268 Correspondence –Notes
Old World and were introduced to Nearctic and Neotropical Bouček, Z. (1982): Oriental chalcid wasps of the genus Epitranus. Journal of regions (Bouček 1982). The hosts of Epitraninae are also little Natural History 16: 577-622. Kazemi, M.-H., Lotfalizadeh, H. (2014): Hockeria magna Bouček (Hymenoptera: known but records suggest they parasitize lepidopterous Chalcididae): New record to Iranian chalcidid fauna. North-Western Journal pests associated with stored products such as Tineidae and of Zoology 10 (1): 183-186. Pyralidae (Bouček 1982). Lotfalizadeh, H., Ebrahimi, E., Delvare, G. (2012): A contribution to the knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. Journal of Entomological Society of Iran 31(2): 67-100. Genus Epitranus Walker, 1834 Lotfalizadeh, H., Jafari-Nadushan, A. (2015): New records of two rare species of Epitranus clavatus (Fabricius, 1804) (Figs. 1A-G) the family Chalcididae (Hymenoptera: Chalcidoidea) in Iran, with data on Chalcis clavata Fabricius, 1804 their associations. Acta Zoologica Bulgarica 67(2): 297-298. Moravvej, S. A., Shishehbor, P., Lotfalizadeh, H. (2016): A checklist of Epitranus falvescens Walker, 1834 Chalcidoidea (Insecta: Hymenoptera) of Khuzestan in southwestern Iran. Epitranus lacteipennis Cameron, 1883 Journal of Insect Biodiversity and Systematics 2: 121-142. Anacryptus insidiosus Masi, 1917 Noyes, J.S. (2017): Universal Chalcidoidea Database. The Natural History Museum,
Material Examined: Iran, Khuzestan province, Ahwaz, Key words: Epitranus clavatus, Epitraninae, Chamran University campus, July 2017, Yellow pan trap, S. Chalcididae, Iran, new record. A. Moravvej leg., 1 ♀. Deposited in the Insect Collection of Chamran University, Ahwaz. Article No.: e177202 Diagnostic features: Body mainly reddish (Fig. 1A), with Received: 04. August 2017 / Accepted: 19. October 2017 Available online: 29. October 2017 / Printed: December 2018 some slightly dark parts; thorax with regular punctuations (Fig. 1D), without patches of hairs, interspaces finely granu- late or partly obliterated; hind femur with fewer than 15 Seyed Abbas MORAVVEJ1*, Hossein LOTFALIZADEH2 teeth which are relatively broader and less regular than in and Parviz SHISHEHBOR1 albipennis and nitens, hind tibia with strong angulate subba- sal tooth, crenulate under hairs and tarsal sulcus with dis- 1. Department of Plant Protection, College of Agriculture, Shahid Chamran tinct oblique carina, extending over more than 3/4 up to- University of Ahvaz, Iran. 2. Department of Plant Protection, East-Azarbaijan Agricultural and Natural wards subbasal tooth (Fig. 1F); hind coxae ventrally with Resources Research and Education Center, Agricultural Research, Education very coarse but not very dense punctuations (Fig. 1A); pro- and Extension Organization (AREEO), Tabriz, Iran. podeum dull, with distinct granulate sculpture, also intersti- * Corresponding author, S.A. Moravvej, E-mail: [email protected] ces on thorax (at least partly) and bottoms of punctures with distinct reticulation, propodeal areolae very dull with reticu- lation, but thorax and occiput slightly shiny; in female peti- ole dorsally flattened and only up to 3 times as long as broad First record of pseudoautotomy in the genus (Fig. 1E); forewing hyaline with strongly reduced pilosity Echinanthera (Serpentes: Colubridae) (Fig. 1G), virtually absent below marginal vein, especially not forming any distinct hairline recurrent from stigmal Urotomy (tail breakage) is a singular defensive strategy in vein, venation distinct, pigmented, costal cell about 2 times lepidosaurian reptiles, allowing an individual to lose por- as long as marginal vein. tions or the entirety of its tail during a predator attack, in- Biology of our examined specimens is unknown in Iran, creasing its chances of escape (Arnold 1984). Its more com- but outside it has been recorded from Tinea sp., T. antricola monly known variation is autotomy, which occurs in the Meyrick, T. palaechrysis Meyrick and Crypsithyris sp. (Lepi- tuatara (Sphenodontidae) and in several lineages of lizards; doptera, Tineidae) (Noyes 2017) thus, its hosts seem to be it is characterized by the intravertebral rupture in special- small Lepidoptera, possibly associated with some tropical, ized planes of the tail, with the capacity of spontaneous frac- probably stored products (Bouček 