Abstract
Species of the varunid genus Parahelice Sakai, Türkay & Yang, 2006, inhabit high intertidal areas of oceanic islands of the tropical Indo-West Pacific region. As several species of Parahelice and Pseudohelice subquadrata (Dana, 1851) were found to be sympatric in some places, and their morphological differences are minor, especially in females, the misidentification of species is not uncommon in the literature. In this study, the DNA barcoding marker, mitochondrial cytochrome c oxidase subunit I (COI), was applied to confirm species identities and this was correlated with the specific characters of males and females. Distributions of three species of Parahelice were also updated, with Par. daviei (Sakai, Türkay & Yang, 2006), Par. pilimana (A. Milne-Edwards, 1873), and Par. pilosa (Sakai, Türkay & Yang, 2006) being new records to Taiwan, and Par. pilosa new to Bali, Indonesia.
References
Chen, H.-N., Høeg, J.T. & Chan, B.K.K. (2013) Morphometric and molecular identification of individual barnacle cyprids from wild plankton: an approach to detecting fouling and invasive barnacle species. Biofouling, 29, 133–145.
https://doi.org/10.1080/08927014.2012.753061Chu, C., Loh, K.H., Ng, C.C., Ooi, A.L., Konishi, Y., Huang, S.-P. & Chong, V.C. (2019) Using DNA barcodes to aid the identification of larval fishes in tropical estuarine waters (Malacca Straits, Malaysia). Zoological Studies, 58, 30.
https://doi.org/10.6620/ZS.2019.58-30Chu, K.H., Schubart, C.D., Shih, H.-T. & Tsang, L.M. (2015) Genetic diversity and evolution of Brachyura. In: Castro, P., Davie, P.J.F., Guinot, D., Schram, F.R. & von Vaupel Klein, J.C. (Eds.), Treatise on Zoology—Anatomy, Taxonomy, Biology—The Crustacea, Complementary to the Volumes Translated from the French of the Traité de Zoologie. 9 (C) (II). Decapoda: Brachyura. Part 2. Brill, Leiden, pp. 775–820.
https://doi.org/10.1163/9789004190832_016
Crane, J. (1975) Fiddler Crabs of the World (Ocypodidae: Genus Uca). Princeton University Press, Princeton, New Jersey, xxiii + 736 pp.
Cumberlidge, N. & Daniels, S.R. (2014) Recognition of two new species of freshwater crabs from the Seychelles based on molecular evidence (Potamoidea: Potamonautidae). Invertebrate Systematics, 28, 17–31.
https://doi.org/10.1071/IS13017
Dai, A.-Y. (1999) Fauna Sinica. Arthropoda: Crustacea: Malacostraca: Decapoda: Parathelphusidae, Potamidae. Science Press, Beijing, 501 pp., 30 pls. [in Chinese]
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
Hamasaki, K., Iizuka, C., Sanda, T., Imai, H. & Kitada, S. (2017) Phylogeny and phylogeography of the land hermit crab Coenobita purpureus (Decapoda: Anomura: Coenobitidae) in the Northwestern Pacific Region. Marine Ecology, 38, e12369.
https://doi.org/10.1111/maec.12369
Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B, 270, 313–321.
https://doi.org/10.1098/rspb.2002.2218
Hebert, P.D.N., Ratnasingham, S. & deWaard, R.J. (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B, 270, S96–S99.
https://doi.org/10.1098/rsbl.2003.0025
Huang, C., Ahyong, S.T. & Shih, H.-T. (2017) Cantopotamon: a new genus of freshwater crabs from Guangdong, China, with descriptions of four new species (Crustacea: Decapoda: Brachyura: Potamidae). Zoological Studies, 56, 41.
https://doi.org/10.6620/ZS.2017.56-41
Japanese Association of Benthology (2012) Threatened Animals of Japanese Tidal Flats: Red Data Book of Seashore Benthos. Tokai University Press, Hatano, xvii + 285 pp. [in Japanese]
Jung, J., Jung, J. & Kim, W. (2018) Subdividing the common intertidal hermit crab Pagurus minutus Hess, 1865 (Decapoda: Anomura: Paguridae) based on molecular, morphological and coloration analyses. Zoological Studies, 57, 61.
https://doi.org/10.6620/ZS.2018.57-61
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
https://doi.org/10.1007/bf01731581
Komai, T., Goshima, S. & Murai, M. (1995) Crabs of the genus Macrophthalmus of Phuket, Thailand (Crustacea: Decapoda: Ocypodidae). Bulletin of Marine Science, 56, 103–149.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549.
