Pectoral-fin glands and delivery apparatus in the catfish genus Brachyrhamdia Myers, 1927 (Siluriformes: Heptapteridae)
DOI:
https://doi.org/10.11606/1807-0205/2021.61.74Keywords:
Axillary glands, Comparative anatomy, Histology, Neotropical ichthyologyAbstract
The Siluriformes, popularly known as catfishes, are probably the vertebrate group with the highest diversity of venomous animals, even though only approximately a hundred venomous catfishes are reported to date. Venomous catfishes might present a delivery system apparatus, formed by an unbranched ray at the leading edge of pectoral and dorsal fins (spine), which can be stiffened and pungent, while venom glands can be present at the surface of such spines and/or the axillary region. This work investigated the presence, morphology and distribution of glands and pectoral-fin delivery apparatus in the heptapterid Brachyrhamdia genus. Pectoral-fin spine external morphology was compared across all valid species in the genus, histological sections of the pectoral-fin spine and axillary regions of B. heteropleura and B. marthae were produced, and dissections of the pectoral girdle region of the mentioned species were analyzed. The histological sections confirmed the presence of pectoral-fin glands at the surface of the pectoral-fin spine of Brachyrhamdia species, and cellular morphology indicates these glands are probably venomous. Also, we found a piriform gland at the axillary region, whose cell morphology is like the reported for other catfishes. However, we cannot currently confirm or deny axillary gland participation in the venom delivery apparatus. This work constitutes the first report of venom glands in Brachyrhamdia, and the first description of Heptapteridae axillary glands.
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References
Albert, J.S.; Tagliacollo, V.A. & Dagosta, F. 2020. Diversification of Neotropical freshwater fishes. Annual Review of Ecology, Evolution, and Systematics, 51: 27-53. http://doi.org/10.1146/annurev-ecolsys-011620-031032
Al-Hassan, J.M.; Thomson, M.; Ali, M. & Criddle, R.C. 1987. Toxic and pharmacologically active secretions from the Arabian Gulf catfish (Arius thalassinus, Ruppell). Journal of Toxicology: Toxin Reviews, 6: 1-43.
Aquino, G.N.D.; Souza, C.C.; Haddad-Jr., V. & Sabino, J. 2016. Injuries caused by the venomous catfish pintado and cachara (Pseudoplatystoma genus) in fishermen of the Pantanal region in Brazil. Anais da Academia Brasileira de Ciências, 88(3): 1531-1537. http://doi.org/10.1590/0001-3765201620150336
Axelrod, H.R. 1987. Two new species of catfishes (Siluriformes, Callichthyidae and Pimelodidae) from the Rio Unini, Amazonas, Brazil. Tropical Fish Hobbyist, 35: 22-25.
Behmer, A.; Tolosa, E.M.C. & Neto, A.G.F. 1976. Manual de técnicas para histologia normal e patológica. São Paulo, EDART/EDUSP.
Birkhead, W.S. 1967. The comparative toxicity of stings of the ictalurid catfish genera Ictalurus and Schilbeodes. Comparative Biochemistry and Physiology, 22(1): 101-111.
Birkhead, W.S. 1972. Toxicity of stings of ariid and ictalurid catfishes. Copeia, 1972(4): 790-807. http://doi.org/10.2307/1442737
Bockmann, F.A. 1998. Análise filogenética da família Heptapteridae (Teleostei, Ostariophysi, Siluriformes) e redefinição de seus gêneros. (Doctoral thesis) Universidade de São Paulo.
Bockmann, F.A. & Miquelarena, A.M. 2008. Anatomy and phylogenetic relationships of a new catfish species from northeastern Argentina with comments on the phylogenetic relationships of the genus Rhamdella Eigenmann and Eigenmann 1888 (Siluriformes, Heptapteridae). Zootaxa, 1780: 1-54. http://doi.org/10.11646/zootaxa.1780.1.1
Bockmann, F.A. & Slobodian, V. 2017. Family Heptapteridae (three-barbeled catfishes). In: Van Der Sleen, P. & Albert, J.S. (Eds.). Field Guide to the Fishes of the Amazon, Orinoco and Guianas 1. New Jersey, Princeton University Press. p. 233-252.
