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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Exploring high-mountain limnic faunas: discovery of a novel endemic bivalve species (Sphaeriidae : Pisidium) in the Nepal Himalayas

Ulrich Bößneck A B C , Catharina Clewing A and Christian Albrecht A
+ Author Affiliations
- Author Affiliations

A Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), D-35392 Giessen, Germany.

B Natural History Museum of Erfurt, Grosse Arche 14, D-99084 Erfurt, Germany.

C Corresponding author. Email: uboessneck@aol.com

Invertebrate Systematics 30(6) 588-597 https://doi.org/10.1071/IS15043
Submitted: 15 September 2015  Accepted: 25 April 2016   Published: 13 December 2016

Abstract

High-mountain regions are known to harbour considerable biodiversity, although it is not all well known. The terrestrial fauna of the world’s largest mountain range, the Himalayas, has been moderately well studied, but this is not the case with the limnic fauna, and especially molluscs. During intensive malacozoological field surveys conducted over the past 20 years, the bivalve family Sphaeriidae has been studied in Nepal along an elevational gradient from 100 to 4010 m above sea level (a.s.l.). Here we describe a new species of Sphaeriidae, Pisidium alexeii, sp. nov., based on comprehensive molecular phylogenetics, anatomy and shell morphology. The species can be clearly distinguished from all other sphaeriid species occurring in Nepal. A molecular phylogeny based on mitochondrial and nuclear data inferred the oriental biogeographical affinity of the new species. The species is ecologically restricted and only occurs at a few sites between 1010 and 1700 m a.s.l. A review and updated checklist of the sphaeriid fauna of Nepal is provided and biodiversity and biogeographical patterns are discussed.

Additional keywords: diversity, endemism, high altitude, molluscs, pea-clam.


References

Abell, R., Thieme, M. L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S. C., Bussing, W., Stiassny, M. L. J., Skelton, P., Allen, G. R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J. V., Heibel, T. J., Wikramanayake, E., Olson, D., Lopez, H. L., Reis, R. E., Lundberg, J. G., Perez, M. H. S., and Petry, P. (2008). Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58, 403–414.
Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation.Crossref | GoogleScholarGoogle Scholar |

Acharya, B. K., Chettri, B., and Vijayan, L. (2011). Distribution patterns of trees along an elevation gradient of Eastern Himalaya, India. Acta Oecologica 37, 329–336.
Distribution patterns of trees along an elevation gradient of Eastern Himalaya, India.Crossref | GoogleScholarGoogle Scholar |

Bharti, H., Sharma, Y. P., Bharti, M., and Pfeiffer, M. (2013). Ant species richness, endemicity and functional groups, along an elevational gradient in the Himalayas. Asian Myrmecology 5, 79–101.

Bhatt, D., and Joshi, K. K. (2011). Bird assemblages in natural and urbanized habitats along elevational gradients in Nainital district (western Himalaya) of Uttarakhand state, India. Current Zoology 57, 318–329.
Bird assemblages in natural and urbanized habitats along elevational gradients in Nainital district (western Himalaya) of Uttarakhand state, India.Crossref | GoogleScholarGoogle Scholar |

Bhatt, J. P., Manish, K., and Pandit, M. K. (2012). Elevational gradients in fish diversity in the Himalaya: water discharge is the key driver of distribution patterns. PLoS One 7, e46237.
Elevational gradients in fish diversity in the Himalaya: water discharge is the key driver of distribution patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2jtbfO&md5=fb12eb04b2ee418d5fc5eec6e496c397CAS |

Bhattarai, K. R., and Vetaas, O. R. (2003). Variation in plant species richness of different life forms along a subtropical elevation gradient in the Himalayas, east Nepal. Global Ecology and Biogeography 12, 327–340.
Variation in plant species richness of different life forms along a subtropical elevation gradient in the Himalayas, east Nepal.Crossref | GoogleScholarGoogle Scholar |

Bhattarai, K. R., and Vetaas, O. R. (2006). Can Rapoport’s rule explain tree species richness along the Himalayan elevation gradient, Nepal? Diversity & Distributions 12, 373–378.
Can Rapoport’s rule explain tree species richness along the Himalayan elevation gradient, Nepal?Crossref | GoogleScholarGoogle Scholar |

