Coral Snake Mimicry: Does It Occur?

Home , Coral snake, Erythrolamprus, Micruroides, Micrurus, Pliocercus, Sonora (snake)

Reprint Series Il September 1981, Volume 213, pp. 1207-1212

Harry W. Greene and Roy W. McDiarmid

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 "empathie" 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. triangulum shows cercus are small (< 80 centimeters total (Lampropeltis triangulum) have a pat- color pattern shifts in concordance with length), brightly marked, rear-fanged in- tern of bright red, yellow, and black changes in the width of red bands and habitants of tropical forest litter (70) and rings but change ontogenetically until the presence or absence of black spots in the provide a particularly good test (71). adults are uniformly black. It was sug- red bands of sympatric Micrurus (53). Although several species have been de- gested that this situation supports a mim- Other examples of color pattern con- scribed from Latin America, apparently icry hypothesis because adult king- cordance in this widely distributed spe- at most two, and perhaps only one, spe- snakes are supposedly too large to effec- cies include black encroachment onto cies should be recognized (72). Color tively mimic local venomous coral the red bands in Oaxaca, Mexico (55), pattern is of three basic types and gener- snakes (3, 5, 6). However, this example where M. ephippifer is similarly pat- ally consistent within populations. Geo- is not compelUng evidence for mimicry terned; breakup of the crossbanded pat- graphic differences correlate very close- as presented, because it is restricted tern to yield spotted or unicolored red ly with the patterns of sympatric front- geographically, because black color in snakes at some localities on the Yucatan fanged coral snakes (73) (Fig. 1). The the adults might have a thermoregulatory Peninsula (55), where M. diastema ex- resemblance extends to general habitus, function (46), and because a sympatric hibits the same eff'ect (56-57); a tendency except that Pliocercus has an extremely front-fanged coral snake (Micrurus al- to form secondary black rings in extreme long tail (74). lem) actually undergoes similar ontoge- southern Mexico (58), where M. elegans Throughout most of Mexico and netic color pattern shifts (47). has such a pattern (Fig. IE); and the northern Central America, Pliocercus 3) Differential abundance of model presence of a pattern of red-orange and and Micrurus have red bands alternating and mimic. A classic criterion for mimic- black rings in Honduras (59), resembUng with yellow-bordered black bands (Fig. ry has been that models must exceed sympatric M. nigrocinctus (60). 1, A and C). The red bands of Micrurus mimics in abundance in order for preda- 2) Micruroides euryxanthus, a small, are relatively wide in southeastern Mexi- tors to profitably avoid a particular prey front-fanged coral snake, inhabits the co and parts of Guatemala (M. diastema, phenotype. Analyses of two large sam- Sonoran Desert of the southwestern M. latifasciata) and northern Yucatan ples (A' = 1175 and 1227) show that ven- United States and northwestern Mexico. (M. diastema); the black and yellow bands are narrow in M. diastema from are very narrow (Fig. IE). Only within and M. stewarti are bicolored; broad southeastern Mexico and Guatemala, the range of M. elegans (parts of south- black bands alternate with red, pink, or and wider in M. latifasciata (Guatemala) em Mexico and adjacent Guatemala) are white rings of equivalent or lesser width and M. diastema (Yucatan). Elsewhere the secondary black rings of Pliocercus (Fig. ID). Pliocercus has a bicolored in southern Mexico (M. browni, M. dia- well developed. The red rings of Pliocer- pattern with such relatively broad black stema, M. nigrocinctus) the red bands cus in this region are relatively wide, bands only where sympatric with these are narrower. Variation in relative band suggesting that here it has combined species. widths of Pliocercus among these areas elements of the color pattern of two Color pattern concordance also ex- parallels that in the sympatric Micrurus. sympatric models (M. diastema and M. tends to at least four unusual localized Within the range oí Pliocercus, only in elegans). variants of Micrurus and Pliocercus. In M. elegans do secondary black rings In lower Central America and north- Hidalgo and Puebla, Mexico, M. bernadi border the yellow rings, and the red rings western South America, M. mipartitus is red with a dorsal pattern of narrow

