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Length, weight, and longevity record for Micrurus frontalis (Duméril, Bibron & Duméril, 1854)

Recorde de comprimento, peso, e longevidade para Micrurus frontalis (Duméril, Bibron & Duméril, 1854)

The South American triadal coral snakes (snakes with three black rings combined with red and white (or yellow rings) include 17 currently recognized species (Silva Júnior et al., 2003) and one of them is Micrurus frontalis (Figure 1a), which is distributed from the Cerrado formations of Central Brazil (including Sao Paulo and Minas Gerais), and west into Goias, and the Brazilian states of Mato Grosso and Mato Grosso do Sul. To the east, M. frontalis reaches the Atlantic coast in the state of Espirito Santo, and to the S-SW it is found in southern Paraguay (Silva Júnior and Sites Junior, 1999SILVA JÚNIOR, N.J. and SITES JUNIOR, J.W., 1999. Revision of the Micrurus frontalis complex (Serpentes: elapidae). Herpetological Monograph, vol. 13, pp. 142-194. http://dx.doi.org/10.2307/1467062.
http://dx.doi.org/10.2307/1467062...
; Campbell and Lamar, 2004CAMPBELL, J.A. and LAMAR, W.W., 2004.The venomous reptiles of the Western Hemisphere. Ithaca: Cornell University Press. ).

Figure 1
(a) Micrurusfrontalis kept in captivity in bark substrate; (b) M. frontalis grasping a thawed Bothropsjararaca.

M. frontalis venom has a postsynaptic neurotoxin that produces loss of muscle strength and death by respiratory paralysis (Lomonte et al., 2016LOMONTE, B., REY-SUÁREZ, P., FERNÁNDEZ, J., SASA, M., PLA, D., VARGAS, N. & CALVETE, J. J., 2016. Venoms of Micrurus coral snakes: Evolutionary trends in compositional patterns emerging from proteomic analyses. Toxicon, vol. 122, pp.7-25. https://doi.org/10.1016/j.toxicon.2016.09.008.
https://doi.org/10.1016/j.toxicon.2016.0...
; Medeiros et al., 2019MEDEIROS, C.R., SOUZA, C.R., LARA, S.N. and GREGO, K.F., 2019. Use of infrared thermography in a case of systemic envenomation by the coral snake Micrurus frontalis (Duméril et al., 1854) in Sao Paulo, Brazil. Toxicon, vol. 163, pp. 70-73. http://dx.doi.org/10.1016/j.toxicon.2019.03.016. PMid:30905699.
http://dx.doi.org/10.1016/j.toxicon.2019...
; Sanz et al., 2019SANZ, L., FREITAS-LIMA, L.N., QUESADA-BERNAT, S., GRAÇA-DE-SOUZA, V.K., SOARES, A.M., CALDERÓN, L.A., CALVETE, J.J. and CALDEIRA, C.A.S, 2019. Comparative venomics of Brazilian coral snakes: Micrurus frontalis, Micrurus spixii spixii, and Micrurus surinamensis. Toxicon, vol. 166, pp. 39-45. http://dx.doi.org/10.1016/j.toxicon.2019.05.001. PMid:31091423.
http://dx.doi.org/10.1016/j.toxicon.2019...
), therefore all accidents must be carefully monitored and evaluated as potentially serious. Its venom is used in the production of Brazilian antielapidic serum, along with the venom of M. corallinus. Both species are maintained at the animal facility of the Laboratory of Herpetology at Butantan Institute (LHBI) to produce the anti-venom serum that is distributed to all Brazilian states by the Ministry of Health.

In May 2009, an adult male of M. frontalis from the State of São Paulo was donated to the LHBI, weighting 145g and with a snout-vent length (SVL) and total length (TL) of 105 cm and 112 cm, respectively. It was given the identification number Mf 0903.

