black rings for each red ring; outer blackrings in contact with red rings, separated from inner black ring byyellow or white rings (TT)12. tricolour tetrads: four black rings for each red ring; outer blackrings in con tact with red rings, oth er black rings separated from o neanother by yellow ( or white) rings ( T T E )13. tricolour pentads: five black rings per red ring; out er black rings incontact with red rings, other black rings separated from oneanother by yellow (o r white) rings ( T P )

contacts black ring on other side (tdte)

( t d )

C. Ringed in white, yellow an d red ( N B R )A. Sadd les of red or orange outlined by black with a light margin on agrey ground colour (Qs)B. Banded with light-outlined red or orange centred dyads on a greyground colour (QDb)C. Ringed by light-outlined red or orange centred dyads on a greyground colour (QD)

IV . Q U A D R I C O L O U R


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THE COLOURATION OF THE VENO MOUS CORAL SNAKES 245It should be noted that in many species of coral snakes and their mimics thescales in the red areas hav e black tips. I n certain cases the am o un t of blackpigment increases ontogenetically and suffuses the red areas, sometimesobliterating the red entirely (e.g. bicolour Micrurus alleni). We have referred tothese patterns as secondarily bicolour patterns ( I I D abo ve ).

TAXONOMIC DISTRIBUTION IN AMERICAN SPECIESNon-venomous or mildly venomous presumptive coral snake mimics

T h e following list is based on published reports and pho tographs an d o ur ownobservations on living or recently killed specimens. Principal literature sourcesinclude, but are not restricted to: Campbell & La m ar (1989); Cei (1986);Co nan t (1975); Dixon & Soini (198 6); d o Am aral (1976); Duellman (1978);Freiberg (1982); Hecht & Marien (1956); Lancini (1979); Mehrtens (1987);Mertens (1956 ); Moo nen, Eriks & Deursen (19 79); Perez-Santos & Moreno( 1988); Pough ( 1988); Roze ( 1966); an d Stebbins ( 1966).Brattstrom (1955) and Pough (1988) provided lists of snakes having coralsnake patterns. We have found that their surveys are rather incomplete andPough's ( 1988; table 1 ) regional comparisons are consequently misleading. Thenumber of American species (1 15; exclusive of the venomous coral snakes)potentially involved in this complex is really quite astonishing and approaches18% of the to tal nu mb er of snake species found in the Am ericas. O f these ab ou t90 % have red in the colour patte rn. W e believe th at we have included in this listall authentic records of New World snakes having a coral snake pattern asdefined above. However, a number of species within the genera Apostolepis,Atractus, and Elapomorphus that have not been described or illustrated from lifemay prove to have substantial amoun ts of red in their colouration a nd might beadded to this listing.An asterisk ( * ) indicates no red, orange or pink in the dorsal colouration.Light areas other th an the red ones in the tricolour patte rns a re usually yellow orwhite. If some oth er light co lour is involved it is noted. For species in which thedorsal pattern does not continue onto the venter, the ventral colouration isindicated. Codes separated by a comma indicate patterns found as variants ondifferent individuals of the same species (e.g. T M , TT). Codes separated by aslash indicate variant patterns found on different parts of the body of oneindividual (e .g. TM/Ttb).AniliusApostolepis (black nuchal collar variably present in some striped forms)scytale-BIRambiniger-Ucd; venter creamussimilis-Ucd; venter whitebum'oi-LS; venter creamcearensis-Ucd; venter creamdorbignyi-Ucd; venter wh iteerythronota--1s; venter cream with paired lateral black spotsfluvitorquata-LS, Uc d ( rar ely ); yellow venterventrimaculatus--1s; venter cream with black crossbandsvillaricae-LS; venter cream