Bhattarai, K. R., Vetaas, O. R., and Grytnes, J. A. (2004). Fern species richness along a central Himalayan elevational gradient, Nepal. Journal of Biogeography 31, 389–400.
Fern species richness along a central Himalayan elevational gradient, Nepal.Crossref | GoogleScholarGoogle Scholar |

Bogan, A. E. (2008). Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595, 139–147.
Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater.Crossref | GoogleScholarGoogle Scholar |

Bößneck, U. (2012). Leben am Limit: Besiedlung von Süßwasser-Habitaten extremer Hochlagen Asiens, Amerikas und Afrikas durch Mollusken (Mollusca: Bivalvia & Gastropoda). In ‘Biodiversität und Naturausstattung im Himalaya IV’. (Eds M. Hartmann and J. Weipert.) pp. 103–106. (Verein der Freunde & Förderer des Naturkundemuseums Erfurt e.V., Erfurt.)

Brandt, R. A. M. (1974). The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1–423.

Chaudhary, R. P. (1998). ‘Biodiversity in Nepal – Status and Conservation.’ (Tecpress Books: Bangkok, Thailand.)

Chettri, B., Bhupathy, S., and Acharya, B. K. (2010). Distribution pattern of reptiles along an eastern Himalayan elevation gradient, India. Acta Oecologica 36, 16–22.
Distribution pattern of reptiles along an eastern Himalayan elevation gradient, India.Crossref | GoogleScholarGoogle Scholar |

Clewing, C., Bößneck, U., Oheimb, P. V. v., and Albrecht, C. (2013). Molecular phylogeny and biogeography of a high mountain bivalve fauna: the Sphaeriidae of the Tibetan Plateau. Malacologia 56, 231–252.
Molecular phylogeny and biogeography of a high mountain bivalve fauna: the Sphaeriidae of the Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |

Colgan, D., Ponder, W. F., and Eggler, P. E. (2000). Gastropod evolutionary rates and phylogenetic relationships assessed using partial 28S rDNA and histone H3 sequences. Zoologica Scripta 29, 29–63.
Gastropod evolutionary rates and phylogenetic relationships assessed using partial 28S rDNA and histone H3 sequences.Crossref | GoogleScholarGoogle Scholar |

Dance, S. P. (1967). Pisidium collected by the 1924 Mount Everest expedition, with descriptions of two new species (Bivalvia: Sphaeriidae). The Journal of Conchology 26, 175–180.

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=b326576d8549dc5561e70b14d1339c77CAS |

Darwall, W., Smith, K., Lowe, T., and Vié, J.-C. (2005). ‘The Status and Distribution of Freshwater Biodiversity in Eastern Africa. IUCN SSC Freshwater Biodiversity Assessment Programme.’ (IUCN: Gland, Switzerland and Cambridge, UK.)

Dirnböck, T., Essl, F., and Rabitsch, W. (2011). Disproportional risk for habitat loss of high-altitude endemic species under climate change. Global Change Biology 17, 990–996.
Disproportional risk for habitat loss of high-altitude endemic species under climate change.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |

Favre, A., Päckert, M., Pauls, S. U., Jähnig, S. C., Uhl, D., Michalak, I., and Muellner-Riehl, A. N. (2015). The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews of the Cambridge Philosophical Society 90, 236–253.
The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas.Crossref | GoogleScholarGoogle Scholar |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primer for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=3ed3b40952948838a8ebb6c4cd36ee0cCAS |

Glöer, P., and Bößneck, U. (2013). Freshwater molluscs from Nepal and North India with the description of seven new species. Archiv für Molluskenkunde: International Journal of Malacology 142, 137–156.
Freshwater molluscs from Nepal and North India with the description of seven new species.Crossref | GoogleScholarGoogle Scholar |

Grau, O., Grytnes, J.-A., and Birks, H. J. B. (2007). A comparison of altitudinal species richness patterns of bryophytes with other plant groups in Nepal, Central Himalaya. Journal of Biogeography 34, 1907–1915.
A comparison of altitudinal species richness patterns of bryophytes with other plant groups in Nepal, Central Himalaya.Crossref | GoogleScholarGoogle Scholar |

