RESUMEN
Rising occurrence of extreme warming events are profoundly impacting ecosystems, altering their functioning and services with significant socio-economic consequences. Particularly susceptible to heatwaves are intertidal shellfish beds, located in estuarine areas already stressed by factors such as rainfall events, red tides, eutrophication, and pollution. In Galicia, Northwestern Spain, these beds support vital shellfisheries, featuring the native clam Ruditapes decussatus and the non-indigenous R. philippinarum. Over recent decades, these populations have experienced notable abundance shifts due to various anthropogenic impacts, including climate change. In this habitat, patches of the seagrass Zostera noltei that coexist with bare sand can act as thermal refuges for benthic organisms such as clams. To assess the impact of heatwaves on these ecosystems, a mesocosm experiment was conducted. Juveniles of both clam species in two habitat types-bare sand and sand with Z. noltei-were exposed to simulated atmospheric heatwaves during diurnal low tide for four consecutive days. Subsequent transcriptomic analysis revealed that high temperatures had a more pronounced impact on the transcriptome of R. philippinarum compared to R. decussatus. The habitat type played a crucial role in mitigating heat stress in R. philippinarum, with the presence of Z. noltei notably ameliorating the transcriptomic response. These findings have direct applications in shellfishery management, emphasizing the importance of preserving undisturbed patches of Z. noltei as thermal refuges, contributing to the mitigation of heatwave effects on shellfish populations.
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Bivalvos , Transcriptoma , Animales , Ecosistema , Arena , Bivalvos/genética , Perfilación de la Expresión GénicaRESUMEN
The increased frequency of heatwaves expected in the context of global warming will affect socio-ecological systems such as shellfish beds at intertidal seagrass meadows. A mesocosm experiment was performed to assess the effects of a simulated atmospheric heatwave during low tide on the bioturbation indicators and growth of the commercial juvenile native Ruditapes decussatus and the introduced clam R. philippinarum, and on their interactions with the seagrass Zostera noltei. Under the heatwave, heat dissipation at 5 cm depth was significantly greater in the sediments below Z. noltei than below bare sand, the photosynthetic efficiency (Fv/Fm) of Z. noltei decreased and the clams tended to grow less. Furthermore, after the heatwave clams below bare sand tended to burrow deeper than those below Z. noltei, indicating that seagrass provided a refuge for clams. Ruditapes philippinarum grew less, and did not burrow as deeply as R. decussatus, which may imply greater vulnerability to desiccation and heat at low tide. The particle displacement coefficient (PDC) of R. philippinarum indicated lower bioturbation values in Z. noltei than in bare sand and was a suitable bioturbation indicator for juvenile Ruditapes spp. clams. In Z. noltei coexisting with R. philippinarum, the Fv/Fm values were higher than without clams after a recovery period, which may be linked to the assimilation of phosphate excreted by the clams and suggests a facilitative interaction. No such interaction was observed with R. deccusatus, probably because of its deeper burrowing depth. The findings suggest reciprocal facilitative interactions between R. philippinarum and Z. noltei and the potential contribution of Z. noltei to the sustainability of clams under global warming scenarios, which may support management actions aimed at enhancing the coexistence between shellfishing activities and seagrass conservation.
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Bivalvos , Arena , Animales , Mariscos , Alimentos Marinos , EcosistemaRESUMEN
Seagrass carbon stocks are vulnerable to physical disturbance. We assessed the effect of clam harvesting on the organic carbon (Corg) stocks in surface sediments in four intertidal Zostera noltei meadows on the Iberian Atlantic coast (Spain and Portugal), by comparing undisturbed and harvested areas. We also monitored the spatial cover of the meadows throughout the growing season. Sedimentary Corg content and Corg stocks were about four times lower in intensively harvested areas than in control areas, but there were not differences between areas with low harvesting pressure and control areas. Reductions of 53-85% in sedimentary Corg stocks of Z. noltei meadows were caused by intensive clam harvesting. The effect of intensive clam harvesting on Corg stocks increased throughout the growing season, but the area covered by the seagrass increased from 21 to 37%, suggesting rapid recovery of seagrass canopies and potential recovery of sedimentary Corg stocks.
