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Special Issue:
Proceedings of the 10th International Conference on Marine Bioinvasions
published March 2020
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This special issue of
"Aquatic Invasions" includes papers presented at the 10th International Conference on Marine Bioinvasions held in Puerto Madryn, Argentina, October 16–18, 2018.
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Editorial |
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Amy E. Fowler, April M.H. Blakeslee, Alejandro Bortolus, Joana Dias, Carolyn K. Tepolt and Evangelina Schwindt
Current research, pressing issues, and lingering questions in marine invasion science: lessons from the Tenth International Conference on Marine Bioinvasions (ICMB-X)
(pp 1–10)
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Research articles |
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Evangelina Schwindt, James T. Carlton, José M. Orensanz, Fabrizio Scarabino and Alejandro Bortolus
Past and future of the marine bioinvasions along the Southwestern Atlantic
(pp 11-29)
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The first comprehensive survey of marine bioinvasions in the southern Southwest Atlantic Ocean (SWA, ca. 33°45′–ca. 54°50′S) published in 2002 reported 31 introduced and 46 cryptogenic species.
In this assessment, we update this work by providing a deep historical perspective of marine biological invasions as well as a full new review of introductions that have occurred over the past
nearly two decades. We reviewed a variety of sources including peer-reviewed journals and monographs, government reports, and museum databases, among others. The previous survey was re-evaluated
and taxonomic experts were also consulted. For each species, the possible status as introduced or cryptogenic, likely vector, likely native region, first collection date if known, and the first
authoritative reference of its SWA occurrence were determined. Species were categorized by biogeographical provinces. Our re-evaluation of species status lowered the 2002 survey to 29 introduced
and 29 cryptogenic species. The result of our analyses added 100 new introduced and 43 new cryptogenic species, making a total of 129 introduced and 72 cryptogenic marine species for the SWA.
Of these 100 species, 67 were found in the literature older than the 2002 survey, and 33 were found as new invasions that occurred since 2002, averaging one new invasion every 178 days. Ships
are the most likely vector of invasions with an additional few species introduced with aquaculture, for ornamental purposes or for stabilizing coastal dunes. Most species are native to either
the North Pacific or North Atlantic Oceans. Most introduced species (51%) occur in the warm temperate SWA marine ecoregion, while fewer (16%) occur in the cold temperate Magellanic marine ecoregion.
Since ships are the main vectors in the region, we forecast that new introductions will continue until regional and international regulations to control ballast water and hull fouling begin to be effective.
Our results urge the creation of long-term assessment programs focused on marine coastal biodiversity as a way to avoid inefficient environmental management based on deficient baseline information.
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Larissa Marques Pires Teixeira and Joel Christopher Creed
A decade on: an updated assessment of the status of marine non-indigenous species in Brazil
(pp 30-43)
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In order to prevent the introduction, control or eradicate non-indigenous species (NIS) which threaten native species, habitats or ecosystems, an essential first step is that countries have
and keep up-to-date lists of species non-indigenous to the region. The last list of marine NIS for Brazil was published a decade ago. We compiled an updated list of marine NIS and revised
the species’ statuses. One-hundred-thirty-eight marine species in 15 classes or functional groups are NIS in Brazil. Brazilian states with greater maritime commerce (greater market share)
had more marine NIS. From the period between the 1950s to 2010, the number of NIS at least doubled each decade. We identified a significant mismatch (underestimation) between the previous
list and this study, which seemed to be due to improved scientific knowledge and an often considerable lag between first record (detection), identification and communication of new marine NIS.
Currently Brazil has 19 invasive, 76 established and 43 detected marine NIS, an increase of 160% in ten years compared to the previous national list. We recommend that Brazil implements
a national database as a rapid, appropriate, flexible and cost effective method of monitoring trends in NIS introductions.
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Alfonso Ángel Ramos-Esplá, Ghazi Bitar, Yassine Ramzi Sghaier, Melih Ertan Çinar, Alan Deidun, Jasmine Ferrario and Aylin Ulman
Symplegma (Ascidiacea: Styelidae), a non-indigenous genus spreading within the Mediterranean Sea: taxonomy, routes and vectors
(pp 44-62)
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Symplegma is a genus of compound ascidians (Fam. Styelidae) with warm water affinities and distribution in tropical and subtropical waters of the Pacific,
Indian and Atlantic Oceans. The first record of this genus (as S. viride) in the Mediterranean was from 1951 in the Levantine Sea, presumably entering
the basin from the Red Sea through the Suez Canal. Subsequently, it has been expanding its distributional range northward along the Levantine Sea coast, probably
following the prevailing surface current direction. Recently, Symplegma has colonized the Aegean, Ionian and Tyrrhenian Seas, where it is spreading quickly,
most likely mediated by shipping (i.e., hull fouling). Some specimens from the Ionian Sea (specifically from Tunisia, Malta) present opaque tunics resembling
the Indo-Pacific Symplegma bahraini; however, morphological studies suggest that the genus in the Mediterranean Sea is represented by a single species,
Symplegma brakenhielmi. The taxonomy of S. brakenhielmi, as well as its spreading routes and possible introduction vectors are analysed.
