Non-indigenous Ascidians Research Articles

Salinity-mediated limitation of asexual reproduction in the colonial ascidian Polyandrocarpa zorritensis

Ascidians are among the most common invasive marine invertebrates worldwide. Many species of non-indigenous ascidians (NIAs) have successfully colonized the Mediterranean Sea, notably within anthropized coastal lagoons and harbors. Although invasive species are generally characterized by their broad ecological tolerance, different ascidian species exhibit varied responses to biotic and abiotic environmental stressors, including temperature and salinity. Acquiring a better understanding about of the impact of such parameters on ascidian life history is crucial for predicting the invasive potential of NIAs. In this study, we investigated the impact of various salinities on the reproduction of the colonial ascidian Polyandorcarpa zorritensis, a species indigenous to Peru and a thriving invader. P. zorritensis undergoes asexual reproduction via a peculiar form of budding named vasal budding and produces resistant spherules, which likely facilitated its dissemination over long distances. Despite its widespread distribution along the Pacific and Atlantic coasts, it is only found in a few Mediterranean coastal areas with a low salinity. We tested the impact of different salinity conditions on the sexual and asexual reproduction rates of P. zorritensis in a controlled laboratory setting. Our experiments showed that the rate of asexual reproduction in colonies bred at 29 or 36 ppt salinity levels, corresponding to the natural range inhabited by P. zorritensis, was higher than those grown in 40 ppt salinity, commonly found in Mediterranean marinas and harbors. The results suggest that, although P. zorritensis has been present in the Mediterranean for several decades, its potential for invasion could be constrained by an intolerance to high salinity.

Facilitation of non-indigenous ascidian by marine eco-engineering interventions at an urban site

Marine artificial structures often support lower native species diversity and more non-indigenous species (NIS), but adding complex habitat and using bioreceptive materials have the potential to mitigate these impacts. Here, the interacting effects of structural complexity (flat, complex with pits) and concrete mixture (standard, or with oyster shell or vermiculite aggregate) on recruitment were assessed at two intertidal levels at an urban site. Complex tiles had less green algal cover, oyster shell mixtures had less brown (Ralfsia sp.) algal cover. At a low tidal elevation, the non-indigenous ascidian Styela plicata dominated complex tiles. Additionally, mixtures with oyster shell supported higher total cover of sessile species, and a higher cover of S. plicata. There were no effects of complexity or mixture on biofilm communities and native and NIS richness. Overall, these results suggest that habitat complexity and some bioreceptive materials may facilitate colonisation by a dominant invertebrate invader on artificial structures.

Recent spread of non-indigenous ascidians (Chordata: Tunicata) in Icelandic harbours

ABSTRACT Global shipping facilitates the introduction of fouling organisms to new geographic areas. The increase in maritime transport in recent decades has led to unprecedented development, where marine coastal waters have become one of the most invaded habitats around the globe. Among the most successful invaders are ascidians. Despite the geographic and oceanographic isolation of Iceland, it is far from being excluded as a recipient region. Ascidians have successfully been able to establish stable populations in Iceland that are slowly expanding around the SW region. Here we report the first record of Ascidiella scabra in Icelandic waters, and the spread of seven non-indigenous ascidians across the S-SW Icelandic harbours. We compare their relative abundances to our survey from 2018. The bulk of these ascidians is not only present in the temperate Atlantic Ocean, but also in the Northwest Pacific and temperate Australasia, revealing that global homogenization of the ascidiofauna is emerging in anthropized coastal areas. The rising of sea surface temperature, driven by climate change, is likely to continue to support the development of this scenario leading to biodiversity loss, which could endanger living resources with severe economic impacts. Highlights Non-indigenous ascidians are spreading across the Icelandic harbours. Ascidiella scabra has arrived to Iceland. Global homogenization of coastal zones is emerging. Climate change will support the development of this scenario.