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Bivalvos , Zosteraceae , Animales , Carbono , Secuestro de Carbono , Ecosistema , Sedimentos GeológicosRESUMEN
Salinity drops in estuaries after heavy rains are expected to increase in frequency and intensity over the next decades, with physiological and ecological consequences for the inhabitant organisms. It was investigated whether low salinity stress increases predation risk on three relevant commercial bivalves in Europe. In laboratory, juveniles of Venerupis corrugata, Cerastoderma edule, and the introduced Ruditapes philippinarum were subjected to low salinities (5, 10 and control 35) during two consecutive days and, afterwards, exposed to one of two common predators in the shellfish beds: the shore crab Carcinus maenas and the gastropod Bolinus brandaris, a non-indigenous species present in some Galician shellfish beds. Two types of choice experiment were done: one offering each predator one prey species previously exposed to one of the three salinities, and the other offering each predator the three prey species at the same time, previously exposed to one of the three salinities. Consumption of both predators and predatory behaviour of C. maenas (handling time, rejections, consumption rate) were measured. Predation rates and foraging behaviour differed, with B. brandaris being more generalist than C. maenas. Still, both predators consumed significantly more stressed (salinity 5 and 10) than non-stressed prey. The overall consumption of the native species C. edule and V. corrugata was greater than that of R. philippinarum, likely due to their vulnerability to low salinity and physical traits (e.g., thinner shell, valve gape). Increasing precipitations can alter salinity gradients in shellfish beds, and thus affect the population dynamics of harvested bivalves via predator-prey interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00227-021-03942-8.
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Designating and managing marine protected areas (MPAs) can mitigate many ocean threats. Banning fishing activities within MPAs enhances the robustness of food-web dynamics and thus increases trophic resilience. Ecosystem function indicators, such as mean trophic level, are increasingly applied in conservation management. Stable isotope analysis is a common tool in trophodynamic studies as it provides information about food sources and trophic level within food webs. In contrast to the traditional top-down approaches in conservation management (mainly for fisheries), this study focuses on bottom-up responses to protection according to the target species in regional small-scale fisheries. The present study aimed to examine how MPA status affects trophodynamics in the rocky reefs of the Illas Atlánticas Marine-Terrestrial National Park (Galicia, NW Spain). Results showed no differences between inside and outside the MPA in species stable isotopic signatures or trophic level. However, these results should be considered with caution due to some limitations in the study design (small number of sites per location, biogeographic differences associated with the island nature of the MPA, or seasonal variability). Nevertheless, the lax fishing management, the lack of proper implementation (the MPA was established in 2002 without a management plan until 2019), and the small size of the studied MPA may result in ineffective conservation outcomes that could have been reflected in the stable isotopic content of the food web. The large number of "paper park" MPAs existing worldwide are not only detrimental to the perception of marine protection, but also provide poor protection of marine ecosystems. Subject to further studies accounting for both environmental and management factors on stable isotope signatures, trophic interactions can form a cost-effective tool for monitoring MPA effectiveness.
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Conservación de los Recursos Naturales , Ecosistema , Animales , Explotaciones Pesqueras , Peces , Cadena Alimentaria , IsótoposRESUMEN
Heat waves are expected to increase in duration and frequency, impacting coastal ecosystems, especially intertidal organisms living near their thermal tolerance limits. Sedentary infaunal species are limited to some extent in escapes from sudden temperature changes, rather modifications to their physiology and behaviour are expected. This may lead to strong ecological and economic impacts on commercial bivalve species, such as Venerupis corrugata, Ruditapes decussatus, the introduced Ruditapes philippinarum and Cerastoderma edule, the most relevant in NW Spain. We investigated lethal and sublethal effects of heat during low tide on these species in the laboratory. Summer temperatures experienced within field, shallow sediments at approximately 2 cm depth i.e. 20 °C (control), 27 °C, 32 °C, and 37 °C, were replicated during four consecutive days and the diffusion of heat at the burrowing depth of each species was estimated; temperature exposure was expressed as degree hours above 22 °C. After two days of tidal exposure, C. edule and V. corrugata suffered significant mortalities, and also the most dramatic decrease in scope for growth (SFG) as well as reduction in burrowing activity. After four days under stress, all species had negative SFG. On recovery, species showed compensation at longer exposures, particularly C. edule. These effects of temperature on mortality, growth potential and burrowing ability may increase the time to achieve commercial size and exposure to predation. Particularly, V. corrugata, with a center of distribution lower in the intertidal and subtidal, and C. edule, shallower in the sediment, may be the most affected. Clearly the intensity and frequency of heat waves will affect these key species in the intertidal sediment flats changing ecosystem functioning and fisheries management strategies.
