Epiphytic hydroids on Posidonia oceanica seagrass meadows are winner organisms under future ocean acidification conditions: evidence from a CO₂ vent system (Ischia Island, Italy)

Abstract

Effects of ocean acidification (OA) on the plant phenology and colonization/settlement pattern of the hydrozoan epibiont community of the leaves of the seagrass Posidonia oceanica have been studied at volcanic CO₂ vents off Ischia (Italy). The study was conducted in shallow Posidonia stands (2.5–3.5 m depth), in three stations on the north and three on the south sides of the vent’s area (Castello Aragonese vents), distributed along a pH gradient. At each station, 10–15 P. oceanica shoots were collected every three months for one-year cycle (Sept 2009–2010). The shoot density of Posidonia beds in the most acidified stations along the gradient (pH < 7.4) was significantly higher than that in the control area (pH = 8.10). On the other hand, we recorded lower leaf lengths and widths in the acidified stations in the whole year of observations, compared to those in the control stations. However, the overall leaf surface (Leaf Area Index) available for epiphytes under ocean acidification conditions was higher on the south side and on both the most acidified stations because of the higher shoot density under OA conditions. The hydrozoan epibiont community on the leaf canopy accounted for seven species, three of which were relatively abundant and occurring all year around (Sertularia perpusilla, Plumularia obliqua, Clytia hemisphaerica). All hydroids species showed a clear tolerance to low pH levels, including chitinous and non-calcifying forms, likely favoured also by the absence of competition for substratum with the calcareous forms of epiphytes selected against OA.

Keywords:

• Seagrasses
• epiphytic hydrozoa
• ocean acidification
• species checklist
• Mediterranean Sea

Introduction

Ocean acidification (OA), combined with other types of natural and/or human stresses, can cause sharp changes in the structure/functioning of benthic communities (Kroeker et al. 2010, 2013; Teixido et al. 2018). Ocean acidification affects mainly the process of calcification of organisms with skeletons and shells composed of calcium carbonate (e.g. corals, molluscs, echinoderms, bryozoans, and many other organisms) (Royal Society 2005; Doney et al. 2009).

The use of natural sites, characterized by natural OA of the marine waters with decreasing pH, increasing pCO₂, and alteration of the carbonate chemistry, has increased in these last decades with respect to mesocosm or laboratory experiments (Guilini et al. 2017; Foo et al. 2018; Gonzalez-Delgado & Hernadez 2018; Rastrick et al. 2018; Auriemma et al. 2019; Mecca et al. 2020). On the island of Ischia (Tyrrhenian Sea, Italy) there are several areas characterized by elevated CO₂ emissions from the sea bottom (Tedesco 1996; Hall-Spencer et al. 2008; Gambi 2014; Foo et al. 2018; Gambi et al. 2020). Among these, the shallow vent system off the Castello Aragonese is the most investigated (Foo et al. 2018). These CO₂ vents may be useful in examining the long-term response of the marine community to OA (Kroeker et al. 2011), especially in complex coastal systems, such as seagrass meadows, forming a model site to investigate how benthic communities associated with the seagrass Posidonia oceanica respond to OA (Garrard et al. 2014; Mecca et al. 2020). P. oceanica is the endemic and most abundant and relevant Mediterranean seagrass ecosystem, supporting a complex community of epiphytic organisms that follows a typical succession model of colonization of the leaves (Van der Ben 1971; Boudouresque et al. 2009). Epiphytes of seagrass contribute significantly to the primary production of the meadow (Buia et al. 1992; Nelson & Waaland 1997; Duarte et al. 2004), and are often more sensitive to environmental changes than the host plant (Delgado et al. 1999; Nesti et al. 2008; Brahim et al. 2010, 2014; Giovannetti et al. 2010), with shifts in species composition (Nesti et al. 2008; Fourqurean et al. 2010) and differences in their spatial distribution and heterogeneity (Piazzi et al. 2004; Martínez-Crego et al. 2010). In particular, epiphytic assemblages of P. oceanica leaves are characterized by short-living organisms that respond quickly to environmental alterations (Boero 1984; Boero & Fresi 1986). Therefore, changes in their ecology and community composition have been used to detect environmental and anthropic impacts (Piazzi et al. 2004; Leoni et al. 2006; Balata et al. 2008; Brahim et al. 2010, 2014; Giovannetti et al. 2010; Mabrouk et al. 2013). Furthermore, dynamics and role of epiphytic organisms in the food web are influenced by the seasonal phenology of the host seagrass (Casola et al. 1987; Lepoint et al. 1999; Mecca et al. 2020). Most of the previous studies have analysed the phenology and variation of the epiphytic community along the acidification gradient at CO₂ vents (Martin et al. 2008; Garrard et al. 2014; Nogueira et al. 2017) providing generally single observations on short periods of investigation (Martin et al. 2008; Guilini et al. 2017; Nogueira et al. 2017), or are related to artificial Posidonia mimics (Donnarumma et al. 2014), as well as utilising the Free Ocean CO₂ Enrichment (FOCE) systems and mesocosm experiments (Cox et al. 2015, 2016 and references herein). Recently, only the paper by Mecca et al. (2020) provides observation of the leaf epiphyte community in a longer time period, coinciding with its higher development (June–October), although without detailed taxonomic analyses.