Untargeted Metabolomics Yields Insights Into the Lipidome of Botrylloides niger Herdman, 1886, An Ascidian Invading the Mediterranean Sea

Human-mediated dispersal of alien species in new biogeographic realms is one of the major drivers of biodiversity change in marine ecosystems. Among others, ascidians are invasive species spreading worldwide, thus causing ecological and economic harms in the recipient environments. An integrated taxonomic approach on selected samples allowed the identification of Botrylloides niger Herdman 1886 as a non-indigenous ascidian forming large aggregates and outcompeting native species in the Fusaro Lake (central-western Mediterranean Sea). This led to the opportunity to investigate in deep its metabolome for the first time. Untargeted mass spectrometry-based metabolomics unveiled B. niger to be a source of nutraceuticals and bioactive natural products, such as lysophospholipids, sulfonolipids, polyunsaturated fatty acids, sphingolipids, monoacylglycerols, and alkaloids. Even if causing ecosystem alterations, our results suggest that B. niger could be exploited for nutritional and/or pharmaceutical purposes, thereby turning a treat in a resource.

A new record of Ascidiella scabra (Müller, 1776) (Ascidiacea, Phlebobranchia) in the southwestern Atlantic

Non-indigenous ascidians are transported across oceans in vessel-hull fouling communities, and regional traffic plays a role in their secondary spread. We found the ascidian Ascidiella scabra (Müller, 1776) in the hull-fouling community of an oceanographic vessel confined to waters of the southwestern Atlantic and Southern Oceans. The previously known distribution of this species was restricted to its native area (Mediterranean Sea and northeastern Atlantic); its presence in the southwestern Atlantic may have been masked in the past by the occurrence of its congener Ascidiella aspersa (Müller, 1776).

Ascidian biodiversity in the shallow waters of the Madeira Archipelago: Fouling studies on artificial substrates and new records

Ascidians are recognized as major invaders on a global scale, found from the poles to the tropics and from shallow to deep sea waters with approximately 3000 known described species worldwide. However, to date only a few opportunistic studies focusing on the ascidian diversity colonizing natural and artificial substrates have been conducted in the Madeira Archipelago (NE Atlantic). Furthermore, little is known about the community composition and distribution of native and non-indigenous ascidians in the islands of the archipelago. In this context, we conducted a 3-phase study that allowed us to report an updated list of ascidian records found on artificial substrates in the Madeira Archipelago. First, to assess ascidian biodiversity colonizing artificial substrates present in the Madeira Archipelago, we conducted standardized monitoring campaigns in four marinas and hull vessel surveys during dry dock inspections. Second, we complemented this inventory with a comprehensive literature search and Museum collection focused on ascidians colonizing both artificial and natural substrates. Third, we investigated the temporal and spatial variability on the recruitment and succession of young vs mature ascidian assemblages. We found 24 ascidian species in all four marinas, from which 13 are NIS and 11 are new records for Madeira Archipelago. In addition, a literature survey found a total of 27 ascidians occurring on both artificial and natural substrates. This study now reveals a total of 39 ascidian species colonizing both artificial and natural substrates and comprises the most up-to-date list for all shallow-water ascidians in the Madeira Archipelago. A total of 15 NIS are now currently known, 9 exclusively from Madeira Island, 1 exclusively from Porto Santo Island and 5 on the two main islands of the archipelago. This study also shows that the spatial and temporal variability of fouling ascidian assemblages are driven by recruitment and succession of NIS rather than by presence of native species. Finally, total ascidian richness and cover was significantly higher in 4-month-old communities than in 8 to 16-month-old communities across all marinas, suggesting that “bare” artificial substrates are the main drivers of NIS success in the region.

Seasonal variability in a nascent population of a non-indigenous colonial ascidian (Didemnum vexillum) near Winchester Bay, Oregon

The non-indigenous colonial tunicate Didemnum vexillum plagues many shellfish aquaculture operations around the world by smothering crop and gear and displacing juvenile bivalves. There are two populations of D. vexillum in Oregon, but little is known regarding their spatial extent, seasonal dynamics, annual variability, reproductive biology, or ecology. SCUBA divers monitored the seasonal variation and spatial extent of the nascent D. vexillum population in its current foothold at Umpqua Aquaculture, a longline oyster farm adjacent to Winchester Bay, Oregon. From May 2011 to November 2016, divers performed biannual subtidal surveys to measure the cover of D. vexillum on anchor lines. We found that this population of D. vexillum exhibited extensive fluctuation in colony during this period, especially between fall and spring. With one exception, cover was greater in the fall than the spring, though this fluctuation cannot be explained by our proxies for salinity or temperature. Seasonally, on average, D. vexillum covered the greatest proportion of line between 5.5 and 6.0 m depth in both the spring (37.5 ± 18.8%) and fall (45.1 ± 16.1%). During individual surveys, the depth of maximum percent D. vexillum cover was more variable, spanning ~ 4.5–6.5 m depth. Overall, we document a net increase in D. vexillum cover at Umpqua Aquaculture between the first and last surveys during the 5-year period. This study is the first published multi-year analysis of D. vexillum in Oregon and represents the longest continuous monitoring period of an in situ population of D. vexillum to date.