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Bivalvos , Cardiidae , Animales , Ecosistema , Calor , EspañaRESUMEN
The abundance and distribution of intertidal canopy-forming macroalgae are threatened by the increase in sea surface temperature and in the frequency and intensity of heatwaves caused by global warming. This study evaluated the physiological response of predominant intertidal macroalgae in the NW Iberian Peninsula (Bifurcaria bifurcata, Cystoseira tamariscifolia and Codium tomentosum) to increased seawater temperature during immersion and increased air temperatures during consecutive emersion cycles. We combined field mensuration and laboratory experiments in which we measured mortality, growth, maximum quantum yield and C:N content of the macroalgae. Air temperature was a critical factor in determining physiological responses and survivorship of all species, whereas high seawater temperature had sublethal effects. Cystoseira tamariscifolia suffered the greatest decreases in Fv/Fm, growth and the highest mortality under higher air temperatures, whereas C. tomentosum was the most resistant and resilient species. Two consecutive cycles of emersion under atmospheric heatwaves caused cumulative stress in all three macroalgae, affecting the physiological performance and increasing the mortality. The potential expansion of the warm-temperate species B. bifurcata, C. tamariscifolia and C. tomentosum in the NW Iberian Peninsula in response to increasing seawater temperature may be affected by the impact of increased air temperature, especially in a region where the incidence of atmospheric heatwaves is expected to increase.
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Chlorophyta/fisiología , Sargassum/fisiología , Algas Marinas/fisiología , Calentamiento Global , Portugal , EspañaRESUMEN
Microbial biofilms can be key mediators for settlement of macrofoulers. The present study examines the coupled effects of microbial biofilms and local environmental conditions on the composition, structure and functioning of macrofouling assemblages. Settlement of invertebrates over a gradient of human-impacted sites was investigated on local biofilms and on biofilms developed in marine protected areas (MPAs). Special attention was given to the presence of non-indigenous species (NIS), a global problem that can cause important impacts on local assemblages. In general, the formation of macrofouling assemblages was influenced by the identity of the biofilm. However, these relationships varied across levels of anthropogenic pressure, possibly influenced by environmental conditions and the propagule pressure locally available. While the NIS Watersipora subatra seemed to be inhibited by the biofilm developed in the MPA, Diplosoma cf. listerianum seemed to be attracted by biofilm developed in the MPA only under mid anthropogenic pressure. The obtained information is critical for marine environmental management, urgently needed for the establishment of prevention and control mechanisms to minimize the settlement of NIS and mitigate their threats.
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Bacterias/metabolismo , Biopelículas , Incrustaciones Biológicas , Invertebrados/fisiología , Aizoaceae/microbiología , Animales , Biopelículas/crecimiento & desarrollo , Briozoos/microbiología , Diatomeas/microbiología , Diatomeas/fisiología , Biología Marina , Presión , Agua de Mar/microbiología , EspañaRESUMEN
The impact of invasive species on recipient communities can vary with environmental context and across levels of biological complexity. We investigated how an established invasive seaweed species affected the biomass, eco-physiology, carbon and nitrogen storage capacity of native seaweeds at sites with a different environmental setting due to a persistent upwelling in northern Spain. We removed the invasive Japanese wireweed Sargassum muticum from intertidal rock pools once every month during a one-year period and used an in-situ stable isotope pulse-chase labeling to estimate gross primary production (GPP), nitrogen uptake rate, 13C-carbon and 15N-nitrogen storage capacities. Following the addition of 13C-enriched bicarbonate and 15N-enriched nitrate to the seawater in the rock pools during the period of the low tide, we sampled macroalgal thalli at incoming tide to determine label uptake rate. After four days, we sampled macroalgal assemblages to determine both label storage capacity and biomass. After one year of removal there was no change in the macroalgal assemblage. However, both the GPP and 13C-carbon storage capacity were higher in the turf-forming Corallina spp. and, sometimes, in the canopy-forming Bifurcaria bifurcata. Nitrogen uptake rate followed similar, but more variable results. Although S. muticum inhibited carbon storage capacity of native species, the assemblage-level 13C-carbon storage was similar in the S. muticum-removed and control rock pools because the presence of the invasive species compensated for the functional loss of native species, particularly at sites where it was most abundant. No obvious effects were observed in relation to the environmental setting. Overall, the effect of the invasive S. muticum on carbon flow appeared to be mediated both by the effects on resource-use efficiency of native species and by its own biomass. Integrating physiological and assemblage-level responses can provide a broad understanding of how invasive species affect recipient communities and ecosystem functioning.