https://doi.org/10.1093/molbev/msy096
Lai, J.C.Y., Shih, H.-T. & Ng, P.K.L. (2017) The systematics of land crabs of the genus Gecarcoidea H. Milne Edwards, 1837, and recognition of a pseudocryptic species, G. humei (Wood-Mason, 1874) from the eastern Indian Ocean (Crustacea: Decapoda: Gecarcinidae). Invertebrate Systematics, 31, 406–426.
https://doi.org/10.1071/IS16052
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.
https://doi.org/10.1093/molbev/msw260
Li, J.-J. & Chiu, Y.-W. (2013) Land Crabs of Hengchun Peninsula. National Museum of Marine Biology & Aquarium, Pingtung, 91 pp. [in Chinese]
Milne-Edwards, A. (1873) Recherches sur la faune carcinologique de la Nouvelle-Calédonie, II. Nouvelles Archives du Muséum d’Histoire Naturelle, 9, 155–332, pls. 4–18.
https://doi.org/10.5962/bhl.title.10410
Ng, N.K., Naruse, T. & Shih, H.-T. (2018) Helice epicure, a new species of varunid mud crab (Brachyura, Decapoda, Grapsoidea) from the Ryukyus, Japan. Zoological Studies, 57, 15.
https://doi.org/10.6620/ZS.2018.57-15
Ng, P.K.L. (1988) The Freshwater Crabs of Peninsular Malaysia and Singapore. Shing Lee, Singapore, 156 pp.
Ng, P.K.L., Guinot, D. & Davie, P.J.F. (2008) Systema Brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bulletin of Zoology, Supplement 17, 1–296.
Ng, P.K.L., Shih, H.-T., Ho, P.-H. & Wang, C.-H. (2017) An updated annotated checklist of brachyuran crabs from Taiwan (Crustacea: Decapoda). Journal of the National Taiwan Museum, 70, 1–208.
https://doi.org/10.6532/JNTM.201712_70(3;4).01
Ng, P.K.L., Wang, C.-H., Ho, P.-H. & Shih, H.-T. (2001) An annotated checklist of brachyuran crabs from Taiwan (Crustacea: Decapoda). National Taiwan Museum Special Publication Series, 11, 1–86.
Nishigaki, K., Saeki, T. & Naruse, T. (2011) New records of Parahelice daviei (Sakai, Türkay and Yang, 2006) and Parahelice pilimana (A. Milne-Edwards, 1873) (Crustacea: Decapoda: Brachyura: Varunidae) from Ishigakijima Island, Ryukyu Archipelago, Japan. Biological Magazine of Okinawa, 49, 85–93. [in Japanese]
Radulovici, A.E., Archambault, P. & Dufresne, F. (2010) DNA barcodes for marine biodiversity: moving fast forward? Diversity, 2, 450–472.
https://doi.org/10.3390/d2040450
Ronquist, F., Huelsenbeck, J.P. & van der Mark, P. (2005) MrBayes. Version 3.1. Manual. Available from: http://mrbayes.csit.fsu.edu/manual.php (accessed 09 August 201)
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MRBAYES 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
https://doi.org/10.1093/sysbio/sys029
Sakai, K., Türkay, M. & Yang, S.-L. (2006) Revision of the Helice/Chasmagnathus complex (Crustacea: Decapoda: Brachyura). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 565, 1–76.
Schubart, C.D., Cannicci, S., Vannini, M. & Fratini, S. (2006) Molecular phylogeny of grapsoid crabs (Decapoda, Brachyura) and allies based on two mitochondrial genes and a proposal for refraining from current superfamily classification. Journal of Zoological Systematics and Evolutionary Research, 44, 193–199.
https://doi.org/10.1111/j.1439-0469.2006.00354.x
Serène, R. (1968) The Brachyura of the Indo-West Pacific region. In: Serène, R. (Ed.), Prodromus for a Check List of the Non-planctonic Marine Fauna of South East Asia. UNESCO, Singapore National Academy of Science Special Publication No. 1. Fauna III CC3. UNESCO, Singapore National Academy of Science, Singapore pp. 33–112.
