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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Contrasting population structures of freshwater atyid shrimps in Hong Kong and their conservation implications

Ka Yan Ma https://orcid.org/0000-0001-5690-2319 A B , Lai Him Chow B , Ling Ming Tsang B , Sammy De Grave C and Ka Hou Chu https://orcid.org/0000-0001-8107-5415 B D
+ Author Affiliations
- Author Affiliations

A School of Ecology, Sun Yat-Sen University, Shenzhen, PR China.

B Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, PR China.

C Oxford University Museum of Natural History, University of Oxford, Oxford, UK.

D Corresponding author. Email: kahouchu@cuhk.edu.hk

Marine and Freshwater Research 72(11) 1667-1678 https://doi.org/10.1071/MF21069
Submitted: 23 February 2021  Accepted: 21 June 2021   Published: 2 August 2021

Abstract

Understanding population connectivity is crucial for effective conservation management. Schemes for speculating potential connectivity patterns over large to medium geographic scales using riverscape and life history features have been developed, but whether they are still applicable over fine scales has rarely been examined. Caridina shrimps (Family Atyidae) constitute a major component of freshwater ecosystems. Nonetheless, although over 20% of atyid species are considered Threatened or Near Threatened on the International Union for Conservation of Nature Red List, a general lack of understanding of the population structure of these species, which typically have restricted distributions, significantly hampers conservation management. Here, we examined the fine-scale population structure of five atyid species in Hong Kong, a highly urbanised metropolis, using the mitochondrial cytochrome oxidase subunit I (COI) gene and four to six microsatellite markers. The results reveal species-specific contrasting phylogeographic patterns, ranging from wide-range genetic panmixia to population differentiation at an extremely small scale of <1 km. This pronounced population structuring may be attributed to the freshwater obligates’ limited dispersal ability, high level of inbreeding and marked demographic fluctuations associated with climate changes since the Pleistocene. The results shed new light on the evolution of this widely distributed shrimp genus and bridge the critical knowledge gap in formulating effective conservation plans.

Keywords: Caridea, conservation genetics, Decapoda, phylogeography.


References

Bernardes, S. C., Pepato, A. R., von Rintelen, T., von Rintelen, K., Page, T. J., Freitag, H., and de Bruyn, M. (2017). The complex evolutionary history and phylogeography of Caridina typus (Crustacea: Decapoda): long-distance dispersal and cryptic allopatric species. Scientific Reports 7, 9044.
The complex evolutionary history and phylogeography of Caridina typus (Crustacea: Decapoda): long-distance dispersal and cryptic allopatric species.Crossref | GoogleScholarGoogle Scholar | 28831142PubMed |

Brown, S. D. J., Collins, R. A., Boyer, S., Lefort, M.-C., Malumbres-Olarte, J., Vink, C. J., and Cruickshank, R. H. (2012). Spider: an R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources 12, 562–565.
Spider: an R package for the analysis of species identity and evolution, with particular reference to DNA barcoding.Crossref | GoogleScholarGoogle Scholar |

Cai, Y., and Ng, N. K. (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 | GoogleScholarGoogle Scholar |

Cai, Y., Ng, P. K. L., and Choy, S. (2007). Freshwater shrimps of the family Atyidae (Crustacea: Decapoda: Caridea) from Peninsular Malaysia and Singapore. The Raffles Bulletin of Zoology 55, 277–309.

Chappell, J., and Shackleton, N. J. (1986). Oxygen isotopes and sea level. Nature 324, 137–140.
Oxygen isotopes and sea level.Crossref | GoogleScholarGoogle Scholar |

Chapuis, M.-P., and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 17150975PubMed |

Chen, Q. H., Chen, W.-J., and Guo, Z.-L. (2018). Caridean prawn (Crustacea, Decapoda) from Dong’ao Island, Guangdong, China. Zootaxa 4399, 315–328.
Caridean prawn (Crustacea, Decapoda) from Dong’ao Island, Guangdong, China.Crossref | GoogleScholarGoogle Scholar | 29690315PubMed |

Chow, L. H., Ma, K. Y., Hui, J. H. L., and Chu, K. H. (2018). Isolation and characterization of polymorphic microsatellite loci for Caridina cantonensis and transferability across eight confamilial species (Atyidae, Decapoda). Zoological Studies (Taipei, Taiwan) 57, 19.