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Karen Lidia Castro, Clara Belen Giachetti, Nicolás Battini, Alejandro Bortolus and Evangelina Schwindt
Cleaning by beaching: introducing a new alternative for hull biofouling management in Argentina
(pp 63-80)
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Recreational vessels favor the secondary spread of exotic marine species hosted on hull biofouling communities through coastal trips. Hull biofouling is also a problem
for vessel owners because it reduces the efficiency and maneuverability of the vessel. This study documents a pioneer case of alternative hull biofouling management
in a context where local regulations prohibit in-water cleaning operations and where there are no shore-based facilities. We designed and put into practice a method
to manually clean a 35 meter long catamaran, by beaching it in a macrotidal beach of Patagonia, Argentina. During the cleaning, all hull biofouling was removed and collected
to prevent organisms from falling on the beach. A total of 12.5 m3 of biofouling was deposited in landfill following regulations for fishing discard material. In addition,
qualitative and quantitative fouling samples were obtained from different hull locations of the vessel, including niche areas. A total of 53 distinct taxa were identified,
including 18 exotic species for Argentina, 7 of which had not been previously reported for the study area. Cleaning by beaching can be used as a convenient biosecurity method
to remove hull biofouling from small and medium size vessels when other methods or facilities on the coast are not available. Our results also provide further evidence
for the potential risk of recreational vessels as vectors for the secondary spread of marine exotic species.
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Catherine Keanly and Tamara B. Robinson
Encapsulation as a biosecurity tool for managing fouling on recreational vessels
(pp 81-97)
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Hull fouling is a dominant vector in marine systems, with recreational vessels playing an important role in intra-regional transfer of biota. Encapsulation (i.e. the wrapping of a structure
in plastic to deprive biota of oxygen and food, ultimately causing their death), offers promise as a tool for treating vessel fouling in situ. However, there is currently no standardised
approach with detailed field application recommendations. In recognition of this gap this study aimed to: 1) use laboratory experiments to establish a timeframe for the effective encapsulation
of yachts, 2) test this approach in the field and 3) consider the practicalities associated with implementing an encapsulation program. Laboratory experiments exposed the ascidian Ciona robusta,
the mussel Semimytilus algosus and fouling communities to four treatments: aerated control in seawater, encapsulation in seawater, aerated seawater with 4% acetic acid and encapsulation
in seawater with 4% acetic acid. All biota in acetic acid died in 24 hours regardless of encapsulation, while in encapsulated seawater mortality of all taxa occurred within three days. In the field
four yachts and five pontoons with high (80–100%) and low (30–50%) fouling cover were encapsulated. It took more than three days to achieve mortality on all structures (pontoons high cover 3.7 days
(± 0.48 SD); pontoons low cover 3.8 days (± 0.42 SD) and yachts 4.3 days (± 0.5 SD)). The discrepancy between laboratory and field results likely reflects an unavoidably higher water to fouling biomass
ratio in field systems. These results suggest that five days may be sufficient for successful encapsulation of yachts. However, in recognition of the limited sample size of yachts in this study,
it is recommended that these findings be used as a basis for further developing region specific protocols through adaptive management. Logistical considerations around the implantation of national
encapsulation programs are also discussed.
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Isabella F. Guilhem, Bruno P. Masi and Joel C. Creed
Impact of invasive Tubastraea spp. (Cnidaria: Anthozoa) on the growth of the space dominating tropical rocky-shore zoantharian Palythoa caribaeorum (Duchassaing and Michelotti, 1860)
(pp 98-113)
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Competition for space directly affects the structure of the sessile benthic communities on hard substrates. On the Brazilian coast Palythoa caribaeorum is an abundant shallow water
mat-forming zoantharian and has fast growth rates. The objective of the present study was to assess the zoantharian’s biotic resistance by investigating changes in growth rates when interacting
with the invasive sun corals Tubastraea tagusensis and T. coccinea on a tropical rocky shore in southeast Brazil. In the experimental design, eight blocks were arranged along
the rocky shore where the growth treatment was applied with four different levels: empty, skeleton, live T. coccinea and live T. tagusensis. We opened up 10 × 10 cm² spaces
in the P. caribaeorum mat into which treatments were transplanted with epoxy putty. Growth measures of the zoantharian were obtained using photographs. During the 184 days of the experiment,
P. caribaeorum had the highest total growth rate in the empty treatment with an average value of 2.124 ± 0.189 mm.mo-1; the treatment with the lowest total growth rate was T. coccinea
with mean value of 1.104 ± 0.117 mm.mo-1. The presence of T. coccinea influenced the growth rate of the zoantharian, unlike its congeneric T. tagusensis, which did not significantly
influence the growth rate of P. caribaeorum. The negative interactions between P. caribaeorum and the invasive Tubastraea spp. were species specific in nature, and the native zoantharian
exhibited quite some biotic resistance to the invasive species, especially to T. tagusensis. This was due to competition, probably mediated both through physical and/or chemical mechanisms and preemptive
occupation of space. Growth rates of P. caribaeorum were dependent on the degree of competitive interaction as well as seasonal differences in light and/or temperature which remain to be elucidated.