Shih, H.-T. (2007) Natural history of the helicid crabs (Crustacea: Varunidae). Wetlands Taiwan, 64, 6–27. [in Chinese]
Shih, H.-T. (2012) Warrior—The Seashore Crabs of Dongsha Island. Marine National Park, Kaohsiung, 159 pp. [in Chinese]
Shih, H.-T., Cai, Y. & Chiu, Y.-W. (2019a) Neocaridina fonticulata, a new land-locked freshwater shrimp (Decapoda: Caridea: Atyidae) from Hengchun Peninsula, Taiwan. ZooKeys, 817, 11–23.
https://doi.org/10.3897/zookeys.817.29332
Shih, H.-T., Cai, Y., Niwa, N. & Nakahara, Y. (2017) A new species of land-locked freshwater shrimp of the genus Neocaridina (Decapoda: Caridea: Atyidae) from Iki Island, Kyushu, Japan. Zoological Studies, 56, 30.
https://doi.org/10.6620/ZS.2017.56-30
Shih, H.-T., Chan, B.K.K. & Ng, P.K.L. (2018) Tubuca alcocki, a new pseudocryptic species of fiddler crab from the Indian Ocean, sister to the southeastern African T. urvillei (H. Milne Edwards, 1852) (Crustacea, Decapoda, Brachyura, Ocypodidae). ZooKeys, 747, 41–62.
https://doi.org/10.3897/zookeys.747.23468
Shih, H.-T., Chan, B.K.K., Teng, S.-J. & Wong, K.J.H. (2015) Crustacean Fauna of Taiwan: Brachyuran Crabs. Vol. II—Ocypodoidea. National Chung Hsing University, Taichung, 320 pp.
Shih, H.-T., Hsu, P.-Y., Shahdadi, A., Schubart, C.D. & Li, J.-J. (2019b) The synonymy of the supratidal crabs Parasesarma cognatum Rahayu & Li, 2013 with P. liho Koller, Liu & Schubart, 2010 (Decapoda: Brachyura: Sesarmidae), based on morphological and molecular evidence, with a note on P. paucitorum Rahayu & Ng, 2009. Zoological Studies, 58. [in press]
Shih, H.-T., Ng, P.K.L., Ravichandran, S. & Prema, M. (2019c) Resurrection of Gelasimus variegatus Heller, 1862, a fiddler crab closely related to Austruca bengali (Crane, 1975) and A. triangularis (A. Milne-Edwards, 1873) (Decapoda, Brachyura, Ocypodidae), from the Bay of Bengal, Indian Ocean. Zoological Studies, 58, 12.
https://doi.org/10.6620/ZS.2019.58-12
Shih, H.-T., Huang, C. & Ng, P.K.L. (2016a) A re-appraisal of the widely-distributed freshwater crab genus Sinopotamon Bott, 1967, from China, with establishment of a new genus (Crustacea: Decapoda: Potamidae). Zootaxa, 4138 (2), 309–331.
https://doi.org/10.11646/zootaxa.4138.2.5
Shih, H.-T., Ng, P.K.L., Davie, P.J.F., Schubart, C.D., Türkay, M., Naderloo, R., Jones, D.S. & Liu, M.-Y. (2016b) Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. Raffles Bulletin of Zoology, 64, 139–175.
Shih, H.-T. & Suzuki, H. (2008) Taxonomy, phylogeny, and biogeography of the endemic mudflat crab Helice/Chasmagnathus complex (Crustacea: Brachyura: Varunidae) from East Asia. Zoological Studies, 47, 114–125.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
https://doi.org/10.1093/bioinformatics/btl446
Theuerkauff, D., Rivera-Ingraham, G.A., Roques, J.A.C., Azzopardi, L., Bertini, M., Lejeune, M., Farcy, E., Lignot, J.-H. & Sucré, E. (2018) Salinity variation in a mangrove ecosystem: A physiological investigation to assess potential consequences of salinity disturbances on mangrove crabs. Zoological Studies, 57, 36.
https://doi.org/10.6620/ZS.2018.57-36
Thurman, C.L., Hopkins, M.J., Brase, A.L. & Shih, H.-T. (2018) The unusual case of the widely distributed fiddler crab Minuca rapax (Smith, 1870) from the western Atlantic: an exemplary polytypic species. Invertebrate Systematics, 32, 1465–1490.
https://doi.org/10.1071/IS18029
Xu, J., Sun, H. & Sun, S. (2011) Molecular phylogeny of the crab genera Helice and Helicana (Crustacea, Decapoda) based on the partial sequences of mitochondrial 16S rRNA gene. Acta Oceanologica Sinica, 33 (5), 124–132. [in Chinese]
Xu, J., Yang, F. & Sun, S. (2010) Morphometrical studies on 10 populations of Helice tientsinensis and Helice latimera (Crustacea, Decapoda) from coasts of China. Acta Hydrobiologica Sinica, 34, 533–540. [in Chinese]
https://doi.org/10.3724/SP.J.1035.2010.00533
Wong, J.Y., Chen, H.-N., Chan, B.K.K., Tan, I.K.P. & Chong, V.C. (2014) A combined morphological and molecular approach in identifying barnacle cyprids from the Matang Mangrove Forest Reserve in Malaysia: essentials for larval ecology studies. Raffles Bulletin of Zoology, 62, 317–329.