Long-term response of Dictyota dichotoma var. intricata (C. Agardh) Greville (Phaeophyceae) to ocean acidification: Insights from high pCO2 vents.

The ocean acidification may severely affect macroalgal communities of the shallowest coastal habitats where they play relevant structural and functional roles. In this paper were investigated the physiological traits of two populations of Dictyota dichotoma var. intricata, living at two different pH for several generations to assess the reasons of the algae reduced abundance at current (8.1) compared to low pH (6.7). Besides, through transplant experiments, the two populations were analysed for the stress response and reversibility of physiological performance at different pH. The long-term acclimation to high pCO2/low pH favours an ecotype characterised by low energetic costs, higher photochemical efficiency and more resistance to the oxidative stress, compared to individuals living at current pH. These traits promoted the growth and reproduction of the community living at pH 6.7, favouring a lower macroalgal diversity, but a higher ecological success under ocean acidification. The similar behaviour observed between Dictyota living at pH 6.7 and transplanted thalli from pH 6.7 to 8.1, suggested a high tolerance to pH changes in the short-term. On the contrary, adaptive responses may have favoured molecular adjustments on the long-term, as showed by the significant differences between the wild populations at pH 8.1 and 6.7. The overall data indicate that both plasticity and adaptive mechanisms may be the reasons for the success of the brown seaweeds under future high pCO2/low pH. The plasticity due to photochemistry adjustments is likely involved in the early response to environmental changes. Conversely, modifications in the photosynthetic biochemical machinery suggest that more complex adaptive mechanisms occurred in the current population of Dictyota living at pH 6.7. Further studies on population genetics will reveal if any differentiation is taking place at the population level or a local adaptation has already occurred in Dictyota and other brown algae under chronic low pH.

Photosynthesis and mineralogy of Jania rubens at low pH/high pCO2: A future perspective.

Corallinales (Rhodophyta) are high Mg-calcite macroalgae and are considered among the most vulnerable organisms to ocean acidification (OA). These sensitive species play fundamental roles in coastal systems as food source and settlement promoters as well as being involved in reef stabilization, and water carbonate balance. At present only a few studies are focused on erect calcifying macroalgae under low pH/high pCO2 and the contrasting results make difficult to predict the ecological consequences of the OA on the coralline algae. In this paper the physiological reasons behind the resistance of Jania rubens, one of the most common calcareous species, to changing ocean pH are analysed. In particular, we studied the photosynthetic and mineralogical response of J. rubens after a three-week transplant in a natural CO2 vent system. The overall results showed that J. rubens could be able to survive under predicted pH conditions even though with a reduced fitness; nevertheless physiological limits prevent the growth and survival of the species at pH6.7. At low pH (i.e. pH7.5), the maximum and effective PSII efficiency decreased even if the increase of Rubisco expression suggests a compensation effort of the species to cope with the decreased light-driven products. In these circumstances, a pH-driven bleaching phenomenon was also observed. Even though the photosynthesis decreased at low pH, J. rubens maintained unchanged the mineralogical composition and the carbonate content in the cell wall, suggesting that the calcification process may also have a physiological relevance in addition to a structural and/or a protective role. Further studies will confirm the hypotheses on the functional and evolutionary role of the calcification process in coralline algae and on the ecological consequences of the community composition changes under high pCO2 oceans.

A massive update of non-indigenous species records in Mediterranean marinas.