Bosher, B.T.; Newton, S.H. & Fine, M.L. 2006. The spines of the channel catfish, Ictalurus punctatus, as an anti-predator adaptation: an experimental study. Ethology, 112: 188-195.
Cameron, A.M. & Endean, R. 1971. The axillary glands of the plotosid catfish Cnidoglanis macrocephalus. Toxicon, 9(4): 345-352. http://doi.org/10.1016/0041-0101(71)90132-2
Cameron, A.M. & Endean, R. 1973. Epidermal secretions and the evolution of venom glands in fishes. Toxicon, 11: 401-410. http://doi.org/10.1016/0041-0101(73)90115-3
Church, J.E. & Hodgson, W.C. 2002. The pharmacological activity of fish venoms. Toxicon, 40: 1083-1093. http://doi.org/10.1016/s0041-0101(02)00126-5
Egge, J.J.D. & Simons, A.M. 2011. Evolution of venom delivery structures in madtom catfishes (Siluriformes: Ictaluridae). Biological Journal of the Linnean Society, 102: 115-129. http://doi.org/10.1111/j.1095-8312.2010.01578.x
Emmett, B. & Cochran, P.A. 2010. The response of a piscivore (Micropterus salmoides) to a venomous prey species (Noturus gyrinus). Journal of Freshwater Ecology, 25: 475-479.
Fricke, R.; Eschmeyer, W.N. & van der Laan, R. 2020. Eschmeyer’s catalog of fishes: genera, species, references. Available: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Access: 15/11/2020.
Greven, H.; Flasbeck, T. & Passia, D. 2006. Axillary glands in the armoured catfish Corydoras aeneus (Callichthyidae, Siluriformes). Verhandlungen der Gesellschaft für Ichthyologie, 5: 65-69.
Guazzelli, G.M. 2003. Relações filogenéticas do gênero Pimelodella Eigenmann and Eigenmann 1888 (Siluriformes, Pimelodidae). (Doctoral thesis) Universidade de São Paulo. São Paulo.
Günther, A. 1880. An introduction to the study of fishes. London, Oxford University.
Gwee, M.C.E.; Gopalakrishnakone, P.; Yuen, R.; Khoo, H.E. & Low, K.S.Y. 1994. A review of stonefish venoms and toxins. Pharmacology & Therapeutics, 64(3): 509-528. http://doi.org/10.1016/0163-7258(94)90022-1
Haddad, V. 2016. Injuries by Vertebrate Aquatic Animals: Phylum Chordata (Fish, Reptiles, and Mammals). In: Haddad, V. Medical emergencies caused by aquatic animals. Switzerland, Springer. p. 35-85. http://doi.org/10.1007/978-3-319-20288-4_3
Haddad, V. & Martins, I.A. 2006. Frequency and gravity of human envenomations caused by marine catfish (suborder Siluroidei): a clinical and epidemiological study. Toxicon, 47(8): 838-843. http://doi.org/10.1016/j.toxicon.2006.02.005
Hahn, S.T. & O’Connor, J.M. 2000. An investigation of the biological activity of bullrout (Notesthes robusta) venom. Toxicon, 38(1): 79-89. http://doi.org/10.1016/s0041-0101(99)00135-x
Halstead, B.W. 1970. Poisonous and venomous marine animals of the world. Volume 3: Vertebrates. The Darwin Press, Princeton.
Halstead, B.W. 1978. Poisonous and venomous marine animals of the world. Princeton, The Darwin Press.
Halstead, B.W. 1988. Poisonous and venomous marine animals of the world. 2.ed. rev. Princeton, The Darwin Press.
