A REPORT ON A CASE OF MELANISM IN A SPECIMEN OF Crotalus durissus terrificus (LAURENTI, 1768)

SILVA, R. J. DA; FONTES, M. R. M.; RODRIGUES, R. R.; BRUDER, E. M.; STEIN, M. F. B.; SIPOLI, G. P. M.; PINHÃO, R.; LOPES, C. A. DE M.

doi:10.1590/S0104-79301999000100008

Abstract

This report documents a case of a melanic specimen of Crotalus durissus terrificus (Laurenti, 1768) found in Bofete, São Paulo State, Brazil. The authors describe this melanic snake, determine the electrophoretic pattern of its venom, and compare the venom of this specimen against that of normal Crotalus durissus terrificus. This report is very important because melanism is a rare chromatic anomaly

chromatic anomalies; melanism; Crotalus durissus terrificus; venom electrophoresis

SHORT COMMUNICATIONS.

A REPORT ON A CASE OF MELANISM IN A SPECIMEN OF Crotalus durissus terrificus (LAURENTI, 1768)

R. J. DA SILVA

, M. R. M. FONTES

, R. R. RODRIGUES

, E. M. BRUDER

, M. F. B. STEIN

, G. P. M. SIPOLI

, R. PINHÃO

, C. A. DE M. LOPES

1 Center for the Study of Venoms and Venomous Animals CEVAP UNESP, Botucatu, State of São Paulo, Brazil, 2 Department of Physics and Biophysics of the Institute of Biosciences of São Paulo State University - UNESP Botucatu, State of São Paulo, Brazil.

ABSTRACT.Crotalus durissus terrificusCrotalus durissus terrificus

KEY WORDS: chromatic anomalies, melanism, Crotalus durissus terrificus, venom electrophoresis.

INTRODUCTION

Chromatic anomalies in snakes are rare(4). Amaral(1-5) reported on the occurrences of albinism, xanthism and erythrism in Brazilian snakes. Other reports were published by Prado(15), Prado and Barros(16), Renault and Schereiber(17), Hoge(11), Hoge and Belluomini(12), Hensley(10), Lema(13), Bücherl(7), Villas and Rivas(20), Miranda et al.(14), Bérnil et al.(6) and Sazima and Di-Bernardo(18).

This study is about a case of melanism in a specimen of Crotalus durissus terrificus (Laurenti, 1768) (Figure 1). This snake was captured in Bofete, São Paulo State, Brazil, on October 4, 1996 as it crossed a road, and then brought to the Center for the Study of Venoms and Venomous Animals - CEVAP - at São Paulo State University where it is kept in captivity for future genetic and reproductive studies. This specimen does not possess the dorsal blotches used to identify this subspecies. However, the authors can confirm that this is a Crotalus durissus terrificus, since it is the only known subspecies in the Botucatu area and the only subspecies that has been brought to CEVAP for about the last 10 years.

FIGURE 1.
Melanic specimen of Crotalus durissus terrificus (Laurenti, 1768).

The main features of this atypical specimen (Figure 1) are: young, female, weight 160 g, 680 mm total length, 60 mm tail length, and 22 mm rattle length. This snake possesses dorsal scale rows 28-24-19, ventrals 176, subcaudals 25-25, entire anal plate, supralabials 14-15 and infralabials 16-17. The dorsal color is light brown and the ventral yellowish white. The paraventral region shows a dark brown longitudinal stripe bordered by a yellowish white scale row. This snake does not possess the dorsal blotches which normally characterize this subspecies.

Reports in literature about chromatic anomalies in Crotalus durissus are generally about albinism(2,4-6,11,16-18,20). However, Amaral(2) reported a case of albinism as follows: ..." this specimen does not show any signs of its stripes or dorsal blotches; its dorsal color is light brown becoming lighter and lighter near the ventral region that is entirely light yellow." We believe that the Amaral(2) paper deals with a case of melanism and not albinism, and that the specimen described in our paper is quite similar to that described by Amaral(2).

Melanism is characterized by marked melanin pigmentation which gives the animal a light brown or dark brown color(19). In contrast, albinism exhibits no apparent melanin, which gives the animal a white yellowish color(19). On the basis of these considerations, we conclude that this paper, as well as that of Amaral(2), deal with a characteristic case of melanism. Besides this report and that of Amaral(2) there are no other publications which describe melanic specimens of Crotalus durissus terrificus establishing this report as very important.

The electrophoretic pattern of proteins in the venom of the melanic snake was determined comparing samples of venom of this specimen with that of a normal specimen of Crotalus durissus terrificus (Laurenti, 1768) of similar size and from the same area (Figure 2 and Table 1). Polyacrylamide gel electrophoresis (PAGE), pH 8.3, was carried out in a discontinuous buffer system as described by Hames and Rickwood(9) and Gahne et al.(8) with some modifications. The proteins that composed the venom were identified using 4% stacking gel and 11% resolving gel.