The Mediterranean Sea is home to over 2/3 of the world's charter boat traffic and hosts an estimated 1.5 million recreational boats. Studies elsewhere have demonstrated marinas as important hubs for the stepping-stone transfer of non-indigenous species (NIS), but these unique anthropogenic, and typically artificial habitats have largely gone overlooked in the Mediterranean as sources of NIS hot-spots. From April 2015 to November 2016, 34 marinas were sampled across the following Mediterranean countries: Spain, France, Italy, Malta, Greece, Turkey and Cyprus to investigate the NIS presence and richness in the specialized hard substrate material of these marina habitats. All macroinvertebrate taxa were collected and identified. Additionally, fouling samples were collected from approximately 600 boat-hulls from 25 of these marinas to determine if boats host diverse NIS not present in the marina. Here, we present data revealing that Mediterranean marinas indeed act as major hubs for the transfer of marine NIS, and we also provide evidence that recreational boats act as effective vectors of spread. From this wide-ranging geographical study, we report here numerous new NIS records at the basin, subregional, country and locality level. At the basin level, we report three NIS new to the Mediterranean Sea (Achelia sawayai sensu lato, Aorides longimerus, Cymodoce aff. fuscina), and the re-appearance of two NIS previously known but currently considered extinct in the Mediterranean (Bemlos leptocheirus, Saccostrea glomerata). We also compellingly update the distributions of many NIS in the Mediterranean Sea showing some recent spreading; we provide details for 11 new subregional records for NIS (Watersipora arcuata, Hydroides brachyacantha sensu lato and Saccostrea glomerata now present in the Western Mediterranean; Symplegma brakenhielmi, Stenothoe georgiana, Spirobranchus tertaceros sensu lato, Dendostrea folium sensu lato and Parasmittina egyptiaca now present in the Central Mediterranean, and W. arcuata, Bemlos leptocheirus and Dyspanopeus sayi in the Eastern Mediterranean). We also report 51 new NIS country records from recreational marinas: 12 for Malta, 10 for Cyprus, nine for Greece, six for Spain and France, five for Turkey and three for Italy, representing 32 species. Finally, we report 20 new NIS records (representing 17 species) found on recreational boat-hulls (mobile habitats), not yet found in the same marina, or in most cases, even the country. For each new NIS record, their native origin and global and Mediterranean distributions are provided, along with details of the new record. Additionally, taxonomic characters used for identification and photos of the specimens are also provided. These new NIS records should now be added to the relevant NIS databases compiled by several entities. Records of uncertain identity are also discussed, to assess the probability of valid non-indigenous status.

Correction: A massive update of non-indigenous species records in Mediterranean marinas.

[This corrects the article DOI: 10.7717/peerj.3954.].

Carbon and nitrogen allocation strategy in Posidonia oceanica is altered by seawater acidification.

Rising atmospheric CO2 causes ocean acidification that represents one of the major ecological threats for marine biota. We tested the hypothesis that long-term exposure to increased CO2 level and acidification in a natural CO2 vent system alters carbon (C) and nitrogen (N) metabolism in Posidonia oceanica L. (Delile), affecting its resilience, or capability to restore the physiological homeostasis, and the nutritional quality of organic matter available for grazers. Seawater acidification decreased the C to N ratio in P. oceanica tissues and increased grazing rate, shoot density, leaf proteins and asparagine accumulation in rhizomes, while the maximum photochemical efficiency of photosystem II was unaffected. The 13C-dilution in both structural and non-structural C metabolites in the acidified site indicated quali-quantitative changes of C source and/or increased isotopic fractionation during C uptake and carboxylation associated with the higher CO2 level. The decreased C:N ratio in the acidified site suggests an increased N availability, leading to a greater storage of 15N-enriched compounds in rhizomes. The amount of the more dynamic C storage form, sucrose, decreased in rhizomes of the acidified site in response to the enhanced energy demand due to higher shoot recruitment and N compound synthesis, without affecting starch reserves. The ability to modulate the balance between stable and dynamic C reserves could represent a key ecophysiological mechanism for P. oceanica resilience under environmental perturbation. Finally, alteration in C and N dynamics promoted a positive contribution of this seagrass to the local food web.

Physiological and Biochemical Analyses Shed Light on the Response of Sargassum vulgare to Ocean Acidification at Different Time Scales.

