Microphytobenthic community composition and primary production at gas and thermal vents in the Aeolian Islands (Tyrrhenian Sea, Italy)
Introduction
The Aeolian archipelago (Tyrrhenian Sea) is characterised by CO2 and temperature diverse conditions and offers a good natural study area for research on shallow benthic (Maugeri et al., 2009) and pelagic systems (Karuza et al., 2012). This type of study areas are gaining importance as the CO2 concentrations are unsustainably rising in the atmosphere and since 1970 the cumulative emissions of CO2 increased by 40%. About 60% of these anthropogenic CO2 emissions have been removed by sinks (ocean and vegetation uptake) and stored in natural carbon cycle reservoirs. The ocean alone has absorbed about 30% of the emitted anthropogenic CO2 causing ocean acidification that, based on models, will range from 0.06 to 0.32 in decrease of pH at the end of the 21st century (IPCC, 2014).
Firstly, the acidification studies were focused mainly at the calcifying organisms because of the direct effect of lower pH on their ability to maintain the external calcium carbonate skeletons (Orr et al., 2005). More attention to the effects of acidification on non-calcinated organisms followed as more complex shifts in marine ecosystem composition and function were highlighted (Fabry et al., 2008, Hall-Spencer et al., 2008, Pörtner, 2008, Riebesell, 2004). The interest towards CO2 vent areas is even higher, because they can be used as natural laboratories to study the impact of CO2 leakage from Carbon Capture and Storage (CCS) systems, a key technology for the disposal of CO2 derived from power plants and other industrial sources (Lewicki et al., 2007). The possible effects of such CO2 releases were already studied on viruses and prokaryotes (Karuza et al., 2012, Rastelli et al., 2015, Tait et al., 2015), phytoplankton (Fu et al., 2007), zooplankton (Halsband and Kurihara, 2013) and also zoobenthos (Basallote et al., 2012, Kita et al., 2013, McConville et al., 2013, Murray et al., 2013). However, even though the microphytobenthos (MPB) are useful bioindicators, responding to the conditions at the sampling site, ubiquitous and easy to sample (Desrosiers et al., 2013) the research conducted on the microalgae in relation with different pCO2 is very limited. Regarding this particular aspect, only a few studies on the MPB communities have been published (Dias et al., 2010, Johnson et al., 2013, Johnson et al., 2015, Raghukumar et al., 2008, Roleda et al., 2015).
Studies considering some functional aspects are even more limited (Wenzhöfer et al., 2000) at the CO2 vent sites. Even though primary production estimates measured in situ with the 14C technique are commonly used to have an overview of the benthic trophic state (Cibic et al., 2012, Krause-Jensen et al., 2012, Rubino et al., 2015), we found no such studies on vents to this date. Therefore, in this study we upgrade the information gained from data on MPB with the main photoautotrophic pathway, the primary production.
Laboratory and mesocosm studies of diatom growth and photosynthesis under elevated pCO2 showed very diverse responses (Gao et al., 2012). Predominately the effect on growth was stimulative (Kim et al., 2006, King et al., 2011, Low-Decarie et al., 2011, Yang and Gao, 2012) or not significant (James et al., 2014, Roleda et al., 2015) but in some cases a negative effect on growth was shown (Ihnken et al., 2011, Low-Decarie et al., 2011, Torstensson et al., 2012). Other effects were reported, like decreased silicification of diatom frustules (Mejía et al., 2013) and selection of larger diatom genera (Johnson et al., 2013) under higher pCO2, both very important responses, as diatoms represent the world's largest contributors to biosilicification. On the other hand, the dominance of smaller sized diatoms has been recorded under higher environmental temperature (Falkowski and Oliver, 2007, Winder et al., 2009).
The majority of the previous studies on the combined effects of pCO2 and temperature on any benthic or pelagic community were conducted in vitro or in mesocosms (Gao et al., 2012). In this field study we assessed the effects of high CO2 and temperature on the microphytobenthic community in the sediments of the Aeolian Islands. In particular, the aims of this study were: i) to investigate to what extent the emission of gas alone and in combination with the high temperature affects the microphytobenthic abundance and its community composition; ii) to detect a possible change in the primary production rate in relation with the gas emission and high temperature; iii) to identify other differences among microphytobenthic assemblages such as different cell size, morphological deformities or diverse degrees of silicification of the diatom frustule.
Therefore, our study gives new insights into the overall pattern of microphytobenthic community response to the extreme environment of shallow hydrothermal vents.
