Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

When molecules and morphology work together: lines of evidence for the validity of Caridina buehleri Roux (Crustacea : Decapoda : Atyidae) and for C. gueryi Marquet, Keith & Kalfatak as its junior synonym

Valentin de Mazancourt A D , Gerard Marquet A , Werner Klotz B , Philippe Keith A and Magalie Castelin A C
+ Author Affiliations
- Author Affiliations

A Muséum national d’Histoire naturelle, DMPA, UMR 7208, CP026, 57, Rue Cuvier, F-75231 Paris, Cedex 05, France.

B Wiesenweg 1, A-6063 Rum, Austria.

C Aquatic Animal Health Section, Fisheries and Oceans Canada, Pacific Biological Station, 3190 Hammond Bay Road, Nanaimo, BC V9T 6N7, Canada.

D Corresponding author. Email: valentin.demazancourt@laposte.net

Invertebrate Systematics 31(2) 220-230 https://doi.org/10.1071/IS16044
Submitted: 4 June 2016  Accepted: 28 November 2016   Published: 26 April 2017

Abstract

The taxonomy of the freshwater shrimps Caridina (Atyidae) is very complex and confused mostly because the morphological characters that have traditionally been used for species delimitation and identification are highly plastic. There is thus a need for an integrative approach to their taxonomy. In total, 42 specimens belonging to either Caridina buehleri Roux, 1934 or Caridina gueryi Marquet, Keith & Kalfatak, 2009 were examined. We combined here morphological data from 12 specimens from the whole distributional range of the species, including type specimens with 16S mtDNA analyses from seven freshly sampled specimens, to verify the specific status of Caridina buehleri from Papua New-Guinea, Central Sulawesi, Western Samoa and the Solomon Islands, and C. gueryi from Vanuatu. The comparison of 24 morphological characters showed that morphological variations of character traits between C. gueryi and C. buehleri are widely overlapping and that no morphological feature can effectively split specimens into two clear groups. Molecular characters corroborated these results, as specimens from both groups were only separated by a 2% p-distance, a genetic distance that is coherent with their potentially high dispersal abilities. We thus consider C. gueryi as a junior synonym of C. buehleri. Finally, C. buehleri is characterised mainly by a styliform and characteristically indented rostrum and a long stylocerite. Detailed re-descriptions of the type specimens of C. buehleri and C. gueryi are given, as well as their geographical and ecological distribution.

Additional keywords: freshwater shrimp, Indo-Pacific, integrative taxonomy, 16S.


References

Bouvier, E.-L. (1925). Recherches sur la morphologie, les variations et la distribution systématique des crevettes d’eau douce de la famille des Atyidés. In ‘Encyclopédie Entomologique. Vol. 4’. (Lechevalier: Paris.)

Cai, Y., and Ng, P. K. L. (1999). A revision of the Caridina serrata species group, with descriptions of five new species (Crustacea: Decapoda: Caridea: Atyidae). Journal of Natural History 33, 1603–1638.
A revision of the Caridina serrata species group, with descriptions of five new species (Crustacea: Decapoda: Caridea: Atyidae).CrossRef | open url image1

Cai, Y., and Ng, P. K. L. (2007). A revision of the Caridina gracilirostris De Man, 1892, species group, with descriptions of two new taxa (Decapoda; Caridea; Atyidae). Journal of Natural History 41, 1585–1602.
A revision of the Caridina gracilirostris De Man, 1892, species group, with descriptions of two new taxa (Decapoda; Caridea; Atyidae).CrossRef | open url image1

Coleman, C. O. (2003). ‘Digital inking’: How to make perfect line drawings on computers. Organisms Diversity and Evolution 3, 303. open url image1

Coleman, C. O. (2006). Substituting time-consuming pencil drawings in arthropod taxonomy using stacks of digital photographs. Zootaxa 1360, 61–68. open url image1

Covich, A. P., Palmer, M. A., and Crowl, T. A. (1999). The role of benthic invertebrate species in freshwater ecosystems. Bioscience 49, 119–128.
The role of benthic invertebrate species in freshwater ecosystems.CrossRef | open url image1

