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Rediscovery of a native freshwater shrimp, Neocaridina denticulata, and expansion of an invasive species in and around Lake Biwa, Japan: genetic and morphological approach

Abstract

Invasive species prevention involves avoiding two aspects: introduction and secondary spread. The latter is essential in places that can become hubs for spreading invasive species. Lake Biwa, the largest lake in Japan, is an important area for biodiversity and fisheries. However, several invasive fish and crustaceans were established in the lake last century. One of the conservation problems in the Lake Biwa region is the unresolved suspicion that the native freshwater shrimp Neocaridina denticulata have been replaced with alien Neocaridina species. To verify whether exotic species have replaced the native Neocaridina population in this region, we estimated the population structure of Neocaridina spp., collected from 19 sites in and around Lake Biwa, based on genome-wide SNPs and mitochondrial DNA. The three detected genetic clusters were characterized by quantitative analysis of multiple morphological traits. Two clusters were identified as non-native N. davidi and the other as native N. denticulata. However, species discrimination based solely on morphological analysis was difficult, highlighting the importance of genetic analysis. We rediscovered the native populations in the region for the first time in a century; however, in 11 sites, the invasive species were dominant. These findings suggest that the native populations are in a critical situation. Furthermore, fishery resource stocking throughout Japan from Lake Biwa can cause the secondary spread of the invasive shrimps from the lake, acting as a hub, to other parts of the country.

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Acknowledgements

We are grateful to Masaki Asano, Shota Kunimatsu, Eugene Agyeman and Masami Hashiguchi for their cooperation in the fieldwork; Takafumi Nakano for registering the specimens and supporting the research in KUZ; Shoko Matsui for supporting the MIG-seq primer selection process; Yuichi Kano for registering the photographs to the database; Keiichi Kakui and Tomoyuki Komai for letting us use their beautiful illustrations; Katsutoshi Watanabe for giving helpful comments to our manuscript.

Funding

This work was partly supported by Grant-in-Aid for JSPS Research Fellow Grant Number JP19J23130 to Yusuke Fuke.

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Contributions

All authors contributed to the study conception and design, sampling, morphometry, and manuscript preparation. All statistical analyses were performed by Keisuke Onuki. Primer development and genetic analysis were performed by Yusuke Fuke. All authors read and approved the final manuscript.

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Correspondence to Keisuke Onuki or Yusuke Fuke.

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10592_2022_1467_MOESM1_ESM.eps

Supplementary file1 (EPS 3031 kb) Supplemental Figure 1 Phylogenetic relationships of the Neocaridina species based on the 596 bp mtDNA COI region. Tree estimation was performed by the maximum likelihood method using IQ-TREE2 based on the HKY+F+I+G4 model. The numbers in each node represent the support values or posterior probability estimated by SH-like approximate likelihood ratio test 1000 times, approximate Bayes test, and the ultrafast bootstrap 1000 times. The bold tip labels represent samples with evidence of identification by morphology in previous studies or this study. The blue tip labels represent haplotypes detected in this study

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Supplementary file3 (XLSX 13 kb)

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Onuki, K., Fuke, Y. Rediscovery of a native freshwater shrimp, Neocaridina denticulata, and expansion of an invasive species in and around Lake Biwa, Japan: genetic and morphological approach. Conserv Genet 23, 967–980 (2022). https://doi.org/10.1007/s10592-022-01467-1

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  • DOI: https://doi.org/10.1007/s10592-022-01467-1

Keywords

  • Invasive species
  • Lake Biwa
  • MIG-seq
  • Mitochondrial DNA
  • Neocaridina
  • Secondary spread