Among the animal groups that settle on Posidonia leaves, hydroids are very diverse and abundant in all Posidonia beds, together with bryozoans. Among them, a few species (Aglaophenia harpago Schenck, 1965, Sertularia perpusilla Stechow, 1919, Campanularia breviscyphia Sars, 1857, and Pachycordyle pusilla (Motz-Kossowska, 1905) are strictly associated with Posidonia, living only on the leaves of this host plant (Picard 1951a; Boero 1981a, 1984; Boero et al. 1985; Boero & Fresi 1986; Piraino & Morri 1990). This association is promoted by certain peculiarity of hydroids, as rapid growth and asexual reproduction by stolonization (Boero 1987). In previous studies, the potential use of benthic hydrozoans as indicators of environmental conditions is investigated (Mergner 1977, 1987; Gili & Hughes 1995; Megina et al. 2013, 2016; Gravili et al. 2017; Yilmaz et al. 2020). They often form characteristic assemblages in different marine habitats presenting a set of life-history traits (sessile colonies, key-actors role in marine food webs, rapid population responses to stress and disturbances) (Boero 1984; Gili & Hughes 1995) that make them suitable candidates for environmental monitoring. Morphological changes suffered by colonies of some species may be indicative of several disturbance factors, such as increased concentrations of heavy metals (Karbe 1972; Theede et al. 1979), particular hydrodynamic conditions (Riedl 1966; Mergner 1972, 1977, 1987; Wedler 1975; Da Silveira & Migotto 1991), climate change effects (Puce et al. 2009; Gonzalez-Duarte et al. 2014; Gravili et al. 2017; Rossi et al. 2019), and anthropogenic impact (Megina et al. 2013, 2016; Topçu et al. 2018; Yilmaz et al. 2020).

The aim of this study is, to highlight the effects of OA conditions on the composition and structure of the hydrozoan epiphytic community of the P. oceanica, and on the phenology of this seagrass along a pH gradient of the Castello-Ischia CO₂ vents system, sampled every three months on a year-long period. In addition, to evaluate the biodiversity of the hydroids recorded in our study sites, a review of the ‘potential’ biodiversity of the Hydrozoa on Posidonia beds was undertaken, to assess both the number and the composition of the species found in a broader and comparative ecological context. Therefore, a further aim of this study is to provide a checklist of the epiphytic hydroids on P. oceanica meadows, based on an up-dated literature analysis.