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Especies Introducidas/tendencias , Microalgas/crecimiento & desarrollo , Algas Marinas/crecimiento & desarrollo , Biodiversidad , Biomasa , Carbono/metabolismo , Ecosistema , Microalgas/metabolismo , Nitrógeno/metabolismo , Sargassum/fisiología , Agua de Mar/análisis , Agua de Mar/química , Algas Marinas/fisiología , EspañaRESUMEN
Habitat-forming species sustain biodiversity and ecosystem functioning in harsh environments through the amelioration of physical stress. Nonetheless, their role in shaping patterns of species distribution under future climate scenarios is generally overlooked. Focusing on coastal systems, we assess how habitat-forming species can influence the ability of stress-sensitive species to exhibit plastic responses, adapt to novel environmental conditions, or track suitable climates. Here, we argue that habitat-former populations could be managed as a nature-based solution against climate-driven loss of biodiversity. Drawing from different ecological and biological disciplines, we identify a series of actions to sustain the resilience of marine habitat-forming species to climate change, as well as their effectiveness and reliability in rescuing stress-sensitive species from increasingly adverse environmental conditions.
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Biodiversidad , Cambio Climático , Ecosistema , Adaptación Fisiológica , Refugio de Fauna , Especificidad de la EspecieRESUMEN
The invasive mussel Xenostrobus securis was recorded for the first time in the Galician Rias Baixas (NW Spain) in 2007, within an area characterized by intense commercial culture of Mytilus galloprovincialis. The main aims of this study were to evaluate whether an immunological assay can be used to detect larvae of this species in field samples of plankton and to determine whether the distribution of larvae matched that of adults. The ability of two monoclonal antibodies to recognize the bivalve was tested by immunofluorescence. Only the M22.8 antibody recognized X. securis larvae. The staining pattern distinguished X. securis from M. galloprovincialis larvae in both laboratory cultures and field samples of plankton. The distribution of larvae did not match that of adults. This tool may prove very useful for monitoring the presence of this invasive species in the plankton, allowing rapid and specific recognition.
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Técnica del Anticuerpo Fluorescente Indirecta/métodos , Especies Introducidas , Mytilidae/inmunología , Plancton/inmunología , Animales , Anticuerpos Monoclonales , Acuicultura , Larva/inmunología , Mytilus , Reproducibilidad de los Resultados , EspañaRESUMEN
The green alga Codium fragile ssp. fragile (hereafter C. fragile) has long been assumed to outcompete and displace its native congeners via cryptic invasion. We analysed the population dynamics of the exotic C. fragile and native congeners and their relative abundance on intertidal shores in N-NW Spain. Our results did not support the existence of current competitive displacement by the exotic species. The presence of C. fragile was clearly seasonal, while the native C. tomentosum was more persistent throughout the year, due to a higher frequency of frond sprouting from perennial basal fragments. However, our results also indicated an increase in the proportion of C. fragile relative to native species towards inner areas of the Bay of Biscay, which was correlated with environmental gradients. The greater tolerance of C. fragile to environmental stress and its opportunistic abilities may favour establishment and spread of the species under a warming scenario.