Cornuet, J. M., and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.
Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data.Crossref | GoogleScholarGoogle Scholar | 8978083PubMed |

Crandall, E. D., Taffel, J. R., and Barber, P. H. (2010). High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae). Heredity 104, 563.
High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae).Crossref | GoogleScholarGoogle Scholar | 19844268PubMed |

De Grave, S. (2013a). Caridina apodosis. In ‘The IUCN Red List of Threatened Species 2013’. e.T198214A2516126. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/198214/2516126

De Grave, S. (2013b). Caridina elongopoda. In ‘The IUCN Red List of Threatened Species 2013’. e.T197578A2491525. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/197578/2491525

De Grave, S. (2013c). Caridina typus. In ‘The IUCN Red List of Threatened Species 2013’. e.T198327A2520928. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/198327/2520928

De Grave, S., and Klotz, W. (2013). Caridina serrata. In ‘The IUCN Red List of Threatened Species 2013’. e.T197804A2500640. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/197804/2500640

De Grave, S., Cai, Y., and Anker, A. (2008). Global diversity of shrimps (Crustacea: Decapoda: Caridea) in freshwater. Hydrobiologia 595, 287–293.
Global diversity of shrimps (Crustacea: Decapoda: Caridea) in freshwater.Crossref | GoogleScholarGoogle Scholar |

De Grave, S., Klotz, W., and Cai, Y. (2013a). Caridina cantonensis (errata version published in 2019). In ‘The IUCN Red List of Threatened Species 2013’. e.T197666A147785963. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/197666/147785963

De Grave, S., Shy, J., and Klotz, W. (2013b). Caridina trifasciata. In ‘The IUCN Red List of Threatened Species 2013’. e.T197794A2500187. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/197794/2500187

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 | GoogleScholarGoogle Scholar | 25807292PubMed |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 22367748PubMed |

Dudgeon, D. (1999). ‘Tropical Asian streams: zoobenthos, ecology and conservation.’ (Hong Kong University Press: Hong Kong SAR, PR China.)

Dudgeon, D. (2011). Asian river fishes in the Anthropocene: threats and conservation challenges in an era of rapid environmental change. Journal of Fish Biology 79, 1487–1524.
Asian river fishes in the Anthropocene: threats and conservation challenges in an era of rapid environmental change.Crossref | GoogleScholarGoogle Scholar | 22136237PubMed |

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 | GoogleScholarGoogle Scholar | 15034147PubMed |

Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Fagan, W. F. (2002). Connectivity, fragmentation, and extinction risk in dendritic metapopulations. Ecology 83, 3243–3249.
Connectivity, fragmentation, and extinction risk in dendritic metapopulations.Crossref | GoogleScholarGoogle Scholar |

Fu, Y.-X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection.Crossref | GoogleScholarGoogle Scholar | 9335623PubMed |

Fujita, J., Nakayama, K., Kai, Y., Ueno, M., and Yamashita, Y. (2011). Comparison of genetic population structures between the landlocked shrimp, Neocaridina denticulata denticulata, and the amphidromous shrimp, Caridina leucosticta (Decapoda, Atyidae) as inferred from mitochondrial DNA sequences. In ‘New Frontiers in Crustacean Biology’. pp. 183–196. (Brill.)

Fujita, J., Zenimoto, K., Iguchi, A., Kai, Y., Ueno, M., and Yamashita, Y. (2016). Comparative phylogeography to test for predictions of marine larval dispersal in three amphidromous shrimps. Marine Ecology Progress Series 560, 105–120.
Comparative phylogeography to test for predictions of marine larval dispersal in three amphidromous shrimps.Crossref | GoogleScholarGoogle Scholar |

Fyfe, J. A., Shaw, R., Campbell, S. D. G., Lai, K. W., and Kirk, P. A. (2000). ‘The Quaternary Geology of Hong Kong Geotechnical Engineering Office.’ (Civil Engineering Department, the Government of the Hong Kong SAR: Hong Kong SAR, PR China.)

Hancock, M. A., Hughes, J. M., and Bunn, S. E. (1998). Influence of genetic and environmental factors on egg and clutch sizes among populations of Paratya australiensis Kemp (Decapoda: Atyidae) in upland rainforest streams, south-east Queensland. Oecologia 115, 483–491.
Influence of genetic and environmental factors on egg and clutch sizes among populations of Paratya australiensis Kemp (Decapoda: Atyidae) in upland rainforest streams, south-east Queensland.Crossref | GoogleScholarGoogle Scholar | 28308268PubMed |

Hayashi, K., and Hamano, T. (1984). The complete larval development of Caridina japonica De Man (Decapoda, Caridea, Atyidae) reared in the laboratory. Zoological Science 1, 571–589.