Fig 1 Geographic color pattern variation in rear-fanged colubrid snakes of the genus Pliocercus in relation to sympatnc front-fanged snakes of the genus Micrurus. The presumed dangerous models, on the left in each set, are (A) M. fulvius, (B) M. limbatus, (C) M. diastema, (D) M. mipartitus, (E) M. diastema, and (F) M. diastema. In (E), the center snake is Pliocercus, and the right snake is M. elegans. For further details see m. cross bars or spots instead of rings; venomous coral snakes have similar col- some other unpleasant characteristic, Pliocercus from this area is similarly or patterns in sympatry by chance or as and the other (the mimic) is edible or patterned. Micrurus limbatus, endemic convergent responses to some nonmi- harmless. The mimic, through its resem- to the Sierra de Tuxtlas, Veracruz, Mex- metic environmental factor (23, 76, 77). blance to the model, deceives a third ico, is bicolored with numerous black We find this highly unlikely for several species (a predator) and thereby suffers and red rings at the type locality (Volcán reasons: (i) the presumed models and less prédation. The deception most often San Martin). A few kilometers away on mimics sometimes occupy different mi- involves bright warning coloration which the eastern shore of Lago Catemaco, it is crohabitats in a single area (78); (ii) the the predator recognizes as unpleasant red with a black nape band and a few pattern shifts in presumed mimics are and avoids. In MüUerian mimicry, two or large, irregular, black dorsal spots and repeated and precisely concordant with more species also resemble each other. bands (Fig. IB). Two Pliocercus from the presumed models over a large geo- Here, however, both species are dis- this locality are red with black nape graphic area, sometimes involving seven tasteful or unpleasant, and both are rec- bands, and have either a single dorsal or eight model patterns; (iii) in one in- ognized and avoided by predators. In black spot or a few spots and broken stance (Pliocercus in southern Mexico) MüUerian mimicry, each species acts as bands; of two offspring from one of these the presumed mimic compromises the a model and mimic. snakes, one was patterned exactly like patterns of two sympatric models (M. Wickler (3, 19) popularized the con- the female (a single black spot), and the diastema and M. elegans); and (iv) in cept of a mUdly venomous model, a other was banded red and black. Mi- several instances the resemblances in- deadly mimic, and a harmless mimic•a crurus diastema from Guatemala and M. clude bizarre color patterns not found situation he termed Mertensian mimicry. nigrocinctus from Honduras have nu- elsewhere in either genus (for example, Smith's studies (24) made it clear that merous red bands separated by black spotted Micrurus and Pliocercus; black any of the venomous coral snakes (rear- bands (elsewhere both are tricolored); Micrurus, Erythrolamprus, and Atrae tus or front-fanged) may be models, but the Pliocercus from these areas have the with white-speckled bands). precise direction of predator deception same color pattern (Fig. IF). Finally, a remains unknown. In any case, all possi- Pliocercus from the Pacific slope of the ble combinations involving coral snakes Sierra Madre, Oaxaca, Mexico, has the Alternative Concepts and Terms can be accommodated within the con- red bands replaced by black middorsally cepts of a Batesian-MüUerian dichotomy (75). It thus closely resembles the adults Classically, mimicry has been divided or continuum (49, 79), and we agree with of an endemic and unusually patterned into two general types: Batesian and Vane-Wright (80) that Mertensian mim- Oaxacan coral snake, M. ephippifer. MüUerian. Batesian mimicry involves re- icry is an unnecessary term. A competing explanation for these semblance between two species, one of Grobman (27) mentioned several ob- similarities is that venomous and non- which (the model) is distasteful or has jections to aposematism in venomous coral snakes (81), and proposed that resemblance to these animals by other snakes be known as pseudomimicry. We agree that two species might resemble each other as a result of some factor or factors other than predator deception (25,42, 43). However, such factors need not be exclusive of aposematism or mimicry; even if they are, such interspecific simUarity has long been termed conver- gence.