In nature, M. frontalis diet consists of animals with fossorial or cryptozoic habits, as amphisbaenians, some snakes and lizards (Silva Junior, 1995SILVA JUNIOR, N.J., 1995. Molecular systematics and evolution of venoms in the South American ‘triad’ Coral Snakes Micrurus, elapidae. Provo: Brigham Young University. PhD Dissertation in Zoology.; Roze, 1996ROZE, J.A. 1996. Coral snakes of the Americas: biology, identification, and venoms. Malabar: Krieger, 328 p.; Silva Junior and Aird, 2001SILVA JUNIOR, N.J. and AIRD, S.D., 2001. Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comparative Biochemistry and Physiology. Toxicology & Pharmacology, vol. 128, no. 3, pp. 425-456. http://dx.doi.org/10.1016/S1532-0456(00)00215-5. PMid:11255115.
http://dx.doi.org/10.1016/S1532-0456(00)...
). During captivity the specimen was offered thawed snakes in a quantity of 40% of its body weight for three consecutive weeks, followed by a 15-day break after which the snake was milked (Mendes et al., 2019MENDES, G.F., STUGINSKI, D.R., LOIBEL, S.M., MORAIS-ZANI, K.D., ROCHA, M.M.T., FERNANDES, W., SANT’ANNA, S.S. and GREGO, K.F., 2019. Factors that can influence the survival rates of coral snakes (Micrurus corallinus) for antivenom production. Journal of Animal Science, vol. 97, no. 2, pp. 972-980. http://dx.doi.org/10.1093/jas/sky467. PMid:30541079.
http://dx.doi.org/10.1093/jas/sky467...
). The thawed preys offered were from various species, as Sibynomorphusmikanii, S. neuwiedi, Oxyrhopusguibei, Tomodondorsatus, Bothropsjararaca, B. alternatus, B. jararacussu, B. atrox, Atractus sp, Crotalus durissus, Philodryas sp and Pantherophisguttatus, which were all well accepted by the male (Figure 1b).

To increase milking efficiency, pilocarpine was administered intradermally (10mg Kg-1) ten minutes before venom extraction (Morais-Zani et al., 2018MORAIS-ZANI, K., SERINO-SILVA, C., GALIZIO, N.C., TASIMA, L.J., PAGOTTO, J.F., ROCHA, M.M.T., MARCELINO, J.R., SANT’ANNA, S.S., TASHIMA, A.K., TANAKA-AZEVEDO, A.M. and GREGO, K.F., 2018. Does the administration of pilocarpine prior to venom milking influence the composition of Micrurus corallinus venom? Journal of Proteomics, vol. 174, pp. 17-27. http://dx.doi.org/10.1016/j.jprot.2017.12.010. PMid:29275045.
http://dx.doi.org/10.1016/j.jprot.2017.1...
). Pilocarpine is a natural alkaloid with cholinergic agonist activity that binds to muscarinic receptors inducing secretion from exocrine glands (NCI THESAURUS, 2020NCI THESAURUS, 2020 [viewed 1 November 2020]. Pilocarpine Base [online]. NIH. Available from: https://ncit.nci.nih.gov/ncitbrowser/ConceptReport.jsp?dictionary=NCI_Thesaurus&ns=NCI_Thesaurus&code=C62068
https://ncit.nci.nih.gov/ncitbrowser/Con...
). Coral snake venom milking is done with tips attached to the proteroglyphs fangs (Figure 2) and afterwards the venom is pipetted to microtubes.

Figure 2
Tips attached to M. frontalis fangs for milking.

The specimen was kept in a glass terrarium measuring 120 cm x 40 cm x 60 cm, with bark previously treated with chlorine solution as substrate, water ad libitum and a shelter made of palm leaf. For 5 years, this specimen alone was responsible for the venom of M. frontalis mixed with the venom of M. corallinus for the production of antielapidic serum distributed through the Brazilian Territory. After 8 years in captivity (3123 days) this male died in 2017 due to heart failure, with a TL of 170 cm and weighing 978g (Figure 3). In literature the maximum length recorded for this specie is 164 cm, and to the best of our knowledge this is the record of Micrurusfrontalis kept for the longest time in captivity. Oliveira et al. (2006)OLIVEIRA, L., RIBEIRO, A.C.O., SCARTOZZONI, C.R.R., GERMANO, V.J. and SALOMÃO, M.D.G., 2006. Manutenção de serpentes em cativeiro no Instituto Butantan: I–longevidade do Gênero Micrurus. Publ. Avul. Inst. Pau Brasil, vol. 8, pp. 55-62., related a longevity record of 1298 days for M. frontalis kept in captivity.

Figure 3
M. frontalis Mf 0903.

The average amount of venom yielded per M. frontalis maintained in captivity at the LHBI in each milking is 70 mg of total venom (from 2018 to present); in contrast, this male yielded 500mg/milking. Graphic 1 shows the growth (weight and length) of the specimen during its 8 years in captivity.

Graphic 1
Growth of Micrurus frontalis during 8 years of captivity.