elaps-BIR, TD, TT, TTEAtructus


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246 J. M . SAVAGE AND J. B. SLOWINSKIetyfhromelas-BIB, BIS; ven ter red with black spotsguenfheri-BIB; ve nt er cr eamlatifrons-TD, T T , T T Eobesus-Tdpoeppingi-BIFreticulatus-U; ven ter creamcoccinea-TDb, Ts r; vente r whitecinch-Tb ; venter creamoccipitalis-TBr, TZ s; often no red; vente r cre am or whitepalarostris-TBr, TZ s; vente r cre amjuveniles of all species-Ucd; vente r whitearticulata-TMbicolor-TZsbreuifacies-BIRgaigeae-Tbgracilis-BIRpauonina BIB* anteriorly; venter tanfemporalis-BIRfenuissima-B IRuiguieri-BIRanomalus-Ucd; vente r cre amguffafa-BIr, Tsr (rare ly) ; ven ter blotchedJavirufa-Tsrlemniscafus-LS; ven trals black with ligh t edgeslefiidur-Ucd, LS; venter whiternerfmi-Ucd; venter whitepuncfatw-LS, Uc d; venter whitetticolor-ucd; vente r whiteaesculapii-BIR, T D , Tsy, T T E , T d abuupnfhuisiz-TDltdte, T T Ebizona-TDgumtheri-BID abo ve/B IR below, T Mmimus-TM, TM spseudocorallw-TMabacura-BIF, BI Fb adult scryfrogramma-TSbrachycephalw-Brb, S; venter white to grey, usually banded with darkcancellafur-BIB; ven te r cr ea mduellman-BIB (red or white); venter red or whiteluficincfw-BIB; ve nter black ishrussafus-BIB; ve nt er crea mscmidoliafus-BIB (w hit e)/ BI B (re d); ven ter imm acu late (wh itelre d) or mottledzcledoni--S; ven ter uni form blackquadranguluris-Tbi; ve nter yellow ishangulata-Tbx (tan)

CemophoraChilomeniscusChionactis

CleliaDipsas

DrepanoidesElaphe

Elapomorphus (black nuchal collar variably present in striped forms)

Erythrolamprus

FaranciaBIB, BIF, BI Fb juveniles

Geophis

GyalopionHelicofis


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THE COLOURATION OF THE VENOMOUS CORAL SNAKES 247HydrodF te sHydropsbicinctu-TX, T X amartii-TMtriangulum-BIR; venter red

getulw-BIB*, B IR * (some)mexicanur-Tsr, QS, Q D b , Q D , BID *pyromclunu-TD; red an d some times wh ite ringstriangulum-Tsr, TS R , TD b, tdv, td, T D , BIR , BID (red rings only)zonutu-BID*, T D , tdrubric&-BIB; ve nte r redunomulur-Tb (some individuals), ot h e n with lateral black blotches as well; venter yellowcpincphalur-BIB; venter with da rk mark ingsfrenata-BIFpoccilogyrus-TDb; venter with da rk marking sdorbigny-Tsb, TY v, BIF, T b R ; most of venter redhistricus-TMb; vente r redsmicinctus-TDb; venter mostly black

fyciah-U, RB, T S R (some individ uals); venter blotchedsebue-TMb, BIS, Ucd , BIS /UcD ; venter creamformosus-U (a du lt s) , BIB; ve nt er cr eamleucomela-TZ; ven ter cre ammclunogcnys-TTb; venter cr ea moccipitulis-Ucd; ven ter cr ea mpctolurius-BIB (mo st indiv idua ls), TZ s; ven ter cr eamrhombifcr-Tbx, Ts b; ven ter cr eamtrigeminur-TTb; vente r creamvmezuclanur-TMb; ven ter cr eamcoronuta-Ucd in juveniles; ven ter creamhuai-RL, sometimes with a mid-dorsal stripe; venter crea mncuwiedii-Ucd in juveniles an d some adu lts; ve nte r creambovullii-TMlmtiginosum-TMlecontci-BIB, T M b , Ts b; venter cream or whiteannulutur-TDb; ven ter cre amvmwtissimur-TMb; ven ter cre amatrocinctur-TZ; ven ter yellowanthracops-TM, TZ , TZ s (no red on venter)unnulutur-BIR, TD/TSRrhinostom-TT, TP , T P /T Trohdei-TTccrvinur-Tb, blotches often sep ara ted on mid-line; venter yellowucmulu-Uc, TZ s, T M / T D / T T

Lampropeltis

LcptodciruLiophis

Lystrophis

NerodiaN m aOryrhopus

Pseudoboa

Rhinobothryum

RhinochcilusScuphiodontophis

ScolecophisSibon

Sirnophis

SiphlophisSonoru


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248 J. M . SAVAGE AND J . B. SLOWINSKImichoacanensis-Uc, B IR , T D , T D /t dsemiannulata-Tb, T Zfminvillii-Ud, LS (rarely); dark ventral markingsrubra-Ucdsupracinch-TDb; ven ter red