Conclusions

The coral snake mimicry hypothesis states that the bright color patterns of venomous species serve as warning sig- nals to predators and that these predators Eilso avoid harmless or other venomous species with similar patterns. Most arguments against mimicry object to the contention that the venomous species possess aposematic color patterns; these objections were based on incorrect assumptions. Ample evidence of diurnal activity in these snakes now exists, and recent experiments demonstrate that at least two species of relevant predators innately avoid coral snake patterns. Most previous support for the mimicry hypothesis was based on indirect argu- Fig. 2. Geographic color pattern variation in the rear-fanged colubrid snake Erythrolamprus ments that are plausibly subject to alter- guentheri in relation to sympatric front-fanged coral snakes of the genus Micrurus. The presumed dangerous models, on the left in each pair, are (A) M. iangsdorffi and (B) M. native explanations. However, concor- margaritiferus. For further details see (82). dant geographic pattern variation strong,- ly suggests that some species of Atrac- Greene (unpublished) and G. P. Engelhardt [Co- that the absence of grooved rear fangs in some peia 1932, 37 (1932)] in Texas indicate that M. individuals of E. aesculapii from Brazil may tus, Erythrolamprus, Lampropeltis, fulvius is primarily diurnal. represent an evolutionary intermediate stage 29. Observations of M. dissoleucus (13) and M. between ungrooved and grooved fangs. If this is Micruroides, Micrurus, and Pliocercus nigrocinctus [(13, 26); O. J. Sexton and H. true, then the evolution of an aposematic or are involved in mimicry systems. The Heatwole, Caribb. J. Sei. 5, 39 (1965); and H. mimetic pattern in Erythrolamprus may enhance W. Greene, unpublished] in Panama; of M. the rapid evolution of a more efficient venom dynamics of these relations remain un- hippocrepis (II) in Belize; of M. browni [R. M. delivery system. certain because most of the snakes in- Blaney and P. K. Blaney, Herpetol. Rev. 9, 92 64. Our information on Erythrolamprus and coral [1978]), of M. diastema (R. W. McDiarmid, snake mimicry is based on (3, 5, 6, 26, 40, 47), volved are venomous; it seems likely unpubhshed), and M. limbatus (R. Zink, person- and R. W. McDiarmid (unpublished). that, in at least some situations, the al communication) in Mexico; of M. nigrocinc- 65. J, A. Peters and B, Orejas-Miranda [Bull. U.S. tus (R. W. McDiarmid, unpublished) in Costa Nati. Mus. 297, HO (1970)] recognized six spe- Micrurus are dangerous Batesian mod- Rica; and of M. eiegans (H. B. Shaffer, unpub- cies of Erythrolamprus. Their ranges from Hon- els. These interactions can be accommo- lished) in Guatemala. duras southward through Central and South 30. Observations of M. frontalis in Paraguay (M. S. America to northern Argentina, Paraguay, and dated within the classical concept of Foster, personal communication) and Uruguay Bolivia generally are allopatric, (E. Gudynas, personal communication); M. mi- 66. Throughout their range, species of Erythrolam- Batesian and Mtillerian mimicry, and the partitus in Venezuela [F. H. Test, O. J. Sexton, prus are diurnal, occur with one to seven species terms Mertensian mimicry and pseudo- H. Heatwole, Misc. Publ. Univ. Mich. 128, 1 of Micrurus, and resemble different species of (1966)]. the venomous models at different sites; Trinidad mimicry are not useful. 31. Observations of M. langsdorffi in Ecuador [W. (40); Costa Rica (47); Venezuela [J. A, Roze E. Duellman, Misc. Publ. Mus. Nat. Hist. Univ. (62)]; Ecuador [W, E, Duellman (31)]; Western References and Notes Kansas 65, 261 (1978)]. Ecudaor, Peru, Brazil, and Paraguay (R, W, 32. Observations of M. putumayensis in Peru [J. R. McDiarmid, unpublished). 