Materials and methods

Study site

The study area is adjacent to the Castello Aragonese, a volcanic dome and islet located at the north-eastern side of Ischia Island (Gulf of Naples, Italy) (40°43.84ʹN 13°57.08ʹE) (Rittmann & Gottini 1981) (Figure 1). Previous and recent gas analyses (Hall-Spencer et al. 2008; Foo et al. 2018; Gambi et al. 2020) showed that the seawater is acidified by gas comprising 90.1–95.3% CO₂, 3.2–6.6% N₂, 0.6–0.8% O₂, 0.08–0.1% Ar and 0.2–0.8% CH₄ (no sulphur present), while both water temperature and salinity do not change respect to normal ambient conditions. The seawater pH ranges from 8.17 (normal value) to as low as 6.57 along a continuous gradient occurring both at the south and the north sides of the Castello (Kroeker et al. 2011; Ricevuto et al. 2014). A shallow Posidonia oceanica meadow subjected to CO₂ emission is present on both sides of the Castello islet (Buia et al. 2003; Garrard et al. 2014; Foo et al. 2018; Mecca et al. 2020). On the south side, the most intense venting activity includes also the Posidonia meadow; this side of the Castello is also more sheltered to wave action and water currents with respect to the north side that is exposed to the dominant north-western winds. At the north side, the active venting area is concentrated on the edge of the Posidonia meadow, and direct gas bubbling is quite limited inside the meadow. The collection of Posidonia shoots for the morphometric analyses and analyses of the epiphytic hydroids are conducted in the shallow Posidonia stands at 2.5–3.5 m depth, in three stations located on the south side (SC, S2, S3) and three on the north side (N1, N2, N3) distributed along a pH gradient (Figure 1). The stations have been selected in relation to mean pH values recorded and proximity to CO₂ emissions (see previous studies, Donnarumma et al. 2014, and for a review Foo et al. 2018). The S3 and N3 stations, acidified sites with extreme low pH, are located in an area with high and dense bubbling (>10 bubbles emissions to m²). Mean pH values are approximately 7.2 at the northern and 6.6 at the southern sites, near the rocky reef (Kroeker et al. 2011; Ricevuto et al. 2014). In these stations, both on the south and north sides, the P. oceanica meadow is very dense (700–800 shoots/m²) with very short leaves due to the frequent grazing by the herbivorous Sarpa salpa (Donnarumma et al. 2014; Mecca et al. 2020; Mirasole et al. 2021). The S2 and N2 stations are located approximately 60 m far from S3 and N3, where the bubbles emissions are reduced compared to the acidified area (<5 bubbles emissions to m²) and therefore subjected to low pH conditions. In fact, S2 and N2 have mean pH values around 7.7–7.8 (Kroeker et al. 2011; Ricevuto et al. 2014) but show a considerable variability in time, also at daily scale (Kroeker et al. 2011). The SC and N1 are control stations, located N1 approx. 80 m from N2, and SC approx. 30 m from S2, and where the CO₂ emissions are absent, and the pH values are those of normal sea waters (8.10) (Ricevuto et al. 2014).

Figure 1. Map of the study area, the Castello vent system off Ischia (Italy) showing the locations of the stations under the influence of CO₂ venting (N2, N3, S2, S3), and the control stations out of the venting area (N1, SC). (Background map from Gambi et al. 2020, modified)

Sampling methods and data analysis

Samplings of Posidonia natural shoots (10–15 shoots) for the morphometric and epiphyte analysis were performed every three months for a whole year, in September and December 2009, March, June, and September 2010. At each station, Posidonia shoot density was measured in October 2010 by counting number of shoots in quadrats 40 × 40 cm (5 replicates per station). On the collected shoots in every station and period, a phenological analysis was performed according to the usual procedure, counting the number of leaves and measuring their length and width (Buia et al. 2004). From these parameters, the leaf surface area of each shoot was calculated, as well as the Leaf Area Index (mean leaf area per shoot x shoot density), which represents the leaf surface developed by the plant in a single bottom square meter (Buia et al. 2004). In addition, for each shoot, the hydroid species present on the leaves have been analysed by considering, position on the leaf (basal, intermediate, apical) distinguishing between internal and external leaf face; the percentage coverage for each species was estimated using a semi-quantitative code: 1 = low (less than 10% cover), 2 = medium (from 10 to 30%), 3 = high (above 30%), and in the case of branched colonies, their height as 1 = low (less than 3 mm); 2 = medium (from 3 to 6 mm); 3 = high (higher than 6 mm). Spatial and temporal trends in colonies’ height and position on the leaves were preliminarily investigated with visual data inspection and variance analysis, resulting not evident or significant. Therefore, they were not considered in further analysis. Trends in leaf coverage for each species and station/site were estimated as average of the semi-quantitative scores for leaf, independently from their position of the leaf shoot (Table S1, supplementary material). Trends in coverage across sites were estimated by ANOVA for the 3 most abundant species, using the 4 sampling periods, the different pH conditions (1, 2, 3), and the different locations (south or north sides) as categorical explanatory variables. The significance of the different variables was assessed via stepwise procedure. The similarity between sites and species was estimated by using Euclidean distance from the semi-quantitative classes of abundance.