Section snippets
Study area
The Aeolian archipelago (Tyrrhenian Sea, Italy) is a ring-shaped volcanic arc, composed of seven islands and 10 seamounts, associated with the Peloritanian–Calabrian orogenic belt. Panarea is the smallest (3.3 km2) of the islands and it represents the emergent part of a wide stratovolcano that is more than 2000 m high and 20 km long where the subduction-related volcanic activity is still present (Tassi et al., 2009). In the early 1980's researchers began to conduct gas geochemistry surveys of
Abiotic parameters
At the bottom, seawater temperature did not vary remarkably among stations or sampling periods, showing similar values during samplings in June 2012, May 2013 and 2014 (19.0 ± 0.1, 18.0 ± 0.4 and 17.5 ± 0.5 °C, respectively) with only October 2012 reaching 23.4 ± 0.0 °C. Salinity was even less variable with an average (over stations and sampling periods) value of 37.9 ± 0.3. The %PAR was quite high, always above 22% with the average irradiance at all stations equal to 619 μE m−2 s−1.
Grain-size
Effect of grain-size and light availability on the microphytobenthic community
In this study area the grain size, particularly the sand fraction, was quite variable among stations and sampling periods. This is mainly due to the strong hydrodynamics of this area, especially at the smaller scale, responsible for the continuous changing of the sediment bottom morphology. Even though depth, grain size and light availability have been previously demonstrated as important selection factors (Cibic et al., 2007, Miles and Sundbäck, 2000), they did not show a significant role
Conclusions
Our study showed a significant influence of the gas vents with high CO2 concentration, and even more a selective response to the combined effect of high CO2 and temperature at the hydrothermal vents, on the MPB community composition and total abundance. This influence was also mirrored in increased PP rates, especially at the hydrothermal vent. Here, even though the MPB diversity was lowered, the adapted species, especially those belonging to the genus Navicula, were capable to survive in very
Acknowledgements
This work has received funding from the European Community's Seventh Framework Program (FP7/2007-2013) under grant agreement n° 265847 (“Sub-seabed CO2 Storage: Impact on Marine Ecosystems” – ECO2). We are grateful to Cinzia Comici and Annalisa Franzo for the samplings and to Federica Cerino for her help in the methodological part of this study and the review of this paper.
References (90)
Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms
Aquat. Toxicol.
(1992)- et al.
Integrated approach to sediment pollution: a case study in the Gulf of Trieste
Mar. Pollut. Bull.
(2008) - et al.
Microphytobenthic primary production as 14C uptake in sublittoral sediments of the Gulf of Trieste (northern Adriatic Sea): methodological aspects and data analyses. Estuarine
Coast. Shelf Sci.
(2008) - et al.
Microphytobenthic biomass, species composition and nutrient availability in sublittoral sediments of the Gulf of Trieste (northern Adriatic Sea). Estuarine
Coast. Shelf Sci.
(2007) - et al.
Bioindicators in marine waters: benthic diatoms as a tool to assess water quality from eutrophic to oligotrophic coastal ecosystems
Ecol. Indic.
(2013) Benthic marine diatom deformities associated with contaminated sediments in Hong Kong
Environ. Int.
(1998)- et al.
Potential acidification impacts on zooplankton in CCS leakage scenarios
Mar. Pollut. Bull.
(2013) - et al.
Virioplankton and bacterioplankton in a shallow CO2-dominated hydrothermal vent (Panarea island, tyrrhenian sea). Estuarine
Coast. Shelf Sci.
(2012) - et al.
Assessment of pH variability at a coastal CO2 vent for ocean acidification studies. Estuarine
Coast. Shelf Sci.
(2011) - et al.
Effects of elevated pCO2 on reproductive properties of the benthic copepod Tigriopus japonicus and gastropod Babylonia japonica
Mar. Pollut. Bull.
(2013)
Environmental toxicology
Effects of elevated CO2 on the reproduction of two calanoid copepods
Mar. Pollut. Bull.
B content and Si/C ratios from cultured diatoms (Thalassiosira pseudonana and Thalassiosira weissflogii): relationship to seawater pH and diatom carbon acquisition
Geochimica et Cosmochimica Acta
Effect of production and biomass of intertidal microphytobenthos on meiofaunal grazing rates
J. Exp. Mar. Biol. Ecol.
Consequences of a simulated rapid ocean acidification event for benthic ecosystem processes and functions
Mar. Pollut. Bull.