1. L, P. Brower, in Topics in the Study of Life, A. Dixon and P. Soini, Contrib. Biol. Geol. Milw. 67. The Linnaean type series of Erythrolamprus Kramer, Ed. (Harper & Row, New York, 1971); Public Mus. 12, 84 (1977)]; and M. tschudii in aesculapii includes a Micrurus [J. A. Peters, D. H. Janzen, Biotropica 12, 77 (1980). Peru (J. Hoffman, personal communication; N. Am. Mus. Novit. No. ¡851, 1 (1957)]. 2. H. W. Greene, Anim. Behav. 25, 245 (1977), K. Johnson, personal communication). 68. J. A. Peters (67) suggested that an ontogenetic 3. W. Wickler, Mimicry in Plants and Animals 33. The color patterns of several species of colu- color pattern shift occurs in E. guentheri, but (McGraw-Hill, New York, 1968). brids (Scaphiodontophis) represent hypothetical specimens of a typical morph and a black and 4. F. H. Pough, Herpetologica 30, 24 (1974). intermediates (5, 6). Variation within Sonora white morph from the Río Cenepa population 5. M. K. Hecht and D. Marien, /. Morphol. 98, 335 michoacanensis demonstrates a sequence of in- are of nearly equal total lengths (58 and 59 cm, (1956). termediates [A. C. Echternacht, Breviora No. respectively). Perhaps polychromatism exists, 6. R. Mertens, Zool. Jahrb. Abt. Syst. Oekol. 1410, 1 (1973)]. as in certain insect mimicry systems (3), but Geogr. Tiere 84, 541 (1956). 34. F. H. Pough [Copeia 1964, 233 (1964)] for Plio- resolution of the situation in Erythrolamprus 7. H. W. Greene and W. F. Pyburn, Biologist 55, cercus in Panama. must await additional material. 144 (1973). 35. P. S. Martin [personal communication, in (5)] 69. Atractus elaps is a relatively small snake occur- 8. J. A. Roze, Am. Mus. Novil. No. 2287, 1 (1967). and S. S. Sweet (personal communication) for ring from low to intermediate elevations in east- 9. S. A. Minton and M. R. Minton, Venomous Pliocercus in Tamaulipas, Mexico. ern Colombia, Ecuador, and Peru eastward into Reptiles (Scribner, New York, 1969); F. W. 36. H. M. Smith [Proc. U.S. Nati. Mus. 93, 393 the Amazon Basin of Brazil. In their review of True, Am. Nat. 17, 26 (1883). (1943)] for Pliocercus in Chiapas, Mexico. geographic variation and color pattern polymor- 10. H. W. Ramsey, W. J. Taylor, I. B. Boruchow, 37. Observations of J. D. Groves (personal commu- phism, J. R. Dixon, R, A. Thomas, and H, W, G. K. Snyder, Am. J. Physiol. 222, 782 nication) on Lampropeltis triangulum in Flori- Greene [Herpetologica 32, 221 (1976)] recog- (1972). da. nized four pattern types. They found no consis- 11. W. T. Neill, Herpetologica 13, 111 (1957). 38. A. F. Skutch, A Naturalist in Costa Rica (Univ. tent geographic trends and reported several pat- 12. T. R. Howell, Condor 59, 74 (1957); H. L. of Florida Press, Gainesville, 1971). terns from single localities in Peru; several spe- Stoddard, Bull. Tall Timbers Res. Stn. 21, 109 39. J. F. Jackson, Copeia 1979, 169 (1979). cies of Micrurus also occur at these localities (1978); J. N. Layne (personal communication) 40. T. C. Boyden, Evolution 30, 73 (1976). [Dixon and Soini (32)], Hecht and Marien (S) saw a shrike attack a small M, fulvius at 1600 41. M. G. Emsley, ibid. 20, 663 (1966). argued that Atractus elaps and its relatives are hours on a cool, overcast day in a fire lane in 42. R. G. Zweifel, Copeia 1952, 152 (1952). Batesian mimics and listed several sympatric scrubby flatwoods on 8 February in central 43. G. H. Thayer, Concealing Coloration in the species of Micrurus as possible models. The Florida. Layne's approach scared the bird, Animal Kingdom (Macmillan, New York, 1909); color plate in Duellman (31) and our experience whereupon the snake uncoiled and moved to J. F. Jackson, W. Ingram III, H. W. Campbell, with the species in the field also convince us that cover. Am. Nat. 110, 1029 (1976); F. H. Pough, Copeia it is a Batesian mimic, R, W, McDiarmid recent- 13. N. G. Smith, Copeia 1969, 402 (1969). 