Predators Associated with Marinas Consume Indigenous over Non-indigenous Ascidians

The establishment of non-indigenous species is influenced both by species traits and the biotic interactions that create resistance to or facilitate invasion. Predation, for example, creates resistance to non-indigenous ascidians in benthic habitats. Daytime surveys of fouling communities on floating docks in the Charleston Marina, Oregon, USA in August 2014 revealed that the indigenous ascidian Distapla occidentalis was present at all sites and was being consumed by the flatworm Eurylepta leoparda and the nudibranch Hermissenda crassicornis. In contrast, the non-indigenous Botrylloides violaceus and Botryllus schlosseri were present at fewer sites and lacked signs of predation. Parallel surveys in July 2015 again revealed predators found on docks were eating the indigenous ascidian. Examination of surrounding intertidal habitats revealed the dominant predators were the hermit crab Pagurus granosimanus and shore crab Hemigrapsus oregonensis, species not found in the marina fouling community. Feeding assays with the four predators and the ascidians showed that the flatworm specialized on the indigenous D. occidentalis, eating it almost 50 times faster than the NIS, which it did not consume. The nudibranch and shore crab mainly fed on D. occidentalis as well, consuming it two to four times faster than the NIS. In contrast, the benthic hermit crab mainly fed on the non-indigenous ascidian, feeding on it almost three times faster than it ate D. occidentalis. Hence, the non-indigenous ascidian likely faced reduced predation pressure in the marina fouling communities, increasing invasion risk. The study also examined several aspects of ascidian palatability, which showed that predator feeding was affected by differences in tunic structure. The study suggests that the different predators in the fouling and benthic communities in this marina have a role in the invasion of ascidians.

Wettability and Substrate Selection in the Larval Settlement of the Solitary Ascidian Phallusia philippinensis (Phlebobranchia: Ascidiidae).

For marine benthic animals, the selection of substrate by larvae is important for their survival, with early post-settlement mortality often being affected by the microenvironment where they settle. We tested the substrate preference of the larvae of the ascidian Phallusia philippinensis toward nine commercially available substrates. In the present assay, the larvae settled on one of four substrates for seven substrate combinations with different wettabilities; we counted the number of settled larvae on each of the four substrates, and Manly's selection indices were compared to determine the preference rank of each substrate. Larvae significantly preferred more hydrophobic and oleophilic substrates to hydrophilic and oleophobic ones. While it is uncertain how the larvae detect the properties of the substrate surface, they might be able to sense the physical force, such as stickiness and repellent force. Although a hydrophobic surface is not common in a natural marine environment, the use of hydrophobic materials (as flypaper-like tools) for ascidian larvae might help to prevent the settlement of non-indigenous ascidians in aquaculture facilities.

Iceland: a laboratory for non-indigenous ascidians

This work was partly supported by the Suðurnes Regional Development Fund under grant no. 34/2017. One of the authors (ARE) received two grants for stays for research staff in foreign centers from the University of Alicante (2018) and from the Generalitat Valenciana (BEST-2019 program).

Updating the list of recent non-indigenous ascidians (Chordata: Tunicata) and its spreading in the Mediterranean Sea. Ten years later (2009-2019)

Updating the list of recent non-indigenous ascidians (Chordata: Tunicata) and its spreading in the Mediterranean Sea. Ten years later (2009-2019)

Core and Dynamic Microbial Communities of Two Invasive Ascidians: Can Host–Symbiont Dynamics Plasticity Affect Invasion Capacity?