Studies regarding macroalgal responses to ocean acidification (OA) are mostly limited to short-term experiments in controlled conditions, which hamper the possibility to scale up the observations to long-term effects in the natural environment. To gain a broader perspective, we utilized volcanic CO2 vents as a "natural laboratory" to study OA effects on Sargassum vulgare at different time scales. We measured photosynthetic rates, oxidative stress levels, antioxidant contents, antioxidant enzyme activities, and activities of oxidative metabolic enzymes in S. vulgare growing at a natural acidified site (pH 6.7) compared to samples from a site with current pH (pH 8.2), used as a control one. These variables were also tested in plants transplanted from the control to the acidified site and vice-versa. After short-term exposure, photosynthetic rates and energy metabolism were increased in S. vulgare together with oxidative damage. However, in natural populations under long-term conditions photosynthetic rates were similar, the activity of oxidative metabolic enzymes was maintained, and no sign of oxidative damages was observed. The differences in the response of the macroalga indicate that the natural population at the acidified site is adapted to live at the lowered pH. The results suggest that this macroalga can adopt biochemical and physiological strategies to grow in future acidified oceans.

Physiological responses of a population of Sargassum vulgare (Phaeophyceae) to high pCO2/low pH: implications for its long-term distribution.

Ocean Acidification (OA) is likely to affect macroalgal diversity in the future with species-specific responses shaping macroalgal communities. In this framework, it is important to focus research on the photosynthetic response of habitat-forming species which have an important structural and functional role in coastal ecosystems. Most of the studies on the impacts of OA involve short-term laboratory or micro/mesocosm experiments. It is more challenging to assess the adaptive responses of macroalgal community to decreasing ocean pH over long-term periods, as they represent the basis of trophic dynamics in marine environments. This work aims to study the physiological traits of a population of Sargassum vulgare that lives naturally in the high pCO2 vents system in Ischia (Italy), in order to predict the species behaviour in a possible OA future scenario. With this purpose, the photosynthetic performance of S. vulgare was studied in a wild, natural population living at low pH (6.7) as well as in a population transplanted from native (6.7) to ambient pH (8.1) for three weeks. The main results show that the photochemical activity and Rubisco expression decreased by 30% after transplanting, whereas the non-photochemical dissipation mechanisms and the photosynthetic pigment content increased by 50% and 40% respectively, in order to compensate for the decrease in photochemical efficiency at low pH. Our data indicated a stress condition for the S. vulgare population induced by pH variation, and therefore a reduced acclimation capability at different pH conditions. The decline of the PSII maximum quantum yield (Fv/Fm) and the increase of PARP enzyme activity in transplanted thalli further supported this hypothesis. The absence of the species at ambient pH conditions close to the vent system, as well as the differences in physiological traits, suggest a local adaptation of S. vulgare at pH6.7, through optimization of photosynthetic performance.

Metabolic responses to high pCO2 conditions at a CO2 vent site in juveniles of a marine isopod species assemblage.

We are starting to understand the relationship between metabolic rate responses and species' ability to respond to exposure to high pCO2. However, most of our knowledge has come from investigations of single species. The examination of metabolic responses of closely related species with differing distributions around natural elevated CO2 areas may be useful to inform our understanding of their adaptive significance. Furthermore, little is known about the physiological responses of marine invertebrate juveniles to high pCO2, despite the fact they are known to be sensitive to other stressors, often acting as bottlenecks for future species success. We conducted an in situ transplant experiment using juveniles of isopods found living inside and around a high pCO2 vent (Ischia, Italy): the CO2 'tolerant' Dynamene bifida and 'sensitive' Cymodoce truncata and Dynamene torelliae. This allowed us to test for any generality of the hypothesis that pCO2 sensitive marine invertebrates may be those that experience trade-offs between energy metabolism and cellular homoeostasis under high pCO2 conditions. Both sensitive species were able to maintain their energy metabolism under high pCO2 conditions, but in C. truncata this may occur at the expense of [carbonic anhydrase], confirming our hypothesis. By comparison, the tolerant D. bifida appeared metabolically well adapted to high pCO2, being able to upregulate ATP production without recourse to anaerobiosis. These isopods are important keystone species; however, given they differ in their metabolic responses to future pCO2, shifts in the structure of the marine ecosystems they inhabit may be expected under future ocean acidification conditions.

The non-indigenous Paranthura japonica Richardson, 1909 (Isopoda: Anthuroidea: Paranthuridae) from the Mar Piccolo lagoon, Taranto (Italy, Mediterranean Sea).