StenorrhimTantilla

ThamnophisCouchi-TbRsirtalis-TbRcompressus-BIL, BIBannulifera-BIRfasciata-BIR*, BIB*philippii-BIR*sartorii-BIR, BIBzweifcli-BIR*elapoides-Uc, BI R, BIS, BIL, T M , TT, T T b , T M b , T M ieuryrom-TZ (no red on ven ter), BIR *, BIRscalari-BIB; venter creamAmong these genera Apostolepis, Clelia, Drepanoides, Elapomorphus, Oxyrhopus,Pseudoboa, Rhinobothpm, Siphlophis, Sonora, Stenorrhina, Tantilla, Tripanurgos andXenopholis have grooved rear-fangs and a venom gland (Duvernoys 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 inhuman beings (Dunn, 1954; Seib, 1980). The putative coral snake mimics listedfor these genera are regarded as mildly toxic and not dangerous to humanbeings, but their venoms are doubtless used to subdue prey. The listed species ofthe genera Clelia and Erythrolamprus, like the venomous coral snakes, areprincipally ophiophagous and Lampropeltis often consumes other snakes.

TripanurgosTropidodipsas

Jlscheri-BIR*, BIB*

Urotheca

Xenopholis

Venomous coral snakesThis review includes all species and putative subspecies listed by Roze (1983,

1987, 1989) and Campbell & Lamar (1989). When all subspecies have the samepattern only the inclusive species name is listed. A double asterisk (** ) indicatesthat some representatives of that taxon have a tricolour monad pattern; a tripleasterisk (***) indicates that some have a bicolour ringed (BIR, BIM) or banded(BIMb) pattern. Unless otherwise noted bicolour species have a black and redpattern.

U N I F O R M ( U )Micrurus diastcma alicnus (U, Uc)**BICOL OUR (BI )BL OT CHE S RINGSB IL M icrurus b d i * * * BIF Leptomirmrus collarisBIL M ic ru w limbatus (some)*** BIF Lcptomicrurus narducciiBIF Lcptomicrurus scutiuentfir


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T H E C O L O U R A TI O N OF THE VENOMOUS CORAL S NAKES 249BANDSBIB Micrurus bernadi BIMBIR Micrurus ephippijier ephippijier (black andyellow above, T M below) BIM

BIMBIRBIR

BIRBIRBIR

BIRBIRBIRBIRBIRBIRBIRBIRBIFBIRBIRBIRBIRBIR

RINGSMicrurus alleni yatesi adul t (black andyellow ab ove, T M below) **Micrurus annellatus annellatus adul t (blackand whi te or red)**Micrurus annellatus balzani adul t (b lackand whi te or red)**Micrurus diastema apiatusMicrurus langsdorfi langsdorfi** (blackand white above, T M below; someTM/BIR)Micrurus langsdorfi omtissimus (black andwhite above, T M below)**Micrurus limbatus (some)Micrurus margaritijierus (black and whi te;white discontinuous; venter black andwhite or black, white and brown)Micrurus mipartitus (black and whi te, orye11ow )Micrurus multijiasciatus (black and whi te,red or yellow)Micrurus multkcutatusMicrurus nigrocinctus divaricatus* *Micrurus nigrocinctus zunilmis* *Micrurus peruvianus (black and yellow)**Micrurus petersi (black and yellow) *Micrurus psyches psyches (black and whi teor yellow)Micrurus psyches donosoiMicrurus psyches medemi (black andyellow)**Micrurus putumaynrris (black and yellow)Micrurus rwtanusMicrurus spurrelli (black an d whi te)Micrurus stewartiT R I C O L O U R M O N AD S ( T M )RINGSMicruroides euryxanthusMicrurus alleni alleniMicrurus alleni yate si juvenile* **Micrurus annellatus annellatus juvenile* **Micrurus annellatus balzani juvenile* **Micrurus annellatus bolivianusMicrurus averyiMicrurus bogcrtiMicrurus browniMicrurus clarkiMicrurus corallinusMicrurus diastema @nisMicrurus diastema aglaeope ( T M a )Micrurus diastema alienusMicrurus diastema diastema (some T M b )Micrurus diastema macdougalliMicrurus diastema sappm'Micrurus distmMicrurus dumm'lii antioguiensisMicrurus dumm'lii carinicaudaMicrurus dumm'lii transandinusMicrurus dumm'lii venezuelmu


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250 J. M. SAVAGE AND J. B. SLOWINSKIRINGS RINGS

M i m r u s ephippifcr zapotecus (TMa, blackspots, bands or saddles in red rings)Micrurus fulv iusMicrurus hippocrepis TM/TMiMicrurus langsdo@ langsdorfz (someTM/BIR)***Micrurus langsdorfz omatissimus* *Micrurus 1atiJiiciatusM i m r u s m c r t mMicrurus ncbularisMicrurus nigrocinctw nigrocinctusMicrurus nigrocinctus babaspulMicrurus nicrocinctus coibmrisMicrurus nigrocinctus divaricatuss * *Micrurus nigrocinctus mosguilmFisMicrurus nigrocinctus zunilms* *Mi mr us pmvianus***Micrurus petcrsi***Mi mr us proximansMicrurus p sych s circinalisMicrurus psyches mcdcmi* *Micrurus psyches paraensisMicrurus psyches remotusMicrurus stdndachncriMicrurus stuartiTRICOLOUR DYADSTRICOLOUR TRIADS (TT)RINGSMicrurus bocourti

