Received: 20 January 2021 | Revised: 6 April 2021 | Accepted: 13 April 2021 DOI: 10.1111/1755-0998.13411 RESOURCE ARTICLE Exploring the vertebrate fauna of the Bird’s Head Peninsula (Indonesia, West Papua) through DNA barcodes Evy Arida1 | Hidayat Ashari1 | Hadi Dahruddin1 | Yuli Sulistya Fitriana1 | Amir Hamidy1 | Mohammad Irham1 | Kadarusman2 | Awal Riyanto1 | Sigit Wiantoro1 | Moch Syamsul Arifin Zein1 | Renny K. Hadiaty1* | Apandi1 | Frengky Krey3 | Kurnianingsih1 | Edy H.P. Melmambessy4 | Mulyadi1 | Henderite L. Ohee5 | Saidin2 | Ayub Salamuk6 | Sopian Sauri1 | Suparno1 | Nanang Supriatna1 | Amir M. Suruwaky2 | Wahyudi Tri Laksono1 | Evie L. Warikar5 | Hadi Wikanta1 | Aksamina M. Yohanita7 | Jacques Slembrouck8 | Marc Legendre8 | Philippe Gaucher9 | Christophe Cochet8 | Erwan Delrieu- Trottin8 | Christophe Thébaud10 | Borja Mila11 | Antoine Fouquet10 | Alex Borisenko12 | Dirk Steinke12 | Régis Hocdé13 | Gono Semiadi1 | Laurent Pouyaud8 | Nicolas Hubert8 1Division of Zoology, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Cibinong, Indonesia 2Politeknik Kelautan dan Perikanan Sorong, Jl. Kapitan Pattimura, Suprau, Indonesia 3Jurusan Perikanan, Fakultas Perikanan dan Ilmu Kelautan, Universitas Papua, Jl. Gunung Salju Amban, Manokwari, Indonesia 4Program Studi Manajemen Sumberdaya Perairan, Fakultas Pertanian, Universitas Musamus, Jl. Kamizaun Mopah Lama, Rimba Jaya, Merauke, Indonesia 5Jurusan Biologi, Fakultas MIPA, Universitas Cendrawasih, Jl. Kamp Wolker Waena Jayapura, Jayapura, Indonesia 6Dinas Kelautan dan Perikanan Kabupaten Kaimana, Jl.Utarum Kampung Coa, Kaimana, Indonesia 7Jurusan Biologi, Fakultas MIPA, Universitas Papua Jl. Gunung Salju - Amban, Manokwari, Indonesia 8UMR 5554 ISEM (IRD, UM, CNRS, EPHE), Université de Montpellier, Montpellier, France 9USR LEEISA- Laboratoire Ecologie, Evolution, Interactions des Systèmes amazoniens, Centre de Recherche de Montabo, cayenne, French Guiana 10UMR 5174 EDB CNRS, Université Paul Sabatier, IRD, Toulouse, France 11Department of Biodiversity and Evolutionary Biology, National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain 12Department of Integrative Biology, Centre for Biodiversity Genomics, University of Guelph, Guelph, ON, Canada 13UMR 9190 MARBEC (IRD, UM, CNRS, IFREMER), Université de Montpellier, Montpellier, France Correspondence Nicolas Hubert, UMR5554- ISEM, Abstract Université de Montpellier, Place Eugène Biodiversity knowledge is widely heterogeneous across the Earth's biomes. Some Bataillon, 34095 Montpellier cedex 05, France. areas, due to their remoteness and difficult access, present large taxonomic knowl- Email: [email protected] edge gaps. Mostly located in the tropics, these areas have frequently experienced a Funding information fast development of anthropogenic activities during the last decades and are there- Fondation Veolia Environnement, Grant/ fore of high conservation concerns. The biodiversity hotspots of Southeast Asia Award Number: Internal; COLAS, Grant/ Award Number: Internal; Bolloré, Grant/ exemplify the stakes faced by tropical countries. While the hotspots of Sundaland Award Number: Internal; Total foundation, (Java, Sumatra, Borneo) and Wallacea (Sulawesi, Moluccas) have long attracted the Grant/Award Number: Internal Evy Arida, Hidayat Ashari, Hadi Dahruddin, Yuli Sulistya Fitriana, Amir Hamidy, Mohammad Irham, Kadarusman, Awal Riyanto, Sigit Wiantoro, Moch Syamsul Arifin Zein and Gono Semiadi Contributed equally to the study ‡Deceased Mol Ecol Resour. 2021;00:1–19. wileyonlinelibrary.com/journal/men © 2021 John Wiley & Sons Ltd | 1 2 | ARIDA ET AL. attention of biologists and conservationists alike, extensive parts of the Sahul area, in particular the island of New Guinea, have been much less explored biologically. Here, we describe the results of a DNA- based inventory of aquatic and terrestrial verte- brate communities, which was the objective of a multidisciplinary expedition to the Bird's Head Peninsula (West Papua, Indonesia) conducted between 17 October and 20 November 2014. This expedition resulted in the assembly of 1005 vertebrate DNA barcodes. Based on the use of multiple species- delimitation methods (GMYC, PTP, RESL, ABGD), 264 molecular operational taxonomic units (MOTUs) were delineated, among which 75 were unidentified and an additional 48 were considered cryptic. This study suggests that the diversity of vertebrates of the Bird's Head is severely under- estimated and considerations on the evolutionary origin and taxonomic knowledge of these biotas are discussed. KEYWORDS amphibians, birds, DNA barcoding, fish, mammals, reptiles 1 | INTRODUCTION endemism (Crayn et al., 2015; Rowe et al., 2008; Unmack et al., 2013). The extent of this endemism is presumed to be vastly