Fig 7 - uploaded by Nikos Andreakis
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2 Life cycle of the invasive red genus Asparagopsis. White arrow indicates the harpoon-like structures characteristic of A. armata which are absent in A. taxiformis. F!: fecundation; R!: meiosis, n: ploidy level
Source publication
Molecular phylogeography has for decades been a frequently used approach to delineate novel evolutionarily significant units (ESUs) and to study the dynamics of invasive species. Next-generation sequencing technology (NGS) and the use of environmental DNA (eDNA) have the potential to revolutionize our way of understanding biodiversity and to establ...
Citations
... The alien Rhodophyte Asparagopsis armata was probably introduced in the western Mediterranean Sea during the 1920s and is now widely distributed throughout the basin Zanolla and Andreakis 2016). A. armata has a heteromorphic life-history with a small filamentous tetrasporophytic phase and a mid-size erect gametophytic phase. ...
... Initially A. taxiformis had colonized only a part of the eastern Mediterranean Sea, but during the 1990s the species' records throughout the basin multiplied and various established invasive populations were reported all over the Mediterranean . This is probably because A. taxiformis is composed of multiple genetically distinct lineages of uncertain taxonomic status (Andreakis et al. 2007(Andreakis et al. , 2009(Andreakis et al. , 2016Zanolla et al. 2014Zanolla et al. , 2015 that have invaded the Mediterranean at different phases. Molecular analyses revealed that two strains exist in the Mediterranean Sea, a strain of Indo-Pacific origin, which is quite widespread in the western basin, but also in the Adriatic Sea and Greece, and a less invasive strain of tropical Atlantic origin, found in the eastern Mediterranean Sea (Andreakis et al. 2007(Andreakis et al. , 2009Verlaque et al. 2015). ...
Biological invasions have become a defining feature of marine Mediterranean ecosystems with significant impacts on biodiversity, ecosystem services, and human health. We systematically reviewed the current knowledge on the impacts of marine biological invasions in the Mediterranean Sea. We screened relevant literature and applied a standardised framework that classifies mechanisms and magnitude of impacts and type of evidence. Overall, 103 alien and cryptogenic species were analysed, 59 of which were associated with both negative and positive impacts, 17 to only negative, and 13 to only positive; no impacts were found for 14 species. Evidence for most reported impacts (52%) was of medium strength, but for 32% of impact reports evidence was weak, based solely on expert judgement. Only 16% of the reported impacts were based on experimental studies. Our assessment allowed us to create an inventory of 88 alien and cryptogenic species from 16 different phyla with reported moderate to high impacts. The ten worst invasive species in terms of reported negative impacts on biodiversity include six algae, two fishes, and two molluscs, with the green alga Caulerpa cylindracea ranking first. Negative impacts on biodiversity prevailed over positive ones. Competition for resources, the creation of novel habitat through ecosystem engineering, and predation were the primary reported mechanisms of negative effects. Most cases of combined negative and positive impacts on biodiversity referred to community-level modifications. Overall, more positive than negative impacts were reported on ecosystem services, but this varied depending on the service. For human health, only negative impacts were recorded. Substantial variation was found among Mediterranean ecoregions in terms of mechanisms of impact and the taxonomic identity of impacting species. There was no evidence that the magnitude of impact increases with residence time. Holistic approaches and experimental research constitute the way forward to better understanding and managing biological invasions.
... Due to increasing globalization, an unprecedented number of introduced species are entering new ecosystems (Bax et al., 2003). These introductions are becoming more frequent, due to widespread global trade and shipping (Ruiz et al., 2000;Byers and Pringle, 2006;Zanolla and Andreakis, 2016). Despite increasing efforts to reduce the risk of invasion along multiple routes of introduction, recent estimates indicate that the rate at which invasive species are detected shows no signs of slowing (Seebens, 2017). ...
Biological invasions have the capacity to introduce non-native parasites. This study aimed to determine whether the invasive green crab population, Carcinus spp., on the Southwestern Atlantic coast of Argentina harbours any symbionts, and whether these may spillover or spillback between native crabs, Cyrtograpsus altimanus and C. angulatus. Macroscopy, histology, and molecular analyses of some parasites were used to describe and compare their diversity across the three species of crab. We also evaluated the susceptibility of invasive Carcinus spp. to a native digenean, Maritrema madrynense, via experimental infections (exposure and cohabitation).
Our results revealed that the green crab pathobiome included similar symbiotic groups to native crabs. This included putative viral, bacterial, and protozoan parasites. Haplosporidium-like observations were recorded in all crab species, and a single green crab was found to be parasitized by an Agmasoma-like microsporidium. Metagenomic analysis of one individual revealed additional symbiotic diversity (46 bacteria, 5 eukaryotic species). The green crabs were infected by more microparasite taxa than the native crabs (5:3). Wild populations of Carcinus spp. were free of metazoan parasites and are shown not to be susceptible to M. madryense under experimental conditions.