De Grave, S., Smith, K. G., Adeler, N. A., Allen, D. J., Alvarez, F., Anker, A., Cai, Y., Carrizo, S. F., Klotz, W., Mantelatto, F. L., Page, T. J., Shy, J.-Y., Villalobos, J. L., and Wowor, D. (2015). Dead shrimp blues: a global assessment of extinction risk in freshwater shrimps (Crustacea: Decapoda: Caridea). PLoS One 10, e0120198.
Dead shrimp blues: a global assessment of extinction risk in freshwater shrimps (Crustacea: Decapoda: Caridea).CrossRef | open url image1

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.CrossRef | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=3779829e13a4c162ef008e41e63c789fCAS | open url image1

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.CrossRef | open url image1

Fryer, G. (2006). Evolution in ancient lakes: radiation of Tanganyikan atyid prawns and speciation of pelagic cichlid fishes in Lake Malawi. Hydrobiologia 568, 131–142.
Evolution in ancient lakes: radiation of Tanganyikan atyid prawns and speciation of pelagic cichlid fishes in Lake Malawi.CrossRef | open url image1

Gerbeaux, P., Goodman, J., Marquet, G., Keith, P. (2014). Freshwater survey of Laulii-Falevao (Upolu) and Mt Salefai (Savai) – Freshwater Contribution to a MNRE funded project for the integration of Climate Change Risks and resilience into Forestry Management in Samoa (ICCRIFS) Project. Report, Department of Conservation Te Papa Atawhai, Muséum national d’Histoire naturelle.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=01675b96feb07335d6568390e1c23744CAS | open url image1

Hayashi, K. I., and Hamano, T. (1984). The complete larval development of Caridina japonica. Zoological Science 1, 571–589. open url image1

Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: a program for the Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
MrBayes: a program for the Bayesian inference of phylogeny.CrossRef | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=82e415832d42a58a58bf16a79056e67dCAS | open url image1

Jugovic, J., Prevorcnik, S., Aljancic, G., and Sket, B. (2010). The atyid shrimp (Crustacea: Decapoda: Atyidae) rostrum: phylogeny versus adaptation, taxonomy versus trophic ecology. Journal of Natural History 44, 2509–2533.
The atyid shrimp (Crustacea: Decapoda: Atyidae) rostrum: phylogeny versus adaptation, taxonomy versus trophic ecology.CrossRef | open url image1

Karge, A., and Klotz, W. (2008). ‘Süßwassergarnelen aus aller Welt.’ (Dähne, Verlag: Ettlingen, Germany.)

Keith, P., Marquet, G., Lord, C., Kalfatak, D., and Vigneux, E. (2010). Vanuatu freshwater fish and crustaceans. Société Française d’Ichtyologie, Paris.

Klotz, W., Karge, A., and von Rintelen, K. (2007). A redescription of two atyid shrimps (Decapoda: Caridina) from Central Sulawesi, Indonesia. Zootaxa 1466, 1–10. open url image1

Klotz, W., and von Rintelen, T. (2014). To ‘bee’ or not to be – on some ornamental shrimp from Guangdong Province, southern China and Hong Kong SAR, with descriptions of three new species. Zootaxa 3889, 151–184.
To ‘bee’ or not to be – on some ornamental shrimp from Guangdong Province, southern China and Hong Kong SAR, with descriptions of three new species.CrossRef | open url image1

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.CrossRef | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=60257dbe2868778a4d0b3f3c019d85e1CAS | open url image1

Marquet, G., Keith, P., and Kalfatak, D. (2009). Caridina gueryi, a new species of freshwater shrimp (Decapoda, Atyidae) from Santo island, Vanuatu. Crustaceana 82, 159–166.
Caridina gueryi, a new species of freshwater shrimp (Decapoda, Atyidae) from Santo island, Vanuatu.CrossRef | open url image1

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans’, pp. 1–8. (IEEE: Piscataway, NJ.)