1982). ture and partial regeneration by the development of a carti- Geographical distribution: This species has been recorded laginous rod in the area previously occupied by the osseous from Oriental (India, Malaysia Taiwan), Nearctic (USA) and tissue (Slowinski & Savage 1995, Savage & Slowinski 1996, Neotropical (Brazil, Guyana) regions (Bouček 1982, Noyes Jagnandan et al. 2014). Another form, termed pseudoautot- 2017); this is a new record of species from Iran. Our finding omy by Slowinski & Savage (1995), is diagnosed by the in- of this species from southern part of Iran (Khuzestan) that tervertebral fracture in random portions of the tail, without located between Oriental and Afrotropical regions seems the capacity for spontaneous rupture or regeneration, and ordinary. Bouček (1982) believes this species is native in the present in some snakes and lizards (Etheridge 1967, Arnold Old World tropics, possibly in South Asia, but was 1984, Slowinski & Savage 1995). In this case, since the tail repeatedly introduced to parts of tropical America. rupture is not spontaneous, it depends on external stimuli in order to occur (Savage & Slowinski, 1996). Acknowledgements. We would like thank Research Deputy of Accordingly to Arnold (1984) and Bateman & Fleming Shahid Chamran University for financial help and reviewers for the (2009), pseudoautotomy is a derived character, present in comments on the manuscript. taxons that lost their capacity to realize autotomy. In snakes, References two distinct forms of this behavior are known: specialized Aydoğdu, M. (2014): Parasitoid abundance of Archips rosana (Linnaeus, 1758) pseudoautotomy, in which the rupture is facilitated by the (Lepidoptera: Tortricidae) in organic cherry orchards. North-Western Journal of Zoology 10(1): 42-47. presence of a long, thick and fragile tail, and non-specialized 269 North-Western Journal of Zoology 14/2 - 2018
Figure 1. Specimen of Echinanthera cephalostriata (MZUSP 21.246) in which the tail breakage was observed. A: Dorsal surface; B: Ventral surface; C: Head views; D: Tail views. Photo- graph credits: Daniella Pereira Fagundes de França.
pseudoautotomy, in which the snakes have a moderately only its head partially exposed. The specimen was thereafter long or even long tail (>35% of total length in adults), but captured with a snake hook, and to our surprise, surfaced without observed modifications for tail breakage (Savage & amongst the leaf litter with a ruptured tail, while its ampu- Slowinski 1996). tated portion presented minimal bleeding and abrupt Even though the anatomical mechanism of the fracture is movements. The adult female (rostro-cloacal length of 434 still poorly known in snakes, there are urotomy records in mm, tail length 140 mm + n) was collected (under collecting several snake families (Hoogmoed & Ávila-Pires 2011, permit SISBIO 31557) and deposited in the Herpetological Dourado et al. 2013, Costa et al. 2014, Padilla-Pérez et al. Collection of the Museu de Zoologia da Universidade de São 2015, Crnobrnja-Isailović et al. 2016, Strugariu et al. 2018). Paulo (MZUSP 21.246). The genus Echinanthera Cope, 1894 belongs to colubrid Several authors have reported cases in which pseudo- snakes (Pyron et al. 2013, Figueroa et al. 2016), comprising autotomy occurs in situations that the tail is grabbed and the six species distributed across the oriental Atlantic region of snake twists its body across its longitudinal axis, until the Brazil (Di-Bernardo 1992). These species are characterized by tail is detached (e.g Cooper & Alfieri 1993, Savage & Slowin- their terrestrial and cryptozoic habits, slender bodies and ski 1996, Marco 2002, Crnobrnja-Isailović et al. 2016, long tails reaching up to 47% of the total body size in some Strugariu et al. 2018), although there is a record of a snake species (Gomes &Marques 2012). Marques & Sazima (2004) able to rupture its tail while twisting it across its body raised the hypothesis that E. cyanopleura (Cope, 1885) and E. (Hoogmoed & Ávila-Pires 2011). Unfortunately, due to the undulata (Wied, 1824) use their tails as defensive mecha- dense leaf litter in which the snake was encountered, we nisms, based on the number of specimens with damaged were unable to observe how the tail breakage occurred in tails examined in collections. Zanella & Cechin (2010) and this case. Gomes & Marques (2012) also provided