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Chlorophyta/fisiología , Ecosistema , Ecología , Dinámica Poblacional , EspañaRESUMEN
Estuarine bivalves are especially susceptible to salinity fluctuations. Stage-specific sensibilities may influence the structure and spatial distribution of the populations. Here we investigate differences on the energetic strategy of thread drifters (3-4 mm) and sedentary settlers (9-10 mm) of Cerastoderma edule over a wide range of salinities. Several physiological indicators (clearance, respiration and excretion rates, O:N) were measured during acute (2 days) and acclimated responses (7 days of exposure) for both size classes. Our results revealed a common lethal limit for both developmental stages (Salinity 15) but a larger physiological plasticity of thread drifters than sedentary settlers. Acclimation processes in drifters were initiated after 2 days of exposure and they achieved complete acclimation by day 7. Sedentary settlers delay acclimation and at day 7 feeding activity had not resumed and energetic losses through respiration and excretion were higher at the lowest salinity treatment. Different responses facing salinity stress might be related to differences in habitat of each stage. For sedentary settlers which occupy relatively stable niches, energy optimisation include delaying the initiation of the energetically expensive acclimation processes while drifters which occupy less stable environments require a more flexible process which allow them to optimize energy acquisition as fast as possible.
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Poor physiological acclimatization to climate change has led to shifts in the distributional ranges of various species and to biodiversity loss. However, evidence also suggests the relevance of non-climatic physical factors, such as light, and biotic factors, which may act in interactive or additive way. We used a mechanistic approach to evaluate the ecophysiological responses of four seaweed species (three dominant intertidal fucoids, Fucus serratus, Ascophyllum nodosum, Bifurcaria bifurcata, and the invasive Sargassum muticum) to different conditions of grazing, light irradiance and ultraviolet (UV) radiation. We performed a large-scale mesocosm experiment with a total of 800 individual thalli of macroalgae. The factorial experimental design included major algal traits, photoacclimation, nutrient stoichiometry and chemical defence as response variables. Few significant effects of the factors acting alone or in combination were observed, suggesting a good capacity for acclimatization in all four species. The significant effects were generally additive and there were no potentially deleterious synergistic effects between factors. Fucus serratus, a species currently undergoing a drastic contraction of its southern distribution limit in Europe, was the most strongly affected species, showing overall lower photosynthetic efficiency than the other species. The growth rate of F. serratus decreased when UV radiation was filtered out, but only in the presence of grazers. Moreover, more individuals of this species tended to reach maturity in the absence of grazers, and the nitrogen content of tissues decreased under full-spectrum light. Only the phlorotannin content of tissues of B. bifurcata and of exudates of A. nodosum, both slow-growing species, were positively affected by respectively removal of UVB radiation and the presence of grazers. The findings for S. muticum, a well-established invasive seaweed across European coasts, suggested similar physiological response of this fast-growing species to different levels of grazing activity and light quality/intensity. As expected, this species grew faster than the other species. Bifurcaria bifurcata and A. nodosum only showed minor effects of light quality and grazing on phlorotannins content, which suggests good resistance of these two long-lived species to the experimental conditions. Mechanistic approaches that are designed to analyse interactive effects of physical and biotic factors provide an understanding of physiological responses of species and help to improve the confidence of predictive distribution models.
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Adaptación Fisiológica , Algas Marinas/fisiología , Cambio Climático , Monitoreo del Ambiente , Europa (Continente) , Fucus/fisiología , Especies Introducidas , Phaeophyceae/fisiologíaRESUMEN
Different combinations of behavioural and physiological responses may play a crucial role in the ecological success of species, notably in the context of biological invasions. The invasive mussel Xenostrobus securis has successfully colonised the inner part of the Galician Rias Baixas (NW Spain), where it co-occurs with the commercially-important mussel Mytilus galloprovincialis. This study investigated the effect of a heatwave on the physiological and behavioural responses in monospecific or mixed aggregations of these species. In a mesocosm experiment, mussels were exposed to simulated tidal cycles and similar temperature conditions to those experienced in the field during a heat-wave that occurred in the summer of 2013, when field robo-mussels registered temperatures up to 44.5°C at low tide. The overall responses to stress differed markedly between the two species. In monospecific aggregations M. galloprovincialis was more vulnerable than X. securis to heat exposure during emersion. However, in mixed aggregations, the presence of the invader was associated with lower mortality in M. galloprovincialis. The greater sensitivity of M. galloprovincialis to heat exposure was reflected in a higher mortality level, greater induction of Hsp70 protein and higher rates of respiration and gaping activity, which were accompanied by a lower heart rate (bradycardia). The findings show that the invader enhanced the physiological performance of M. galloprovincialis, highlighting the importance of species interactions in regulating responses to environmental stress. Understanding the complex interactions between ecological factors and physiological and behavioural responses of closely-related species is essential for predicting the impacts of invasions in the context of future climate change.