Halstead, B.W. & Smith, R.L. 1954. Presence of an axillary venom gland in the Oriental catfish Plotosus lineatus. Copeia, 1954(2): 153-154.
Halstead, B.W.; Kuninobu, L.S. & Hebard, H.G. 1953. Catfish stings and the venom apparatus of the mexican catfish, Galeichthys felis (Linnaeus). Transactions of the American Microscopical Society, 72(4): 297-314.
Innes, W.T. & Myers, G.S. 1950. The “Imitator catfish,” which mimics a Corydoras. The Aquarium, 19: 222-223.
Jawad, L.A. 2018. Dangerous fishes of the eastern and southern Arabian Peninsula. Cham, Springer. http://doi.org/10.1007/978-3-319-57926-9
Kiehl, E.; Rieger, C. & Greven, H. 2006. Axillary gland secretions contribute to the stress-induced discharge of a bactericidal substance in Corydoras sterbai (Callichthyidae, Siluriformes). Verhandlungen der Gesellschaft für Ichthyologie, 5: 111-115.
Kubicek, K.M.; Britz, R. & Conway, K.W. 2019. Ontogeny of the catfish pectoral-fin spine (Teleostei: Siluriformes). Journal of Morphology, 280(3): 339-359. http://doi.org/10.1002/jmor.20947
Lundberg, J.G. & McDade, L.A. 1986. On the South American catfish Brachyrhamdia imitator Myers (Siluriformes, Pimelodidae), with a phylogenetic evidence for a large intrafamilial lineage. Notulae Nature, 463: 1-24.
Magalhães, G.S.; Lopes-Ferreira, M.; Junqueira-de-Azevedo, I.L.M.; Spencer, P.J.; Araújo, M.S.; Portaro, F.C.V.; Ma, L.; Valente, R.H.; Juliano, L.; Fox, J.W.; Ho, P.L. & Moura-da-Silva, A.M. 2005. Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie, 87(8): 687-689. http://doi.org/10.1016/j.biochi.2005.03.016
Nelson, J.S.; Grande, T.C. & Wilson, M.V.H. 2016. Fishes of the world. 5.ed. New Jersey, Wiley.
Ota, R.R.; Message, H.J.; da Graça, W.J. & Pavanelli, C.S. 2015. Neotropical Siluriformes as a model for insights on determining biodiversity of animal groups. PlosONE, 10(7): e0132913. http://doi.org/10.1371/journal.pone.0132913
Perrière, C. & Goudey-Perrière, F. 2003. Poisonous catfishes: venom apparatus, acanthotoxins, crinotoxins and other skin secretions. In: Arratia, G.; Kapoor, B.G.; Chardon, M. & Diogo, R. Catfishes. New Jersey, Science Publishers. v. 1, p. 291-314.
Reed, H.D. 1907. The poison glands of Noturus and Schilbeodes. American Naturalist, 41: 553-566.
Remington, C.L. 1963. Historical backgrounds of mimicry. In: International Congress of Zoology, 16º. Proceedings. Washington, ICZ, 1964. p. 145-149.
Sabaj, M.H. 2016. Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Available: https://asih.org/sites/default/files/documents/symbolic_codes_for_collections_v6.5_2016.pdf. Access: 16/08/2016.
Sands, D.D. 1985. Brachyrhamdia, cryptic or mimetic catfishes from South America: Zoomimesis, camouflage or mimicry. In: Sands, D. (Ed.). Catfishes of the World. Self published, Scotland. p. 51-58.
Schultz, L.P. 1944. The catfishes of Venezuela, with descriptions of thirty-eight new forms. Proceedings of the United States National Museum, 94: 173-338, pls. 1-14.