1976, 834 (1976); J. D. Goodman and J. M. ly collected an essentially black and white 14. C. W. Myers (personal communication) experi- Goodman, Herpetologica 32, 145 (1976); J. A. morph of Atractus elaps among eight more enced pain and swelling from the bite of a small Endler, Evol. Biol. 11, 319 (1978). typically patterned individuals along the Rio (385 mm) M. mipartitus in Panama. Humans 44. E. B. Poulton, Essays on Evolution (Clarendon, Santiago in northern Peru. This snake is black have experienced local pain from the bite of Oxford, 1908), pp. 1889-1907. with 29 complete, narrow white rings and 11 Micruroides [F. E. Russell, Toxicon 5, 39 45. J. R. G. Turner in Ecological Genetics and partial white rings. A single partial ring immedi- (1967)]. Some vipers control the quantity of Evolution: Essays in Honour of E. B. Ford, R. ately posterior to the anus is the only red color venom injected during a bite (N. AUon and E. Creed, Ed. (Blackwell, Oxford, 1971). dorsaily. Other than this ring and traces of red Kochva, /. Exp. Zool. 38, 71 (1974)], but wheth- 46. K. L. Williams, Puhl. Biol. Geol. Milw. Public on the chin, ventral 14, and subcaudals 15-16 er this is true of Micrurus is not known. Mus. 2, 226 (1978), and 20-21, the entire ventral surface is black and 15. C. R. Halter, Copeia 1923, 104 (1923). 47. J. M. Savage and J. L. Vial, Rev. Biol. Trop. 21, white. The previously unrecorded pattern of A, 16. An M. lemniscatus (FMNH 75950) in Trinidad 295 (1974). elaps is similar to sympatric Micrurus margariti- was found dead on a trail beside a dead house 48. F. H. Pough, L. P. Brower, H, R. Meek, S. R. ferus, parallels the situation described for Eryth- cat, and in Panama an M. nigrocinctus (FMNH Kessel, Proc. Nati. Acad. Sei. U.S.A. 70, 2261 rolamprus, and strengthens the argument for 68088) was brought in by a cat, which subse- (1973), mimicry. quently died (from notes with specimens in the 49. J, R, G, Turner, Evol. Biol. 10, 163 (1977), 70. Pliocercus has a Duvernoy's gland and en- Field Museum of Natural History, Chicago). 50. L, P, Brower, J, Alcock, J, V. Z. Brower, in larged, ungrooved rear fangs; it is closely related 17. For a survey of Duvernoy's gland in colubrid Ecological Genetics and Evolution: Essays in to other colubrids known to possess toxic saliva snakes, see A. M. Taub [Bull. Am. Mus. Nat. Honour of E. B. Ford, R. Creed, Ed, (Black- [C. W. Myers (18)]. R, L. Selb [Toxicon 18, 399 Hist. 138, 1 (1967)]; D. M. McKinstry [Toxicon well, Oxford, 1971), (1980)] reported severe local effects from the 16, 523 (1978)] reviewed toxicity of venoms of 51. E. C, Terhune, Am. Nat. Ill, 435 (1977). bite of a very small Pliocercus. rear-fanged colubrids. 52. C. Gans, Evolution 15, 72 (1961). 71. The close resemblance of Pliocercus to Mi- 18. The venom-conducting teeth of rear-fanged 53. R. G. Zweifel, Bull. Am. Mus. Nat. Hist. 119,77 crurus at three localities was mentioned by snakes can be single or paired, and grooved or (1960). Hecht and Marien (5) and C. M. Bogart [cited as ungrooved [see C. W. Myers, Bull. Am. Mus. 54. R. Conant, Proc. N. Engl. Zool. Club 11, 3 personal communication in K. P. Schmidt, Fiel- Nat. Hist. 153, 1 (1974)]. (1943). diana Zool. 39, 201 (1958)]. 19. Most discussions of coral snake coloration attri- 55. A. C. Günther, Biología Centrali-Americana. 