Hoeh, W. R., Stewart, D. T., and Guttman, S. I. (2002). High fidelity of mitochondrial genome transmission under the doubly uniparental modes of inheritance in freshwater mussels (Bivalvia: Unionoidea). Evolution 56, 2252–2261.
High fidelity of mitochondrial genome transmission under the doubly uniparental modes of inheritance in freshwater mussels (Bivalvia: Unionoidea).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38jisVKqtg%3D%3D&md5=13af8fc9b8c235944263ab93ab9c1f06CAS |

Hoorn, C., Mosbrugger, V., Mulch, A., and Antonelli, A. (2013). Biodiversity from mountain building. Nature Geoscience 6, 154.
Biodiversity from mountain building.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFWnu74%3D&md5=5e360b947ece18eedde33c75099ffd7fCAS |

Hu, J., Xie, F., Li, C., and Jiang, J. (2011). Elevational patterns of species richness, range and body size for spiny frogs. PLoS One 6, e19817.
Elevational patterns of species richness, range and body size for spiny frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsFGqtr8%3D&md5=30a27bc477d4c7e70711528ea2de561bCAS |

Kappes, H., and Haase, P. (2012). Slow but steady: dispersal of freshwater molluscs. Aquatic Sciences 74, 1–14.
Slow but steady: dispersal of freshwater molluscs.Crossref | GoogleScholarGoogle Scholar |

Körner, C. (2001). Alpine ecosystems. In ‘Encyclopedia of Biodiversity’. (Eds S. A. Levin.) pp. 133–144. (Academic Press: San Diego, CA.)

Körner, C., and Spehn, E. (2002). ‘Mountain Biodiversity: a Global Assessment.’ (Parthenon Publishing: London.)

Korniushin, A. V. (2006). Revision of some little collections of Sphaeriidae from New Guinea, with the description of a new species. Heldia 6, 1–10.

Korniushin, A., and Bößneck, U. (2003). New records of little known Pisidium species from West Nepal and review of the fauna of Sphaeriidae (Mollusca: Bivalvia) in the Himalaya Region. In ‘Biodiversität und Naturausstattung im Himalaya’. (Eds M. Hartmann and H. Baumbach.) pp. 57–61. (Verein der Freunde und Förderer des Naturkundemuseums Erfurt e.V.: Erfurt, Germany.)

Kuiper, J. G. J. (1960a). Pisidium artifex, eine neue Art aus Kenya. Archiv für Molluskenkunde 89, 67–74.

Kuiper, J. G. J. (1960b). Die Pisidien des Ochridsees, Mazedonien, nebst Bemerkungen über die Verbreitung der Pisidien in der Balkanhalbinsel und den Donauländern. Beaufortia 88, 219–231.

Kuiper, J. G. J. (1967). A collection of Pisidium (Mollusca, Bivalvia) from the Philippines and the Bismarck Archipelago. Videnskabelige Meddelelser Dansk Naturhistorisk Forening 130, 137–141.

Kuiper, J. G. J. (1987). Pisidium maasseni n. sp., a new species from Lake Prespa, Jugoslavia (Bivalvia, Sphaeriidae). Basteria 51, 163–165.

Kuiper, J. G. J., and Hinz, W. (1984). Zur Fauna der Kleinmuscheln in den Anden. Archiv für Molluskenkunde 114, 137–156.

Lee, T., and Ó Foighil, D. (2003). Phylogenetic structure of the Sphaeriidae, a global clade of freshwater bivalve molluscs, inferred from nuclear (ITS-1) and mitochondrial (16S) ribosomal gene sequences. Zoological Journal of the Linnean Society 137, 245–260.

