2016. Journal of Arachnology 44:85-87 SHORT COMMUNICATION The South African scorpion Pseudotychas ochmceus (Hirst, 1911) (Scorpiones: Buthidae) can reproduce by parthenogenesis Michael Seiter', Frederic D. Schramm^ and Alexander BartheF: * Group of Arthropod Ecology and Behavior, Division of Plant Protection, Department of Crop Sciences, University of Natural Resources and Life Sciences, Peter Jordan Strasse 82, 1190 Vienna, Austria. E-Mail: [email protected]; “Wehrdaer Weg 38a, 35037 Marburg, Germany; ^Auerbacher StraBe 29, 8228 Rodewisch, Germany. Abstract. Of all scorpion species described to date, only a small fraction are known to reproduce without fertilization by a male, instead producing offspring by parthenogenesis. Here we show that isolated females of the buthid Pseudolychas ochraceus (Hirst, 1911) are capable of parthenogenetic reproduction and we provide data on the postembryonic growth of this species. Keywords: Arachnida, scorpions, asexual reproduction, postembryonic and embryonic development Sexual reproduction is the predominant reproductive strategy in and deposited in the Natural History Museum Vienna, Austria multicellular eukaryotes and as such the vast majority of animal spe¬ (NHMW 27605). Specimens were studied, measured, and photo¬ cies develop from a zygote produced by the fusion of a female and graphed with a stereomicroscope (Leica M205A) equipped with a Leica a male gamete (Williams 1975). Parthenogenesis, the development of DFC420 camera. Digital images were processed using Adobe Photo¬ offspring from unfertilized eggs, occurs in diverse invertebrate and ver¬ shop ® 8.0 to optimize contrast features of the micrographs. The speci¬ tebrate taxa, albeit at a low frequency (White 1978). With the excep¬ mens were identified using the key by Prendini (2004) and the original tion of mites in which various types of parthenogenetic reproduction first description by Hirst (1911). The sex was determined by the pres¬ are known to occur and parthenogenesis is prevalent in certain families ence or absence of enlarged first pectinal teeth, a dimorphic trait ob¬ (Oliver 1971; Sabelis 1985), asexual reproduction is quite rare in other servable in all postembryonic stages of this species (Fig. 1). arachnid orders (Bell 1982). Parthenogenesis is known to occur in sev¬ Our results derived from five wild-caught second instar females. eral species of spiders (Edwards et al. 2003), harvestmen (Tsurusaki They were reared in isolation in captivity. One of them reached matu¬ 1986), amblypygids (Armas 2000; Weygoldt 2005, 2007; Seiter & rity (FO) and gave birth to two female offspring (FI), which after Wolff 2014) and scorpions (review in Francke 2008; Lourengo 2008), reaching adulthood gave birth to all-female litters of 9 and 15 offspring and is strongly suspected to occur in some species of pseudoscorpions (F2), respectively. Three F2 specimens reached adulthood, and pro¬ (Dashdamirov & Golovatch 2005), schizomids (Nedved et al. 2011; duced three all-female litters of one, two and three offspring. One fe¬ Zawierucha et al. 2013) and palpigrades (Christian & Christophoryova male gave birth after 217 days following final ecdysis (n = 1). The 2013) based on the observation of all-female populations or a pro¬ first instar specimens molted an average of 12 days after birth and con¬ nounced scarcity of males. Although the majority of claims about par¬ secutive moltings took place after 95 days (instar III), 135 days (instar thenogenetic reproduction in scorpion species were proven by IV), 205 days (instar V) and 248 days (instar VI, adult) of postembry- experimental evidence, some are based on field observations or uneven onic growth (n = 2). sex distributions in samples of collected species alone (Francke 2008; In a critical review, Francke (2008) proposed that the parturition of LourenQO 2008). During a revision of the scorpion genus Pseudolychas a captive isolated female collected immature in the wild is the minimal Kraepelin, 1911, Prendini (2004) observed only five males in 115 pre¬ evidence required to conclude that a