Rapid response of the active microbial community to CO2 exposure from a controlled sub-seabed CO2 leak in Ardmucknish Bay (Oban, Scotland)
Int. J. Greenh. Gas Control
Deep-sea and shallow-water hydrothermal vent communities: two different phenomena?
Chem. Geol.
Low-pH waters discharging from submarine vents at Panarea Island (Aeolian Islands, southern Italy) after the 2002 gas blast: origin of hydrothermal fluids and implications for volcanic surveillance
Appl. Geochem.
Gas geochemistry of natural analogues for the studies of geological CO2 sequestration
Appl. Geochem.
In situ microsensor studies of a shallow water hydrothermal vent at Milos, Greece
Mar. Chem.
Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity
Mar. Environ. Res.
Lethal effects on different marine organisms, associated with sediment–seawater acidification deriving from CO2 leakage
Environ. Sci. Pollut. Res.
Evidence of a recent input of magmatic gases into the quiescent volcanic edifice of Panarea, Aeolian Islands, Italy
Geophys. Res. Lett.
Effects of elevated temperature and CO2 on intertidal microphytobenthos
BMC Ecol.
Water Quality–Guidance Standard for the Routine Sampling and Pre-treatment of Benthic Diatoms from Rivers
Effect of pH on the growth and carbon uptake of marine phytoplankton
Mar. Ecol. Prog. Ser.
Living Marine Benthic Diatoms as Indicators of Nutrient Enrichment: a Case Study in the Gulf of Trieste. Diatoms: Classification, Ecology and Life Cycle
Benthic ecosystem functioning in hydrocarbon and heavy-metal contaminated sediments of an Adriatic lagoon
Mar. Ecol. Prog. Ser.
Different fixatives and chloridric acid concentrations in microphytobenthic primary production estimates using radiolabeled carbon: their use and misuse
Limnol. Oceanogr. Methods
In Situ Primary Production Measurements as an Analytical Support to Remote Sensing-an Experimental Approach to Standardize the 14C Incorporation Technique
Meiofaunal biodiversity on hydrothermal seepage off Panarea (aeolian islands, tyrrhenian sea)
The Marine Benthic Diatoms in China
Modern seawater acidification: the response of foraminifera to high-CO2 conditions in the Mediterranean Sea
J. Geol. Soc.
Studies on the autecology of the marine diatom Thalassiosira nordenskioeldii. II. The influence of cell size on growth rate, and carbon, nitrogen, chlorophyll a and silica content
J. Phycol.
Effect of shallow hydrothermal venting on the richness of benthic diatom species
Cah. De. Biol. Mar.
Impacts of ocean acidification on marine fauna and ecosystem processes
ICES J. Mar. Sci. J. du Conseil
Diatom teratological forms and environmental alterations: a review
Hydrobiologia
Mix and match: how climate selects phytoplankton
Nat. Rev. Micro
A universal driver of macroevolutionary change in the size of marine phytoplankton over the Cenozoic
Proc. National Acad. Sci.
Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria)
J. Phycol.
Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming
Mar. Ecol. Prog. Ser.
Flore des diatomées: eaux douces et saumâtres
AlgaeBase
Volcanic carbon dioxide vents show ecosystem effects of ocean acidification
Nature
Bacillariophyta (Diatoms) of the Bahamas
Cited by (17)
Effects of acidification on the biogeochemistry of unvegetated and seagrass marine sediments
2024, Marine Pollution BulletinPosidonia bonsai: Dwarf Posidonia oceanica shoots associated to hydrothemal vent systems (Panarea Island, Italy)
2023, Aquatic BotanyCitation Excerpt :The area consists of numerous and diversified hydrothermal submerged emissions of gas and hot waters of volcanic origin, including the “Smoking land” a recently described site with more than 200 active chimneys (Esposito et al., 2018). These features make the zone one of the most suitable places in the Mediterranean to study various aspects related to CO2 capture and storage, by geologists, the geochemistry of the hydrothermal fluids, as well as to assess the effects of water acidification on benthic (Goffredo et al., 2014; Rogelja et al., 2016; Esposito et al., 2017, 2021) and pelagic organisms and habitats (Karuza et al., 2012), including P. oceanica (Vizzini et al., 2010; Guilini et al., 2017; Gaglioti et al., 2019). Bonsai or dwarf Posidonia shoots were observed and sampled the 2nd and 4th October 2021, and between 30th September and 9th October 2022, respectively during the 5th and the 6th edition of the Panarea School of scientific diving, a permanent yearly event to study the unique hydrothermal vents system of this island (Gambi et al., 2018).
