For marine meta-populations with source-sink dynamics knowledge about genetic connectivity is important to conserve biodiversity and design marine protected areas (MPAs). We evaluate connectivity of a Mediterranean sessile species, Pinna nobilis. To address a large geographical scale, partial sequences of cytochrome oxidase I (COI, 590 bp) were used to evaluate phylogeographical patterns in the Western Mediterranean, and in the whole basin using overlapping sequences from the literature (243 bp). Additionally, we combined (1) larval trajectories based on oceanographic currents and early life-history traits and (2) 10 highly polymorphic microsatellite loci collected in the Western Mediterranean. COI results provided evidence for high diversity and low inter-population differentiation. Microsatellite genotypes showed increasing genetic differentiation with oceanographic transport time (isolation by oceanographic distance (IBD) set by marine currents). Genetic differentiation was detected between Banyuls and Murcia and between Murcia and Mallorca. However, no genetic break was detected between the Balearic populations and the mainland. Migration rates together with numerical Lagrangian simulations showed that (i) the Ebro Delta is a larval source for the Balearic populations (ii) Alicante is a sink population, accumulating allelic diversity from nearby populations. The inferred connectivity can be applied in the development of MPA networks in the Western Mediterranean.
Exotic species often face new environmental conditions that are different from those that they are adapted to. The tropical seagrass Halophila stipulacea is a Lessepsian migrant that colonized the Mediterranean Sea around 100 years ago, where at present the minimum seawater temperature is cooler than in its native range in the Red Sea. Here, we tested if the temperature range in which H. stipulacea can exist is conserved within the species or if the exotic populations have shifted their thermal breadth and optimum due to the cooler conditions in the Mediterranean. We did so by comparing the thermal niche (e.g. optimal temperatures, and upper and lower thermal limits) of native (Saudi Arabia in the Red Sea) and exotic (Greece and Cyprus in the Mediterranean Sea) populations of H. stipulacea . We exposed plants to 12 temperature treatments ranging from 8 to 40°C for 7 days. At the end of the incubation period, we measured survival, rhizome elongation, shoot recruitment, net population growth and metabolic rates. Upper and lower lethal thermal thresholds (indicated by 50% plant mortality) were conserved across populations, but minimum and optimal temperatures for growth and oxygen production were lower for Mediterranean populations than for the Red Sea one. The displacement of the thermal niche of exotic populations towards the colder Mediterranean Sea regime could have occurred within 175 clonal generations.
Marine macrophytes, especially macroalgae, form highly productive ecosystems, with a global net primary production of about 2 Pg C year −1 spread across 4 million km 2 in coastal areas (Duarte, 2017). Marine macrophytes export most of their net production to the global ocean and seafloor (Duarte & Cebrián, 1996;
The introduction and establishment of exotic species often result in significant changes in recipient communities and their associated ecosystem services. However, usually the magnitude and direction of the changes are difficult to quantify because there is no pre‐introduction data. Specifically, little is known about the effect of marine exotic macrophytes on organic carbon sequestration and storage. Here, we combine dating sediment cores (210Pb) with sediment eDNA fingerprinting to reconstruct the chronology of pre‐ and post‐arrival of the Red Sea seagrass Halophila stipulacea spreading into the Eastern Mediterranean native seagrass meadows. We then compare sediment organic carbon storage and burial rates before and after the arrival of H. stipulacea and between exotic (H. stipulacea) and native (C. nodosa and P. oceanica) meadows since the time of arrival following a Before‐After‐Control‐Impact (BACI) approach. This analysis revealed that H. stipulacea arrived at the areas of study in Limassol (Cyprus) and West Crete (Greece) in the 1930s and 1970s, respectively. Average sediment organic carbon after the arrival of H. stipulacea to the sites increased in the exotic meadows twofold, from 8.4 ± 2.5 g Corg m−2 year−1 to 14.7 ± 3.6 g Corg m−2 year−1, and, since then, burial rates in the exotic seagrass meadows were higher than in native ones of Cymodocea nodosa and Posidonia oceanica. Carbon isotopic data indicated a 50% increase of the seagrass contribution to the total sediment Corg pool since the arrival of H. stipulacea. Our results demonstrate that the invasion of H. stipulacea may play an important role in maintaining the blue carbon sink capacity in the future warmer Mediterranean Sea, by developing new carbon sinks in bare sediments and colonizing areas previously occupied by the colder thermal affinity P. oceanica.
The spread of exotic species to new areas can be magnified when favored by future climatic conditions. Forecasting future ranges using species distribution models (SDMs) could be improved by considering physiological thresholds, because models solely based on occurrence data cannot account for plasticity due to acclimation of individuals to local conditions over their life-time or to adaptation due to selection within local populations. This is particularly relevant for the exotic seagrass Halophila stipulacea, which colonized the Mediterranean Sea a century ago and shifted its thermal niche, coping with a colder regime. Here, we used two hybrid models combining correlative SDMs with the thermal limits for growth of native and exotic H. stipulacea populations to predict the distribution of the species in its native (Indian Ocean and Red Sea) and exotic ranges (Mediterranean Sea and Caribbean Sea) under two scenarios forecasting limited (RCP 2.6) and severe (RCP 8.5) future climate changes by 2050 and 2100. Then, we assessed the differences between hybrid models based on native Red Sea thermal limits (niche conservatism: 17–36°C) and on exotic Mediterranean thermal limits (local adaptation: 14–36°C). At the Mediterranean exotic range, the local adaptation hybrid model accurately agreed with the present distribution of the species while the niche conservatism-based hybrid model failed to predict 87% of the current occurrences of the species. By contrast, both hybrid models predicted similar species distributions for the native range and exotic Caribbean range at present and projected that H. stipulacea will maintain its current worldwide under all future greenhouse gas emission scenarios. The hybrid model based on Mediterranean thermal limits projected the expansion of H. stipulacea through the western Mediterranean basin (except the gulf of Leon) under the most severe scenario (RCP 8.5) by 2100, increasing its distribution by 50% in the Mediterranean. The future expansion of H. stipulacea is related to its capacity to cope with warm waters and it may become a relevant species in the future, particularly under the projected decline of native Mediterranean seagrasses, resulting in important shifts in seagrass communities and overall ecosystem functions.