72. Color pattern variation in Pliocercus is based on bute Mertensian mimicry to Wickler (3); Hecht Reptilia and Batrachia (Dulau, London, 1893), J. M. Savage and J. L, Vial (47); A. K. Smith, and Marien (5) and Mertens (6) mentioned it, p. 109 and plate 38. Jr., thesis, Baylor University (1969); L. D. Wil- and Mertens acknowledged reading (5) in manu- 56. D. F. Eraser, Copeia 1973, 1 (1973). son and D. D. Dugas, Bull. South. Calif. Acad. script. 57. R. M. Blaney and P. K. Blaney, Herpetologica Sei. 71, 159 (1972); H. W. Greene, /. Herpetol. 20. C. F. Swynnerton, /. S. Afr. Ornithol. Union 2, 35, 276 (1979). 3, 27 (1969); , unpublished. J. A. Peters 32(1915). 58. Based on No. 180251 in the University Kansas and B. Orejas-Miranda (6J) recognized seven 21. P. H. Klopfer, Am. Nat. 91, 61 (1957). Museum of Natural History, allopatric species apparently distinguished only 22. R. H. MacArthur [personal communication in 59. L. Porras (personal communication); J. R. Mey- by difference in color pattern. Variation within Klopfer (27)], Greene and Pyburn (7), and D. er and L. D. Wilson, Bull. South. Calif. Acad. and between populations suggests that no more Otte [Annu. Rev. Ecol. Syst. 5, 385 (1974)] Sei. 70, 106 (1971). than two species can be recognized; elapoides in suggested that predators innately avoid coral 60. L. D. Wilson and J. R. Meyer, ibid. 71, 139 Mexico and northern Central America (includ- (1972), ing andrewsl, bicolor, and euryzonus aequalis); 23. F. R. Gehlbach, Forma Functio 5, 311 (1972). 61. Snakes of the genus Erythrolamprus are mildly and euryzonus in Central America and northern 24. S. M. Smith, Science 187, 759 (1975); Nature venomous colubrids whose bite can cause sub- South America [including annelatus, arubricus, (London) 265, 535 (1977); Anim. Behav. 26, 988 stantial pain and swelling in humans (26), and dimidiatus (47)]. (1978). 62. The grooved nature of the rear fangs varies 73. Color pattern variation in Micrurus is based on 25. B. H. Brattstrom, Evolution 9, 217 (1955). considerably among species of Erythrolamprus (5, 8, 47, 57); L. D. Wilson and J. R. Meyer (60); 26. E. R. Dunn, ibid. 8, 97 (1954). in Venezuela [J, A. Roze, La Taxonomía K. P. Schmidt (71); E. R. Dunn, Proc. Acad. 27. A. B. Grobman, J. Herpetol. 12, 1 (1978). y Zoogeografía de los Ofidios en Venezuela Nat. Sei. Philadelphia 92, 105 (1940); H. W. 28. Observations by Neil! (//), D. R. Jackson and (University of Central Venezuela, Caracas, Greene, unpublished. R. Franz (Herpetologica, in press), J. S. Godley 1966)]. 74. A. H. Savitzky (personal communication) point- (personal communication), and J. D. Groves 63. A. do Amaral commented [Serpentes do Brasil ed out that Pliocercus resembles Micrurus in (personal communication) in Florida; and H. W. (Edit. University of Sao Paulo, Brasilia, 1977)] size because it has an exceptionally long tail; front-fanged coral snakes have exceptionally . Grobman (27) concluded that little or no préda- subspecies of L. triangulum, one subspecies of short tails and elongate bodies. tion occurs on coral snakes because no records L. pyromelana, five subspecies of L. zonata, 75, H. M. Smith and D. A. Langebartel, J. Wash. exist in the U.S. Fish and Wildlife Service files, and two subspecies of Rhinocheilus lecontei are Acad. Sei. 39, 409 (1950). and, therefore, that the banded color patterns of largely or completely allopatric to venomous 76, F. R. Gehlbach (23, p. 319) concluded that coral snakes are not adaptive. We suspect that coral snake models and that they do bear some "color resemblance alone does not confer spe- few records of prédation exist for most snakes, resemblance to the latter. However, none of cial protection on colubrid snakes, hence may and that this