scorpion species is parthenogenet¬ served specimens of Pseudolychas ochraceus (Hirst, 1911) and sug¬ ic. Furthermore, Francke (2008) discusses previous claims of the oc¬ gested that this species might be capable of asexual reproduction. By currence of parthenogenesis in scorpion species and presents rearing captive-born female specimens under isolation until matura¬ arguments why establishment of parthenogenesis should not be based tion and observing that these gave birth to an all-female brood without on parturition of immature wild-caught specimens alone. Two key being inseminated, we show that females of P. ochraceus from a popu¬ arguments are a reported case of a post-parturition molt in Tityus Uru¬ lation located in the vicinity of Onderstepoort, Pretoria, Gauteng guay ensis Borelli, 1901 (Toscano-Gadea 2001) and the common occur¬ Province in South Africa are capable of parthenogenetic reproduction. rence of iteroparity (Polis & Sissom 1990), which could cast doubt on All specimens were collected near Onderstepoort, Pretoria, Gauteng the establishment of parthenogenesis by the parturition of specimens Province in South Africa and were found under stones, bark and leaf that were not entirely raised under conditions of isolation. Although litter in humid microhabitats. Captive-bom specimens were kept in iso¬ other post-parturition molts have never been observed in scorpions, lation as soon as they left their mother’s back after reaching the second further confirmation of such an event would have serious implications instar. Specimens were kept in plastic terraria of different sizes using on establishing parthenogenesis based on parturition of wild caught standard methods. The enclosures contained a 1 cm deep layer of specimens. Therefore, we follow the more stringent criteria proposed soil-sand mixture and pieces of bark for the specimens to hide among. by Francke (2008) to confirm the previously suspected parthenogenesis Food consisted of nymphs of Acheta domesticus (Linnaeus, 1758). All in P. ochraecus (Prendini 2004): raising captive born females to matu¬ specimens were reared under the same conditions (29 ± 1°C, 35 ± 5% rity in isolation and showing that these can reproduce without being relative humidity and 16:8 h L:D photoperiod) and fed in intervals of inseminated. Following these criteria, parthenogenesis was previously seven days. Dead specimens were stored in ethanol (70% solution) established for seven buthid and one hormurid scorpion species to 85 86 JOURNAL OF ARACHNOLOGY Figure 1.—Pseudolychas ochra- ceus specimen in captivity. A. Adult female with second instar offspring. B. Pectinal area with the elongated first pecten, charac¬ teristic of females. Photos by Jonas Wolff. which we now add P. ochraecus as the eighth buthid scorpion of which which would represent a case of geographic parthenogenesis as de¬ parthenogenetic reproduction was shown by parturition of a captive- scribed by Vandel (1928). born female raised in isolation (Tab. 1) We note that the description This explanation is further substantiated by the observation that of parthenogenesis in Tityus stigmurus (Thorell, 1876) by Ross (2010) parthenogenetic reproduction facilitates dispersal by human activi¬ leaves little room to question the ability of this species to reproduce ties, as only one specimen has to be introduced to a new habitat to parthenogentically, however, the females used in this study were only found a new population. Many spiders introduced to European isolated in a subadult state. greenhouses are parthenogenetic and populations of introduced schi- Based on our data, we cannot say whether the P. ochraecus speci¬ zomids and palpigrades apparently exclusively consist of females mens collected at Onderstepoort for our study belong to an all-female (Nedved et al. 2011; Christian & Christophoryova 2013; Zawierucha population reproducing exclusively by parthenogenesis. However, Pre- et al. 2013). A well-known example for the potential of fast and ef¬ ndini (2004) points out that most of the preserved specimens available fective dispersal of