FIGURE 2.
Electrophoretic patterns of venoms from the normal (Lane 1) and melanic (Lane 2) specimens of Crotalus durissus terrificus (Laurenti, 1768).

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TABLE 1.
Molecular weight and density of electrophoretic bands of venoms from normal (Lane 1) and melanic (Lane 2) specimens of Crotalus durissus terrificus (Laurenti, 1768).

After loading the samples, the buffer chamber was connected to the power supply, and the cathode connected to the bottom buffer chamber. Electrophoresis was carried out in a constant run initially keeping a current of 15.5 mA at 100 V until the Bromophenol Blue indicator reached the resolving gel. The current was then adjusted to about 25 mA at 250 V. The run was carried out at 4ºC for 9 hours. Electrophoresis was analyzed using the Pharmacia Biotech ImageMaster® VDS system.

The results obtained from the electrophoretic pattern of the venoms of the two snakes demonstrate that the compositions are quite different. This may be observed either by the difference in the quantity of protein fractions found in each venom or by the slight differences in molecular weight and/or electrical charges detected in some proteins present in both venoms (Figure 2 and Table 1). We observed that: 1) there are four quite similar fractions present in the two venoms (B1, B2, B7 and B8); 2) fractions B9 and B11, present in both venoms, show slight differences in molecular weight and/or electrical charges; 3) venom of the normal specimen of Crotalus durissus terrificus has five fractions (B3, B4, B5, B6 and B14) which are not present in the venom of the melanic specimen. In contrast, the venom of the melanic specimen shows three fractions (B10, B12 and B13) which do not occur in the venom of the normal specimen; 4) of the eleven protein fractions found in the venom of the normal specimen, four showed a density higher than 10%, while in the venom of the melanic specimen this was only observed in 6 of the 9 protein fractions.

With regard to the electrophoretic pattern of the venom of the melanic specimen, the differences observed in this study might be due to the influence of one or more factors related to regional distribution, age, diet, etc., as postulated by Willense(21). However, we hypothesize that the possible genetic alterations that account for the abnormal color pattern might also influence the venom composition of this specimen. Further studies are needed to shed more light on this subject.

ACKNOWLEDGEMENT

The authors express their thanks to Heloisa Maria Pardini Toledo for the English review.

01Rev. Mus. Paulista, 1927, 15,

02 AMARAL A. Da ocorrência de albinismo em cascavel, Crotalus terrificus (Laur.).Rev. Mus. Paulista, 1927, 15, 55-7.

03 AMARAL A. Albinismo em "dorme-dorme", Sibynomorphus turgidus (Cope, 1868).Rev. Mus. Paulista, 1927, 15, 61-2.

04 AMARAL A. Notas sobre chromatismo de ophidios. II. Casos de variação de colorido de certas serpentes. Mem. Inst. Butantan, 1932, 7, 81-7.

05 AMARAL A. Notas sobre chromatismo de ophidios. III. Um caso de xantismo e um novo de albinismo, observados no Brasil.Mem. Inst. Butantan, 1933/34, 8, 151-3.

06 BÉRNILS RS, MOURA-LEITE JC, AJUZ RG. Albinismo em Crotalus durissus (Serpentes: Viperidae) do Estado do Paraná - Brasil.Biotemas, 1990, 3, 129-32.

07 BÜCHERL W.Acúleos que matam:no mundo dos animais peçonhentos. São Paulo: Melhoramentos, 1971. 152p.

08 GAHNE B, JUNEJA RK, GROUMUS J. Horizontal polyacrylamide gradient gel electrophoresis for the simultaneous phenotyping of transferrin, post-transferrin, albumin and post-albumin in the blood of cattle.Anim. Blood Groups Biochem. Genet., 1977, 8, 127-37.

09 HAMES BD, RICKWOOD D.Gel electrophoresis of proteins.2.ed. New York: Oxford University Press, 1990. 383p.

10 HENSLEY M. Albinism in North American amphibian and reptiles. Publ. Mus. Mich. State Univ., 1959, 1, 133-59.

11 HOGE AR. Herpetologische Notizen: Farbenaberration bei brasilianischen Schlangen.Mem. Inst. Butantan, 1952, 24, 269-70.

12 HOGE AR, BELLUOMINI HE. Aberrações cromáticas em serpentes brasileiras. Mem. Inst. Butantan, 1957/58, 28, 95-8.

13 LEMA T. Notas sobre os répteis do Rio Grande do Sul, Brasil. VII. Albinismo parcial em Leimadophis poecilogyrus pictostriatus Amaral (Serpentes: Colubridae).Iheringia. Ser. Zool., 1960, 13, 20-7.