Page, T. J., and Hughes, J. M. (2011). Neither molecular nor morphological data have all the answers; with an example from Macrobrachium (Decapoda: Palaemonidae) from Australia. Zootaxa 2874, 65–68. open url image1

Page, T., Choy, S., and Hughes, J. (2005). The taxonomic feedback loop: symbiosis of morphology and molecules. Biology Letters 1, 139–142.
The taxonomic feedback loop: symbiosis of morphology and molecules.CrossRef | 1:CAS:528:DC%2BD2MXpsVaqu74%3D&md5=ac9594cc8e5960f190adf803b7e1ae47CAS | open url image1

Page, T. J., von Rintelen, K., and Hughes, J. M. (2007). An island in the stream: Australia’s place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina). Molecular Phylogenetics and Evolution 43, 645–659.
An island in the stream: Australia’s place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina).CrossRef | 1:CAS:528:DC%2BD2sXlt1alt7k%3D&md5=3cc6fc11312587f550ad582198bf73d0CAS | open url image1

Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In ‘Molecular Systematics’. (Eds D. M. Hillis, B. K. Mable and C. Moritz.) pp. 205–247. (Sinauer Associates: Sunderland, MA.)

Pringle, C. M., Blake, G. A., Covich, A. P., Buzby, K. M., and Finley, A. (1993). Effects of omnivorous shrimp in a montane tropical stream: sediment removal, disturbance of sessile invertebrates and enhancement of understory algal biomass. Oecologia 93, 1–11.
Effects of omnivorous shrimp in a montane tropical stream: sediment removal, disturbance of sessile invertebrates and enhancement of understory algal biomass.CrossRef | open url image1

Richard, J., and Clark, P. F. (2009). African Caridina (Crustacea: Decapoda: Caridea: Atyidae): redescriptions of C. africana Kingsley, 1882, C. togoensis Hilgendorf, 1893, C. natalensis Bouvier, 1925 and C. roubaudi Bouvier, 1925 with descriptions of 14 new species. Zootaxa 1995, 1–75. open url image1

Richard, J., and Clark, P. F. (2014). Caridina simoni Bouvier, 1904 (Crustacea: Decapoda: Caridea: Atyoidea: Atyidae) and the synonymy by Johnson, 1963. Zootaxa 3841, 301–338.
Caridina simoni Bouvier, 1904 (Crustacea: Decapoda: Caridea: Atyoidea: Atyidae) and the synonymy by Johnson, 1963.CrossRef | open url image1

Roux, J. (1934). Notes de carcinologie mélanésienne. I. Décapodes d’eau douce de l’Archipel Bismarck et des îles de l’Amirauté. Revue Suisse de Zoologie 41, 217–234.
Notes de carcinologie mélanésienne. I. Décapodes d’eau douce de l’Archipel Bismarck et des îles de l’Amirauté.CrossRef | open url image1

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.CrossRef | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=c868f257e775d7586364223c6888c21aCAS | open url image1

Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.CrossRef | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=0047ba3b5231ef0904a5c2560f64ab2cCAS | open url image1

Tamura, K., Stetcher, 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 | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=31e52c88992083420b0597f29824352bCAS | open url image1

von Rintelen, K., and Cai, Y. (2009). Radiation of endemic species flocks in ancient lakes: systematic revision of the freshwater shrimp Caridina H. Milne Edwards, 1837 (Crustacea: Decapoda: Atyidae) from the ancient lakes of Sulawesi, Indonesia, with the description of eight new species. The Raffles Bulletin of Zoology 57, 343–452. open url image1

von Rintelen, K., Karge, A., and Klotz, W. (2008). News from a small island – first record of a freshwater shrimp (Decapoda, Atyidae, Caridina) from Peleng, Banggai Islands, Indonesia. Journal of Natural History 42, 2243–2256.
News from a small island – first record of a freshwater shrimp (Decapoda, Atyidae, Caridina) from Peleng, Banggai Islands, Indonesia.CrossRef | open url image1



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (228 KB) Export Citation