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Neotropical stingless bees Melipona quadrifasciata exploit the carcass of the giant toad Rhinella icterica in Southeast Brazil PDF

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Preview Neotropical stingless bees Melipona quadrifasciata exploit the carcass of the giant toad Rhinella icterica in Southeast Brazil

Tropical Natural History 18(2): 146-149, October 2018 2018 by Chulalongkorn University Short Note Neotropical stingless bees Melipona quadrifasciata exploit the carcass of the giant toad Rhinella icterica in Southeast Brazil IVAN SAZIMA Museu de Zoologia, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-863 Campinas, São Paulo, BRAZIL * Corresponding Author: Ivan Sazima ([email protected]) Received: 2 May 2018; Accepted: 6 August 2018 Stingless social bees (Meliponini) occur quadrifasciata) exploiting the carcass of the in most tropical and subtropical regions of yellow cururu toad (Rhinella icterica), a the world, including Africa, America, species of the R. marina complex, in the Australia and Southeast Asia1. As occurs Atlantic Forest of the Rio de Janeiro with most bee species, the meliponines highlands in Southeast Brazil. forage on flowers from which they gather I observed the bees on the toad carcass at their most important food resources, nectar the edge of a trail (22°26’40’’S, 44°36’40” and pollen1. Aside from flowers, some W, 936 m altitude) in a highland Atlantic meliponine species exploit less conventional Forest at the Itatiaia National Park in resources such as carrion, blood, urine, Itatiaia, Rio de Janeiro state, southeast animal flesh or hide, fungi, and rotten fruits, Brazil, on 22 September 2017. I recorded and in the Neotropics, a variety of the behavior of the bees on the toad carcass meliponine bees forages habitually on near midday, at a temperature ranging about carrion, notably several species of the genus 30° C and air humidity of about 40%. I Trigona1,2,3,4,5,6,7,8. observed the bees with unaided eyes from a Giant toads of the Rhinella marina group distance of 30-50 cm and documented their are renowned for their large parotoid glands behaviour on the carcass with photographs. that secrete powerful venom9. This venom During the observational sessions, I used the notwithstanding, a few opportunistic ad libitum and sequence samplings14, both vertebrate scavengers such as snakes, birds, of which are adequate to record fortuitous or and mammals feed on dead giant toads, rare events. No vouchers were taken due to although the venom glands are not the status of protected area at the consumed10,11,12. However, most small observation site. This characteristic carcasses such as those of toads are meliponine species was provisionally consumed mostly by insects, which seem identified in the field and latter confirmed in immune to bufotoxins10,11,13. Various the lab as Melipona quadrifasciata stingless meliponine bee species, including anthidioides15. two or three of the genus Melipona, exploit One to two Melipona quadrifasciata vertebrate carcasses4,7,8, but I found no individuals exploited the toad carcass at the records of meliponine bees making use of time of the observations. The bees hovered toad carcasses, still less those of the large over or moved on the remains, where they species of the genus Rhinella2. I report here investigated the surface with their antennae, on the mandaçaia stingless bee (Melipona stopping from time to time at some SAZIMA – NEOTROPICAL STINGLESS BEES EXPLOIT THE CARCASS OF THE GIANT TOAD 147 FIGURE 1. The stingless bee Melipona quadrifasciata exploits the eye socket of the carcass of the giant toad Rhinella icterica. Note the large almond-shaped venom gland behind the toad’s eye. particular places of the carcass that was at novel information on carrion use by the least stage of decomposition (dry). One meliponine bees. In a study that used lizard of them stopped at the eye socket of the and toad carcasses as bait in Costa Rica, carcass (Fig. 1), where it seemed to chew a seven species of the meliponine genus little and regurgitate a liquid (water?) and Trigona exploited the carcass of the large imbibe it again two to three times, flying lizard Iguana iguana, but the carcass of the away afterwards. This exploiting behaviour giant marine toad Rhinella marina received was repeated at some other parts of the no visits of meliponine bees2. Carrion- carcass, including a broken hind limb and exploiting meliponine bees are found mostly the venom gland. At a given moment, one of among Trigona species1,4. However, the the individuals stopped to clean the behaviour I report herein for M. antennae with its forelegs, while the other quadrifasciata was somewhat similar to that entered the carcass through a rupture on the described for these carrion-feeding Trigona back (Fig. 2). It emerged about 30 sec latter species, including to regurgitate water on and proceeded to investigate the carcass. I the carcass and imbibe it again1. Carrion was unable to say whether the individuals exploitation by meliponine bees seems were the same through the whole related to intake of some nutrients such as observation period, despite their striking salts, amino acids, lipids and others, which yellow markings on the black abdomen. would vary with the carrion type, i.e. animal The exploitation of Rhinella icterica toad species, and decay stage1. carcass by Melipona quadrifasciata is a 148 TROPICAL NATURAL HISTORY. 