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Caprella Mutica in the Southern Hemisphere: Atlantic Origins, Distribution, and Reproduction of an Alien Marine Amphipod in New Zealand

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Caprella Mutica in the Southern Hemisphere: Atlantic Origins, Distribution, and Reproduction of an Alien Marine Amphipod in New Zealand Vol. 7: 249–259, 2009 AQUATIC BIOLOGY Published online November 19, 2009 doi: 10.3354/ab00197 Aquat Biol OPEN ACCESS Caprella mutica in the Southern Hemisphere: Atlantic origins, distribution, and reproduction of an alien marine amphipod in New Zealand Kate J. Willis1,*, Chris M. C. Woods1, Gail V. Ashton2 1National Institute for Water and Atmospheric Research, PO Box 8602, Riccarton, Christchurch, New Zealand 2Smithsonian Environmental Research Centre, 3150 Paradise Drive, Tiburon, California 94920, USA ABSTRACT: The caprellid amphipod Caprella mutica, a native of northeast Asia, was first detected in the Southern Hemisphere in the Port of Timaru, New Zealand, in 2002. It has since become estab- lished in the Port of Lyttelton and at 2 aquaculture sites in the Marlborough Sounds in New Zealand. Direct sequencing of C. mutica mitochondrial DNA (cytochrome c oxidase subunit I gene) identified 3 haplotypes: 1 unique to New Zealand and 2 previously found in non-native Atlantic populations. Higher haplotype diversity and lower FST distances between the Port of Lyttelton and global popula- tions suggest Lyttelton may be the introduction site in New Zealand. C. mutica populations were sampled on 7 occasions, primarily in winter, and densities generally exceeded 10 000 ind. m–2, con- trasting with the winter declines seen in native and European populations. Sex ratios were generally close to 0.5 and the proportion of brooding females ranged from 0 to 98%. In the Marlborough Sounds, juveniles comprised 32 to 38% of the population regardless of season, brooding females were present throughout the year and males were dominant in winter. Population structure and adult size in the Port of Lyttelton differed with habitat type in August 2008; densities were higher, adults significantly larger on floating than on fixed structures and juveniles and brooding females domi- nated on vessel hulls. Given the high level of anthropogenic activity and connectivity between coastal locations, it is likely that C. mutica will continue to spread in New Zealand. KEY WORDS: Caprellid amphipod · Bioinvasion · COI gene · Population genetics · Population biology · Dispersal · Hull fouling Resale or republication not permitted without written consent of the publisher INTRODUCTION Europe has been rapid and represents a range exten- sion of ~1200 km along the west coast of Norway and The caprellid amphipod Caprella mutica Schurin, ~1000 km to the west coast of Ireland (Cook et al. 2007) 1935 is indigenous to sub-boreal waters of northeast Asia from its first recorded location in The Netherlands in (Peter the Great Bay, Vladivostok, Russia) and was iden- 1995 (Platvoet et al. 1995). Ashton et al. (2008a) reported tified from Possjet Bay, Russia (Vassilenko 1967) and the presence of C. mutica in the Aleutian Islands of Akkeshi Bay, Japan (Arimoto 1976). The first reports of Alaska, where it may have been present since at least C. mutica outside its native habitat were from the Pacific 2002. C. mutica is the first reported non-indigenous and Atlantic coasts of North America in the 1970s (Carl- marine species (NIMS) in the Aleutian Archipelago ton 1979) and 1980s (Marelli 1981, Cohen & Carlton (Ashton et al. 2008a). The global distribution of C. mutica 1995). Reviews of its global distribution indicate that, can be attributed to shipping, aquaculture activities and in the last 40 yr, C. mutica has spread throughout the recreational boating, with localised dispersal on drifting northern hemisphere along the coasts of Europe, North macroalgae (Ashton 2006). Carlton (1979) suggested that America and Canada (Ashton et al. 2007, Cook et C. mutica arrived on the Pacific and Atlantic coasts of al. 2007, Frey et al. 2009). Dispersal of C. mutica within North America either as a result of numerous, indepen- *Email: [email protected] © Inter-Research 2009 · www.int-res.com 250 Aquat Biol 7: 249–259, 2009 dent cross-oceanic introductions with oyster spat, or from The development of a surveillance programme for small-scale transport following its first introduction NIMS in New Zealand by the Ministry of Fisheries (Carlton 1996). Direct sequencing of mitochondrial DNA Biosecurity New Zealand, with the first baseline sur- indicates that C. mutica was introduced to Europe either veys undertaken in 2001, has provided a unique directly from Asia or from the Atlantic coast of North opportunity to establish a baseline distribution of America (Ashton et al. 2008b). The presence of haplo- Caprella mutica. Since the baseline surveys, its spread types common to both Atlantic coastlines indicates trans- has been monitored during regular biosecurity activi- Atlantic transport routes and/or the same source popula- ties in ports and marinas throughout New Zealand, and tions. Non-native populations on the Pacific coast of opportunistically through other aquaculture-related