14 MIRANDA ME, VALLEJO MT, GRISOLIA CS. Nota sobre casos de albinismo en ofidios argentinos. Hist. Nat., 1985, 5, 121-4.

15 PRADO A. Notas ofiológicas. 3. Mais um caso de albinismo em serpente.Mem. Inst. Butantan, 1939, 13, 9-11.

16 PRADO A, BARROS FP. Notas ofiológicas. 9. Duas cascavéis albinas do Brasil. Mem. Inst. Butantan, 1940, 14, 31-2.

17 RENAULT L, SCHREIBER G. Considerações sobre albinismo em cascavel. Folia Clin. Biol., 1949, 16, 91-2.

18 SAZIMA I, DI-BERNARDO M. Albinismo em serpentes neotropicais. Mem. Inst. Butantan, 1991, 53, 167-73.

19 STEADMAN, TL. Steadman dicionário médico ilustrado.25.ed. Rio de Janeiro: Guanabara Koogan, 1996. 1657p.

20 VILLA J, RIVAS A. Tres serpientes albinas de Nicaragua.Rev. Biol. Trop., 1971, 19, 159-63.

21 WILLENSE, GT. Individual variation in snake venom. Comp. Biochem. Physiol., 1978, 61, 553-7.

References

01 AMARAL A. Albinismo em "cobra coral".Rev. Mus. Paulista, 1927, 15, 3-9.
02 AMARAL A. Da ocorrência de albinismo em cascavel, Crotalus terrificus (Laur.).Rev. Mus. Paulista, 1927, 15, 55-7.
03 AMARAL A. Albinismo em "dorme-dorme", Sibynomorphus turgidus (Cope, 1868).Rev. Mus. Paulista, 1927, 15, 61-2.
04 AMARAL A. Notas sobre chromatismo de ophidios. II. Casos de variação de colorido de certas serpentes.Mem. Inst. Butantan, 1932, 7, 81-7.
05 AMARAL A. Notas sobre chromatismo de ophidios. III. Um caso de xantismo e um novo de albinismo, observados no Brasil.Mem. Inst. Butantan, 1933/34, 8, 151-3.
06 BÉRNILS RS, MOURA-LEITE JC, AJUZ RG. Albinismo em Crotalus durissus (Serpentes: Viperidae) do Estado do Paraná - Brasil.Biotemas, 1990, 3, 129-32.
07 BÜCHERL W.Acúleos que matam:no mundo dos animais peçonhentos. São Paulo: Melhoramentos, 1971. 152p.
08 GAHNE B, JUNEJA RK, GROUMUS J. Horizontal polyacrylamide gradient gel electrophoresis for the simultaneous phenotyping of transferrin, post-transferrin, albumin and post-albumin in the blood of cattle.Anim. Blood Groups Biochem. Genet., 1977, 8, 127-37.
09 HAMES BD, RICKWOOD D.Gel electrophoresis of proteins.2.ed. New York: Oxford University Press, 1990. 383p.
10 HENSLEY M. Albinism in North American amphibian and reptiles. Publ. Mus. Mich. State Univ., 1959, 1, 133-59.
11 HOGE AR. Herpetologische Notizen: Farbenaberration bei brasilianischen Schlangen.Mem. Inst. Butantan, 1952, 24, 269-70.
12 HOGE AR, BELLUOMINI HE. Aberrações cromáticas em serpentes brasileiras. Mem. Inst. Butantan, 1957/58, 28, 95-8.
13 LEMA T. Notas sobre os répteis do Rio Grande do Sul, Brasil. VII. Albinismo parcial em Leimadophis poecilogyrus pictostriatus Amaral (Serpentes: Colubridae).Iheringia. Ser. Zool., 1960, 13, 20-7.
14 MIRANDA ME, VALLEJO MT, GRISOLIA CS. Nota sobre casos de albinismo en ofidios argentinos. Hist. Nat., 1985, 5, 121-4.
15 PRADO A. Notas ofiológicas. 3. Mais um caso de albinismo em serpente.Mem. Inst. Butantan, 1939, 13, 9-11.
16 PRADO A, BARROS FP. Notas ofiológicas. 9. Duas cascavéis albinas do Brasil. Mem. Inst. Butantan, 1940, 14, 31-2.
17 RENAULT L, SCHREIBER G. Considerações sobre albinismo em cascavel. Folia Clin. Biol., 1949, 16, 91-2.
18 SAZIMA I, DI-BERNARDO M. Albinismo em serpentes neotropicais.Mem. Inst. Butantan, 1991, 53, 167-73.
19 STEADMAN, TL. Steadman dicionário médico ilustrado.25.ed. Rio de Janeiro: Guanabara Koogan, 1996. 1657p.
20 VILLA J, RIVAS A. Tres serpientes albinas de Nicaragua.Rev. Biol. Trop., 1971, 19, 159-63.
²¹21 WILLENSE, GT. Individual variation in snake venom. Comp. Biochem. Physiol., 1978, 61, 553-7.