References

  • CAMPBELL, J.A. and LAMAR, W.W., 2004.The venomous reptiles of the Western Hemisphere Ithaca: Cornell University Press.
  • LOMONTE, B., REY-SUÁREZ, P., FERNÁNDEZ, J., SASA, M., PLA, D., VARGAS, N. & CALVETE, J. J., 2016. Venoms of Micrurus coral snakes: Evolutionary trends in compositional patterns emerging from proteomic analyses. Toxicon, vol. 122, pp.7-25. https://doi.org/10.1016/j.toxicon.2016.09.008
    » https://doi.org/10.1016/j.toxicon.2016.09.008
  • MEDEIROS, C.R., SOUZA, C.R., LARA, S.N. and GREGO, K.F., 2019. Use of infrared thermography in a case of systemic envenomation by the coral snake Micrurus frontalis (Duméril et al., 1854) in Sao Paulo, Brazil. Toxicon, vol. 163, pp. 70-73. http://dx.doi.org/10.1016/j.toxicon.2019.03.016 PMid:30905699.
    » http://dx.doi.org/10.1016/j.toxicon.2019.03.016
  • MENDES, G.F., STUGINSKI, D.R., LOIBEL, S.M., MORAIS-ZANI, K.D., ROCHA, M.M.T., FERNANDES, W., SANT’ANNA, S.S. and GREGO, K.F., 2019. Factors that can influence the survival rates of coral snakes (Micrurus corallinus) for antivenom production. Journal of Animal Science, vol. 97, no. 2, pp. 972-980. http://dx.doi.org/10.1093/jas/sky467 PMid:30541079.
    » http://dx.doi.org/10.1093/jas/sky467
  • MORAIS-ZANI, K., SERINO-SILVA, C., GALIZIO, N.C., TASIMA, L.J., PAGOTTO, J.F., ROCHA, M.M.T., MARCELINO, J.R., SANT’ANNA, S.S., TASHIMA, A.K., TANAKA-AZEVEDO, A.M. and GREGO, K.F., 2018. Does the administration of pilocarpine prior to venom milking influence the composition of Micrurus corallinus venom? Journal of Proteomics, vol. 174, pp. 17-27. http://dx.doi.org/10.1016/j.jprot.2017.12.010 PMid:29275045.
    » http://dx.doi.org/10.1016/j.jprot.2017.12.010
  • NCI THESAURUS, 2020 [viewed 1 November 2020]. Pilocarpine Base [online]. NIH. Available from: https://ncit.nci.nih.gov/ncitbrowser/ConceptReport.jsp?dictionary=NCI_Thesaurus&ns=NCI_Thesaurus&code=C62068
    » https://ncit.nci.nih.gov/ncitbrowser/ConceptReport.jsp?dictionary=NCI_Thesaurus&ns=NCI_Thesaurus&code=C62068
  • OLIVEIRA, L., RIBEIRO, A.C.O., SCARTOZZONI, C.R.R., GERMANO, V.J. and SALOMÃO, M.D.G., 2006. Manutenção de serpentes em cativeiro no Instituto Butantan: I–longevidade do Gênero Micrurus. Publ. Avul. Inst. Pau Brasil, vol. 8, pp. 55-62.
  • ROZE, J.A. 1996. Coral snakes of the Americas: biology, identification, and venoms Malabar: Krieger, 328 p.
  • SANZ, L., FREITAS-LIMA, L.N., QUESADA-BERNAT, S., GRAÇA-DE-SOUZA, V.K., SOARES, A.M., CALDERÓN, L.A., CALVETE, J.J. and CALDEIRA, C.A.S, 2019. Comparative venomics of Brazilian coral snakes: Micrurus frontalis, Micrurus spixii spixii, and Micrurus surinamensis Toxicon, vol. 166, pp. 39-45. http://dx.doi.org/10.1016/j.toxicon.2019.05.001 PMid:31091423.
    » http://dx.doi.org/10.1016/j.toxicon.2019.05.001
  • SILVA JUNIOR, N.J. and AIRD, S.D., 2001. Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comparative Biochemistry and Physiology. Toxicology & Pharmacology, vol. 128, no. 3, pp. 425-456. http://dx.doi.org/10.1016/S1532-0456(00)00215-5 PMid:11255115.
    » http://dx.doi.org/10.1016/S1532-0456(00)00215-5
  • SILVA JÚNIOR, N.J. and SITES JUNIOR, J.W., 1999. Revision of the Micrurus frontalis complex (Serpentes: elapidae). Herpetological Monograph, vol. 13, pp. 142-194. http://dx.doi.org/10.2307/1467062
    » http://dx.doi.org/10.2307/1467062
  • SILVA JUNIOR, N.J., 1995. Molecular systematics and evolution of venoms in the South American ‘triad’ Coral Snakes Micrurus, elapidae Provo: Brigham Young University. PhD Dissertation in Zoology.
  • SILVA JÚNIOR, N.J. & BUCARETCHI, F. 2003. Mecanismos de ação do veneno elapídico e aspectos clínicos de acidentes. In: J.L.C. CARDOSO, V. HADDAD JUNIOR and F.S. FRANÇA, eds. Animais Peçonhentos no Brasil–Biologia, Clínica e Terapêutica dos Acidentes 2. ed. São Paulo: Editora Sarvier, pp 99-107.

Publication Dates

  • Publication in this collection
    11 Oct 2021
  • Date of issue
    2023

History

  • Received
    03 May 2021
  • Accepted
    10 June 2021
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