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Bilge water as a vector for the spread of marine pests: a morphological, metabarcoding and experimental assessment

Authors:
Lauren M. Fletcher at Cawthron Institute
Lauren M. Fletcher
Anastasija Zaiko at Sequench Ltd
Anastasija Zaiko
  • Sequench Ltd
Javier Atalah at Cawthron Institute
Javier Atalah
Ingrid Richter at Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute
Ingrid Richter
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Vessel movements are considered the primary anthropogenic pathway for the secondary spread of marine non-indigenous species. In comparison to the well-studied mechanisms of hull fouling and ballast water, the importance of bilge water for domestic and cross-regional spread of non-indigenous species is largely unknown and has the potential to compromise the overall effectiveness of biosecurity management actions. In this study, the diversity and abundance of biological material contained in bilge water from 30 small vessels (<20 m) was assessed using traditional and molecular identification tools (metabarcoding of the 18S rRNA gene). Laboratory-based studies were also used to investigate the relationship between voyage duration and propagule success. A large taxonomic diversity in organisms was detected, with 118 and 45 distinct taxa identified through molecular and morphological analyses, respectively. Molecular techniques identified five species recognised as non-indigenous to the study region in 23 of the 30 bilge water samples analysed. Larvae and fragments passed through an experimental bilge pump system relatively unharmed. Time spent in the bilge sump was found to affect discharge success, particularly of short-lived and sensitive larvae, but survival for 3 days was observed. Our findings show that bilge water discharges are likely to pose a non-negligible biosecurity threat and that further research to identify high-risk vessel operating profiles and potential mitigation measures are warranted.
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ORIGINAL PAPER
Bilge water as a vector for the spread of marine pests:
a morphological, metabarcoding and experimental
assessment
Lauren M. Fletcher .Anastasija Zaiko .Javier Atalah .Ingrid Richter .
Celine M. Dufour .Xavier Pochon .Susana A. Wood .Grant A. Hopkins
Received: 4 January 2017 / Accepted: 18 June 2017 / Published online: 21 June 2017
ÓSpringer International Publishing AG 2017
Abstract Vessel movements are considered the
primary anthropogenic pathway for the secondary
spread of marine non-indigenous species. In compar-
ison to the well-studied mechanisms of hull fouling
and ballast water, the importance of bilge water for
domestic and cross-regional spread of non-indigenous
species is largely unknown and has the potential to
compromise the overall effectiveness of biosecurity
management actions. In this study, the diversity and
abundance of biological material contained in bilge
water from 30 small vessels (\20 m) was assessed
using traditional and molecular identification tools
(metabarcoding of the 18S rRNA gene). Laboratory-
based studies were also used to investigate the
relationship between voyage duration and propagule
success. A large taxonomic diversity in organisms was
detected, with 118 and 45 distinct taxa identified
through molecular and morphological analyses,
respectively. Molecular techniques identified five
species recognised as non-indigenous to the study
region in 23 of the 30 bilge water samples analysed.
Larvae and fragments passed through an experimental
bilge pump system relatively unharmed. Time spent in
the bilge sump was found to affect discharge success,
particularly of short-lived and sensitive larvae, but
survival for 3 days was observed. Our findings show
that bilge water discharges are likely to pose a non-
negligible biosecurity threat and that further research
to identify high-risk vessel operating profiles and
potential mitigation measures are warranted.
Keywords Anthropogenic spread Dispersal High-
throughput sequencing Non-indigenous species
Pathway management Translocation
Introduction
Non-indigenous species (NIS) can dramatically
change the composition and functioning of native
biological communities, as well as impact on local
Electronic supplementary material The online version of
this article (doi:10.1007/s10530-017-1489-y) contains supple-
mentary material, which is available to authorized users.
L. M. Fletcher (&)A. Zaiko J. Atalah
I. Richter C. M. Dufour X. Pochon
S. A. Wood G. A. Hopkins
Cawthron Institute, Private Bag 2, Nelson 7010, New
Zealand
e-mail: lauren.fletcher@cawthron.org.nz
A. Zaiko
Marine Science and Technology Center, Klaipeda
University, H. Manto 84, 92294 Klaipeda, Lithuania
X. Pochon
Institute of Marine Science, University of Auckland,
Private Bag 92019, Auckland 1142, New Zealand
S. A. Wood
Environmental Research Institute, University of Waikato,
Private Bag 3105, Hamilton 3240, New Zealand
123
Biol Invasions (2017) 19:2851–2867
DOI 10.1007/s10530-017-1489-y
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Its role as a potential transporter was already demonstrated for several invasive algae [23,24], and for the invasive ascidian Didemnum vexillum [25]. To date, studies on the transport of NIS through bilge waters are very few, although their role as NIS vectors is widely recognized [26,27]. These authors, investigating the taxonomic diversity in bilge water samples with different techniques (morphological and molecular), identified the presence of NIS and demonstrated the important contribution of such studies to a better understanding of the potential spread of marine organisms. ...