Ascidians (Chordata, Ascidiacea) are considered to be prominent marine invaders, able to tolerate highly polluted environments and fluctuations in salinity and temperature. Here, we examined the seasonal and spatial dynamics of the microbial communities in the inner-tunic of two invasive ascidians, Styela plicata (Lesueur 1823) and Herdmania momus (Savigny 1816), in order to investigate the changes that occur in the microbiome of non-indigenous ascidians in different environments. Microbial communities were characterized using next-generation sequencing of partial (V4) 16S rRNA gene sequences. A clear differentiation between the ascidian-associated microbiome and bacterioplankton was observed, and two distinct sets of operational taxonomic units (OTUs), one core and the other dynamic, were recovered from both species. The relative abundance of the dynamic OTUs in H. momus was higher than in S. plicata, for which core OTU structure was maintained independently of location. Ten and seventeen core OTUs were identified in S. plicata and H. momus, respectively, including taxa with reported capabilities of carbon fixing, ammonia oxidization, denitrification, and heavy-metal processing. The ascidian-sourced dynamic OTUs clustered in response to site and season but significantly differed from the bacterioplankton community structure. These findings suggest that the associations between invasive ascidians and their symbionts may enhance host functionality while maintaining host adaptability to changing environmental conditions.

Effect of Acetic acid treatment on the control of non-indigenous ascidians in farmed Indian pearl oyster Pinctada fucata

Effect of Acetic acid treatment on the control of non-indigenous ascidians in farmed Indian pearl oyster Pinctada fucata

Anthropogenic factors influencing invasive ascidian establishment in natural environments

Marine environments are constantly impacted by bioinvasions. Invasive ascidians (Chordata, Tunicata) are well-known for their ability to rapidly overgrow any available substrate. While the majority of studies have investigated the factors contributing to the successful establishment of ascidians on artificial substrates, the anthropogenic factors that contribute to such establishment on natural substrates have rarely been investigated. Here, we studied non-indigenous ascidians presence on natural substrate for the first time, using underwater field surveys at eight natural sites along the Israeli Mediterranean coast, in order to provide an analysis of factors assisting their establishment. The findings revealed that sites exposed to extended sewage-spill events experimented a reduction in native ascidian species. Understanding which factors alter ascidian population is essential for further monitoring efforts, to protect areas that are more susceptible to invasion, and for developing effective management tools to control further spread of invasive species in natural environments.

Monitoring the magnitude of marine vessel infestation by non-indigenous ascidians in the Mediterranean

Invasive ascidians (Chordata, Tunicata) are dominant nuisance organisms. The current study investigated the role of marine vessels in their dispersal and introduction. An examination of 45 dry-docked marine vessels, comprising recreational, commercial, and military craft, in five Israeli shipyards along the Mediterranean coast, revealed non-indigenous ascidians (NIA) on every second vessel investigated. Military vessels featured the highest ascidian abundance and richness, potentially related to their maintenance routine. Niche areas on the vessels such as sea chests and the propeller exhibited the highest occurrence of ascidians. Overall, these findings provide strong evidence that marine vessels play an acute role in NIA introduction and dispersal, with military vessels and niche areas on all the vessels being more susceptible to serving as vectors. A discovery of a new introduced species during the surveys suggests that the monitoring of marine vessels can serve as an effective tool for the early detection of NIA.

Richness and zoogeography of ascidians (Tunicata: Ascidiacea) in eastern Canada

Managers and policymakers in eastern Canada embrace science-based management of nonindigenous species and may benefit from having comprehensive regional species checklists at subnational jurisdictional levels. In this paper, regional checklists provide an account of the richness of ascidians in eastern Canada. Records of 58 ascidians resulted from reviewing 108 published sources, accessing data from two online databases, and collecting some common indigenous ascidian specimens. Analysis comparing the similarity of species among nine regions indicates that there is greater similarity in species composition between contiguous regions than between noncontiguous regions and suggests that there are four zoogeographic clusters in eastern Canada. Our checklists can inform managers and policymakers of the diversity of the ascidian taxa and can minimize taxonomic uncertainties of established nonindigenous and prospective invading species, for example, by identifying indigenous species that are congeners of nonindigenous species. The maintenance of checklists can be a valuable tool for the management of nonindigenous species as baselines to estimate changes in richness and to document the invasion status of nonindigenous species over time. For example, more importance can be placed on the spread of nonindigenous ascidians from one zoogeographic cluster to another than spread within the same cluster.