Our results suggest a reduction/escape of macroparasites (trematode Maritrema madrynense; acanthocephalan Profilicollis chasmagnathi) in invasive Carcinus spp. compared to their native competitors.
... (García et al., 2018). Due to the wide physiological adaptations of C. fragile and its preference for higher temperatures during the reproductive season (Hanisak, 1979), new potential niches for its settlement are proliferating under current climatic conditions (Zanolla & Andreakis, 2016). Spatio-temporal information of native and invasive Codium spp. is crucial for evaluating whether patterns of competitive displacement or coexistence take place in Cantabrian Sea, where rising sea-surface temperatures have favored the spread of warm-water nonindigenous species over the past three decades (Díez, Muguerza, Santolaria, Ganzedo, & Gorostiaga, 2012). ...
... In addition, the taxonomic identification of different Codium spp. based on phenotypic traits is particularly challenging (Zanolla & Andreakis, 2016), often requiring molecular identification. Therefore, a more rapid and accurate detection tool is needed to monitor and/or control the distribution of invasive seaweed, which is less weather and tide dependent and incorporates the advantages of molecular identification. ...
... eDNA has proved useful for the detection of aquatic invertebrates (Deiner, Fronhofer, Mächler, Walser, & Altermatt, 2016;Mächler, Deiner, Steinmann, & Altermatt, 2014) and vertebrates (Piaggio et al., 2014;Sigsgaard et al., 2016;Takahara et al., 2013), but the information on the aquatic plants and algae is still limited. Only a few studies have addressed the detectability of aquatic plants or algae with eDNA (Fujiwara, Matsuhashi, Doi, Yamamoto, & Minamoto, 2016;Keller, Hilderbrand, Shank, & Potapova, 2017;Scriver, Marinich, Wilson, & Freeland, 2015;Zimmermann, Glöckner, Jahn, Enke, & Gemeinholzer, 2015), due to the limited availability of reference databases (Cristescu, 2014) and the lineage-specific barcodes (Zanolla & Andreakis, 2016). To be useful for detecting seaweed, eDNA barcodes need to be specific (Verbruggen et al., 2010) and have a suitable resolution across multiple regions (Zanolla & Andreakis, 2016) within the suspected introduced range of targeted taxa (Geller, Darling, & Carlton, 2010). ...
Aim:
Codium fragile, an invasive seaweed, has spread widely during the last century, impacting on local seaweed communities through competition and disturbance. Early detection of C. fragile can help on its control and management. Environmental DNA (eDNA) has proved successful for early detection of aquatic invasive species but its potential use for seaweed remains understudied. We used a species-specific eDNA qPCR approach to investigate the spatial distribution, abundance, and coexistence of the invasive C. fragile and three native Codium species (Codium vermilara, Codium tomentosum, and Codium decorticatum) in the Cantabrian Sea.
Location:
Bay of Biscay, Northern Atlantic Coast of the Iberian Peninsula; two ports, a beach and a rocky cliff.
Methods:
We designed species-specific primers in barcoding regions targeting short fragments of the rbcL gene for the invasive Codium species, and the elongation factor Tu (tufA) gene for the native species, to assess their spatial and seasonal distributions using quantitative real-time PCR in samples collected during summer, autumn, and winter.
Results:
We found seasonal differences in the presence of the invasive Codium fragile and two of the native Codium species, but did not detect C. decorticatum at any point. Species distribution patterns produced with qPCR targeting species-specific eDNA coincided with the known distribution based on previous conventional sampling, with a seasonal alternance of C. fragile and C. vermilara, and a marked dominance of invasive C. fragile in ports, which are known hotspots for invasive species.
Main conclusions:
Our results demonstrate the utility of using eDNA for early detection and monitoring of invasive seaweed. Native and invasive Codium spp. displayed significant seasonal and spatial differentiation that needs to be taken into account in risk management. Regular monitoring of ports and adjacent areas using eDNA should help to assess the potential expansion of invasive Codium and the need for management interventions to avoid the displacement of native seaweed.
... Presently, community interactions among freeliving and parasitic species are being modified, disrupted, or even augmented by the establishment of novel species into marine systems around the world (Ruiz et al. 1999, Prenter et al. 2004, Dunn & Hatcher 2015, Jackson 2015. These introductions are becoming increasingly frequent given progressively efficient and widespread global trade and shipping methods (Ruiz et al. 2000, Seebens et al. 2013 which have made species boundaries more fluid in recent decades (Byers & Pringle 2006, Zanolla & Andreakis 2016. Consequently, the community ecology and evolutionary biology of numerous marine biota are being influenced by novel and highly dynamic ecological forces and species interactions (Lavergne et al. 2010, Viard et al. 2016, including tightly linked symbiotic relationships (e.g. ...
