Abstract
Charybdis japonica is a recently established invasive crab in north-eastern New Zealand that is native to East Asia. Since its detection in 2000, C. japonica has spread to adjacent estuaries from the introduction site at the Ports of Auckland and established 127 km north in Whangarei Harbour. We assessed the invasion history from comparisons of genetic population diversity and mixed-stock analysis from the mitochondrial control region and nuclear ribosomal internal transcribed spacer-1, to describe the invasive population’s genetic structure, infer a possible source of origin and hypothesize the composition of the founding colonists. High diversity and distinct genetic structuring were found within and among native localities from Japan, China, Taiwan and South Korea. Crabs collected at New Zealand locations (Auckland, Whangaparaoa and Whangarei) had lower diversity and were genetically homogenous. This indicated C. japonica experienced a bottleneck on colonization, but the resultant founder effects have not prevented C. japonica from establishing and spreading along New Zealand’s north-eastern coast. Among the sampled native localities, mixed-stock and multidimensional scaling analyses revealed Japan as the most likely source of the New Zealand invasion. The presence of three mitochondrial haplotypes and five ITS-1 alleles identified from the earliest samples in 2002 suggested that the founding New Zealand population descended from as few as three individuals. Evidence also suggests the occurrence of a second invasion event into Whangarei, New Zealand. Our study has provided the baseline for a more precise examination of Japan as the source of the invasive C. japonica population in New Zealand and suggests the importance of this recurring invasion pathway.
This is a preview of subscription content, access via your institution.





References
ADFG (2003) SPAM version 3.7b: statistics program for analyzing mixtures. Alaska department of fish and game, commercial fisheries division, gene conservation laboratory, Anchorage, Alaska
Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30
Archdale MV, Kuwahara O (2005) Comparative fishing trials for Charybdis japonica using collapsible box-shaped and dome-shaped pots. Fish Sci 71:1229–1235
Asif JH, Krug PJ (2012) Lineage distribution and barriers to gene flow among populations of the globally invasive marine mussel Musculista senhousia. Biol Invasions 14:1431–1444
Bax N, Williamson A, Aguero M et al (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful. Approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300
Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium: effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627
Blakeslee AMH, McKenzie CH, Darling JA et al (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891. doi:10.1111/j.1472-4642.2010.00703.x
Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45
Bossdorf O, Auge H, Lafuma L et al (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11
Byers JE, Pringle JM (2006) Going against the flow: retention, range limits and invasions in advective environments. Mar Ecol Prog Ser 313:27–41
Carson HL (1990) Increased genetic variance after a population bottleneck. TREE 5:228–230
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570
Chu KH, Li CP, Ho HY (2001) The first internal transcribed spacer (ITS-1) of ribosomal DNA as a molecular marker for phylogenetic and population analyses in Crustacea. Mar Biotechnol 3:355–361
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886. doi:10.1016/j.marpolbul.2007.03.011
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466
Crooks JA, Soule ME (1999) Lag times in populations explosions of invasive species: causes and implications. In: Sandlund OTSPJ, Viken A (eds) Invasive species and biodiversity management. Kluwer Academic Publishers, Dordrecht, pp 103–125
Dai AY, Yang S (1991) Crabs of the China seas. China Ocean Press, Beijing
Darling JA (2014) Genetic studies of aquatic biological invasions: closing the gap between research and management. Biol Invasions 17:951–971
Darling JA, Bagley MJ, Roman J et al (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007
Debevec EM, Gates RB, Masuda M, Pella J, Reynolds J, Seeb LW (2000) SPAM (version 3.2): statistics program for analyzing mixtures. J Hered 91:509–510
Dineen JF, Clark PF, Hines AH et al (2001) Life history, larval description, and natural history of Charybdis hellerii (Decapoda, Brachyura, Portunidae), an invasive crab in the western Atlantic. J Crustac Biol 21:774–805
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449
Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Facon B, Genton BJ, Shykoff J et al (2006) A general eco-evolutionary framework for understanding bioinvasions. TREE 21:130–135
Facon B, Hufbauer RA, Tayeh A et al (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427
Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253
Fowler AE, Muirhead JR, Taylor RB (2013) Early stages of a New Zealand invasion by Charybdis japonica (A. Milne-Edwards, 1861) (Brachyura: Portunidae) from Asia: behavioral interactions with a native crab species. J Crustac Biol 33:672–680
Fridley JD, Stachowicz JJ, Naeem S et al (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17
Froglia C (2012) First record of Charybdis japonica (Crustacea: Decapoda: Portunidae) in the Mediterranean Sea. Mar Biodivers Rec 5:e33
Geller J, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393
Golani D, Azzurro E, Corsini-Foka M et al (2007) Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biol Lett 3:541–545
Goldstien SJ, Schiel DR, Gemmekk NJ (2010) Regional connectivity and coastal expansion: differentiating pre-border and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885
Goldstien SJ, Dupont L, Viard F, Hallas PJ, Nishikawa T, Schiel DR, Gemmell NJ, Bishop JD (2011) Global phylogeography of the widely introduced North West Pacific ascidian Styela clava. PLoS ONE 6(2):e16755. doi:10.1371/journal.pone.0016755
Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices. Institute of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland. http://www2.unil.ch/popgen/softwares/fstat.htm
Grant WS, Leslie RW (1993) Effect of metapopulation structure on nuclear and organellar DNA variability in semi-arid environments of southern Africa. Afr J Sci 89:287–293
Grapputo A, Bisazza A, Pilastro A (2006) Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbruki). Ital J Zool 73:67–73
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704
Gust N, Inglis GJ (2006) Adaptive multi-scale sampling to determine an invasive crab’s habitat usage and range in New Zealand. Biol Invasions 8:339–353
Handley LJL, Estoup A, Evans DM et al (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428
Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79
Hedrick PW (2005) Genetics of populations, 3rd edn. Jones and Bartlett Publishers, Sudbury
Herborg LM, Weetman D, Van Oosterhout C, Hanfling B (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242
Inglis G (2001) Criteria for selecting New Zealand ports and other points of entry that have a high risk of invasion by new exotic marine organisms. Report prepared for the New Zealand Ministry of Fisheries. National Institute of Water and Atmospheric Research, Christchurch
Jukes TH, Cantor CR (1969) Evolution of protein molecules. Academic Press, New York
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Kalinowski ST, Muhlfeld CC, Guy CS, Cox B (2010) Founding population size of an aquatic invasive species. Conserv Genet 11:2049–2053
Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866
Kim KB (2001) Growth and reproduction of Charybdis japonica (A. Milne-Edwards) (Decapoda: Portunidae) in Korean waters. Ph.D., Pukyong National University
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. TREE 16:199–204
Kolbe JJ, Glor RE, Schettino LR et al (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181
Kowarik I (1995) Time lags in biological invasions with regard to the success and failure of alien species. In: Pyšek P, Prach K, Rejmanek M, Wade M (eds) Plant invasions—general aspects and special problems. SPB Academic, Amsterdam, pp 15–38
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. PNAS 104:3883–3888
Lessa EP (1990) Multidimensional analysis of geographic genetic structure. Syst Biol 39:242–252
Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasion: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Maderspacher F (2011) The benefits of bottlenecks. Curr Biol 21:R171–R173
McLay CL (1988) Brachyura and crab-like anomura of New Zealand. Leigh Laboratory Bulletin No 22. Leigh Marine Laboratory, University of Auckland, Auckland
Mooney HA, Hobbs RJ (2000) Invasive species in a changing world. Island Press, Washington
Muirhead JR, Gray DK, Kelly DW et al (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035. doi:10.1111/j.1365-294X.2008.03669.x
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Neilson ME, Wilson RR (2005) mtDNA singletons as evidence of a post-invasion genetic bottleneck in yellowfin goby Acanthogobius flavimanus from San Francisco Bay, California. Mar Ecol Prog Ser 296:197–208
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