Holland, M. M., and Parson, W. (2011). GeneMarker®HID: a reliable software tool for the analysis of forensic STR data. Journal of Forensic Sciences 56, 29–35.
GeneMarker®HID: a reliable software tool for the analysis of forensic STR data.Crossref | GoogleScholarGoogle Scholar | 20887353PubMed |

Hughes, J. M. (2007). Constraints on recovery: Using molecular methods to study connectivity of aquatic biota in rivers and streams. Freshwater Biology 52, 616–631.
Constraints on recovery: Using molecular methods to study connectivity of aquatic biota in rivers and streams.Crossref | GoogleScholarGoogle Scholar |

Hughes, J. M., Huey, J. A., and Schmidt, D. J. (2013). Is realised connectivity among populations of aquatic fauna predictable from potential connectivity? Freshwater Biology 58, 951–966.
Is realised connectivity among populations of aquatic fauna predictable from potential connectivity?Crossref | GoogleScholarGoogle Scholar |

Hurwood, D. A., and Hughes, J. M. (2001). Nested clade analysis of the freshwater shrimp, Caridina zebra (Decapoda: Atyidae), from north-eastern Australia. Molecular Ecology 10, 113–125.
Nested clade analysis of the freshwater shrimp, Caridina zebra (Decapoda: Atyidae), from north-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 11251792PubMed |

Jombart, T. (2008). Adegenet: an R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
Adegenet: an R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar | 18397895PubMed |

Jombart, T., and Collins, C. (2015). ‘A Tutorial for Discriminant Analysis of Principal Components (DAPC) using adegenet 2.0. 0.’ (Imperial College London, MRC Centre for Outbreak Analysis and Modelling: London, UK.)

Jombart, T., Devillard, S., and Balloux, F. (2010). Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11, 94.
Discriminant analysis of principal components: a new method for the analysis of genetically structured populations.Crossref | GoogleScholarGoogle Scholar | 20950446PubMed |

Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., and Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587.
ModelFinder: fast model selection for accurate phylogenetic estimates.Crossref | GoogleScholarGoogle Scholar | 28481363PubMed |

Kamvar, Z. N., Tabima, J. F., and Grünwald, N. J. (2014). Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281.
Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction.Crossref | GoogleScholarGoogle Scholar | 24688859PubMed |

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 | GoogleScholarGoogle Scholar | 25544138PubMed |

Knowlton, N., and Weigt, L. A. (1998). New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London – B. Biological Sciences 265, 2257–2263.
New dates and new rates for divergence across the Isthmus of Panama.Crossref | GoogleScholarGoogle Scholar |

Leigh, J. W., and Bryant, D. (2015). popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.
popart: full-feature software for haplotype network construction.Crossref | GoogleScholarGoogle Scholar |

Linke, S., Pressey, R. L., Bailey, R. C., and Norris, R. H. (2007). Management options for river conservation planning: condition and conservation re-visited. Freshwater Biology 52, 918–938.
Management options for river conservation planning: condition and conservation re-visited.Crossref | GoogleScholarGoogle Scholar |

Lowe, W. H., and Allendorf, F. W. (2010). What can genetics tell us about population connectivity? Molecular Ecology 19, 3038–3051.
What can genetics tell us about population connectivity?Crossref | GoogleScholarGoogle Scholar | 20618697PubMed |

March, J. G., and Pringle, C. M. (2003). Food web structure and basal resource utilization along a tropical island stream continuum, Puerto Rico. Biotropica 35, 84–93.
Food web structure and basal resource utilization along a tropical island stream continuum, Puerto Rico.Crossref | GoogleScholarGoogle Scholar |

March, J. G., Pringle, C. M., Townsend, M. J., and Wilson, A. I. (2002). Effects of freshwater shrimp assemblages on benthic communities along an altitudinal gradient of a tropical island stream. Freshwater Biology 47, 377–390.
Effects of freshwater shrimp assemblages on benthic communities along an altitudinal gradient of a tropical island stream.Crossref | GoogleScholarGoogle Scholar |

McDowall, R. M. (2008). Diadromy, history and ecology: a question of scale. Hydrobiologia 602, 5–14.
Diadromy, history and ecology: a question of scale.Crossref | GoogleScholarGoogle Scholar |

Page, T. J., and Hughes, J. M. (2007). Phylogeographic structure in an Australian freshwater shrimp largely pre-dates the geological origins of its landscape. Heredity 98, 222–231.
Phylogeographic structure in an Australian freshwater shrimp largely pre-dates the geological origins of its landscape.Crossref | GoogleScholarGoogle Scholar | 17213864PubMed |

Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update.Crossref | GoogleScholarGoogle Scholar | 22820204PubMed |

Piry, S., Luikart, G., and Cornuet, J. M. (1999). BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. The Journal of Heredity 90, 502–503.
BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., and Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |

Sodhi, N. S., Koh, L. P., Brook, B. W., and Ng, P. K. L. (2004). Southeast Asian biodiversity: an impending disaster. Trends in Ecology & Evolution 19, 654–660.
Southeast Asian biodiversity: an impending disaster.Crossref | GoogleScholarGoogle Scholar |

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.Crossref | GoogleScholarGoogle Scholar | 2513255PubMed |

Tsang, L. M., Tsoi, K. H., Chan, S. K.-F., Chan, T. K.-T., and Chu, K. H. (2017). Strong genetic differentiation among populations of the freshwater shrimp Caridina cantonensis in Hong Kong: implications for conservation of freshwater fauna in urban areas. Marine and Freshwater Research 68, 187.
Strong genetic differentiation among populations of the freshwater shrimp Caridina cantonensis in Hong Kong: implications for conservation of freshwater fauna in urban areas.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |

Werner, U. (2003). ‘Shrimps, Crayfishes, and Crabs in the Freshwater Aquarium.’ (Aquaristik: Rodgau, Germany.)