Silva, G.C.; Sabino, J.; Alho, C.J.R.; Nunes, V.L.B. & Haddad, V. 2010. Injuries and envenoming by aquatic animals in fishermen of Coxim and Corumbá municipalities, State of Mato Grosso do Sul, Brazil: identification of the causative agents, clinical aspects and first aid measures. Revista da Sociedade Brasileira de Medicina Tropical, 43(5): 486-490. http://doi.org/10.1590/S0037-86822010000500002
Silva, G.S.C.; Roxo, F.F.; Melo, B.F.; Ochoa, L.E.; Bockmann, F.A.; Sabaj, M.H; Jerep, F.C.; Foresti, F.; Benine, R.C. & Oliveira, C. 2021. Evolutionary history of Heptapteridae catfishes using ultraconserved elements (Teleostei, Siluriformes). Zoologica Scripta, 2021, 00: 1-12. http://doi.org/10.1111/zsc.12493
Slobodian, V. 2013. Taxonomia, Sistemática e Biogeografia de Brachyrhamdia Myers, 1927 (Siluriformes: Heptapteridae), com uma investigação sobre seu mimetismo com outros Siluriformes. (Masters dissertation) Universidade de São Paulo. Ribeirão Preto.
Slobodian, V. & Bockmann, F.A. 2013. A new Brachyrhamdia (Siluriformes: Heptapteridae) from Rio Japurá basin, Brazil, with comments on its phylogenetic affinities, biogeography and mimicry in the genus. Zootaxa, 3717(1): 1-22. http://doi.org/10.11646/zootaxa.3717.1.1
Smith, W.L. & Wheeler, W.C. 2006. Venom evolution widespread in fishes: a phylogenetic road map for the bioprospecting of piscine venoms. Journal of Heredity, 97(3): 206-17. http://doi.org/10.1093/jhered/esj034
Smith, W.L.; Stern, J.H.; Girard, M.G. & Davis, M.P. 2016. Evolution of Venomous Cartilaginous and Ray-Finned Fishes. Integrative and Comparative Biology, 56(5): 950-961. http://doi.org/10.1093/icb/icw070
Taylor, W.R. & Van Dyke, G.C. 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9(2): 107-119.
Vanscoy, T.; Lundberg, J.G. & Luckenbill, K.R. 2015. Bony ornamentation of the catfish pectoral-fin spine: comparative and developmental anatomy, with an example of fin-spine diversity using the Tribe Brachyplatystomini (Siluriformes, Pimelodidae). Proceedings of the Academy of Natural Sciences of Philadelphia, 164: 177-212.
Vernick, S.H. & Chapman, G.B. 1968. Ultrastructure of axillary glands of the toadfish Opsanus tau. Chesapeake Science, 9(3): 182-197.
Whitear, M.; Zaccone, G.; Fasulo, S. & Licata, A. 1991. Fine structure of the axillary gland of the brown bullhead (Ictalurus nebulosus). Journal of Zoology, 224: 669-676.
Wright, J.J. 2009. Diversity, phylogenetic distribution, and origins of venomous catfishes. BMC Evolutionary Biology, 9(1): 282. http://doi.org/10.1186/1471-2148-9-282
Wright, J.J. 2012. The evolutionary ecology of venomous catfishes, with a focus on members of the north American family Ictaluridae (Teleostei: Siluriformes). (Doctoral thesis) Michigan University, Ann Arbor.
Wright, J.J. 2015. Evolutionary History of Venom Glands in the Siluriformes. In: Gopalakrishnakone, P. & Malhotra, A. (Eds.). Evolution of Venomous Animals and Their Toxins. Dordrecht, Springer. p. 1-19. http://doi.org/10.1007/978-94-007-6727-0_9-1
Zaccone, G.; Kapoor, B.G.; Fasulo, S. & Ainis, L. 2001. Structural. histochemical and functional aspects of the epidermis of fishes. Advances in Marine Biology, 40: 255-347.
Zaccone, G.; Tagliaferro, G.; Fasulo, S.; Contini, A.; Ainis, L. & Licata, A. 1990. Serotonin-like immunoreactivity in the epidermal club cells of teleost fishes. Histochemistry, 93(4): 355-357.
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