Allelopathic interactions between phytobenthos and meiofaunal community in an Adriatic benthic ecosystem: Understanding the role of aldehydes and macroalgal structural complexity
2022, Science of the Total EnvironmentCitation Excerpt :Dinoflagellates were present at low densities, except during the bloom of Ostreopsis cf. ovata, which was the main dinoflagellate and showed its typical blooming trend, with maximum abundances recorded in late summer (September) and within ranges previously observed (e.g. Gémin et al., 2020). The main diatom genera found in the present study (e.g. Navicula, Cylindrotheca, Lyrella, Cocconeis, Gyrosigma A.H. Hassall, 1845, Licmophora C. Agardh, 1827, Nitzschia, Mastogloia Thwaites ex W.Smith, 1856, Striatella C. Agardh, 1832, Coscinodiscus Ehrenberg, 1839) are among the most common on Mediterranean macroalgae and in the microphytobenthos, particularly in the Adriatic Sea (Carnicer et al., 2015; Accoroni et al., 2016; Rogelja et al., 2016; Pennesi and Danovaro, 2017; Ternon et al., 2020). Species belonging to the orders Naviculales and Lyrellales on DP, to the Licmophorales on CC and, generally, to centric diatoms on both algae, showed an inverse trend (low density at T1 and high at subsequent times) with the production of PUAs by macroalgae.
Nitrogen as the main driver of benthic diatom composition and diversity in oligotrophic coastal systems
2019, Science of the Total EnvironmentCitation Excerpt :Despite the importance of marine benthic diatoms in the functioning of coastal ecosystems (Van den Hoek et al., 1979; MacIntyre et al., 1996; Cahoon, 1999), little is known on environmental factors driving their structure and composition (e.g. Cibic et al., 2007a, 2007b, 2012, Cibic and Blasutto, 2011). The focus of previous studies was mainly on ecosystems characterized by tidal flats (e.g. Agatz et al., 1999), estuaries and brackish waters such as Venice lagoon (Facca and Sfriso, 2007) or extreme environments (e.g. gas and thermal vents in the Aeolian Islands- Rogelja et al., 2016). In such systems, salinity and light can play a significant role in driving benthic diatom assemblage structure (e.g. Admiraal, 1984; Underwood, 1994; Underwood et al., 1998; Hillebrand and Sommer, 1997; Weckström and Juggins, 2005; Borja and Dauer, 2008; Ulanova et al., 2009; Du et al., 2017).
Natural and anthropogenic disturbances shape benthic phototrophic and heterotrophic microbial communities in the Po River Delta system
2019, Estuarine, Coastal and Shelf ScienceCitation Excerpt :The qualitative identification of MPB assemblages was carried out using floras listed in Cibic and Blasutto (2011) as well as identification keys of freshwater microalgae by Canter-Lund and Lund (1995). Diatom life modes were distinguished based on literature (Round, 1971; Cibic et al., 2007; Rogelja et al., 2016; Rubino et al., 2016) into the following living forms: planktonic (truly planktonic species which settled on the substratum from the water column), tychopelagic (diatoms that are loosely associated with the sediment, commonly found in the water column) and benthic species. The latter were further divided into: epiphytic (attached to macroalgae, phanerogams or other substrata), epipsammic (living on sand) and epipelic (living freely on soft sediments) forms.
Assessing marine environmental status through microphytobenthos assemblages colonizing the Autonomous Reef Monitoring Structures (ARMS) and their potential in coastal marine restoration
2017, Marine Pollution BulletinCitation Excerpt :Planktonic and periphytic diatoms are included in many water quality monitoring programmes worldwide (Kireta et al., 2012; El-Karim, 2014), and they are routinely utilized in freshwater systems, whereas applications to marine water are still limited (Cibic et al., 2012; B-Béres et al., 2016; Desrosiers et al., 2013). Diatom assemblages have been utilized also for the study of the effects of contamination by heavy metals, where this group showed also the presence of teratogenic forms in response to this kind of pollution (Rogelja et al., 2016; Siqueiros-Beltrones et al., 2014). Recent studies showed that the assemblage structure of benthic diatoms and other microscopic benthic components can be modified by altered environmental conditions and some taxa can be used as bio-indicator both at the level of genus and species (Desrosiers et al., 2013; Hill et al., 2001; Pusceddu et al., 2009).