Whitlock, M. C., and McCauley, D. E. (1990). Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups. Evolution 44, 1717–1724.
Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups.Crossref | GoogleScholarGoogle Scholar | 28567815PubMed |

Weir, B. S. (1996). ‘Genetic Data Analysis II: Methods for Discrete Population Genetic Data.’ (Sinauer Associates, Inc.: Sunderland, MA, USA.)

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
| 28563791PubMed |

Wong, W. Y., Ma, K. Y., Tsang, L. M., and Chu, K. H. (2017). Genetic legacy of tertiary climatic change: a case study of two freshwater loaches, Schistura fasciolata and Pseudogastromyzon myersi, in Hong Kong. Heredity 119, 360–370.
Genetic legacy of tertiary climatic change: a case study of two freshwater loaches, Schistura fasciolata and Pseudogastromyzon myersi, in Hong Kong.Crossref | GoogleScholarGoogle Scholar | 28792491PubMed |

Wong, W. Y., Chow, L. H., Wu, T. H., Ma, K. Y., Tsang, L. M., and Chu, K. H. (2019). Conservation of freshwater wildlife in Hong Kong: a genetic perspective. Aquatic Conservation 29, 2204–2218.
Conservation of freshwater wildlife in Hong Kong: a genetic perspective.Crossref | GoogleScholarGoogle Scholar |

Woolschot, L., Hughes, J. M., and Bunn, S. E. (1999). Dispersal among populations of Caridina sp. (Decapoda: Atyidae) in coastal lowland streams, south-eastern Queensland, Australia. Marine and Freshwater Research 50, 681–688.
Dispersal among populations of Caridina sp. (Decapoda: Atyidae) in coastal lowland streams, south-eastern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Wu, T. H., Tsang, L. M., Chen, I.-S., and Chu, K. H. (2016). Multilocus approach reveals cryptic lineages in the goby Rhinogobius duospilus in Hong Kong streams: role of paleodrainage systems in shaping marked population differentiation in a city. Molecular Phylogenetics and Evolution 104, 112–122.
Multilocus approach reveals cryptic lineages in the goby Rhinogobius duospilus in Hong Kong streams: role of paleodrainage systems in shaping marked population differentiation in a city.Crossref | GoogleScholarGoogle Scholar | 27421567PubMed |

Wu, T. H., Tsang, L. M., Chow, L. H., Chen, I.-S., and Chu, K. H. (2019). Cryptic lineages and hybridization of the predaceous chub Parazacco spilurus (Actinopterygii, Cypriniformes, Xenocyprididae) in Hong Kong. Hydrobiologia 826, 99–111.
Cryptic lineages and hybridization of the predaceous chub Parazacco spilurus (Actinopterygii, Cypriniformes, Xenocyprididae) in Hong Kong.Crossref | GoogleScholarGoogle Scholar |

Yam, R. S. W., and Cai, Y. (2003). Caridina trifasciata, a new species of freshwater shrimp (Decapoda: Atyidae) from Hong Kong. The Raffles Bulletin of Zoology 51, 277–282.

Yam, R. S. W., and Dudgeon, D. (2005a). Genetic differentiation of Caridina cantonensis (Decapoda: Atyidae) in Hong Kong streams. Journal of the North American Benthological Society 24, 845–857.
Genetic differentiation of Caridina cantonensis (Decapoda: Atyidae) in Hong Kong streams.Crossref | GoogleScholarGoogle Scholar |

Yam, R. S. W., and Dudgeon, D. (2005b). Inter- and intraspecific differences in the life history and growth of Caridina spp. (Decapoda: Atyidae) in Hong Kong streams. Freshwater Biology 50, 2114–2128.
Inter- and intraspecific differences in the life history and growth of Caridina spp. (Decapoda: Atyidae) in Hong Kong streams.Crossref | GoogleScholarGoogle Scholar |

Yam, R. S. W., and Dudgeon, D. (2005c). Stable isotope investigation of food use by Caridina spp. (Decapoda : Atyidae) in Hong Kong streams. Journal of the North American Benthological Society 24, 68–81.
Stable isotope investigation of food use by Caridina spp. (Decapoda : Atyidae) in Hong Kong streams.Crossref | GoogleScholarGoogle Scholar |