Anthropogenic impacts on marine ecosystems have led to a decline of biodiversity across the oceans, threatening invaluable ecosystem services on which we depend. Ecological temporal data to track changes in diversity are relatively rare, and the few long-term datasets that exist often only date back a few decades or less. Here, we use eDNA taken from dated sediment cores to investigate changes over approximately the last 100 years of metazoan communities in native (Cymodocea nodosa and Posidonia oceanica) and exotic (Halophila stipulacea) seagrass meadows within the eastern Mediterranean Sea, at two locations in Greece and two in Cyprus. Overall, metazoan communities showed a high turnover of taxa during the past century, where losses of individual taxa in a seagrass meadow were compensated by the arrival of new taxa, probably due to the arrival of exotic species introduced in the Mediterranean Sea from the Suez Canal or the Gibraltar Strait. Specifically, bony fishes (Class Actinopteri) and soft corals (Class Anthozoa) presented significantly higher richness in the past (before the 1980s) than in the most recent time periods (from 1980–2017) and some Cnidarian orders were solely found in the past, whereas sponges and Calanoids (Class Hexanauplia), an order of copepods, showed an increase in richness since the 1980s. Moreover, the Phyla Porifera, Nematoda and the Classes Staurozoa, Hydrozoa and Ophiuroidea were detected in P. oceanica meadows but not in C. nodosa and H. stipulacea, which led to P. oceanica meadows having twice the richness of other seagrasses. The greater richness resulted from the more complex habitat provided by P. oceanica. The combination of eDNA and sediment cores allowed us to reconstruct temporal patterns of metazoan community diversity and provides a novel approach to follow natural communities back in time in the absence of time series and baseline data. The ongoing loss of P. oceanica meadows, likely to be compounded with future warming, might lead to a major loss of biodiversity and the replacement by other seagrass species, whether native or exotic, does not compensate for the loss.
Seagrass species play a critical role in the mitigation of climate change by acting as valuable carbon sinks and storage sites. Another important ecosystem service of this coastal vegetation is nutrient removal. However, coastal ecosystems are under increasing pressure of global warming and associated establishment of invasive species. To elucidate the respective contributions of seagrass species Posidonia oceanica and Cymodocea nodosa and the non-native macroalga Halimeda incrassata as primary producers and nutrient sinks in coastal habitats we conducted in-situ incubations in the North-western Mediterranean Sea. Measured metabolic activity and nutrient removal as well as calcification rates in these habitats over a 24 h period in spring and summer confirmed that the endemic seagrass P. oceanica represents a valuable ecosystem with high O2 production and considerable carbon capture. The documented regression of P. oceanica meadows with higher temperatures and decline in autotrophy as measured here causes concern for the continuity of ecosystem services rendered by this habitat throughout the Mediterranean Sea with progressing climate warming. In contrast, the enhanced performance of C. nodosa and the calcifying alga H. incrassata with increasing temperatures, under expected rates of future warming is uncertain to mitigate loss of productivity in case of a potential shift in marine vegetation. This could ultimately lead to a decline in ecosystem services, decreased carbon storage and mitigation of climate change. Furthermore, this study provides a first estimate for the growth rate of H. incrassata in the Mediterranean Sea, supporting evidence for the mechanism of its rapid extension.
Abstract. The increasing rates of CO2 due to anthropogenic activities are causing important potential climate threats for the Mediterranean Sea: ocean acidification and warming. In this region, two seagrass species, Posidonia oceanica and Cymodocea nodosa can play a crucial role in climate change mitigation. Through their metabolic activity, they can act as carbon sinks; buffer lowering pH values during the day and store carbon in the sediment underneath their meadows. In this study we analyse the metabolism synthesized from published data on seagrass community metabolism and from own results to evaluate trends through time of these two species comparing two methodologies: benthic chambers and multiparametric sensors. Furthermore, we analysed seasonal trends of both seagrass species´ metabolic rates and their variation between the Eastern and Western Mediterranean basins, with no significant results despite the clear visual trends. Our analysis revealed that there are significant differences between methodologies, with multiparametric sensors estimating higher rates, but unable to differentiate between habitats and useful to assess seagrass metabolism at a community level whereas benthic chambers are capable to evaluate rates at a seagrass species level. We found significant differences between the two Mediterranean regions for both methodologies, with highest rates of Net Community Production found in the Easter basin. At a species level, we found that Posidonia was more productive compared to Cymodocea. Furthermore, 86.7 % of the metabolic values reflected that the meadows were acting as carbon sinks in the Western basin.
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