A case of viviparity in a tropical non-parasitizing earwig (Dermaptera Spongiphoridae)

Tropical Zoology 22: 237-241, 2009 A case of viviparity in a tropical non-parasitizing earwig (Dermaptera Spongiphoridae) Petr Kočárek Department of Biology and Ecology, University of Ostrava, CZ-710 00 Ostrava, Czech Republic (E-mail: petr.kocarek@osu.cz) Received 25 March 2009, accepted 30 June 2009 Hitherto studied species of non-parasitizing earwigs are oviparous and ovoviviparity has been found in only one species, Marava arachidis (Yersin 1860). Earwigs lay eggs and then exhibit maternal brood care. During the study of Dermaptera material collected in Papua New Guinea a female of Chaetospania borneensis (Dubrony 1879) (Spongiphoridae Sparattinae) was found with developing embryos in its abdomen, which documents its viviparity. The abdomen contained six embryos in different stages of development, and the most distal embryo was the fully developed nymph without any membraneous chorion. Specialised organs, such as vesicula cephalica and pseudoplacenta known in Arixeniidae and Hemimeridae, were not observed. key words: viviparity, ovoviviparity, reproduction, Chaetospania, Spongiphoridae, Dermaptera. INTRODUCTION The Dermaptera include about 2000 described species, but the life history, reproductive biology, and nymphal development are known for only a few species (see Haas 2003, Matzke & Klass 2005). Two highly specialized families Hemimeridae and Arixeniidae, with ca 20 species epizoicly parasitizing bats (Rentz & Kevan 1991) or giant rats (Rehn & Rehn 1935, Popham 1984), differ from the other families in their viviparity. The non-parasitic species are known to lay eggs and then exhibit maternal brood care (Albouy & Caussanel 1990, Haas 2003), but the current knowledge of earwig life histories is limited to only a few species of the families Forficulidae, Chelisochidae, Labiduridae, Spongiphoridae, Anisolabididae and Pygidicranidae (Albouy & Caussanel 1990, Matzke & Klass 2005). Most general information about earwig biology is based on the two most studied species Forficula auricularia (Linnaeus 1758) (e.g. Chapman 1917, Behura 1956, Lamb 1976, Kočárek 1998, Kölliker 2007

238 P. Kočárek and many others) and Labidura riparia (Pallas 1773) (e.g. Tawfik et al. 1972; Shepard et al. 1973; Vancassel 1973, 1977; Radl & Linsenmair 1991 and others). Ovoviviparity has been found in only one species, Marava arachidis (Yersin 1860): the females deposit their eggs with developed embryos and the 1st instar nymphs emerge from the eggshells 10 to 20 min after deposition (Herter 1943, 1965; Patel & Habib 1978). During the study of Dermaptera material collected in Papua New Guinea, I found a female of Chaetospania borneensis (Dubrony 1879) with developing embryos in its abdomen which documents its viviparity. C. borneensis and M. arachidis are members of the family Spongiphoridae, which includes about 500 non-parasitizing species with only fragmentary knowledge of their biology (Steinmann 1990; Haas 2003, 2006; Matzke & Klass 2005). The details of this finding are the subject of this contribution. MATERIAL AND METHODS The study female of Chaetospania borneensis (Dubrony 1879) was collected by Malaise trap operated for 1 year in Halopa village, Madang prov. in Papua New Guinea (GPS 05 4 60 S 145 42 59 E). The Malaise trap was set in primary rain forest at 600 m a.s.l. for 1 year. The female was collected in November 2000 and stored in 70% ethyl alcohol. The specimen was dissected under an Olympus SZ51 stereomicroscope and the embryos and their position in the abdomen was studied in detail and documented by an Olympus Camedia C-3030 digital camera. The species was identified with the use of Steinmann s key (Steinmann 1990) and the taxonomic database by Haas (2006). The material is deposited in the author s private collection. RESULTS AND DISCUSSION The abdomen of the female of Chaetospania borneensis contained six embryos in different stages of development. The position of the embryos after the opening of the abdomen by cutting the abdominal sternites is documented by microphotographs (Figs 1-2). The walls of the gonoduct were probably destroyed during dissection of the abdominal sternites and thus were not observed. Each successive embryo situated more distally in the abdomen was more developed then the previous one. The first embryo was enveloped in coverings and no segmentation was visible. No membranous chorion was detected on the surface of the oldest embryo. The body of this embryo was ochreously pigmented with dark-brown setae and black eyes. When the egg tooth on the frons of the embryo is not observed, the nymphs are probably 1st instar nymphs and not pronymphs (Matzke & Klass 2005). The cuticle bearing the egg tooth is generally regarded as the latest embryonic cuticle (= cuticle of pronymph) (Matzke & Klass 2005). Similarly, Herter (1943, 1965) reported the presence of only 4 nymph instars, with the loss of the stage of pronymph in M. arachidis. Reduction of the pronymph stage is probably associated with Eudermaptera (Matzke &

