Reprint Series Il September 1981, Volume 213, pp. 1207-1212 Coral Snake Mimicry: Does It Occur? Harry W. Greene and Roy W. McDiarmid Copyright © 1981 by the American Association for the Advancement of Science 11 September 1981, Volume 213, Number 4513 mildly venomous, rear-fanged snakes are Batesian or MüUerian models, and the front-fanged coral snakes are actually Batesian (79) or MüUerian mimics. This is unlikely to apply in areas where only Coral Snake Mimicry: front-fanged coral snakes and truly harmless colubrid mimics exist (for ex- Does It Occur? ample, Micrurus and Lampropeltis, in western Mexico). 4) Individual predators may learn the Harry W. Greene and Roy W. McDiarmid consequences of attacking coral snakes by observing the fate of conspecifics that are bitten {20, 21). However, such "em- pathie" or social learning could operate Batesian and MüUerian mimicry, stud- clude strong neurotoxins capable of kill- only in species in which young or adults ied extensively in arthropods, are rare ing large mammals, including humans (9- forage together. Even in situations phenomena among vertebrates (1-4). //). Thus, an early and persistent objec- where empathie learning can occur, con- The possibility that brightly colored, tion to the hypothesis that coral snake ventional learning (if the bitten predator venomous and nonvenomous New patterns are aposematic has been that a survived) or selection for innate avoid- World coral snakes comprise a mimicry small predator will not survive to profit ance (if the bitten predator died) also system has been widely debated for al- from the experience of being bitten (5). may operate (7). most a century (5, 5, 6) and is mentioned Five ways in which this "deadly model" 5) A simple but, until recently, under- dogmatically in textbooks and other gen- problem could be circumvented have emphasized mechanism is innate avoid- eral works (7). Unfortunately, the pri- been suggested (7): ance {22): an individually variable, ge- netically based response of potential predators to brightly ringed snakes and a Summary. Field observations and experimental evidence refute previous objec- subsequent reduction in fitness in those tions to the coral snake mimicry hypothesis. Concordant color pattern variation with the greatest tendency to attack ven- spanning hundreds of miles and several presumed venomous models strongly omous coral snakes. This hypothesis is suggests that several harmless or mildly venomous colubrld snakes are indeed supported by the responses of inexperi- mimics of highly venomous elaplds. enced predatory mammals {23) and birds {24) to coral snake color patterns. Smith's studies {24) are particularly con- mary literature on this topic is highly 1) Very small individuals of front- vincing because (i) motmots and kiska- speculative, often relies on erroneous fanged species, incapable of delivering a dees feed on small reptiles in tropical assumptions, and usually addresses only deadly quantity of venom, may be the forests, (ii) naive birds were tested, and the first of two questions: (i) Are color models. Likewise, small coral snakes (iii) she treated bright colors and a ringed patterns of venomous species aposemat- probably can be dispatched more easily pattern independently in her experi- ic? (ii) Do similar color patterns provide than larger snakes by a predator {12), ments. an advantage to harmless species and to and they may be less likely to deliver Another persistent and inappropriate other venomous species during predator venom. objection to the mimicry hypothesis is encounters? In this article we discuss 2) Small predators may become ill, that front-fanged coral snakes are noc- some widely held misconceptions and but not die, because of the supposedly turnal and, therefore, not subject to at- summarize new evidence bearing on ineffective venom delivery system of tack by diurnal predators with color vi- these issues. front-fanged coral snakes. The outcome sion (5, 5, 25-27). Observations on vari- of encounters with adult Micrurus and ous North {28), Central {11, 26, 29), and Micruroides varies greatly, including South American {30-32) species show Coral Snake Pattern as a successful prédation on the snakes {11- that these snakes often are active during Warning Signal 13), painful or debilitating nonfatal ef- daylight. Moreover, those hidden during fects (14), and death of the predator (9- the day are subject to discovery by pred- The New World coral snakes•about 11, 15, 16). ators that search in surface litter {23). 