brief mentions over Our record possibly corroborates the hypothesis raised the tail damage of E. cyanopleura and E. undulata specimens, by Marques & Sazima (2004), although the species men- respectively. Still, urotomy records for neotropical snakes tioned by these authors were not directly examined in this are rare (Costa et al. 2014) and this behavior was never ob- study. Accordingly to Martins (1994), terrestrial species with served within the genus Echinanthera. long tails possibly use them for specific means, such as uro- During fieldwork conducted in the Estação Ambiental tomy, since long tails are usually observed in arboreous, and São Camilo (Coordinates: -24.1827º, -46.7888º, Datum WGS rarely in terrestrial taxa. In the case of Echinanthera, this 84), municipality of Itanhaém, São Paulo state, in an after- could also be the norm, although a genus-wide analysis noon in September 2012, an individual of E. cephalostriata Di- needs to be undertaken. Bernardo 1996 was observed still under the leaf litter, having Absent or reduced bleeding after tail breakage in snakes 270 Correspondence –Notes has been reported by other authors (Dourado et al. 2013, Pyron, R.A., Burbrink, F.T., Wiens, J.J. (2013): A phylogeny and revised Ribeiro & Mesquita 2014, Padilla-Pérez et al. 2015). This classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13(1): 93. could indicate the presence of sphincters within the veins Ribeiro, S.C., Mesquita, D.O. (2014): Drymoluber brazili (Brazil’s woodland and arteries located in the tail of E. cephalostriata, in order to racer): Defensive behaviour. The Herpetological Bulletin 129: 30. stop blood loss during urotomy, as recorded for some lizard Savage, J.M., Slowinski, J.B. (1996): Evolution of coloration, urotomy and coral snake mimicry in the snake genus Scaphiodontophis (Serpentes: Colubridae). species (Arnold 1984). Biological Journal of the Linnean Society 57(2): 129–194. The first confirmed record of urotomy for E. cephalostriata Slowinski J.B., Savage, J.M. (1995): Urotomy in Scaphiodontophis: Evidence for corroborates the speculations that Echinanthera species may the multiple tail break hypothesis in snakes. Herpetologica 51(3): 338–341. Strugariu, A., Dinca, P.C., Zamfirescu, S.R. (2018): Deliberate tail loss use their tails as a defensive mechanism. However, this ob- (pseudoautotomy) in a viperid snake. North–Western Journal of Zoology servation suggests further studies regarding urotomy within 14(1): 144–146. the genus: (1) evaluate the presence/absence of sphincters Zanella, N., Cechin, S.Z. (2010): Reproductive biology of Echinanthera cyanopleura (Serpentes: Dipsadidae) in southern Brazil. Zoologia 27(1): 30–34. used to stop blood loss within Echinanthera spp.; (2) assess if there is a breakage plane or specialized musculature that as- Key words: Echinanthera, defensive behaviour, sists in tail breakage; (3) analyze if there is urotomy within urotomy, snakes, tail breakage. other closely related genera and evaluate if there are geo- graphical or sexual variations or trends within interspecific Article No.: e187501 tail breakage frequencies. These, and several other themes, Received: 14. March 2017 / Accepted: 31. January 2018 Available online: 01. February 2018 / Printed: December 2018 are still unanswered questions within a new and enigmatic defensive behavior in genus Echinanthera. Arthur Diesel ABEGG1,*, Acknowledgments. We thank Diego Cavalheri for the field work as- Raissa Marina Silva SIQUEIRA2, sistance, and to Daniella Pereira Fagundes de França and Hussam El Flora Roncolatto ORTIZ1 Dine Zaher for kindly allowing access and photographing the and Omar Machado ENTIAUSPE-NETO3 specimen under their care in the Museu de Zoologia da Universi- dade de São Paulo (MZUSP) collection. 1. Instituto Butantan, Laboratório Especial de Coleções Zoológicas, Avenida Vital Brasil, 1.500, Butantã, CEP 05503-900 São Paulo, SP, Brazil. References 2. Laboratório de Herpetologia, Museu de Zoologia da Universidade de São Arnold, E.N. (1984): Evolutionary aspects of tail shedding in lizards and their Paulo - Avenida Nazaré, 481, Ipiranga, CEP 04263-000, São Paulo, SP, Brazil. relatives. Journal of Natural History. 18(1): 127–169. 3. Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Bateman, P.W., Fleming, P.A. (2009): To cut a long tail short: A review of lizard Laboratório de Vertebrados. Av. Itália km 8, caudal autotomy studies carried out over the last 20 years. Journal of CEP 96203-900, Rio Grande, RS, Brazil. Zoology 277(1): 1–14. *Corresponding author, A.D., Abegg, E-mail: [email protected] Cooper, W.E., Alfieri, K.J. (1993): Caudal autotomy in the eastern garter snake,