a parthenogenetic scorpion is the South American in museum collections (of which ~96 % are female) were collected in buthid species Tityus serndatus (Lutz & Mello, 1922), which original¬ suburban habitats of the major South African cities of the Gauteng ly occurred only in a restricted region of the Brazilian state Minas conurbation where this species is abundant. In the regions outside of Gerais but nowadays has widely spread to cities throughout the the cities less influenced by human activities this species is more rarely country (Lourenqo & Cloudsley-Thompson 1996). Therefore, facili¬ found and in some cases was never recorded. This could indicate that tated dispersal of parthenogenetic reproducing populations is an at¬ sexually reproducing populations of P. ochraceus, in which females tractive explanation of why only females of P. ochraceus were could be facultatively parthenogenetic, predominantly occur in sparse¬ collected in cities situated in regions where this species does not oc¬ ly sampled non-urban habitats, whereas asexual all-female populations cur naturally. It would be interesting to test whether females from are present in suburban habitats; a population distribution pattern presumably all-female populations can reproduce with males from sexual populations to learn whether parthenogenesis in these popula¬ Table 1.—Scorpion species in which the capability to reproduce by tions is obligate or facultative. parthenogenesis was established by fulfillment of the criterion that a ACKNOWLEDGMENTS captive-bom female raised to adulthood in isolation gives birth. Within Buthidae, species are given in chronological order by record We want to thank Michiel Cozijn (The Netherlands) for reviewing year. the manuscript and for fruitful discussion on this topic. Furthermore, we are grateful to Jonas Wolff (University of Kiel, Germany) for tak¬ Species Record of parthenogenesis ing the photographs and to the anonymous reviewers for their detailed Hormuridae Laurie, 1896 peer review. Liocheles australasiae Yamazaki & Makioka (Fabricius, 1775) (2004) LITERATURE CITED Buthidae (Koch, 1837) Amias, L.F. de. 2000. Parthenogenesis in Amblypygi (Arachnida). Tityus serndatus Lutz & Matthiesen (1962) Avicennia 12/13; 133-134. Mello, 1922 Bell, G. 1982. The Masterpiece of Nature; the Evolution and Genetics Tityus uruguayensis Borelli, 1901 Zolessi (1985) of Sexuality. University of California Press, Berkeley. Tityus trivittatus Kraepelin, 1898 Toscano-Gadea (2004) Christian, E. & J. Christophoryova. 2013. Eukoenia florenciae (Ara¬ Hottentotta hottentotta Lourenpo & Ythier (2007) chnida: Palpigradi): Lessons from a newcomer to Central Europe (Fabricius) and the island of Tenerife. Biologia 68:1182-1188. Hottentotta cahoverdensis LourenQO, Ythier & Dashdamirov, S. & S.I. Golovatch. 2005. Miscellanea chernetologica Lourengo & Ythier, 2006 Cloudsley-Thompson (2007) (Arachnida: Pseudoscorpiones), based on the collection of the Nat¬ Tityus neblina Lourengo, 2008 Lourengo & Cloudsley- ural History Museum in Vienna, Part 1. Arthropoda Selecta Thompson (2010) 14:299-301. Tityus conjluens Borelli, 1899 Seiter (2012) Edwards, R.L., E.H. Edwards & A.D. Edwards. 2003. Observations of Pseudolychas ochraceus This study Theotima mimitissimus (Araneae, Ochyroceratidae), a parthenoge¬ (Hirst, 1911) netic spider. Journal of Arachnology 31:274-277. SEITER ET AL.—A NEW CASE OF ASEXUAL REPRODUCTION IN SCORPIONS 87 Francke, O.F. 2008. A critical review of reports of partheno¬ Seiter, M. 2012. Developmental stages and reproductive biology in genesis in scorpions (Arachnida). Revista Iberica de Aracnologia Tityus confluens Borelli, 1899 and Tityus ocelote (Francke & 16:93-104. Stockwell, 1987) (Scorpiones, Buthidae). Revista Iberica de Ara¬ Hirst, S. 1911. Descriptions of new scorpions. Annals and Magazine of cnologia 21:113-118. Natural History 8:462-473. Seiter, M. & J. Wolff 2014. Description of Sarax buxtoni (Gravely, 1915) (Arachnida: Amblypygi: Charinidae) and a new case of par¬ Lourenfo, W.R. 2008. Parthenogenesis in scorpions: Some history - thenogenesis in Amblypygi from Singapore. Journal of Arachnol- new data. Journal of Venomous Animals and Toxins including ogy 42:233-239. Tropical Diseases 14:19-44. Toscano-Gadea, C.A. 2001. Is Tityus Uruguayensis Borelli, 1901 really Lourengo, W.R. & J.L. Cloudsley-Thompson. 