A synthesis of marine invasive species research and management in the ROPME Sea Area

The Regional Organization for the Protection of the Marine Environment (ROPME) was formed in 1978 as an inter-governmental organization to coordinate efforts undertaken by Bahrain, Iran, Iraq, Kuwait, Oman, Qatar, Saudi Arabia and the United Arab Emirates to protect the marine environment in the Arabian Gulf, the Gulf of Oman and the open coastal waters of Oman in the Arabian Sea (Naqvi, 2009; Figure 1). With production and export of crude oil and natural gas being the mainstay of the economies of the ROPME countries, initial objectives centred on assessments of oil pollution, as well as pollution from land-based sources associated with industrialization and urbanization (UNEP, 1983). The ROPME Sea Area provides about 50% of world energy requirements, which also makes it the largest recipient of ships' ballast water in the world with more than 45,000 vessels (20,000 oil tankers) visiting the region annually, the majority of which will discharge ballast water to load cargo for export (Globallast, 2002; IMO, 2009a). The volume of ballast water discharged annually in the ROPME Sea Area is not readily available, although Endresen et al. (2004) estimated 194 million tonnes of ballast water were discharged in the Middle East by large crude oil carriers in 1996.As a primary location for ballast water discharges globally, one presumes that the ROPME Sea Area is at greatest risk of aquatic introductions, however, ballast volume is not necessarily a good indicator of the abundance or diversity of species introduced (Ruiz et al., 2013). Further, in addition to introduction effort, it is widely recognized that both environmental conditions and biological community interactions are important determinants of establishment success (Colautti et al., 2006; Blackburn et al., 2011). The ROPME Sea Area is a semi-enclosed water body with intensely hot summers and short cool winters, extensive air and water temperature fluctuations (annual surface temperature range 12 to 35°C), relatively high salinity (up to 70 parts per thousand along the southernmost parts of the inner Gulf), high turbidity and low exchange of water with the open sea (IMO, 2009b; Naqvi, 2009). The potential for survival and establishment of introduced aquatic species arriving from numerous locations around the world under these conditions has not been explored to date.The objective of this article is to review the marine invasive species activities undertaken in the ROPME Sea Area, from early awareness initiatives to recent science and management activities. We searched for results of projects published in the primary scientific literature and in the gray literature published by the International Maritime Organization, and reviewed the presentations and papers contributed to the international conference Marine Invasive Species: Management of ballast water and other vectors held in Muscat, Oman, in February 2014. Finally, we present an outlook of potential activities that could be undertaken to advance management of marine invasive species in the ROPME Sea Area.Early activities associated with marine invasive species were initiated under the auspices of the Global Ballast Water Management Programme (GloBallast), a joint initiative of the International Maritime Organization (IMO) and the United Nations Development Programme Global Environment Facility (UNDP-GEF). Globallast was established to reduce the transfer of harmful marine species in ships' ballast water by helping developing countries to implement voluntary ballast water management measures and to prepare for the implementation of the international Convention for the Control and Management of Ships' Ballast Water and Sediments (IMO, 2000). Initially, GloBallast operated through six Demonstration Sites representing the main developing regions of the world, including Khark Island, Iran. Activities in Iran included a ballast water risk assessment for the import and export of invasive marine species (Clarke et al., 2003). The work was initiated in January 2002, and a Regional Conference on Ballast Water Control and Management was held in Tehran (Iran) in June 2002.The objectives of the 2002 Conference were fourfold: (1) to raise awareness about invasive marine species and ballast water as a primary vector and the related Globallast activities in Iran; (2) to ascertain the status of invasive marine species and ballast water management arrangements in the ROPME Sea Area; (3) to evaluate and approve a draft Regional Action Plan; (4) to agree on a mechanism to implement and coordinate regional activities (Globallast, 2002). The Conference assembled approximately 30 participants, comprised of maritime and environmental experts from the ROPME member states and representatives from regional shipping and oil industries as well as ROPME and Globallast. In only three days, it was noted that the issue of marine invasive species was only just beginning to be of concern for ROPME member states but the area may be characterized as extremely high risk due to the volume of oil transportation passing through the region (Globallast, 2002). Due