Patti FP, Gambi MC (2001) Phylogeography of the invasive polychaete Sabella spallanzanii (Sabellidae) based on the nucleotide sequence of internal transcribed spacer 2 (ITS2) of nuclear rDNA. Mar Ecol Prog Ser 215:169–177
Pella J, Masuda M (2001) Bayesian methods for analysis of stock mixtures from genetic characters. Fish Bull 99:151–167
Pérez-Portela R, Turon X, Bishop JDD (2012) Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Mar Ecol Prog Ser 451:93–105
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Pringle JM, Blakeslee AM, Byers JE, Roman J (2011) Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range. Proc Natl Acad Sci 108:15288–15293
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201
Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc Lond 273:2453–2459
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. TREE 22:454–464
Sakai T (1976) Crabs of Japan and the adjacent seas. Kondansaha Ltd, Tokyo
Sambrook J, David WR (2001) Molecular cloning: a laboratory manual. Cold Spring Harbour Press, New York
Selkoe KA, Toonen RJ (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar Ecol Prog Ser 436:291–305
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102
Smith PJ, Webber WR, McVeagh SM et al (2003) DNA and morphological identification of an invasive swimming crab, Charybdis japonica, in New Zealand waters. N Z J Mar Freshw Res 37:753–762
Statistics New Zealand (2012) Exports and imports tables. http://www.stats.govt.nz/products–and–services/table–builder/table–builder–exportsimports.htm Accessed 7 June 2012
Stefaniak L, Zhang H, Gittenberger A et al (2012) Determining the native region of the putatively invasive ascidian Didemnum vexillum Kott, 2002. J Exp Mar Biol Ecol 422:64–71
Stepien CA, Brown JE, Neilson ME, Tum MA (2005) Genetic diversity in invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Anal 25:1043–1060
Tepolt CK, Darling JA, Bagley MJ et al (2009) European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population. Divers Distrib 15:997–1009
Tittensor DP, Mora C, Jetz W et al (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466:1098–1101
Tooman LK (2008) A genetic investigation into the population structure and invasion dynamics of Charybdis japonica (Crustacea: Decapoda: Portunidae) within New Zealand. University of Auckland, Auckland
Uwai SY, Nelson W, Neill K et al (2006) Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes origins and succession of introduced populations. Phycologia 45:687–695
Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218
Waples RS (1990) Temporal changes of allele frequency in pacific salmon - implications for mixed-stock fishery analysis. Can J Fish Aquat Sci 47:968–976
Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450
Webber R (2001) Space invaders: crabs that turn up in NZ unannounced. Seaf N Z 9(10):80–84
Wee DPC, Ng PKL (1995) Swimming crabs of the genera Charybdis de Haan, 1833, and Thalamita Latreille, 1829 (Crustacea: Decapoda: Brachyura: Portunidae) from peninsular Malaysia and Singapore. Raffles Bull Zool 43:1–128
Werle E, Schneider C, Renner M et al (1994) Convienient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res 22:4354–4355
Yatsuzuka K (1952) The metamorphosis and growth of the larvae of Charybdis japonica A. Milne Edward. Bull Jpn Soc Sci Fish 17:353–358
Acknowledgments
Funding for research was provided by the University of Auckland. Thanks to the management of the Weiti River Boat Club, Westhaven Marina, Halfmoon Bay Marina and Westpark Marina for permission to collect the Auckland samples. We are very grateful to the numerous people who contributed time and effort to the collection of potential source and non-Auckland samples, including T.Y. Chan (National Taiwan Ocean University), M.V. Archdale (Kagoshima University), S. Ahyong (Australia Museum), S.K. Lee (Seoul National University) and G. Townsend (Northland Regional Council, Whangarei). Thanks to the reviewers whose suggestions have significantly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: T. Reusch.
Reviewed by Undisclosed experts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wong, N.A., Tooman, L.K., Sewell, M.A. et al. The population genetics and origin of invasion of the invasive Asian paddle crab, Charybdis japonica (A. Milne-Edwards, 1861) (Brachyura: Portunidae) in north-eastern New Zealand. Mar Biol 163, 133 (2016). https://doi.org/10.1007/s00227-016-2906-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2906-y
Keywords
- Native Locality
- Genetic Bottleneck
- Invasive Population
- Mitochondrial Control Region
- Zealand Population