CORRESPONDENCE TO:

R. J. DA SILVA - CEVAP/UNESP, Distrito de Rubião Junior, S/N, 18.618-000, Botucatu, São Paulo, Brasil.

Fax/Phone:55 14 821 3963 - E-mail: cevap@botunet.com.br

Publication Dates

Publication in this collection
16 Apr 1999
Date of issue
1999

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 01 AMARAL A. Albinismo em "cobra coral".Rev. Mus. Paulista, 1927, 15, 3-9.

[2] 02 AMARAL A. Da ocorrência de albinismo em cascavel, Crotalus terrificus (Laur.).Rev. Mus. Paulista, 1927, 15, 55-7.

[3] 03 AMARAL A. Albinismo em "dorme-dorme", Sibynomorphus turgidus (Cope, 1868).Rev. Mus. Paulista, 1927, 15, 61-2.

[4] 04 AMARAL A. Notas sobre chromatismo de ophidios. II. Casos de variação de colorido de certas serpentes.Mem. Inst. Butantan, 1932, 7, 81-7.

[5] 05 AMARAL A. Notas sobre chromatismo de ophidios. III. Um caso de xantismo e um novo de albinismo, observados no Brasil.Mem. Inst. Butantan, 1933/34, 8, 151-3.

[6] 06 BÉRNILS RS, MOURA-LEITE JC, AJUZ RG. Albinismo em Crotalus durissus (Serpentes: Viperidae) do Estado do Paraná - Brasil.Biotemas, 1990, 3, 129-32.

[7] 07 BÜCHERL W.Acúleos que matam:no mundo dos animais peçonhentos. São Paulo: Melhoramentos, 1971. 152p.

[8] 08 GAHNE B, JUNEJA RK, GROUMUS J. Horizontal polyacrylamide gradient gel electrophoresis for the simultaneous phenotyping of transferrin, post-transferrin, albumin and post-albumin in the blood of cattle.Anim. Blood Groups Biochem. Genet., 1977, 8, 127-37.

[9] 09 HAMES BD, RICKWOOD D.Gel electrophoresis of proteins.2.ed. New York: Oxford University Press, 1990. 383p.

[10] 10 HENSLEY M. Albinism in North American amphibian and reptiles. Publ. Mus. Mich. State Univ., 1959, 1, 133-59.

[11] 11 HOGE AR. Herpetologische Notizen: Farbenaberration bei brasilianischen Schlangen.Mem. Inst. Butantan, 1952, 24, 269-70.

[12] 12 HOGE AR, BELLUOMINI HE. Aberrações cromáticas em serpentes brasileiras. Mem. Inst. Butantan, 1957/58, 28, 95-8.

[13] 13 LEMA T. Notas sobre os répteis do Rio Grande do Sul, Brasil. VII. Albinismo parcial em Leimadophis poecilogyrus pictostriatus Amaral (Serpentes: Colubridae).Iheringia. Ser. Zool., 1960, 13, 20-7.

[14] 14 MIRANDA ME, VALLEJO MT, GRISOLIA CS. Nota sobre casos de albinismo en ofidios argentinos. Hist. Nat., 1985, 5, 121-4.

[15] 15 PRADO A. Notas ofiológicas. 3. Mais um caso de albinismo em serpente.Mem. Inst. Butantan, 1939, 13, 9-11.

[16] 16 PRADO A, BARROS FP. Notas ofiológicas. 9. Duas cascavéis albinas do Brasil. Mem. Inst. Butantan, 1940, 14, 31-2.

[17] 17 RENAULT L, SCHREIBER G. Considerações sobre albinismo em cascavel. Folia Clin. Biol., 1949, 16, 91-2.

[18] 18 SAZIMA I, DI-BERNARDO M. Albinismo em serpentes neotropicais.Mem. Inst. Butantan, 1991, 53, 167-73.

[19] 19 STEADMAN, TL. Steadman dicionário médico ilustrado.25.ed. Rio de Janeiro: Guanabara Koogan, 1996. 1657p.

[20] 20 VILLA J, RIVAS A. Tres serpientes albinas de Nicaragua.Rev. Biol. Trop., 1971, 19, 159-63.

[21] ²¹21 WILLENSE, GT. Individual variation in snake venom. Comp. Biochem. Physiol., 1978, 61, 553-7.