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Mytilidae/fisiología , Estrés Fisiológico , Animales , Cambio Climático , Rayos Infrarrojos , Especies Introducidas , Mytilidae/clasificación , Especificidad de la EspecieRESUMEN
We examined the patterns of distribution and abundance, and reproductive traits (presence of gametophytes and size at time of reproduction) in the invasive Codium fragile ssp. fragile and the native C. tomentosum and C. vermilara on intertidal habitats of NW Spain at two dates. All three species coexist in the locations and habitats studied, although abundances were low. We found a greater proportion of C. fragile ssp. fragile towards the east of the Cantabrian coast and on upper levels on the shore, where conditions are more stressful. The proportion of thalli bearing gametangia in C. fragile ssp. fragile was greater than in the native species in all habitats. The presence of gametangia was size-dependent for all species, with the invasive species maturing at a smaller size, which combined with the previous features, might confer competitive advantages to this species over the native species. We also demonstrated that molecular analyses are necessary for the correct identification of C. fragile subspecies.
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Chlorophyta/fisiología , Especies Introducidas , Chlorophyta/clasificación , Chlorophyta/genética , Densidad de Población , Dinámica Poblacional , EspañaRESUMEN
Ongoing changes in natural diversity due to anthropogenic activities can alter ecosystem functioning. Particular attention has been given to research on biodiversity loss and how those changes can affect the functioning of ecosystems, and, by extension, human welfare. Few studies, however, have addressed how increased diversity due to establishment of nonindigenous species (NIS) may affect ecosystem function in the recipient communities. Marine algae have a highly important role in sustaining nearshore marine ecosystems and are considered a significant component of marine bioinvasions. Here, we examined the patterns of respiration and light-use efficiency across macroalgal assemblages with different levels of species richness and evenness. Additionally, we compared our results between native and invaded macroalgal assemblages, using the invasive brown macroalga Sargassum muticum (Yendo) Fensholt as a model species. Results showed that the presence of the invader increased the rates of respiration and production, most likely as a result of the high biomass of the invader. This effect disappeared when S. muticum lost most of its biomass after senescence. Moreover, predictability-diversity relationships of macroalgal assemblages varied between native and invaded assemblages. Hence, the introduction of high-impact invasive species may trigger major changes in ecosystem functioning. The impact of S. muticum may be related to its greater biomass in the invaded assemblages, although species interactions and seasonality influenced the magnitude of the impact.
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Ecosystem engineers such as mussels may affect strongly both the structure of benthic assemblages and the ecosystem functioning. The black-pygmy mussel Limnoperna securis is an invasive species that is spreading along the Galician coast (NW Spain). Its current distribution overlaps with the distribution of the commercial native mussel species Mytilus galloprovincialis, but only in the inner part of two southern Galician rias. Here, we analysed the assemblages associated with clumps of the two mussel species and evaluated if the invasive species increased complexity of habitat. To measure complexity of clumps we used a new method modified from the "chain and tape" method. Results showed that the identity of the mussel influenced macrofaunal assemblages, but not meiofauna. L. securis increased the complexity of clumps, and such complexity explained a high percentage of variability of macrofauna. The shift in dominance from M. galloprovincialis to L. securis may alter habitat structure and complexity, affecting the macrofaunal assemblages with unpredictable consequences on trophic web relations.
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Organismos Acuáticos/fisiología , Biota , Ecosistema , Especies Introducidas , Mytilidae/fisiología , Animales , Estuarios , EspañaRESUMEN
Invasive species represent a serious threat to natural ecosystems through a range of negative effects on native species in the region invaded. The invasive species Sargassum muticum has invaded several temperate regions worldwide including the Galician rocky shoreline (northwestern Spain) in Western Europe. The main aim of this study was to assess if colonization by S. muticum has any effect on native algal assemblages by experimental removal of S. muticum. We predicted that in those plots where S. muticum plants were removed, the structure of native algal assemblages would differ from that in plots where S. muticum plants were untouched. In addition, we predicted that the effect of Sargassum removal would be more important than other causes of variability at the small scale investigated. Results indicated limited impact of S. muticum on native assemblages. The impact was only evident on the total number of native taxa and two understory morpho-functional groups, filamentous and foliose algae, rather than on the entire macroalgal assemblages.