Simulated overfishing and natural eutrophication promote the relative success of a non-indigenous ascidian in coral reefs at the Pacific coast of Costa Rica

This study was supported by a German Academic Exchange Service (DAAD) scholarship to the first author. S. Carvalho is funded by the Saudi Aramco-KAUST Center for Marine Environmental Observations (SAKMEO). We thank the Centro de Investigacion en Ciencias del Mar y Limnologia (CIMAR) at the University of Costa Rica in San Jose for logistical support. We also would like to acknowledge the laboratory assistance team of the Leibniz Center for Tropical Marine Ecology (ZMT) D. Dasbach, M. Birkicht and D. Peterke. We thank Joao Curida for his artistry in the production of Figure 1, C. We thank the anonymous reviewers, and the editors of Aquatic Invasions for their careful reading of our manuscript and their insightful comments and suggestions.

Seasonal patterns of settlement of introduced and native ascidians in bivalve cultures in the Ebro Delta (NE Iberian Peninsula)

Seasonal patterns of settlement of introduced and native ascidians in bivalve cultures in the Ebro Delta (NE Iberian Peninsula)

Ongoing expansion of the worldwide invader Didemnum vexillum (Ascidiacea) in the Mediterranean Sea: high plasticity of its biological cycle promotes establishment in warm waters.

Non-indigenous ascidians are of particular concern to aquaculture industry and, paradoxically, the activities associated with it represent an important way to translocate these species worldwide. In 2012 a non-indigenous ascidian was found covering the oyster crops in the Ebro Delta (Western Mediterranean). We have identified the ascidian genetically and morphologically as Didemnum vexillum Kott, 2002. This finding indicates that the species is currently expanding its distribution in the Mediterranean Sea, as it has recently been found in the eastern basin (Venice, Adriatic Sea). Introduced populations of D. vexillum are found in temperate and cold waters worldwide, and a successful establishment in the Mediterranean implies a remarkable capacity of adaptability to warm, subtropical conditions. We assessed the life cycle (growth and reproduction) of the ascidian at the studied site. The species has a marked seasonal cycle, with regression in the warmest months and reappearance during winter. In spring D. vexillum reaches its maximum abundance, followed by a peak in reproduction just before regression. This cycle is reversed with respect to the one observed in colder waters, highlighting a plastic biological cycle of this invader and an hitherto unknown ability to establish itself in warm waters. We also analysed the genetic structure of the population of the Ebro Delta and the one established in the Lagoon of Venice using COI sequence data. The low genetic diversity in our samples (three haplotypes) was consistent with what is observed in the introduced populations worldwide. It is likely that the ascidian was introduced with oyster stock from bivalve cultures in the Atlantic French coasts, where the same three haplotypes have been reported. The high boating activity in the Ebro Delta makes further human-mediated transport of the species highly likely, and nearby fishing grounds can be severely affected if invaded. It is urgent to implement measures to prevent the continuous expansion of this ascidian pest in the Mediterranean.Electronic supplementary materialThe online version of this article (doi:10.1007/s10530-015-0861-z) contains supplementary material, which is available to authorized users.

Distribution of the non-indigenous colonial ascidian Didemnum vexillum (Kott, 2002) in the Bay of Fundy and on offshore banks, eastern Canada

The invasive colonial ascidian Didemnum vexillum (Kott, 2002) was initially discovered in the fall of 2013 near Parrsboro, Nova Scotia. A rapid response survey was conducted in April 2014 to confirm the presence of the species and to determine its distribution near the original detection site. Subsequent surveys between May and August 2014 examined the dredge contents collected during sea scallop stock assessment surveys on German Bank, northern Browns Bank, eastern Georges Bank and in the Bay of Fundy region. The presence of D. vexillum was confirmed at 22 of 30 stations sampled in four areas of the Minas Basin and Minas Channel region in the northern Bay of Fundy during the rapid response survey. The scallop surveys confirmed the presence of D. vexillum at 9 of 829 stations sampled in the Bay of Fundy region, including 7 in the Minas Basin, 1 off Digby Gut and another off the coast of Yarmouth. Due to the presence of a native species, D. albidum, in the region, a PCR assay was developed to distinguish D. vexillum from all other species in the region. Once the PCR assay was validated this assay was used to confirm all positive identifications in this study. Colonies overgrew rocks, bivalve shells and seaweeds or were retrieved as large dislodged fragments. They were in an overwintering state in April, but healthy, and observed to grow into dense mats in summer. In other regions of the world, D. vexillum has been reported to foul shellfish and aquaculture gear, smother benthic organisms such as the sea scallop (Placopecten magellanicus), and overgrow substrates, suggesting this new colonial invasive ascidian poses a potential threat to Eastern Canada aquaculture and commercial benthic fisheries.