Zoologica Scripta Deep cox1 divergence and hyperdiversity of Trigonopterus weevils in a New Guinea mountain range (Coleoptera, Curculionidae) ALEXANDER RIEDEL,DAAWIA DAAWIA &MICHAEL BALKE Submitted: 31 March 2009 Riedel, A., Daawia, D. & Balke, M. (2010). Deep cox1 divergence and hyperdiversity Accepted: 8 July 2009 of Trigonopterus weevils in a New Guinea mountain range (Coleoptera, Curculionidae).— doi:10.1111/j.1463-6409.2009.00404.x Zoologica Scripta, 39, 63–74. Trigonopterus is a little-known genus of flightless tropical weevils. A survey in one locality, the Cyclops Mountains of West New Guinea, yielded 51 species, at least 48 of them unde- scribed. In this study, we show that mtDNA sequencing, or DNA barcoding, is an effective and useful tool for rapid discovery and identification of these species, most of them mor- phologically very difficult to distinguish even for expert taxonomists. The genus is hyperdi- verse in New Guinea and different species occur on foliage and in the litter layer. Morphological characters for its diagnosis are provided. Despite their external similarity, the genetic divergence between the species is high (smallest interspecific divergence 16%, mean 20%). We show that Trigonopterus are locally hyperdiverse and genetically very strongly structured. Their potential for rapid local biodiversity assessment surveys in Mela- nesia is outlined (a-diversity); providing a regional perspective on Trigonopterus diversity and biogeography is the next challenge (b-diversity). Corresponding author: Alexander Riedel, Staatliches Museum fu¨r Naturkunde, Erbprinzenstr 13, D-76133 Karlsruhe, Germany. E-mail: [email protected] Daawia Daawia, Jurusan Biology, FMIPA-Universitas Cendrawasih, Kampus Waena-Jayapura, Papua, Indonesia. E-mail: [email protected] Michael Balke, Zoologische Staatssammlung, Mu¨nchhausenstr. 21, D-81247 Mu¨nchen, Germany. E-mail: [email protected] Introduction many of the species are still undescribed and it is almost Beetles form a major part of global biodiversity and with impossible to identify the described ones without compari- 62 000 described species and possibly more than 150 000 son with the historic type material. A commonly applied undescribed ones, the weevils (Curculionoidea) are the remedy in all sorts of biodiversity studies is sorting to dominating group among them (Oberprieler et al. 2007). morphospecies by parataxonomists. This approach has its Weevils are especially diverse in tropical forests. Although merits, but the results depend strongly on the experience they constitute a high proportion of terrestrial biodiver- of the parataxonomist, regardless of the academic level or sity, they are largely ignored during surveys and decision cultural background. Not surprising, sorting to morpho- making in conservation programmes. For example, during species (and the authors include themselves here when it a Rapid Biodiversity Assessment (RAP) of Conservation comes to taxa they are not particularly familiar with) has International in the Cyclops mountains of West New Gui- be shown to suffer often from high error rates (Krell nea, only four entomologists (covering butterflies and 2004). aquatic insects) out of 30 scientists participated, whereas DNA sequencing has recently been promoted as a tool the remainder studied vertebrates or plants (Richards & to help overcome this impediment, DNA barcoding being Suryadi 2002). One of the reasons behind this imbalance currently the most popular approach (Hebert et al. 2003; is certainly the ‘taxonomic impediment’ (Hoagland 1996): Schindel & Miller 2005; Stoeckle & Hebert 2008). How- the lack of taxonomic expertise for many of the megadi- ever, surprisingly few studies have to date sought to use verse taxa such as weevils (Wheeler et al. 2004). In fact, DNA sequence data, or barcode data, for rapid biodiversity ª 2009 The Authors. Journal compilation ª 2009 The Norwegian Academy of Science and Letters d Zoologica Scripta, 39, 1, January 2010, pp 63–74 63 Hyperdiversity of Trigonopterus weevils d A. Riedel et al. assessment. Initial studies by Smith et al. (2005) (Madaga- examined for safe identification. However, not a single scan ants) and Borisenko et al. (2008) (Surinamese small illustration of these structures has ever been published. mammals) found good congruence between morphological Preparation of specimens, especially extraction of their identification and barcode clusters. Among the ants, some- genitalia, is difficult and time-consuming. The fusion of times more conservative morphospecies than molecular body sutures and the extensive defense adaptations make a ‘species’ delineation (i.e. genetically diverse morphospecies fast dissection, comparable with that of other beetles, with up to 16% cox1 p-distance), and higher