does not necessarily reflect actual them resembles Micrurus as much as do the simply represent concealing (disruptive) color- prédation rates. Grobman also cited brightly subspecies of L. triangulum (amaura, annulata, ation." However, javelinas (Tayassu) and coatis patterned bellies in other burrowing snakes as elapsoides) that are sympatric with M. fulvius (Nasua) responded significantly more often to evidence that this feature is not adaptive, but did (54). Rhinocheilus lecontei antoni has much his coral snake model with "fright" and to the not mention that some such species (for exam- brighter and more contrasting red, yellow, and normal snake model with "prédation" [Fisher ple, Farancia abacura, Diadophis punctatus) black markings in northwestern Mexico where it Exact Test, P < .05, for data in table 1 of (23)]. have defensive displays that suddenly expose occurs sympatrically with M. distans and Mi- 77 Gehlbach (23) also found similar frequencies of a the bright colors [H. W. Greene, J. Herpetol. 7, cruroides euryxanthus neglectus (R. W. banded morph in populations of a colubrid 143 (1973)]. Grobman [table 1 in (27)] examined McDiarmid, unpublished). snake. Sonora episcopa, where they occur allo- the distributions of 28 taxa said to resemble 82. Color patterns in the figures are based on pre- patrically or sympatrically to Micrurus fulvius. coral snakes, and concluded (p. 7) that "the served museum specimens. Museum numbers He concluded (23, p. 318) that "no mimetic frequency of races of nonvenomous snakes and specific localities are on file with the au- advantage is apparent." We agree, but suggest 'mimicking' the coral snake is independent of thors. that no such advantage is to be expected be- the presence of a model." However, we can 83. We thank the many herpetologists who permit- cause even the banded morph of S. episcopa reach exactly the opposite conclusion on the ted us to study specimens, loaned color slides, bears no special resemblance to a local coral basis of figures, maps, and color pattern descrip- or assisted in other ways. Versions of the manu- snake; the banded S. episcopa morph is bicol- tions in Conant (77) and R. C. Stebbins [A Field script were criticized by W. Altimari, G. M. ored, brown or reddish brown with narrow dark Guide to Western Reptiles and Amphibians Burghardt, J. E. Cadle, J. A. Campbell, A. C. crossbars•see color illustrations of it and M. (Houghton Miiflin, Boston, 1966)]. Chionactis Echternacht, M. S. Foster, J. D. Groves, F. H. fulvius in R. Conant, A Field Guide to Reptiles palarostris and eastern populations of C. occipi- Pough, W. F. Pyburn, J. A. Roze, A. H. Sa- and Amphibians of Eastern and Central North talis annulatus closely resemble the sympatric vitzky, R. L. Selb, W. W. Tolbert, and D. B. America (Houghton Mifflin, Boston, 1975). Micruroides euryxanthus. Chilomeniscus cinc- Wake. F. J. Irish prepared the excellent illustra- 78, In the Gómez Farias region of Tamaulipas, tus, three subspecies of Chionactis occipitalis, tions. Greene was supported by the University Mexico, Pliocercus occurs only in cloud forest, Lampropeltis triangulum multistrata, and L. t. of Texas at Arlington, Foundation for Environ- and M. fulvius is found in tropical deciduous and syspila are largely or entirely allopatric to and mental Education, Field Museum of Natural semievergreen forests [P. S. Martin, Misc. Publ. do not particularly resemble front-fanged coral History (Karl P. Schmidt Fund), Center for Mus. Zool. Univ. Mich. 101, 1 (1958)]. Note that snakes. We must point out that Ficimia quan- Latin American Studies (UCB), Smithsonian mimicry requires only that model and mimic drangularis is