From a management perspective, the manual removal of Tubastraea spp. will allow native species such as P. caribaeorum to recover space and thus foster ecosystem recovery.
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Daniel M. Lins and Rosana M. Rocha
Cultivated brown mussel (Perna perna) size is reduced through the impact of three invasive fouling species in southern Brazil
(pp 114-126)
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Invasive species reduce the productivity of shellfish mariculture worldwide. Brown mussel culture harvests were examined for invasive species in the state of Santa Catarina – the most important region
for shellfish mariculture in Brazil. For the first time, we describe here the impact of the three most abundant invasive species on harvested Perna perna. The ascidian Didemnum perlucidum,
the barnacle Megabalanus coccopoma, and the bryozoan Schizoporella errata were all associated with smaller mussel size. Fouled mussels were 19–36% smaller and weighed ~ 60% less than
non-fouled mussels. Reductions in mussel size were greatest for shell weight and size when associated with D. perlucidum and tissue dry weight for M. coccopoma. This large reduction
in productivity indicates that management of these fouling species should be prioritized to protect the mussel fishery.
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Felipe Theocharides Oricchio and Gustavo Muniz Dias
Predation and competition interact to determine space monopolization by non-indigenous species in a sessile community from the southwestern Atlantic Ocean
(pp 127-139)
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Non-indigenous fouling species (NIS) often dominate coastal facilities, such as harbors and marinas. Along the subtropical Coast of Brazil, sessile
communities from artificial habitats are mostly dominated by the NIS ascidian Didemnum perlucidum and the bryozoan Schizoporella errata,
which show contrasting life-history traits. To understand the dynamics between these species and better predict the identity of the dominant NIS
in the sessile community, we conducted an experiment where colonies of S. errata, D. perlucidum and the cryptogenic ascidian
Botrylloides niger were submitted to the following three interaction scenarios: colonies growing without competition, under intraspecific
competition and under interspecific competition. All competition treatments were crossed with the following two predation treatments: exposed or protected
to predators. The experiment was repeated in two different seasons (Winter and Summer). When released from predation and competition, the three species
grew at least 10 times faster in the Summer than in the Winter, and S. errata always grew slower than the ascidian species. Predation reduced
D. perlucidum survival in the Winter but not during the Summer, when the fast colony growth seemed to buffer partial colony removal by predation.
Colonial growth of B. niger was affected by competition only in treatments without predators, growing almost 50% more without competition than when
competing, regardless of the competitors’ identity. When exposed to predation, D. perlucidum was more limited by interspecific than intraspecific
competition. S. errata growth was not affected by biotic interactions and was linked to intrinsic seasonal variation. Mineralized clonal organisms,
such as bryozoans, were less predated than most of the ascidians species but they grew slower. Ascidians were more often predated but were also strong
competitors that were able to overgrow several taxa. The contrasting growth strategies resulted in different successes of NIS and cryptogenic species
at the studied locality. Ascidians were favored under low predation pressure while bryozoans were survivors when predation was intense.
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Pablo Yorio, Nicolás Suárez, Tatiana Kasinsky, Miriam Pollicelli, Cynthia Ibarra and Alejandro Gatto
The introduced green crab (Carcinus maenas) as a novel food resource for the opportunistic kelp gull (Larus dominicanus)
in Argentine Patagonia
(pp 140-159)
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Introduced species are one of the main threats to biological diversity, but they can also facilitate native species through mechanisms such as trophic
subsidy. We quantified the diet of breeding kelp gulls (Larus dominicanus) and their consumption of the introduced green crab (Carcinus maenas)
at five colonies located along over 600 km of coastline in Patagonia, Argentina, and analyzed differences in consumption rates among breeding locations.