to the inextricable connectivity of each State's coastal marine environment, it was unanimously agreed that individual efforts would be futile without regional cooperation and coordination of ballast water control and management activities (Globallast, 2002). Finally, the Conference adopted a Resolution to endorse the draft Regional Strategic Action Plan (subject to a number of amendments and clarifications discussed during the meeting), identifying ROPME as the body to coordinate activities under the Plan, and set out to implement IMO Guidelines requiring ballast water exchange within the region (Globallast, 2002).The Globallast risk assessment for Khark Island was semi-quantitative – identifying the relative risk of different trading routes, rather than the specific risk posed by any single tank discharge. The risk assessment considered the frequency and volume of ballast water events, environmental similarity between Khark Island and each of its ballast source and destination ports, as well as the potential for transfer of high risk species from source ports (Clarke et al., 2003). The risk assessment did not include any biological information from ballast water surveys in the region. It appears that ballast water surveys were initiated about the same time, but results were never published (Kagari et al., 2010). The risk assessment identified ports such as Kaohsiung (Taiwan), Okinawa (Japan), Chiba (Japan) and Ulsan (Korea) as being highest risk while low risk ports were mainly in northern Europe, North America and South Africa (Clarke et al., 2003). The project also indicated that any marine invasive species introduced into the ROPME Sea Area (or nearby Red Sea and west Arabian Sea) could be spread quickly by local ship movements.Following the adoption of the IMO Convention for the Control and Management of Ships' Ballast Water and Sediments in 2004, the ROPME Council identified ballast water exchange area(s) outside the ROPME Sea Area as a matter of priority, in order to efficiently address the issue of marine invasive species in ships' ballast water and sediments (IMO, 2008, 2009a). Ballast water exchange regulations were subsequently applied, effective 1 November 2009, requiring all ships to exchange or treat all ballast water taken up outside the ROPME Sea Area in accordance with regulation B-4 of the Convention (IMO, 2009b). Finally, Iran ratified the Convention in 2011 (IMO, 2011).The conference Marine Invasive Species: Management of ballast water and other vectors was held in Muscat, Oman in February 2013, organized by the Aquatic Ecosystem Health and Management Society (AEHMS) and the Ministry of Environment and Climate Affairs (MECA) of Oman. The conference was convened under the patronage of His Excellency Sayyid Hamood Bin Faisal Al Busaidi, Minister of the Interior. The opening ceremony included a welcome by His Excellency Najeeb bin Ali Al-Rawas of MECA, followed by opening remarks by Koji Sekimizu of the International Maritime Organization (IMO) (pre-recorded), Mohammad Badran of the Regional Organization for the Protection of the Marine Environment (ROPME) and Mohiuddin Munawar of the AEHMS. A short movie about ballast water issues was shown. The opening ceremonies were graced with the presence of many ministers and dignitaries. The theme sessions of the conference included vectors and pathways, impacts of invasive species, risk assessment, and management strategies. The conference attracted 8 expert keynote speakers from around the world, as well as 2 featured, 31 oral, and 12 poster presenters. The sessions were a grand success, being well attended by over 300 people from various sectors such as researchers, students, policy makers, media, and industry.This conference was unique in that it was an inaugural event held in the Middle East to highlight the issue of marine invasive species in the area and to build scientific capacity for local researchers.A pre-conference capacity building workshop was organized to promote the understanding of biological invasions as a serious environmental threat. The workshop was designed for students from the region, and delivered by graduate student members of the Canadian Aquatic Invasive Species II research network and Sultan Qaboos University.This presentation reviewed the history of invasion theory, from Charles Darwin to Charles Elton to modern literature, covering theories from evolution, island ecology and biogeography. Different approaches to the study of invasive species were discussed with a view to provide ideas for future research by participants.This presentation examined the importance of various introduction vectors (e.g. ballast water, live fish trade, canals) for primary and secondary spread of aquatic invasive species.This presentation provided a general introduction to risk assessment for biological invasions. Risk assessment methods to identify risky species (i.e. species-based risk assessment) and risky transportation vectors (i.e. vector-based risk assessment) were discussed using case studies.This presentation examined how the impact of an invasive species can vary greatly over its invaded range due to the context of the