(None)

MMMMMMMMMMMM

imcrus catamayenuicrurus decoratusicrurus dissolnccusicrurus dummlii dumcriliiicrurus dummlii colombianusicrurusjlifomisi mr us ronhJkwiatusicrurus ronhlisicrurus hcmprichiiicrurus ibibobocai mr us isozonus~ i m r u saticollarisM i m r u s lcmniscatus

Micrurus spixiiMicrurus surinammisMicrurus tschudiiTRICOLOUR TETRADS (TTE)(None)TRICOLOUR PENTADS (TP)RINGSMicrurus elcgans (black blotches in someorange rings)TRICOLOUR WHITE, YELLOWAND RED (NBR)RINGSMicrurus langsdorfi langsdorfz**. * * *

Micrurus sangilmis

, Significantly, the head pattern and colouration in tricolour venomous coralsnakes generally corresponds to that on the body. In most species having thetricolour monad pattern, the white or yellow head band or nuchal collar, blacknuchal collar and postnuchal light collar represent the first monad. Micruroideseuryxanthus is an exception for although it has a white nuchal collar it lacks ablack one and the first monad is located several head lengths posterior to thenuchal region.

In typical tricolour triad forms the black nuchal collar is the anterior blackelement 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 inlacking red on the dorsum of the head.

COLOURATION AND MIMICRYThe 56 species of venomous coral snakes are essentially restricted to the

Neotropics in distribution, although one species (Micrurusfuluius) occurs in thesouth-eastern United States and another (Micruroides euryxanthus) is found in thesouthern arid regions of New Mexico and Arizona and in adjacent Mexico.Members of this lineage are active at night and during the day under conditionsof low illumination (i.e. inside forests). They tend to be secretive and feedprimarily on other snakes (including their own species), although several SouthAmerican forms (Micrurus lemniscatus and Micrurus surinamensis) also eat


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THE COLOURATION OF THE VENO MOUS CORAL SNAKES 25 Ifreshwater fishes and one (Micrurus hemprichii ortoni) prefers onychophorans(genus Periputus). Known predators on coral snakes are primarily birds (seeBrugger, 1989) and snake-eating snakes. Available evidence indicates thatenvenomation by coral snakes may kill large raptors but there are recorded casesof successful avian predation on these snakes (Smith, 1969).

Many species of coral snakes exhibit defensive behaviours that are keyed toreducing predation. Some or all of these behaviours may be used by a singleindividual 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 tailabout. In addition the head may be withdrawn from hiding and swung from sideto side with the mouth open and ready to bite any object that is contacted, thebody may be snapped back and forth almost spasmodically, the tail may be usedto strike aggressively or waved to divert attention from the head and the contentsof 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 alsoan antipredator defense that performs an aposematic (warning) function andthat 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 agoconcluded that mimicry was involved. Contrasting patterns of alternating blackand 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 crypticfunction serving to hide them from predators (Brattstrom, 1955; Jackson,Ingram & Campbell, 1976; Pough, 1976). However, there now seems to be littlequestion that the bright coral snake colour patterns combined with the unusualbehaviours described above are important antipredator defences that actthrough the vision of potential predators on venomous coral snakes to warn themthat 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 probablyinvolves learning based upon an unpleasant experience with a coral snake bite.Because of their short fangs and the need to chew to ensure envenomation, coralsnakes frequently inject only small and not necessarily deadly amounts of venomso that predators probably often survive bites (e.g. Smith, 1969). The carefullydesigned experiments of S. Smith (1975, 1977), however, demonstrate innateavoidance of a coral snake pattern by several potential avian predators,including motmots (Eumomota) and kiskadees (Pitunow). Smiths studiesconvincingly established the reality of aposematic colouration in coral snakesand their mimics.