North America are genetically distinct, indicating a route research. We present information on the distribution, of introduction independent from that of the Atlantic origins and population biology of C. mutica in New (Ashton et al. 2008b). Zealand. In non-native European and Canadian populations on artificial structures, densities in excess of 10 000 ind. m–2, in summer (Boos 2009, Frey et al. 2009, Ashton et MATERIALS AND METHODS al. in press), are considerably higher than those re- ported from natural near-bottom habitat in Caprella Distribution of Caprella mutica in New Zealand. To mutica’s native range in northeast Asia (Fedotov 1991, establish the baseline distribution of C. mutica in New Vassilenko 2006). During winter in native and Euro- Zealand ports and marinas, we reviewed the species pean populations, reproduction is curtailed and popu- lists in the baseline survey reports for 13 ports and 3 lation densities are significantly reduced or possibly marinas surveyed between 2001 and 2005 for native absent in some locations. and non-native marine species (Fig. 1a). Records of the Fig. 1. (A) Commercial shipping ports (P) and marinas (M) in New Zealand where baseline surveys for native and non-native spe- cies have been conducted. Ports surveyed in summer 2001–2002 and resurveyed in summer 2004–2005 are indicated in bold; those surveyed in summer 2002–2003 are indicated in plain text. Marinas at Auckland, Opua and Whangarei were surveyed in 2002–2003. (B) Distribution of marine farm biofouling sampling stations in Pelorus Sound, Marlborough Sounds, New Zealand. (d) Positive recordings of Caprella mutica (year of first detection); (+) negative recordings Willis et al.: Caprella mutica in the Southern Hemisphere 251 presence of C. mutica in the Port of Lyttleton are re- (GenBank accession nos. DQ466220–466523; Ashton ported from ongoing surveillance programmes for NIMS et al. 2008b). Novel unique sequences were deposited in ports and marinas around New Zealand. In the with GenBank. C. equilibra and C. acanthogaster Marlborough Sounds, the presence or absence of (accession nos. DQ466519–466521) were used as out- C. mutica is reported from aquaculture sites visited groups for the phylogenetic analyses. Sequences were during research investigating fouling development on edited and aligned using Sequencher 4.8 (Gene and around Greenshell™ mussel farms in 2007 and Codes) and trimmed to a length of 533 bp. 2008 (Fig. 1b). Modeltest 3.7 (Posada & Crandall 1998) was used to Origins and dispersal. Specimens of Caprella mutica, determine the appropriate model parameters for maxi- collected in April 2008 from floating tyre fenders in the mum likelihood (ML) analysis in PAUP* 4.0b10 (Swof- Port of Lyttelton in June 2008 and from mussel lines in ford 2002). The Hasegawa-Kishino-Yano + gamma (Γ) Waihinau Bay, Marlborough Sounds, were immedi- model (–ln L = 1889.5066 [AIC]; base frequencies set ately preserved in 99% ethanol. Individuals were con- to A = 0.3684, C = 0.1674, G = 0.2062, T = 0.2580; firmed to be C. mutica (Arimoto 1976) by stereomicro- transition/tranversion (Ti/tv) ratio = 6.2804; gamma scope. DNA was extracted from whole animals using a correction = 0.1573) was found to be the best fit to Qiagen BioSprint 96 DNA Blood Kit. All genetic analy- the data; all other options in PAUP* remained as sis was conducted at the Smithsonian’s Laboratories of default for the ML heuristic analyses. Bayesian analy- Analytical Biology in Suitland, Maryland, USA. sis was implemented using MrBayes v.3.1.2 (Ronquist A ~550 bp fragment of the mitochondrial cytochrome & Huelsenbeck 2003). ML bootstrap analyses were c oxidase subunit I (mtDNA COI) gene was amplified conducted with 500 replicates (Felsenstein 1985) using using the primers COI4F (5’-AAC AYY TAT TYT GAT the same settings as the heuristic search in GARLI TCT TTG GTC ACC C-3’) and COI2R (5’-GGR TAR (Zwickl 2006). Arlequin 3.0 (Excoffier et al. 2005) was TCW GAR TAW CGN CGA GGT ATC CC-3’) (modi- used to calculate pairwise FST measures between sites. fied from Ashton et al. 2008b). The PCR (Saiki et al. Total variation within the non-native populations was 1988) was run on an MJ Research Tetrad Thermal analysed by including all geographically isolated pop- Cycler (Bio-Rad Laboratories). The 10 µl reaction vol- ulations independently in an analysis of molecular ume consisted of 1 µl (~20 to 50 ng) DNA, 1× PCR variance (AMOVA). buffer (BioLine), 1.5 mM MgCl2 (BioLine), 0.5 mM Population biology. Individuals of Caprella mutica deoxynucleoside triphosphate (dNTP) mix (BioLine), were collected from between 0 and 5 m depth on 7 0.3 µM of each primer and 0.5 U Taq DNA polymerase occasions between December (summer) 2006 and (BioLine). Thermal cycling conditions were: 95°C for August (winter) 2008 (Table 1) from boat hulls, fixed 5 min followed by 35 cycles of denaturation at 95°C for mooring piles and floating tyre fenders in Magazine 30 s, annealing at 52°C for 30 s and extension at 72°C Bay Marina in Lyttleton Harbour (December 2006) and for 45 s, followed by a final extension at 72°C for 3 min the Port of Lyttelton (June, August and November (modified from Witt & Hebert 2000).
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