Viviparity in a tropical non-parasitizing earwig 239 Klass 2005). The comparison of the developmental rate of the youngest and oldest embryo of C. borneensis is documented in Fig. 3. These observations document the viviparity of fully developed nymphs, not the typical ovoviviparity known in M. arachidis (Herter 1965, Patel & Habib 1978). However, according to some definitions (see Hagan 1951), this case also belongs to the ovoviviparity category, because in truly viviparous species the developing offspring obtains its food from the mother through a pseudoplacenta or other highly specialised organ. Females of M. arachidis lay eggs with fully developed embryos in one batch. The time between egg deposition and nymphal emergence lasts 9.35 min on average, with a maximum of 21.5 and a minimum of 4.3 min and the nymphal emergence from the eggs is facilitated by the mother eating the membraneous chorion (Patel & Habib 1978). Patel & Habib (1978) demonstrated by dissection that the development of the individual embryos in the female s reproductive system is at the same stage at the same time. This contrasts with the different rates of development in embryos of C. borneensis. Females of this species probably give birth to their offspring successively within a few days. The difference is also in the presence of egg coverings, as the eggs of M. arachidis are enveloped in an egg chorion during hatching. The observed situation also contrasts with the pseudoplacental viviparity known in Arixeniidae and Hemimeridae, no specialised organs, such as vesicula cephalica and pseudoplacenta, were observed (Hagan 1951). The embryos of Arixeniidae and Hemimeridae have always been found to be of the same size and the same stage of development in the female s abdomen (Rehn & Rehn 1935, Hagan 1951). In C. borneensis, there seems to be a different mechanism of viviparity than those described in these dermapteran groups. M. arachidis and C. borneensis are both members of the earwig family Spongophoridae; M. arachidis belongs to subfamily Spongiphorinae and C. borneensis to subfamily Sparattinae (Haas 2006). The present findings suggest a trend to viviparity as a reproductive strategy within this group, Figs 1-3. Abdominal dissection of the female of Chaetospania borneensis. Fig. 1, The most distal embryo visible after cutting the subgenital plate; Fig. 2, Position of the embryos after cutting the abdominal sternites (soft tissues have been partly removed); Fig. 3, Comparison of the stage of development of the youngest and the oldest embryo.

240 P. Kočárek although these two species are currently the only tropical representatives of the family Spongophoridae with at least partially known biology. Viviparity could be an adaptive strategy in tropical wet climates minimizing the higher risk of infestation by fungi. Females of other oviparous species care for the laid eggs by extensive licking with the mouthparts, which probably includes the application of secretions with germicide function (Shepard et al. 1973, Günther & Herter 1974). This study clearly documented the viviparity of the earwig Chaetospania borneensis, but subsequent detailed studies on more specimens and especially on living individuals are needed. ACKNOWLEDGEMENTS The Chaetospania borneensis material was obtained thanks to the support of the New Guinea Bintang Research Centre, funded mainly by the U.S. National Science Foundation (DEB-97-07928). I thank my colleague Lukáš Čížek (České Budějovice, Czech Republic) for the donation of material and cooperation, and two anonymous reviewers for their constructive suggestions. References Albouy V. & Caussanel C. 1990. Dermaptères ou Perce-oreilles. Faune de France 75. Paris: Federation Française des Sociétés de Sciéncés Naturelles, 245 pp. Behura B.K. 1956. The biology of the European earwig, Forficula auricularia Linn. The Annales of Zoology 1: 117-142. Chapman T.A. 1917. Notes on early stages and life history of earwig (Forficula auricularia L.). The Entomologist s Record and Journal of Variation 29: 25-29. Günther K. & Herter K. 1974. 11. Ordnung Dermaptera (Ohrwürmer), pp. 1-158. In: Helmcke J.G. et al., Edits. Handbuch der Zoologie 4 (2), 2/11. Berlin: De Gruyter. Haas F. 2003. 12. Ordnung Dermaptera, Ohrwürmer, pp. 173-180. In: Dathe H.H., Edit. Lehrbuch der Spezzielen Zoologie, Band I: Wirbellose Tiere, 5. Teil: Insecta. Heidelberg, Berlin: Spektrum Academischer Verlag. Haas F. 2006. Earwig Research Centre ERC. The site on earwig biology. Available at: http://www.earwigsonline.de/navigation.html (visited 15 November 2008). Hagan H.R. 1951. Embryology of the viviparous insects. New York: The Ronald Press Company, 472 pp. Herter K. 1943. Zur Fortpflanzungsbiologie eines Lebendgebärenden ohrwurmes (Prolabia arachidids Yersin). Zeitschrift für Morphologie und Ökologie der Tiere 40: 158-180. Herter K. 1965. Vergleichende Beobachtungen und Betrachtungen über die Fortpflanzungsbiologie der Ohrwürmer. Zeitschrift für Naturforschung 20: 365-375. Kočárek P. 1998. Life cycles and habitat associations of three earwig (Dermaptera) species in lowland forest and its surroundings. Biologia, Bratislava 53: 205 211. Kölliker M. 2007. Benefits and costs of earwig (Forficula auricularia) family life. Behavioral Ecology and Sociobiology 61: 1489-1497. Lamb J. 1976. Parental behavior in the Dermaptera with special reference to Forficula auricularia (Dermaptera, Forficulidae). Canadian Entomologist 108: 609-619.

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