underestimated, The Earth's biosphere has been unevenly explored with some geographic because recent DNA- based species inventories purported large num- regions relatively well surveyed and others lacking taxonomic baselines bers of undescribed taxa (Kadarusman et al., 2012; Riedel et al., 2013). and awaiting large- scale screening of their biotas. The resulting gaps in Unfortunately, the rapid acceleration of deforestation in New Guinea taxonomic knowledge impede conservation planning and management, during the last decades (Austin et al., 2019; Filer et al., 2009; Nelson a situation particularly evident in species- rich tropical areas experiencing et al., 2014; Shearman & Bryan, 2011), is putting many species and extensive infrastructure development (e.g., roads, dams and agriculture) their habitats at risk, calling for comprehensive inventories of fauna and deforestation over the past few decades. This is particularly dra- and flora to facilitate conservation planning. matic for highly endemic biotas of tropical insular systems that have be- In the last 15 years, DNA barcoding, the use of the mitochon- come increasingly accessible to human activity and biological invasions drial cytochrome oxidase I gene as an internal species tag (Hebert and, as a consequence, are mostly endangered (Hoffman et al., 2010; et al., 2003; Hebert et al., 2003), has been providing a major boost Myers et al., 2000; Schipper et al., 2008). Southeast Asia exemplifies the to documenting biodiversity. Initially designed to overcome limits of stakes associated with the conservation of species- rich biota in insular morphology- based species- level identification, it has increasingly tropical systems. Of the four main biogeographic provinces in this area, been accepted as a tool to capture species boundaries and as a foun- three (Sundaland, Wallacea, and the Philippines) have been recognized dation for automated molecular species identification and detection as biodiversity hotspots because they harbour an exceptional number (April et al., 2011; Blagoev et al., 2015; Delrieu- Trottin et al., 2019; of endemic species, and intense anthropogenic pressures threaten their deWaard et al., 2019; Kerr et al., 2007). The utility of DNA barcod- existence (Hoffman et al., 2010; Myers et al., 2000; Thiault et al., 2019). ing, however, always depends on the taxonomic coverage of the Both Sundaland (Java, Sumatra and Borneo) and Wallacea (Sulawesi, associated DNA barcode reference library which, in turn, requires Moluccas) have long captured the attention of biologists and served solid taxonomic knowledge of the biotas under scrutiny (Hubert & as early model systems in biogeographic studies (Mayr, 1944; Wallace, Hanner, 2015). Several studies have emphasized the benefits of inte- 1859). In particular, vertebrate assemblages in both regions have been grating a standardized DNA- based approach into the inventories of actively documented over the last two decades, resulting in the descrip- poorly known faunas (de Araujo et al., 2018; Dahruddin et al., 2017; tion of hundreds of new species (Hubert et al., 2015) and the assessment Milá et al., 2012; Monaghan et al., 2009; Riedel et al., 2013; Sholihah of associated phylogenetic and biogeographic patterns (de Bruyn et al., et al., 2020; Smith et al., 2005, 2008; Sonet et al., 2018; Tänzler et al., 2013; den Tex et al., 2010; Esselstyn et al., 2013; Hutama et al., 2017; 2012; Vacher et al., 2020). Newly developed DNA- based species de- Lim et al., 2017; O’Connell et al., 2018; Pinheiro et al., 2017; Rowe et al., limitation methods (Fujiwasa & Barraclough, 2013; Kekkonen et al., 2019; Wood et al., 2012). 2015; Monaghan et al., 2009; Puillandre et al., 2012; Ratnasingham In contrast, the northern part of Sahul, for example, the island of & Hebert, 2013; Zhang et al., 2013) further speeded up the pace New Guinea, has received comparatively little attention, as a result of species discovery by dramatically increasing the throughput and of limited accessibility. Delimited from Wallacea to the west by the lowering analytical costs (Butcher et al.,2012; Riedel et al., 2013). Lyddeker line, its component lineages show multiple affinities with the One of the more geologically intricate regions of the island of neighbouring Wallacea or Australia, while also displaying high levels of New Guinea is its northwest portion, known as the Bird's Head ARIDA ET AL. | 3 Peninsula, particularly the Lengguru karstic massif, in the West Western part of the Bird's Head Peninsula (Figure 1). Freshwater Papua province. This massif originated from the subduction of the fishes were sampled using electrofishing gear and cast nets. Bats and Australian and Pacific plates that resulted in the development of birds