Li, J., He, Q., Hua, X., Zhou, J., Xu, H., Chen, J., and Fu, C. (2009). Climate and history explain the species richness peak at mid‐elevation for Schizothorax fishes (Cypriniformes: Cyprinidae) distributed in the Tibetan Plateau and its adjacent regions. Global Ecology and Biogeography 18, 264–272.
Climate and history explain the species richness peak at mid‐elevation for Schizothorax fishes (Cypriniformes: Cyprinidae) distributed in the Tibetan Plateau and its adjacent regions.Crossref | GoogleScholarGoogle Scholar |

McCain, C. M., and Grytnes, J.-A. (2010). Elevational gradients in species richness. In ‘Encyclopedia of Life Sciences (ELS)’. 10.1002/9780470015902.a0022548. (John Wiley & Sons: Chichester, UK.)

Merckx, V. S. F. T., Hendriks, K. P., Beentjes, K. K., Mennes, C. B., Becking, L. E., Peijnenburg, K. T. C. A., Afendy, A., Arumugam, N., de Boer, H., Biun, A., Buang, M. M., Chen, P.-P., Chung, A. Y. C., Dow, R., Feijen, F. A. A., Feijen, H., Feijen-van Soest, C., Geml, J., Geurts, R., Gravendeel, B., Hovenkamp, P., Imbun, P., Ipor, I., Janssens, S. B., Jocque, M., Kappes, H., Khoo, E., Koomen, P., Lens, F., Majapun, R. J., Morgado, L. N., Neupane, S., Nieser, N., Pereira, J. T., Rahman, H., Sabran, S., Sawang, A., Schwallier, R. M., Shim, P.-S., Smit, H., Sol, N., Spait, M., Stech, M., Stokvis, F., Sugau, J. B., Suleiman, M., Sumail, S., Thomas, D. C., van Tol, J., Tuh, F. Y. Y., Yahya, B. E., Nais, J., Repin, R., Lakim, M., and Schilthuizen, M. (2015). Evolution of endemism on a young tropical mountain. Nature 524, 347–350.
Evolution of endemism on a young tropical mountain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlaju73J&md5=92af1f69184787f76879e3be9ae3ae6dCAS |

Nesemann, H., and Sharma, S. (2005). Illustrated checklist of pea clams (Mollusca: Bivalvia: Sphaeriidae) from Nepal. Himalayan Journal of Sciences 3, 57–65.

Nesemann, H., Korniushin, A., Khanal, S., and Sharma, S. (2001). Molluscs of the families Sphaeriidae and Corbiculidae (Bivalvia: Veneroidea) of Nepal (Himalayan midmountains and terai), their anatomy and affinities. Acta Conchyliorum 4, 1–33.

Nesemann, H., Sharma, S., Sharma, G., Khanal, S. N., Pradhan, B., Shah, D. N., and Tachamo, R. D. (2007). ‘Aquatic Invertebrates of the Ganga River System. Mollusca, Annelida, Crustacea (in Part).’ (Sunil Uprety: Chandi Publisher, Kathmandu, Nepal.)

Odhner, N. H. (1940). Sphaeriids from the Dutch East Indies especially from New Guinea. A revision. Nova Guinea, N. S. 4, 113–131.

Oheimb, P. V. v., Albrecht, C., Riedel, F., Bößneck, U., Zhang, H., and Wilke, T. (2013). Testing the role of the Himalaya Mountains as a dispersal barrier in freshwater gastropods (Gyraulus spp.). Biological Journal of the Linnean Society. Linnean Society of London 109, 526–534.
Testing the role of the Himalaya Mountains as a dispersal barrier in freshwater gastropods (Gyraulus spp.).Crossref | GoogleScholarGoogle Scholar |

Päckert, M., Martens, J., Sun, Y.-H., Severinghaus, L. L., Nazarenko, A. A., Ting, J., Töpfer, T., and Tietze, D. T. (2012). Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes). Journal of Biogeography 39, 556–573.
Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes).Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘The Simple Fool’s Guide to PCR.’ (University of Hawaii: Honolulu, HI.)