b-diversity impossible even for an expert. Thus, the routine identifica- from molecular taxonomic units vs. morphospecies were tion of a large number of specimens on the basis of mor- found. This means that different localities have very simi- phological characters alone is impossible for Trigonopterus. lar looking species which parataxonomists tend to lump together into the same morphospecies, a well-documented The area problem with morphospecies sorting, cf. Krell (2004). The Cyclops Mountains are one of the most clearly While sequence data can thus assist in the rapid delivery defined and isolated New Guinea mountain ranges, situ- of biodiversity assessment of relevant data, it has also been ated on the North coast of Indonesian Papua (formerly shown that incomplete lineage sorting and organelle cap- Irian Jaya), close to the border with Papua New Guinea ture might lead to erroneous results (e.g. Monaghan et al. (Fig. 1). They extend over 45 km from Tanahmerah Bay 2006). Consequently, taxa require individual evaluation. In in the West, to Jayapura, the capital of Papua, in the East. this study, we explore the potential of DNA sequencing or To the South, they are bordered by Lake Sentani; to the barcoding for rapid surveys of a very diverse but neglected North, they drop to the Pacific Ocean. The highest peak, group of phytophagous beetles in Melanesia. Mt. Rafeni, is 1880 m high (van Royen 1965; Polhemus & Richards 2002). The taxon The Cyclops Mountains represent a former island that Trigonopterus Fauvel is a genus of flightless, apterous wee- was accreted to northern New Guinea in the Tertiary. vils placed in the Cryptorhynchinae of Curculionidae There are uncertainties about the precise timing of events, (Morimoto 1978; Alonso-Zarazaga & Lyal 1999), distrib- but the formation of the island arc may have begun in the uted from Eastern Sumatra to Samoa and from New Cale- Eocene, while the collision occurred between Miocene and donia to the Philippines. The centre of its diversity Pliocene (Monnier et al. 1999). Probably, the same island appears to be in New Guinea. Trigonopterus inhabit tropi- arc also included all or some of the following terranes: Ar- cal forests, both on foliage and in the litter layer. In New fak, Biak, Japen, Van Rees, Foja, Torricelli, Prince Alexan- Guinea, the foliage-frequenting species are a prominent der, Adelbert, Finisterre and Saruwaged (Polhemus 2007). element of the local arthropod fauna. Sometimes more The vegetation of the Cyclops Mountains was studied than 50% of the phytophagous beetles collected by beat- in detail by van Royen (1965). Forest types change quite ing forest undergrowth are Trigonopterus. They possess a markedly with elevation and range from tropical lowland pectoral receptacle into which the rostrum and the anten- forest to montane forest dominated by Araucaria and Not- nae can fit when the weevil is alarmed. Trigonopterus wee- hofagus in the upper elevations. Such montane habitats are vils attain a typical defense position, thanatosis, by folding well-isolated from others in the region. The nearest area the legs over the ventral side of the body. Also, the elytra would be the Bewani Mountains in the East (c. 100 km), are fused with each other and with the thorax, thus form- the Central Range in the South (c. 130 km) and the Foja ing a solid capsule. In combination with an extraordinary Mountains in the West (c. 150 km). These montane habi- well-sclerotized cuticle, the body of these weevils can tats are likely to harbour a variety of endemic plant and withstand considerable pressure. animal species. Sir David’s Long-beaked Echidna (Zaglos- Trigonopterus weevils are excellent indicator organisms sus attenboroughi) is so far known to inhabit the upper ele- for biodiversity monitoring in Melanesia, being present vations of the Cyclops Mountains only. It was described as and easily collected in the majority of natural habitats. recently as 1998 by Flannery and Groves. There are no Their a-diversity is high and our unpublished data also endemic bird or butterfly species recorded, which can be suggest very high b-diversity. Trigonopterus’s ability to dis- accounted for by their high mobility. A look at other, less perse over degraded habitat is presumably very limited mobile species would be rewarding to identify endemism because of their flightlessness and small size. Yet, Trigon- on species level. opterus remained poorly known. The majority of the 90 Apart from its rich biodiversity, its importance as a named species were described before 1930 (Pascoe 1885; water catchment area for nearby Sentani and the provincial Faust 1898; Heller, 1916). The species are usually very capital Jayapura is one of the reasons why the area is offi- similar to each other externally,