Several individuals of Paranthura japonica, a non-indigenous isopod species, recently recorded on Italian coasts, have been collected from the Mar Piccolo basin, Taranto (Italy). This finding extends the distributional range of the species southwards in the Mediterranean, including a semi-enclosed coastal basin, which is considered the second Italian hotspot for the introduction of alien species. The characteristics of the place reinforce the hypothesis that its introduction is linked to shellfish trade and farming. Remarks on the morphology and ecology are included.

Chemoreception of the Seagrass Posidonia Oceanica by Benthic Invertebrates is Altered by Seawater Acidification.

Several plants and invertebrates interact and communicate by means of volatile organic compounds (VOCs). These compounds may play the role of infochemicals, being able to carry complex information to selected species, thus mediating inter- or intra-specific communications. Volatile organic compounds derived from the wounding of marine diatoms, for example, carry information for several benthic and planktonic invertebrates. Although the ecological importance of VOCs has been demonstrated, both in terrestrial plants and in marine microalgae, their role as infochemicals has not been demonstrated in seagrasses. In addition, benthic communities, even the most complex and resilient, as those associated to seagrass meadows, are affected by ocean acidification at various levels. Therefore, the acidification of oceans could produce interference in the way seagrass-associated invertebrates recognize and choose their specific environments. We simulated the wounding of Posidonia oceanica leaves collected at two sites (a control site at normal pH, and a naturally acidified site) off the Island of Ischia (Gulf of Naples, Italy). We extracted the VOCs and tested a set of 13 species of associated invertebrates for their specific chemotactic responses in order to determine if: a) seagrasses produce VOCs playing the role of infochemicals, and b) their effects can be altered by seawater pH. Our results indicate that several invertebrates recognize the odor of wounded P. oceanica leaves, especially those strictly associated to the leaf stratum of the seagrass. Their chemotactic reactions may be modulated by the seawater pH, thus impairing the chemical communications in seagrass-associated communities in acidified conditions. In fact, 54% of the tested species exhibited a changed behavioral response in acidified waters (pH 7.7). Furthermore, the differences observed in the abundance of invertebrates, in natural vs. acidified field conditions, are in agreement with these behavioral changes. Therefore, leaf-produced infochemicals may influence the structure of P. oceanica epifaunal communities, and their effects can be regulated by seawater acidification.

Occurrence of mucous aggregates and their impact on Posidonia oceanica beds.

Mucous macro-aggregates of both pelagic and benthic origin are recurrently observed in the meadows formed by the seagrass Posidonia oceanica around the island of Ischia (Gulf of Naples, Italy). In the past two decades, major events occurred in 1991, 1993 and 2000, when a thick layer of mucilage covered vast areas of the meadows. To investigate the environmental triggers for mucilage formation and the effects of macro-aggregates on the functional and structural status of P. oceanica, a number of abiotic and biotic parameters were monitored over three years within the frame of a research project on Adriatic and Tyrrhenian mucilages (MAT). Basic environmental parameters (salinity, temperature, irradiance, dissolved oxygen concentration) in the water column and inorganic nutrient concentrations above and within P. oceanica meadows were measured. As descriptors of the status of the seagrass, shoot density and the nitrogen content of the leaves were monitored. Moreover, a reconstructive technique (lepidochronology) was employed to track back annual plant production. During the three-year study, mucous aggregates produced by benthic algae were observed in spring-summer and a major event of macro-aggregates of pelagic origin affecting P. oceanica canopy was observed in autumn 2000. Each of these episodes was observed for a few weeks to one month. We hypothesize nutrient limitation to explain the short duration of the benthic algal blooms that were responsible of macroaggregate formation; a highly dynamic circulation resulted in the dispersion of the pelagic aggregates deposited on the meadows. None of the descriptors of the structure of the meadow and of plant performance showed any obvious alterations in relation to the occurrence of mucilage coverage. Presumably, the short duration of the mucilage episodes recorded were not enough to induce such alterations, at least at the temporal and spatial scales considered.