invasion, such as the abiotic conditions of the invaded habitat and how well-suited the invader is to those conditions. By understanding how impact varies in different contexts we can improve our ability to predict where invasive species may have their strongest impacts on native communities.This presentation dealt with the impact of algal blooms on the Omani waters as reflected by physical, chemical and biological changes.Given below are summaries of the conference theme sessions as documented by the session Chairs and rapporteurs. Further information about keynote presentations listed can be found in this special issue which is devoted to the publication of the keynote papers.Keynotes:Sarah Bailey – Ballast water as a global vector for aquatic invasive speciesGreg Ruiz – Invasion history and vector dynamics in coastal marine ecosystems: a North American perspectiveAdnan Al-Azri – Intensity and frequency of Harmful Algal Blooms (HABs) in the coastal water of Oman: a possible role of ballast waterSummary of Session 1:Katharine Carney reported that vessels arriving to Chesapeake Bay, USA achieved 99% compliance with requirements for ballast water exchange, as reflected by the incidence of 90% oceanic vs. 10% coastal organisms in ballast water samples. The future impact of growing coal exports and the Panama Canal expansion were discussed.Sergey Dobretsov described biofouling communities of bryozoans, barnacles, seaweeds, and tunicates on ship hulls and artificial substrata in Muscat waters. More fouling species were found in polluted waters. Of considerable interest was the fact that the Cochlodinium harmful bloom in December 2008 killed fouling communities. Nadezhda Berezina characterised nonindigenous Malacostracan crustaceans in the Baltic Sea. More introduced species occurred in disturbed ecosystems. Reza Naderloo provided another example of biodiversity surveys (crustaceans, fish, algae, polychaetes) in progress in the ROPME region. Major taxonomic uncertainties exist and hinder recognition of what are indigenous and what are introduced species.Keynotes:Patricia Glibert – Altered nutrient composition and its effect on suitability for species introductions and the cascade of impacts on food webs and nutrient biogeochemistryMartin Kernan – Climate change and the impact of invasive species on aquatic ecosystemsSummary of Session 2:Josie Iacarella presented functional response (measured as the proportion of available prey consumed) as an effective tool for predicting alien impacts in aquatic ecosystems under different biotic and abiotic variables. Sergey Piontkovski examined long-term records of nitrates, diatoms, and productivity to discern if increased salinity and temperature due to climate change is facilitating invasive species in Omani waters. Hamed Al Gheilani gave an overview of harmful algal blooms (including invasive species) and their effects in Omani waters on fish, shellfish, coral and desalination plants in Muscat. Adil M. Al Qasmi described the impact of agricultural inputs and ship anti-fouling coatings on microalgae. In Oman, persistent organotin tributyltin (TBT) contamination in semi-closed areas has been correlated with harmful algae and cyanobacteria blooms. Faiza Al-Yamani (Featured speaker) spoke about potential ecological and economic impacts of ballast-mediated marine invasive species on Kuwait's marine biodiversity. Fatme Al Anouti described the first study in Abu Dhabi to use rapid PCR-based assays to identify bacteria in ballast water and ballast tank biofilm. Abdulrahman Al-Muftah presented results of phytoplankton surveillance in Qatari waters. This study found that multiple factors contribute to red tide in Qatari waters including eutrophication, ballast water discharge and modification of coastline. Katie Pagnucco combined field experiments with surveys across abiotic gradients to disentangle the influence of habitat degradation and an invasive species (Round Goby) on benthic communities. Finally, noting that all invasion-induced changes are not necessarily adverse, Alexey Maximov described how ecosystem engineering by invasive polychaetes in the Gulf of Finland (Baltic Sea) resulted in cardinal reconstructions of the whole ecosystem.Keynotes:Nick Mandrak – Risk assessment – cornerstone of aquatic invasive species programsSummary of Session 3:Farrah Chan presented a formal vector-based risk assessment approach using ballast water discharged in the Canadian Arctic as a case study. Kimberly Holzer compared commercial vessel traffic patterns, ballast water management and propagule pressure through time for three major U.S. port systems to examine the current status and limitations of ballast water management in each region. Danielle Verna reviewed reported vessel route and ballast water management patterns through time to assess the risk of ballast-borne non-native species to Alaska during an era of ballast water policy changes, finding that exemptions from management requirements leave substantial risk of ballast-borne species invasions in Alaska despite national policies in place. Joaquim Goes talked about a shift in plankton dynamics and structure, and productivity in the Arabian