sympatric with Micruroides, but Tropical Research Institute (Noble Fund), and exist within the foraging range of relevant preda- in the northern part of its range it does not Museum of Vertebrate Zoology (Alexander tors, not actual syntopy (5). especially resemble a coral snake. However, the Fund); McDiarmid was supported by the Uni- 79 P. M. Sheppard and J. R. G. Turner, Evolution intensity of red in the color pattern increases to versity of South Florida, Organization for Tropi- 31, 452 (1977). the south where it is sympatric with Micrurus cal Studies, U.S. Fish and 'Wildlife Service, and 80, R. I. Vane-Wright, Biol. J. Linn. Soc. 8, 25 distans and Micruroides euryxanthus (R. W. National Science Foundation (grant to O. B. (1976). McDiarmid, unpublished). We agree that four Berlin, UCB).

contamination by the vast excess of characteristic ER membrane proteins that are left behind. The question then arises as to how this vital task of purification can be accomplished. The Golgi Apparatus: The Golgi apparatus is strategically located in the midst of this sorting process, interposed between the ER and the Two Organdíes in Tandem final destinations. To help clarify the relation between Golgi structure and James E. Rothman function, we must understand (i) why the mixture of proteins exported from ER needs to pass through the Golgi before sorting can be completed, and (ii) why all Present in all eukaryotic cells, the Gol- synthesized or initially found in the same of the necessary purification cannot be gi apparatus is generally agreed to be of compartment, the endoplasmic reticu- completed at the level of the ER, without fundamental importance in the process- lum (ER). Herein lies a sorting problem the involvement of a Golgi apparatus. ing and sorting of newly synthesized of considerable proportions (7). The Clues to these central problems have proteins. However, the underlying prin- newly synthesized membrane proteins now emerged from several independent ciples that must somehow relate the Gol- destined for export from the ER are lines of investigation. After a brief re- gi's striking stacklike structure to its exact functions have been elusive. The possibility that the Golgi may carry out a Summary. The Golgi apparatus consists of distinct eis and trans compartments that previously unsuspected form of sorting, may act sequentially to refine the protein export of the endoplasmic reticulum by the sorting of endoplasmic reticulum removing escaped endoplasmic reticulum proteins. Refinement may be a multistage proteins in multiple stages, is explored in process akin to fractional distillation; the stack of cisternae comprising the eis Golgi this article, and may provide the needed may be the plates In this distillation tower. The trans Golgi, consisting of the last one connection between structure and func- or two cisternae, may be the receiver that collects from the eis Golgi only Its most tion. refined fraction for later distribution to specific locations throughout the cell. Many different proteins that must ulti- mately reside in such diverse cellular compartments as the surface membrane, present in only trace amounts at any view of the biochemistry and morpholo- secretion granules, and lysosomes are given moment. Yet, within minutes of gy of the Golgi apparatus, I point out synthesis, these proteins are removed how these recent developments suggest The author is an associate professor in the Depart- from the ER and delivered to their sepa- a novel but speculative view of this or- ment of Biochemistry, Stanford University, Stan- ford, California 94305. rate destinations, virtually free of any ganelle. Specifically, I propose that the