Pseudocochlodinium profundisulcus Resting Cysts Detected in the Ballast Tank Sediment of Ships Arriving in the Ports of China and North America and the Implications in the Species' Geographic Distribution and Possible Invasion.

Lixia Shang,Zhangxi Hu,Yunyan Deng,Yuyang Liu,Wen Tian,Yangchun Han,Ying Zhong Tang,Xinyu Zhai

doi:10.3390/ijerph19010299

Abstract

Over the past several decades, much attention has been focused on the dispersal of aquatic nonindigenous species via ballast tanks of shipping vessels worldwide. The recently reclassified dinoflagellate Pseudocochlodinium profundisulcus (previously identified as Cochlodinium sp., Cochlodinium geminatum, or Polykrikos geminatus) was not reported in China until 2006. However, algal blooming events caused by this organism have been reported almost every year since then in the Pearl River Estuary and its adjacent areas in China. Whether P. profundisulcus is an indigenous or an invasive species has thus become an ecological question of great scientific and practical significance. In this study, we collected the sediments from ballast tanks of ships arriving in the ports of China and North America and characterized dinoflagellate resting cysts via a combined approach. We germinated two dark brownish cysts from the tank of an international ship (Vessel A) arriving at the Jiangyin Port (China) into vegetative cells and identified them as P. profundisulcus by light and scanning electron microscopy and phylogenetic analyses for partial LSU rDNA sequences. We also identified P. profundisulcus cyst from the ballast tank sediment of a ship (Vessel B) arriving in the port of North America via single-cyst PCR and cloning sequencing, which indicated that this species could be transported as resting cyst via ship. Since phylogenetic analyses based on partial LSU rDNA sequences could not differentiate all sequences among our cysts from those deposited in the NCBI database into sub-groups, all populations from China, Australia, Japan, and the original sources from which the cysts in the two vessels arrived in China and North America were carried over appeared to share a very recent common ancestor, and the species may have experienced a worldwide expansion recently. These results indicate that P. profundisulcus cysts may have been extensively transferred to many regions of the world via ships’ ballast tank sediments. While our work provides an exemplary case for both the feasibility and complexity (in tracking the source) of the bio-invasion risk via the transport of live resting cysts by ship’s ballast tanks, it also points out an orientation for future investigation.

Highlights

A ship’s ballast tanks carrying ballast water and sediments were proved to be responsible for the dispersal of toxic phytoplankton worldwide [1,2,3,4,5,6,7]
There were usually more dinoflagellate cells within ballast sediments compared to that in ballast water, e.g., >300 million Alexandrium cysts existing in sediments of one single ballast tank in a ship entering an Australian port [1], which implied the great threat of ballast tank sediments to marine ecosystem, human health, and economic development [1,10,17,18]
A resting cyst of P. profundisulcus in the Sample NA collected from a double-bottom tank of the Vessel B entering Windsor Port was isolated and observed, which was yellowish-brown, irregularly round with lobed ornaments around the cyst wall (identified as Polykrikos geminatum, see picture in Shang et al (2019) [10])

Summary

Introduction

A ship’s ballast tanks carrying ballast water and sediments were proved to be responsible for the dispersal of toxic phytoplankton worldwide [1,2,3,4,5,6,7]. A large number of studies have focused on the introduction potency of ballast sediments, which can be accumulated in the bottom of the tanks and are difficult to be washed off [8,9,10]. Gymnodiniales are the major order of dinoflagellates, many species of which have ecological significance due to the ability to form harmful algal blooms (HABs). Pseudocochlodinium profundisulcus (reported as Cochlodinium sp., Cochlodinium geminatum or Polykrikos geminatus [19]) was firstly reported to form bloom in April 2006 in the coastal water of Zhuhai, Guangdong province, China [20]. Blooms caused by this species have occurred frequently in the South China Sea, whereas blooming areas from several to 300 km have the maximum cell density up to 4.13 × 107 cells·L−1 [21,22,23,24,25]

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Discussion

Conclusion