Invasive species can introduce parasites to, and/or acquire new parasites from, novel regions, thereby greatly influencing community interactions, including symbiotic relationships involving parasites. Host-switching of native and non-native parasites could enhance or dilute parasite transmission and spread among hosts. We investigated the effect of host invasion on trematode parasitism in 2 Newfoundland (Canada) bays: one invaded by European green crabs Carcinus maenas and the other not yet invaded. To determine the influence of C. maenas on host-parasite relationships, we assessed trematode prevalence in 3 native hosts: 2 Littorina spp. snails and Atlantic rock crabs Cancer irroratus (first- and second-intermediate hosts for microphallid trematodes, respectively). We found no difference in trematode prevalence between the bays among the 4 host species. However, cyst abundance was significantly higher in C. maenas versus C. irroratus in the bay where the crab distributions overlap, while it was lower in C. irroratus in the invaded versus uninvaded bay, suggesting a dilution of infection in the native host. Sequencing data of microphallid trematodes detected 4 genetically divergent lineages: a cosmopolitan lineage found in all host species; 2 lineages dominant in C. irroratus , suggesting a native origin for the trematodes that now use C. maenas as an additional host; and 1 lineage represented just in C. maenas in Europe. This is the first study to demonstrate the magnitude of trematode infection in crab hosts in Newfoundland, including the commercially valuable native C. irroratus . Our results demonstrate the influence that species introductions can have on parasite life cycles in native systems under recent host invasion.
... Both Asparagopsis species are considered among the "worst invasive alien species threatening biodiversity in Europe" (EEA 2007) and among the "100 worst invasive seaweeds in the Mediterranean Sea" ( Streftaris and Zenetos 2006). Genetic studies have confirmed two cryptic lineages (L1, L2) in the cold-temperate A. armata and six (L1 to L6) in the tropical A. taxiformis ( Andreakis et al. 2004, 2016, Dijoux et al. 2014). Due to their cryptogenic status, the native range of each lineage remains undetermined ( Dijoux et al. 2014). ...
The mitochondrial genetic diversity, distribution and invasive potential of multiple cryptic OTUs of the red invasive seaweed Asparagopsis were assessed by studying introduced Mediterranean and Hawaiian populations. Invasive behavior of each Asparagopsis OTU was inferred from phylogeographic reconstructions, past historical demographic dynamics, recent range expansion assessments and future distributional predictions obtained from demographic models. Genealogical networks resolved Asparagopsis gametophytes and tetrasporophytes into four A. taxiformis and one A. armata cryptic OTUs. Falkenbergia isolates of A. taxiformis L3 were recovered for the first time in the western Mediterranean Sea and represent a new introduction for this area. Neutrality statistics supported past range expansion for A. taxiformis L1 and L2 in Hawaii. On the other hand, extreme geographic expansion and an increase in effective population size were found only for A. taxiformis L2 in the western Mediterranean Sea. Distribution models predicted shifts of the climatically suitable areas and population expansion for A. armata L1 and A. taxiformis L1 and L2. Our integrated study confirms a high invasive risk for A. taxiformis L1 and L2 in temperate and tropical areas. Despite the differences in predictions among modelling approaches, a number of regions were identified as zones with high invasion risk for A. taxiformis L2. Since range shifts are likely climate-driven phenomena, future invasive behavior cannot be excluded for the rest of the lineages.
In this study we present basic population data of the red macroalga Asparagopsis taxiformis, widely recognized as invasive in the Mediterranean Sea. A 13-month field study was carried out on a population located in southern Spain, addressing its phenology, population dynamics and demography. We further tested whether biomass variations were related to environmental variables at the study site. Gametophytes were present year-round while tetrasporophytes were only found in spring and summer. Recruitment capacity and vegetative growth of the gametophytes are discussed as important modulators for the population structure and enhancers of its persistence. Thallus size-time histograms revealed a high prevalence of small shoots that showed high mortality that was not related to self-thinning. Biomass of A. taxiformis was higher from March to July. Vegetative growth was the main way the gametophyte population was maintained, although the presence of tetrasporophytes and fertile gametophytes in the field confirms that sexual reproduction also occurs. Its continuous and high recruitment, in terms of the number of smallest shoots, makes this southern population of A. taxiformis a source of future invasive populations due to the intensive maritime traffic in the region.