... On the other hand, it was demonstrated to be an interesting tool to complement biodiversity assessment. Its application to bilge water species composition seems to be a promising tool in NIS identification, as highlighted by [27,36]. Fletcher et al. [27] reported that morphological assessments of bilge water samples provided less taxonomic resolution compared to metabarcoding, and 70% of the identified taxa were putative NIS, supporting the usefulness of the method. ...
... Its application to bilge water species composition seems to be a promising tool in NIS identification, as highlighted by [27,36]. Fletcher et al. [27] reported that morphological assessments of bilge water samples provided less taxonomic resolution compared to metabarcoding, and 70% of the identified taxa were putative NIS, supporting the usefulness of the method. On the other hand, Ponchon et al. [36], focusing on the biodiversity patterns of dead/alive organisms in bilge water by metabarcoding analysis of co-extracted eDNA and eRNA, concluded that the presence of an OTU from a NIS in the eDNA-only group may assist in early detection, although they recommend further research to improve understanding of the persistence of RNA in the environment. ...
eDNA Metabarcoding Analysis as Tool to Assess the Presence of Non-Indigenous Species (NIS): A Case Study in the Bilge Water
Article
Full-text available
One of the most important causes of biodiversity loss are non-indigenous species (NIS), in particular invasive ones. The dispersion of NIS mainly depends on anthropogenic activities such as maritime traffic, which account for almost half of the total NIS introduction in the European seas, as reported by the European Environmental Agency. For this reason, NIS management measures are mainly focused on commercial ports (i.e., ballast water management and Marine Strategy Framework Directive monitoring), underestimating the role of marinas and tourist harbors; these host small vessels (<20 m), such as recreational, fishery, and sail ones without ballast waters, but are also responsible for NIS arrival and spread through the bilge water as well as from hull fouling. With the aim of paying attention to marinas and tourist harbors and validating an innovative molecular methodology for NIS surveillance and monitoring, in the present work, eDNA metabarcoding of cytochrome oxidase subunit I (COI) was applied to both bilge waters and adjacent ones to assess species composition and particularly NIS presence. A total of 140 OTUs/species with extra-Mediterranean distribution were found in the bilge samples; several of these are most likely ascribed to food contamination (e.g., Salmo salar). Excluding food contamination species, twelve of these found in the bilge waters were already known as NIS in the Mediterranean Sea, belonging to algae, mollusks, crustaceans, annelids, echinoderms, and fishes. Nine of these species are new to Italian waters. The results obtained in the present work support the importance of NIS monitoring in marinas and small harbors, particularly in the bilge waters, through eDNA metabarcoding, having detected several potential NIS that otherwise would not have been discovered.
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... On the other hand, high throughput sequencing (HTS) techniques -such as metabarcoding -are ideally placed to process large volumes of samples, to simultaneously provide identifications for both target and non-target taxa. For the past decade, most studies focusing on detection of invertebrates for biosecurity using metabarcoding have relied on short-read sequencing platforms such as Illumina MiSeq (Comtet et al. 2015;Batovska et al. 2016;Fletcher et al. 2017;Piper et al. 2019;Martoni et al. 2023 a,b). These works relied on the fact that short-read sequencing platforms have a generally much lower error rate compared to longer-read sequencers such as Oxford Nanopore Technologies (ONT) MinION (Piper et al. 2019). ...
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... Entrainment is complex, with many interacting factors influencing its success and magnitude, including the life stage, reproductive mode and behaviour of the species interacting with the vessel, vessel characteristics and movement patterns, and environmental factors. Generally, NIS can be entrained by vessels through biofouling of submerged surfaces (Davidson et al., 2009), via uptake in ballast water or bilge water (Fletcher et al., 2017;Hewitt et al., 2009b), or via entanglement in anchoring gear or submerged equipment (Clarke Murray et al., 2011). Several thousand species are entrained globally each day just within ballast water (Carlton, 1999), with single vessels able to entrain several hundred genera (Ardura et al., 2021). ...
