Invasion Pathway of the Ctenophore Mnemiopsis leidyi in the Mediterranean Sea

Sara Ghabooli,Hugh J. MacIsaac,Tamara A. Shiganova,Stefano Piraino,Dror L. Angel,Veronica Fuentes,Melania E. Cristescu,Elizabeta Briski,Delphine Thibault-Botha,Erik V. Thuesen

doi:10.1371/journal.pone.0081067

Abstract

Gelatinous zooplankton outbreaks have increased globally owing to a number of human-mediated factors, including food web alterations and species introductions. The invasive ctenophore Mnemiopsis leidyi entered the Black Sea in the early 1980s. The invasion was followed by the Azov, Caspian, Baltic and North Seas, and, most recently, the Mediterranean Sea. Previous studies identified two distinct invasion pathways of M. leidyi from its native range in the western Atlantic Ocean to Eurasia. However, the source of newly established populations in the Mediterranean Sea remains unclear. Here we build upon our previous study and investigate sequence variation in both mitochondrial (Cytochrome c Oxidase subunit I) and nuclear (Internal Transcribed Spacer) markers in M. leidyi, encompassing five native and 11 introduced populations, including four from the Mediterranean Sea. Extant genetic diversity in Mediterranean populations (n = 8, N a = 10) preclude the occurrence of a severe genetic bottleneck or founder effects in the initial colonizing population. Our mitochondrial and nuclear marker surveys revealed two possible pathways of introduction into Mediterranean Sea. In total, 17 haplotypes and 18 alleles were recovered from all surveyed populations. Haplotype and allelic diversity of Mediterranean populations were comparable to populations from which they were likely drawn. The distribution of genetic diversity and pattern of genetic differentiation suggest initial colonization of the Mediterranean from the Black-Azov Seas (pairwise F ST = 0.001–0.028). However, some haplotypes and alleles from the Mediterranean Sea were not detected from the well-sampled Black Sea, although they were found in Gulf of Mexico populations that were also genetically similar to those in the Mediterranean Sea (pairwise F ST = 0.010–0.032), raising the possibility of multiple invasion sources. Multiple introductions from a combination of Black Sea and native region sources could be facilitated by intense local and transcontinental shipping activity, respectively.

Highlights

Introduction of non-indigenous species (NIS) beyond their native range is considered a principal threat to marine ecosystems worldwide [1]
We found twelve different haplotypes in native populations, all of which were present in introduced populations except for Ml01 from Peninsula Valdes, the single private haplotype at this site
Out of eight haplotypes observed in the Mediterranean Sea, only Ml11 was not recovered from native populations in North America

Summary

Introduction

Introduction of non-indigenous species (NIS) beyond their native range is considered a principal threat to marine ecosystems worldwide [1]. The rate of such introductions accelerated in the past few decades in conjunction with increased maritime shipping and global trade [2,3]. Genetic analyses have revealed pathways of M. leidyi introduction into major Eurasia Seas [32,33,34]. M. leidyi entered the Black Sea via ships’ ballast water from the Gulf of Mexico region. Secondary introduction into Caspian Sea likely occurred through ballast water discharged by a vessel after transiting the Volga-Don canal [51].

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Results

Conclusion