1996. Effects of human parthenogenetic? Pp. 359-364. In Scorpions 2001. In Memoriam activities on the environment and the distribution of dangerous spe¬ Gary A.Polis. (V. Fet & P.A. Selden, eds.). Burnham Beeches, Bucks. cies of scorpions. Pp. 49-60. In Envenomings and their Treatments. Toscano-Gadea, C.A. 2004. Confirmation of parthenogenesis in (C. Bon, M. Goyffon, eds.). Editions Fondation M. Mer- Tityus trivittatus Kraepelin 1898 (Scorpiones, Buthidae). Journal ieux, Lyon. of Arachnology 32:866-869. Louren?o, W.R. & J.L. Cloudsley-Thompson. 2010. The life cycle of Tsurusaki, N. 1986. Parthenogenesis and geographic variation of sex Tityus (Atreus) neblina Lourengo, 2008 (Scorpiones, Buthidae) in ratio in two species of Leiobunum (Arachnida, Opiliones). Zoologi¬ ‘Cerro de la Neblina’, BrazilWenezuela. Boletin de la Sociedad cal Science 3:517-532. Entomologica Aragonesa 47:293-298. Vandel, A. 1928. La parthenogenese geographique: Contribution a Louren^o, W.R. & E. Ythier. 2007. Confirmation of reproduction by r etude biologique et cytologique de la parthenogenese naturelle. parthenogenesis in Hottentotta hottentotta (Fabricius) (Scorpiones, Bulletin de Biologie France Belgique 62:164-281. Buthidae). Acta Biologica Paranaense, Curitiba 36:213-217. Weygoldt, P. 2005. Biogeography, systematic position, and reproduc¬ LourenQO, W.R., E. Ythier & J.L. Cloudsley-Thompson. 2007. Parthe¬ tion of Charinus ioanniticus (Kritscher 1959), with the description nogenesis in Hottentotta caboverdensis Lourengo & Ythier, 2006 of a new species from Pakistan (Chelicerata, Amblypygi, Charini¬ (Scorpiones, Buthidae) from the Cape Verde islands. Boletin de la dae). Senckenbergiana Biologica 85:43-56. Sociedad Entomologica Aragonesa 41:193-196. Weygoldt, P. 2007. Parthenogenesis and reproduction in Charinus Matthiesen, F.A. 1962. Parthenogenesis in scorpions. Evolution ioanniticus (Kritscher, 1959) (Chelicerata, Amblypygi, Charinidae). 16:255-256. Bulletin of the British Arachnological Society 14:81-84. Nedved, O., S. Pekar, P. Bezdecka, E. Liznarova, M. Rezac, M. White, M.J.D. 1978. Modes of Speciation. W.H. Freeman, San Fran¬ Schmitt et al. 2011. Ecology of Arachnida alien to Europe. BioCon- cisco, California. trol 56:539-550. Williams, G.C.D. 1975. Sex and Evolution. Princeton University Press, Princeton, New Jersey. Oliver, J.H. Jr. 1971. Parthenogenesis in mites and ticks (Arachnida: Yamazaki, K. & T. Makioka. 2001. Ovarian structural features reflect¬ Acari). American Zoologist 11:283-299. ing repeated pregnancies and parturitions in a viviparous scorpion, Polis, G.A. & W.D. Sissom. 1990. Life history. Pp. 161-223. In The Bi¬ Liocheles australasiae. Zoological Science 18:277-282. ology of Scorpions. (G. A. Polis, ed.). Stanford University Press, Zawierucha, K., P. Szymkowiak, M. Dabert & M. Harvey. 2013. First Stanford, California. record of the schizomid Stenochrus portoricensis (Schizomida: Hub- Prendini, L. 2004. Systematics of the genus Pseudolychas Kraepelin bardiidae) in Poland, with DNA barcode data. Turkish Journal of (Scorpiones: Buthidae). Annals of the Entomological Society of Zoology 37:357-361. America 97:37-63. Zolessi, L.C. de. 1985. La partenogenesis en le escorpion amarillo Ross, L.K. 2010. Confirmation of parthenogenesis in the medically Tityus uruguayensis (BoxdW, 1990) (Scorpionida: Buthidae). Revista significant, synanthropic scorpion Tityus stigmurus (Thorell, 1876) de la Facultad de Humanidades y Ciencias. Tercera Epoca. Serv. (Scorpiones: Buthidae). Revista Iberica de Aracnologia 18:115-121. Ciencias Biologicas 1:25-32. Sabelis, M.W. 1985. Reproduction. Pp 73-81. In Spider Mites: Their Biology, Natural Enemies and Control. Volume IB. (W. Helle & M.W. Sabelis, eds.). Elsevier Science Publisher, Amsterdam. Manuscript received 16 September 2015, revised 6 January 2016.