Sea ecosystem as a result of recent climatic trends. Mohammad Badran (Featured speaker) informed the audience on the IMO GloBallast program in response to threats of ships' ballast water pathogenic and invasive species. Igor Polikarpov reported on new and probably invasive harmful dinoflagellates in the northwest Arabian Gulf. Nicole Schwartz used risk assessment to identify future invaders in a recently constructed German deepwater port (Jade-Weser-Port) based on a list of high impact algal species in connected ports. Harri Pettitt-Wade compared gut contents and stable isotopes in pairs of highly successful and less successful aquatic invasive species to determine if more successful invaders would maintain a broad and more flexible ecological niche. Magnus Thorlacius presented evidence that invasive round gobies from newly established populations were both bolder and more active than those from populations that had been established for a longer time, revealing the importance of intraspecific behavioral traits in the colonization of novel environments. Behdokht Mirzaei Asl introduced a project aiming to shrink a critical gap in baseline knowledge through the development of an atlas and database of native and non-native species in the ROPME Sea Area based on research and a biodiversity cruise. Finally, Gustav Hellstrom presented ways to use acoustic telemetry in the study and management of invasive fish both in inland and coastal waters, as exemplified by a high resolution 3D-tracking study of invasive Lake Trout in Sweden.Keynotes:Gustaaf Hallegraeff – Transport of harmful marine microalgae via ship's ballast water: management, treatment and mitigationAhmad Parhizi – ROPME SEA Area Strategic Action Plan (SAP) and its roadmap ballast water management of Session presented a new approach to invasive and native fish communities from water samples. This new provides a to species presence and abundance and gave a overview of and information systems for harmful algal blooms. study of threats such as sea marine and marine invasive species. such as Sea and are available from different and can be used to and a to the of harmful algal blooms. used a novel of PCR-based designed to a region of the for high resolution to between of the harmful algal bloom species from different described a project to the of ballast water treatment under conditions the – can in ballast water for scientific to their ballast Finally, provided an overview of the risk of vessel biofouling as a vector for new introductions to Oman, as well as a for capacity to identify risk vessels based on vessel and the of the the session of a presentation of the conference theme a and from the keynote The introduction of aquatic nonindigenous species their native is a major to global to economies related to and water and to water are identified as introduction vectors globally, and are to in in locations such as Oman and the ROPME Sea Area where shipping is with global such as and climate are important of species introductions, and are important factors to and address in the management of aquatic nonindigenous activities can be identified and using a risk activities in any one region will be effective and with to regional and international and the Ballast Water Management Convention and its requirements for ballast water discharge into for of aquatic nonindigenous species, risk assessment and rapid using as a risk assessments to identify the import in the region of of biodiversity and environmental to be used for environmental across scientific and industries that are or aquatic nonindigenous species in order to activities and within and between can advance scientific research on marine invasive species in the region by and research and both within Oman and more or other could be established to the listed have been a number of listed to address the issue of invasive species as well as marine species which can be used as a to future research and management in the ROPME Sea Area et al., et al., et al., is a to or taxonomic using both and modern to of native non-native species. is a for baseline and biodiversity to risk assessment, early and response and the impacts of introduced species. of invasion vectors (i.e. of and (i.e. for introduction of invasive species is to risk assessment and to Finally, development of effective and control are to or control introduced species. With to marine invasive species the environment – a approach across could improve research and management are to methods and ballast water has been identified as a vector globally, of live organisms associated with and as well as have also been identified as important – future research is to examine the relative risk of vectors other than ballast one of the and welcome of the conference appears to be the of awareness of the and of invasive species in countries outside the where the has less This has resulted in the and more or less of knowledge and to the management of invasive species. This special issue will be a effective tool in the scientific between as have been by the about future on the ecology of and marine invasive species.

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