18(2), OCTOBER 2018 FIGURE 2. Two Melipona quadrifasciata individuals exploit the carcass of the giant toad Rhinella icterica, one of them entering through a rupture on the toad’s back. Meliponine carrion feeders find desiccation16. Studies using carcasses of carcasses quickly during the dry season2,3, venomous toads as bait would be instructive and the observations I report herein were to investigate whether meliponine bees undertaken after an unusually warm and dry exploit this carrion type very occasionally, austral autumn in the Itatiaia highland or whether toad carrion exploitation by forest. Apparently, the toad carcass attracted meliponines is restricted to particular the meliponine bees despite its dryness, and individuals, populations, sites, or seasons. the regurgitating and imbibing behaviour I recorded may compensate for the carcass ACKNOWLEDGEMENTS dryness. The exploitation of the desiccated venomous toad by M. quadrifasciata seems I thank Marlies Sazima for loving noteworthy, as fragments of sun-dried support in the field and at home, verification carcasses of the invasive giant marine toad of the bee identification (besides thoughtful R. marina are highly toxic to aquatic comments on the observations and the Australian native vertebrates and manuscript). Earlier grants from the CNPq invertebrates16. This latter study16 partly made my studies on natural history of disagrees with the notion that toad venom is Atlantic Forest fauna possible. ineffective for invertebrates10. The toxicity of R. marina sun-dried carcasses endures for many months after the animal’s death and SAZIMA – NEOTROPICAL STINGLESS BEES EXPLOIT THE CARCASS OF THE GIANT TOAD 149 LITERATURE CITED 9. Toledo, R.C. and Jared, C. 1995. Cutaneous granular glands and amphibian venoms. Comp. 1. Roubik, D.W. 1989. Ecology and natural history Biochem. Physiol. 111A: 1-29. of tropical bees. Cambridge University Press, 10. Cabrera-Guzmán, E.C., Crossland, M.R., Cambridge, x+514pp. Pearson, D., Webb, J.K. and Shine, R. 2015. 2. Cornaby, B.W. 1974. Carrion reduction by Predation on invasive cane toads (Rhinella animals in contrasting tropical habitats. marina) by native Australian rodents. J. Pest Biotropica 6: 51-63. Sci. 88: 143-153. 3. Crewe, R.M. 1985. Bees observed foraging on 11. Abernethy, E.F., Turner, K.S., Beasley, J.C., an impala carcass. Bee World 66: 8. DeVault, T.L., Pitt, W.C. and Rhodes Jr., O.E. 4. Baumgartner, D. and Roubik, D.W. 1989. 2016. Carcasses of invasive species are Ecology of necrophilous and filth-gathering predominantly utilized by invasive scavengers stingless bees (Apidae: Meliponinae) of Peru. J. in an island ecosystem. Ecosphere 7: e01496. Kans. Entomol. Soc. 62: 11-22. 12. Oliveira, I.S., Ribeiro, V.M., Pereira, E.R. 5. Oliveira, M.L. and Morato, E.F. 2000. and Vitule, J.R.S. 2016. Predation on native Stingless bees (Hymenoptera, Meliponini) anurans by invasive vertebrates in the feeding on stinkhorn spores (Fungi, Phallales): Atlantic Rain Forest, Brazil. Oecologia robbery or dispersal? Rev. bras. Zool. 17: 881- Australis 20: 70-74. 884. 13. Rofela, C., Tsifoanya, M.T., Kwafo, R. and 6. Lorenzon, M.C.A and Matrangolo, C.A.R. Tuadzra, E.K.A. 2017. Necrophagous insects 2005. Foraging on some nonfloral succession on carrions’ of two tropical animals. resources by stingless bees (Hymenoptera, Eur. J. Zool. Res. 5: 1-9. Meliponini) in a Caatinga region. Braz. J. 14. Altmann, J. 1974. Observational study of Biol. 65: 291-298. behaviour: sampling methods. Behaviour 49: 7. Silveira, O.T., Esposito, M.C., Santos Jr., 227-267. J.N. and Gemaque, F.E. 2005. Social wasps 15. Batalha-Filho, H., Melo, G.A.R., Waldschmidt, and bees captured in carrion traps in a A.M., Campos, L.A.O. and Fernandes-Salomão, T.M. 2009. Geographic distribution and spatial rainforest in Brazil. Entomol. Sci. 8: 33-39. differentiation in the color pattern of abdominal 8. Gomes, L., Gomes, G, Oliveira, H.G., stripes of the Neotropical stingless bee Melipona Morlin Jr., J.J., Desuo, I.C., Queiroz, quadrifasciata (Hymenoptera: Apidae). M.M.C.., Gianotti, E. and Von Zuben C.J. Zoologia 26: 213-219. 2007. Occurrence of Hymenoptera on Sus 16. Crossland, M., Brown, G. and Shine, R. scrofa carcasses during summer and winter 2011. The enduring toxicity of road-killed cane seasons in southeastern Brazil. Rev. Bras. toads (Rhinella marina). Biol. Invasions 13: Entomol. 51: 394-396. 2135-2145.

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