Thamnophis s. sirtalis. Amphibia.-Reptilia 14(1): 86–89. Costa, H.C., Moura, M.R., Feio, R.N. (2014): A tale of lost tails: Pseudoautotomy in the Neotropical snake genus Drymoluber (Serpentes: Colubridae). Canadian Journal of Zoology 92(9): 811–816. Crnobrnja-Isailović, J., Ćorović, J., Halpern, B. (2016): Deliberate tail loss in Contribution to the individual marking Dolichophis caspius and Natrix tessellata (Serpentes: Colubridae) with a brief techniques for small lizards: heat branding review of pseudoautotomy in contemporary snake families. North–Western Journal of Zoology 12(2): 367–72. on Ablepharus kitaibelii (Bibron & Bory de Di-Bernardo, M. (1992): Revalidation of the genus Echinanthera Cope, 1894, and Saint-Vincent, 1833) its conceptual amplification (Serpentes, Colubridae). Comunicações do Museu de Ciências da PUCRS. Série Zoologia 5(13): 225–256. Dourado, Â.C.M., Oliveira, L., Prudente, A.L.C. (2013): Pseudoautotomy in When studying the population characteristics of diminutive Dendrophidion dendrophis and Mastigodryas bifossatus (Serpentes: Colubridae): lizards with secretive lifestyle, researchers will inevitably be Tail Morphology and Breakage Frequency. Copeia 2013(1): 132–141. Etheridge, R. (1967): Lizard caudal vertebrae. Copeia 1967(4): 699–721. faced with the problem of individual recognition. The Snake- Figueroa, A., McKelvy, A.D., Grismer, L.L., Bell, C.D., Lailvaux. S.P. (2016): A eyed skink Ablepharus kitaibelii, distributed from Southern species-level phylogeny of extant snakes with description of a new colubrid Slovakia to Anatolia (see Vergilov et al. 2016), is one of the subfamily and genus. PloS One 11(9): e0161070. Gomes, C.A., Marques, O.A.V. (2012): Food habits, reproductive biology, and few scincid species in Europe, being the smallest lizard on seasonal activity of the Dipsadid snake, Echinanthera undulata (Wied, 1824), the continent, and is the best example for this issue. Its ecol- from the Atlantic forest in Southeastern Brazil. South American Journal of ogy and biology have received little attention and remain Herpetology 7(3): 233–240. Hoogmoed, M.S., Ávila-Pires, T.C.S. (2011): A case of voluntary tail autotomy poorly studied (Pasuljević 1965, 1966, 1975, 1976, Herczeg et in the snake Dendrophidion dendrophis (Schlegel, 1837) (Reptilia: Squamata: al. 2007). Heat/freeze branding has been used for marking Colubridae). Boletim do Museu Paraense Emílio Goeldi 6(2): 113–117. different reptiles (e.g. snakes Clark 1971, Lewke & Stroud Jagnandan, K., Russell, A.P., Higham, T.E. (2014): Tail autotomy and 1974, Winne et al. 2006 or turtles Woodbury & Hardy 1948, subsequent regeneration alter the mechanics of locomotion in lizards. The Journal of Experimental Biology 217: 3891–3897. Clark 1971). Stumpel (1985) implemented branding with a Marco, A. (2002): Coluber hippocrepis (Horseshoe Whip Snake): caudal autotomy. cordless soldering iron with a micro tip when studying an Herpetological Review 33(3): 210. Anguis fragilis population. He placed tiny point-shaped Marques, O.A.V., Sazima, I. (2004): História Natural dos Répteis da Estação Ecológica Juréia-Itatins. pp. 257-277. In: Marques, O.A.V., Duleba, W. (Org.). marks on the ventral scales and mentioned that even though Estação Ecológica Juréia-Itatins: Ambiente Físico, Flora e Fauna – Holos, their conspicuity decreased strongly over time they re- Ribeirão Preto. mained observable throughout the six-month study period. Martins, M. (1994): História Natural e Ecologia de uma Taxocenose de Serpentes de Mata na Região de Manaus, Amazônia Central, Brasil. Similar approach was performed by Ferreiro & Galán (2004) (Doctoral thesis). Universidade Estadual de Campinas, Campinas. for the same species, using an ophthalmic cautery but point Padilla-Pérez, D.J., Murillo-Monsalve, J.D., Rincon-Barón, E.J., Daza, J.M. burns were made on the dorsal scales and in addition to (2015): Non-specialized caudal pseudoautotomy in the Emerald Racer snake Drymobius rhombifer (Günther, 1860). Herpetology Notes 8: 567–569. adults the neonates were also marked. Marking ventral