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Full-text available
  • Feb 2024
  • SCI TOTAL ENVIRON
Nonindigenous marine species are impacting the integrity of marine ecosystems worldwide. The invasion rate is increasing, and vessel traffic, the most significant human-assisted transport pathway for marine organisms, is predicted to double by 2050. The ability to predict the transfer of marine species by international and domestic maritime traffic is needed to develop cost-effective proactive and reactive interventions that minimise introduction, establishment and spread of invasive species. However, despite several decades of research into vessel-mediated species transfers, some important knowledge gaps remain, leading to significant uncertainty in model predictions, often limiting their use in decision making and management planning. In this review, we discuss the sequential ecological process underlying human-assisted biological invasions and adapt it in a marine context. This process includes five successive stages: entrainment, transport, introduction, establishment, and the subsequent spread. We describe the factors that influence an organism's progression through these stages in the context of maritime vessel movements and identify key knowledge gaps that limit our ability to quantify the rate at which organisms successfully pass through these stages. We then highlight research priorities that will address these knowledge gaps and improve our capability to manage biosecurity risks at local, national and international scales. We identified four major data and knowledge gaps: (1) quantitative rates of entrainment of organisms by vessels; (2) the movement patterns of vessel types lacking maritime location devices; (3) quantifying the release (introduction) of organisms as a function of vessel behaviour (e.g. time spent at port); and (4) the influence of a species' life history on establishment success, for a given magnitude of propagule pressure. We discuss these four research priorities and how they can be addressed in collaboration with industry partners and stakeholders to improve our ability to predict and manage vessel-mediated biosecurity risks over the coming decades.
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... Beyond aquaculture, vessels have been a prolific vector for international and domestic spread of marine pests and pathogens more broadly (Georgiades et al. 2021;Ashton et al. 2022;Pagenkopp Lohan et al. 2022). Ships and boats routinely transfer biofouling, ballast water, and bilge water, often with a range of microbes and potential parasites entrained (Ruiz et al. 2000;Davidson et al. 2018, Fletcher et al. 2017Pagenkopp Lohan et al. 2020). ...
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... Therefore, outside harbor stations showed expectedly lower diversity for NIS eDNA signal, likely receiving incursions via secondary spread from harbor hotspots and creating a 'hub-and-spoke network' 44 . Recreational boating between marinas and nature sites effectively facilitate the local spread of NIS and define distribution patterns 45,46 . The crab Pilumnus minutus, frequenctly recorded to be transported through sea chests 47 and the polychaete worm Polydora cornuta were prevalent for 18S rRNA gene in coastal water stations. ...
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Aotearoa New Zealand’s Northern region is a major gateway for the incursion and establishment of non-indigenous species (NIS) populations due to high numbers of recreational and commercial vessels. This region also holds a unique marine ecosystem, home to many taonga (treasured) species of cultural and economic importance. Regular surveillance, eradication plans and public information sharing are undertaken by local communities and governmental organizations to protect these ecosystems from the impact of NIS. Recently, considerable investments went into environmental DNA (eDNA) research, a promising approach for the early detection of NIS for complementing existing biosecurity systems. We applied eDNA metabarcoding for elucidating bioregional patterns of NIS distributions across a gradient from harbors (NIS hotspots) to open seas (spreading areas). Samples were collected during a research cruise sailing across three Aotearoa New Zealand harbors, Waitematā, Whangārei and Pēwhairangi (Bay of Islands), and their adjacent coastal waters. The small-ribosomal subunit (18S rRNA) and mitochondrial cytochrome c oxidase I (COI) genes were screened using the online Pest Alert Tool for automated detection of putative NIS sequences. Using a probabilistic modelling approach, location-dependent occupancies of NIS were investigated and related to the current information on species distribution from biosecurity surveillance programs. This study was collaboratively designed with Māori partners to initiate a model of co-governance within the existing science system.
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... The majority of NIS, which use the recreational boats as the main vector in marinas, show affinity for the AHS of the hull of the boats (Fletcher et al., 2017). For that reason, it is expected that these species may colonize similar habitats, as the lateral surface of pontoons, instead of soft substrates. ...
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Introduction: Update of the Global Maritime Transport and Ballast Water Management Book First Edition
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