50 species of Micruroides and Micrurus, 3) Many colubrid snakes, including of the cosmopolitan family Elapidae most presumed coral snake mimics, have Harry W. Greene is assistant curator of lierpetol- {8)•usually have a single, enlarged, can- enlarged rear fangs on the maxillary ogy in the Museum of Vertebrate Zoology and an assistant professor of zoology, University of Califor- aliculate tooth on each maxillary bone. bones that conduct toxic secretions from nia, Berkeley 94720. Roy W. McDiarmid is curator The venoms of these animals, referred to paired Duvernoy's glands, which are lo- of reptiles and amphibians in the U.S. Fish and Wildlife Service, National Museum of Natural His- here as front-fanged coral snakes, in- cated in the head {17,18). Possibly, these tory, Washington, D.C. 20560. SCVSMCE.MÛ1 • -JX3•J.I. SEET,E,MSBJ&.iaai. Mi3,6,Mlß.iMJMiiJ~>-^.aysm.MDJix-,-j^,- :-i- Mimicry and Coral Snal(es omous coral snakes do exceed their non- This species has relatively wider red venomous counterparts in collections bands and narrower yellow bands in Si- The mimicry hypothesis postulates in- from Panama and Brazil, respectively (3, naloa, Mexico, where its distribution creased survival of coral snake pheno- 6, 26). However, the relevance of these overlaps that of Micrurus distans, a larg- types among a spectrum of available studies is uncertain because of possible er front-fanged species with unusually patterns, and implies that this survival collection biases and because the neces- wide red and narrow yellow bands (8, results from the exposure of predator sary ratio of models to mimics is depen- 53). populations to a dangerous coral snake dent on the relative noxiousness of each 3) Rear-fanged colubrid snakes of the model. A series of successive approxi- (48, 49). genus Erythrolamprus occur in tropical mations to a coral snake pattern exists forests of Central and South America, among living snake species, and even and their bites can produce painful within and among populations of a single Geograpliic Concordance in symptoms in man (61-63). The most species (33). The presumed models and Color Patterns striking among several color pattern mimics are sometimes diurnal (11, 26, shifts apparently associated with mimic- 28-32, 34-37) and are attacked by birds Avian predators can precisely distin- ry (64-67) occurs in the Amazonian re- (34, 38) and mammals (16, 39). However, guish among alternative color patterns gion of southeastern Ecuador and adja- the unlikelihood of observing the crucial (45, 49-51), and increased resemblance cent Peru. In this area, Micrurus langs- interactions in the field (differential sur- to a model can result in an increased dorfii and M. steindachneri have black vival of mimics as a result of predator advantage for a mimic during predator and red bands of about equal widths avoidance) and the problems of conduct- encounters (3, 48-52). For these reasons, (three to four dorsal scales) separated by ing appropriate experiments make direct geographic concordance in color pattern hght yellow or white bands about one proof for the coral snake mimicry system between presumed models and mimics scale wide. In this same region, Erythro- difficult to obtain. has been viewed as strong circumstantial lamprus guentheri has the same pattern. Studies of mimicry in other organisms evidence for mimicry in other snakes Micrurus margaritiferus occurs in the almost always have relied on indirect (52) and in insects (3). The argument for lower reaches of the Ríos Cenepa and evidence (3, 40), including: coral snake mimicry would be greatly Santiago in northern Peru, and has a 1) Coincidence of model and mimic in strengthened if it were shown that wide- pattern of speckled white bands on a one region and a lack of mimics in areas spread, presumed mimics consistently black background. Of four E. guentheri lacking models. This criterion has been have concordant color pattern shifts as from the Rio Cenepa locality, two have used to argue both for (5, 41) and against presumed models with different color the typical tricolored pattern described (25, 27) coral snake mimicry. The ambi- patterns drop in and out of sympatry (45, for eastern Ecuador and two are essen- guity is caused by the likelihood of multi- 49, 53). Here we summarize four such tially identical to the sympatric, bizarre- ple functions for brightly ringed patterns, examples of geographic concordance: ly colored M. margaritiferus (Fig. 2). including background matching, protean 1) Lampropeltis triangulum (a non- This pattern of white speckled bands on effects, and prey location (25,42,43); the venomous colubrid) differs from most a black background apparently occurs possibility that migratory predators are North and Central American Micrurus in only in these sympatric populations in involved (44); and the possibility that that the yellow or white rings are sepa- both genera (68). A similar black and allopatry among some possible models rated from the red rings by black rings, white patterned Atractus elaps, a non- and mimics is a comparatively recent rather than lying between the red and venomous colubrid, recently was found phenomenon (5, 45). black rings. However, within the United sympatric with M. margaritiferus along 2) Coincidence of size of model and States, these snakes resemble Micrurus the Rio Santiago (69). mimic. In the uplands of the Costa Rica- more closely in areas of sympatry (54). 4) Colubrid snakes of the genus Plio- Panama border, juvenile kingsnakes In western Mexico, L.