Park, J. K., and Ó Foighil, D. (2000). Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments. Molecular Phylogenetics and Evolution 14, 75–88.
Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFemtQ%3D%3D&md5=5ec4e3fd1d82946a367e45ea99a74c94CAS |

Phiri, E. E., and Daniels, S. R. (2013). Hidden in the highlands: the description and phylogenetic position of a novel endemic freshwater crab species (Potamonautidae: Potamonautes) from Zimbabwe. Invertebrate Systematics 27, 530–539.
Hidden in the highlands: the description and phylogenetic position of a novel endemic freshwater crab species (Potamonautidae: Potamonautes) from Zimbabwe.Crossref | GoogleScholarGoogle Scholar |

Poudyal, C. P., Chang, C., Oh, H.-J., and Lee, S. (2010). Landslide susceptibility maps comparing frequency ratio and artificial neural networks: a case study from the Nepal Himalaya. Environmental Earth Sciences 61, 1049–1064.
Landslide susceptibility maps comparing frequency ratio and artificial neural networks: a case study from the Nepal Himalaya.Crossref | GoogleScholarGoogle Scholar |

Rahbek, C. (1995). The elevational gradient of species richness: a uniform pattern? Ecography 18, 200–205.
The elevational gradient of species richness: a uniform pattern?Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inferences under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inferences under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=eb4d9b9211c4f59088b8e30c23025081CAS |

Schöniger, M., and von Haeseler, A. (1994). A stochastic model for the evolution of autocorrelated DNA sequences. Molecular Phylogenetics and Evolution 3, 240–247.
A stochastic model for the evolution of autocorrelated DNA sequences.Crossref | GoogleScholarGoogle Scholar |

Schultheiß, R., Albrecht, C., Bößneck, U., and Wilke, T. (2008). The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa. Hydrobiologia 615, 141–156.
The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa.Crossref | GoogleScholarGoogle Scholar |

Seddon, M., Appleton, C., Van Damme, D., and Graf, D. (2011). Freshwater molluscs of Africa: diversity, distribution, and conservation. In ‘The Diversity of Life in African Freshwaters: Under Water, Under Threat. An Analysis of the Status and Distribution of Freshwater Species Throughout Mainland Africa’. (Eds W. R. T. Darwall, K. G. Smith, D. J. Allen, R. A. Holland, I. J. Harrison and E. G. E. Brooks.) pp. 92–125. (IUCN: Cambridge, UK and Gland, Switzerland.)

Shrestha, T. K. (2003). ‘Wildlife of Nepal: a Study of Renewable Resources of Nepal Himalayas.’ (Steven Simpson Books, Norwich, UK.)

Spehn, E. M., Rudmann-Maurer, K., Körner, C., and Maselli, D. (2010). ‘Mountain Biodiversity and Global Change.’ (GMBA-DIVERSITAS: Basel, Switzerland.)

Subba, B. R., and Gosh, T. K. (2000). Some freshwater molluscs from eastern and central Nepal. Journal of the Bombay Natural History Society 97, 452–455.

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=03ff7cc7d33ff928f46a243ed7d97fb2CAS |

Thapa, N. B., and Thapa, D. P. (1969). ‘Geography of Nepal: physical, economic, cultural & regional.’ (Orient Longman: Telangana, India.)

Wilke, T., Davis, G. M., Qiu, D., and Spear, R. C. (2006). Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism. Malacologia 48, 143–157.

Xia, X., and Lemey, P. (2009). Assessing substitution saturation with DAMBE. In ‘The Phylogenetic Handbook: a Practical Approach to DNA and Protein Phylogeny’. (Eds P. Lemey, M. Salemi and A.-M. Vandamme.) pp. 615–630. (Cambridge University Press: Cambridge, UK.).

Xia, X., Xie, Z., Salemi, M., Chen, L., and Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.
An index of substitution saturation and its application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1WhtrY%3D&md5=30eeffc3f6a14009a2410f217268d879CAS |

Xu, B., Cao, J., Hansen, J., Yao, T., Joswia, N., Wang, N., Wu, G., Wang, M., Zhao, H., Yang, W., Liu, X., and He, J. (2009). Black soot and the survival of Tibetan glaciers. Proceedings of the National Academy of Sciences of the United States of America 106, 22114–22118.
Black soot and the survival of Tibetan glaciers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtlWktg%3D%3D&md5=f33a24cb385daccbe41715d0399f6019CAS |