Results based on pellet analysis (n = 961 pellets) showed that kelp gulls consumed green crabs during most or part of the breeding cycle at all study locations
(0–73.9%, depending on location, year and breeding stage). Green crab consumption differed among breeding locations, with lower consumption further from the reported
location of first Argentinean introduction (Golfo San Jorge, Chubut, Patagonia) in 1999–2000. Despite kelp gulls regularly consumed green crabs at most breeding
locations, this invasive species was not an important component in their diet. Both stomach content and stable isotope analyses from breeding kelp gulls indicated
that the main prey were fish such as Argentine anchovy and Argentine hake (Engraulis anchoita and Merluccius hubbsi, respectively) and squat lobster
(Munida gregaria). At Isla Vernaci Este and Punta Tombo, green crabs were found in only one stomach of all kelp gull age classes sampled (incubating adults
(n = 42), young chicks (n = 75), and old chicks (n = 105)). Based on carbon and nitrogen isotopic values from blood samples from incubating adults (n = 54), Bayesian
mixing model outputs showed that green crabs contributed 7.3–23.9% to the overall diet. The study showed that the relatively recent introduction of green crabs
supplements the available prey base of a widely distributed and abundant predator, the kelp gull, at least during its breeding season in a large coastal sector
of central Patagonia. The extent to which the kelp gull in coastal Patagonia may be shaping the establishment, abundance, and population dynamics of the introduced
green crab is still unknown and will require further research.
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Henn Ojaveer, Aleksei Turovski and Kristiina Nõomaa
Parasite infection of the non-indigenous round goby (Neogobius melanostomus) in the Baltic Sea
(pp 160-176)
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Parasites may play several critical functions in marine ecosystems, including possibly influencing introduction success or modifying the roles of non-indigenous species.
Based on seasonally replicated sampling, we have investigated parasite communities and infection rates of the non-indigenous round goby Neogobius melanostomus in two localities
in the NE Baltic Sea, characterised by different invasion trajectories. The parasite community of the fish was very rich, consisting of at least 24 native parasite species, with moderate
mean infection intensity – 9.4 parasites per host. In total 78% of fish were infected with parasites, most frequently hosting 1–3 parasite species per fish. The trematode Diplostomum spathaceum
had the highest prevalence (46%), while the acanthocephalan Corynosoma strumosum and the trematode Tylodelphys clavata had the highest infection intensity (mean 6.8 and 7.2, respectively).
The seasonal dynamics of prevalence were similar in both localities, with the lowest number of infected fish being found immediately after winter with no clear patterns/differences between other seasons.
Broadly similar patterns appeared both for species richness and infection intensity. Both localities displayed very similar patterns of occurrence frequency: both had a few parasite species which were
specific to one locality and five species that occurred more frequently in one of the two localities. Binomial regression of the probability of infection identified season, total body length,
and sex as significant predictors, but not the locality of sampling. The quantitative model revealed that infection intensity was positively linked to total body length and parasite species richness,
and was on average 2.7 individuals higher in summer and autumn than in winter and spring.
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April M.H. Blakeslee, Matt Ruocchio, Chris S. Moore and Carolyn L. Keogh
Altered susceptibility to trematode infection in native versus introduced populations of the European green crab
(pp 177-195)
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Non-indigenous species (NIS) often experience a reprieve from infection by their co-evolved indigenous parasite load when they invade novel regions.
Yet absolute escape from parasites may be precluded (notably with time) by introductions of parasites from the native range, by novel parasite acquisitions
in the non-indigenous range, or both. As a result, NIS infection susceptibility may differ or change in indigenous versus novel regions due to divergent
coevolutionary histories and parasite selective pressures – thereby influencing host resistance and/or compatibility. To investigate this question,
we reciprocally exposed native (Europe) and non-native (eastern North America) individuals of the globally-invasive green crab, Carcinus maenas,
to trematode parasites from both regions. We found that infection susceptibility differed by parasite origin: native European crabs exposed to native European
parasites had lower infection prevalence and abundance, and the lowest proportion of irregular trematode metacercarial cysts or encapsulated metacercarial cysts
(due to host immunity), compared with a treatment demonstrating possible prior coevolutionary history (~ 200 years ago) between the host and its parasites (invaded
North American crabs exposed to native European parasites). Metacercarial cyst abundance was higher in the treatment with little to no coevolutionary history between
host and parasite (native European crabs exposed to native North American trematodes) compared to a treatment with recent association in the last two centuries
(invasive North American crabs exposed to native North American parasites). Our study provides further evidence that infection susceptibility can differ depending
on coevolutionary history, which may be rapidly influenced by altered parasite selection pressures. It also provides greater understanding of the impact
of human-mediated introductions on the coevolutionary dynamics of organisms worldwide.
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Last update: 21 March 2020
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© 2020 Regional Euro-Asian Biological Invasions Centre (REABIC)
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