Both Batesian and Miillerian mimicry have been proposed as explanations forthe coral snake mimicry guild. Additionally, Wickler (1968) popularized theconcept that the highly venomous coral snakes and the harmless mimics weremimicking the mildly toxic, rear-fanged forms, a type of mimicry he calledMertensian. However, we agree with Greene & McDiarmid (1981) that theterm is unnecessary since i t represents a form of Batesian mimicry. That somekind of mimicry is involved is attested to by the precise resemblances incolouration between non-coral snakes and sympatric venomous coral snakes andthe concordant geographic variation between the two (Savage & Vial, 1974;Greene & McDiarmid, 1981; Roze, 1983). We support the concept that Batesian


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252 J. M . SAVAGE AND J. B. SLOWINSKImimicry is involved with the venomous coral snakes being the models and theother forms the mimics. Nevertheless, it seems unlikely that all of the diversecolour patterns described in this paper actually evoke an avoidance response inpredators. Consequently, we have attempted to identify those colour patternsthat are most likely to be involved in coral snake mimicry and the taxa whichmay be regarded with some confidence to be members of the coral snake mimicguild.There can be little question that snakes having ringed tricolour patterns(I II B ) are mimics since these patterns are identical to, or closely resemble themost common colourations in venomous coral snakes. Similarly, tricolour formshaving the black body bands arranged in monads, dyads or triads (IIA 8-10)resemble both tricolour ringed coral snakes and ringed mimics in their dorsalpatterns and are almost certainly mimics as well.Most snakes exhibiting other non-ringed tricolour patterns are probablymimics. However, we are sceptical regarding the role of the colour patterns inElaphe (Tsr, BIr) and Nerodia (U , T S R , RB) and do not consider the patterns inThamnophis and Farancia erytrogramma (TS) to be involved in mimicry since theyd o not even superficially resemble the pa ttern of an y venomous coral snake. T h eseveral quadrico lour patter ns (IV A -C ) ar e essentially m odifications of tricolourones and snakes having them are considered mimics.Snakes having bicolour ringed or banded patterns (IIB-C ) of black an d redare doubtless mimics of similarly marked venomou s co ral snakes. T h e same m aybe said for bicolour black and white or yellow ringed forms since they havepatterns typical of some bicolour venomous coral snakes. We are dubious as towhether all black and white or yellow banded snakes (BIB*) are mimics sincethis pattern has a cryptic function a n d is frequently found in arb orea l forms or inspecies that do not co-occur geographically with venomous coral snakes. Themimetic role of all oth er bicolour black an d red p attern s is question able altho ughthose with a substantial amount of red may sufficiently resemble banded orunicolour species to gain some protection.Although only one species (Micrurus diastema) of venomous coral snakesincludes individuals that have a uniform red body, we believe that thiscolouration serves an apo sematic function in these individu als an d in a series ofmildly toxic an d harmless snakes. Consequently, we regard the la tte r as memb ersof the mimic guild although the suspected role of the uniform, bright redcolouration remains to be confirmed.

According to this analysis the following genera contain species that may beregarded as coral snake mimics; an asterisk (*) means that all members of thegenus 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 a n dXenopholis* .Those individuals interested in further investigation of coral snake mimicryshould concentrate their attention on these genera and co-occurring venomouscoral snakes. More studies are certainly in order to determine how widespreadinnate avoidance of coral snakes by predators may be. In addition, althoughdifficult to test, the role of em path etic learnin g in the origin a n d mainten ance of


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T H E C O L O U R A T I O N O F T H E V E N O M O U S C O R A L S N AK E S 253coral snake mimicry is an are a needing furthe r exploration. W e suspect th at b othinnate an d learned behaviours, eac h specific to different groups of predators, a reinvolved in predator avoidance of the coral snake mimic guild. Hopefully thedetailed description of colouration presented above will provide a basis for suchstudies and precise evaluations of aposematic behaviour involving specificmodels and their sympatric look-alike mimic(s).

RE FE RE N CE SAMARAL, A. DO., 1976. Serpentes do Brasil: Iconografa Colorida. 2nd edition. Editora da Universidade de SHoBRA T T ST RO M, B. H., 1955. T he coral snake mimic problem and protective coloration. Evolution, 9:BRUGGER, K. E., 1989. Red-tailed hawk dies with coral snake in talons. Copeia, 1989: 508-510.CAMPBELL,J. A. & LAMAR, W. W. , 1989. The Venomous Reptiles of Latin America. Ithaca, New York: CornellCEI , J. M., 1986. Reptiles del Centro, Ccntro-oestey Sur de la Argentina. Herpetofauna de la s


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254 J. M. SAVAGE AND J. B. SLOWINSKISCH MI D T , K . P. & SCHMIDT, F . J. W., 1925. New coral snakes from Peru.

savage, slowinski - 1992 - the colour at ion of the venomous coral snakes (family elapidae) and...

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