Bibliographic survey on hydroids associated to Posidonia oceanica meadows

To better evaluate and compare our findings with previous works on epiphytic hydroids on Posidonia oceanica meadows, an inclusive bibliographic survey was performed (indexed and non-indexed journals, and grey literature). Papers have been obtained through Servizi Informatici Bibliotecari di Ateneo (S.I.B.A.) of the University of Salento (Lecce), “Web of Science” and the “Biological Abstracts” were consulted, as well. For the taxonomy, our survey follows the extensive revision of the information found in the World Register of Marine Species (Appeltans et al. 2011).

Results

Shoot density and morphometric analysis of Posidonia oceanica along the pH gradient

Posidonia oceanica shoot density showed, both at the north and south sides, a significant decrease (two-way ANOVA, F = 14.67, p = 0.000, d.f. 5) from the extreme low pH stations (S3 and N3) to the control ones (SC and N1). As outlined in Donnarumma et al. (2014), the shoot density values were the highest at the most acidified stations: S3 = 1014 ± 73; N2 = 708 ± 98; N3 = mean 858 ± 85 (s.d.) shoot m²; S2 = 726 ± 123; N1 = 438 ± 88; SC = 494 ± 125. The mean leaf length as well as the mean shoot surface was higher on the south side respect to the north (two-way ANOVA, leaf surface F = 7.01; p = 0.013, d.f. 1; leaf length F = 5.25; p = 0.02, d.f. 1). The mean leaf length in stations S3, N2, and N3 always showed lower values than all the other ones (two-way ANOVA, F = 2.87; p = 0.03, d.f. 5, Tukey post-hoc comparisons). Leaf surface showed higher values on the south side and especially in the S2 station (two-way ANOVA, F = 3.97; p = 0.009, d.f. 5, Tukey post hoc comparisons). The Leaf Area Index showed higher values on the south side, respect to the north, and in the extreme low pH stations, with the following values: N1 = 3.3, N2 = 4.5; N3 = 5.4; S1 = 5.4; S2 = 11.4; S3 = 7.2. This indicates that although in the most acidified stations the leaves are shorter, the higher density compensates so that the space (surface) potentially available for epiphyte colonization is even higher than in the control stations.

Hydrozoan epiphytic assemblage along the pH gradient

Seven species of Hydrozoa were recorded in the Castello’ samples: Campanularia breviscyphia, Clytia hemisphaerica, Eudendrium simplex, Halecium pusillum, Obelia dichotoma, Plumularia obliqua, Sertularia perpusilla (Table I). Among them, S. perpusilla and P. obliqua are relatively common (found, respectively, on 11% and 5% of the analysed P. oceanica leaves) and distributed among all sampling sites (Table I). C. breviscyphia is less abundant (found on 2% of the analysed leaves) and has been observed mostly in SC and N1 sites. The other species are rare (<10 records in total). A sligthly higher abundance of C. breviscyphia in control sites with normal pH conditions (especially in SC) is the only significant spatial trend detectable from the semi-quantitative evaluation of the species presence and abundances (Tables II and Tables III). We did not observe any significant seasonal trend in overall community composition and species abundances and occurrences. Being common in all sites, S. perpusilla and P. obliqua are similar in their distribution (Figure 2). However, P. obliqua is partially replaced by C. breviscyphia in the sites SC and N1, which are therefore associated, while all other associations among species, or species and sites are weak (Figure 2).

Table I. List of the seven hydrozoan species found in this study on the CO₂ vents, and their average abundance score (calculated from the semi-quantitative classification of abundance 1 = low, 2 = medium, 3 = high) for each station

	Campanularia breviscyphia	Clytia hemisphaerica	Eudendrium simplex	Halecium pusillum	Obelia dichotoma	Plumularia obliqua	Sertularia perpusilla
N1	0.69 ± 0.49	0 ± 0	0 ± 0	0.06 ± 0	0.04 ± 0	0.45 ± 0.67	0.94 ± 0.84
N2	0.17 ± 0.03	0.04 ± 0.02	0.08 ± 0.03	0 ± 0	0 ± 0	0.9 ± 0.1	1.06 ± 0.67
N3	0.1 ± 0	0 ± 0	0 ± 0	0 ± 0	0 ± 0	0.54 ± 0.37	0.97 ± 1.13
SC	0.54 ± 0.56	0.05 ± 0	0 ± 0	0.12 ± 0.13	0 ± 0	0.31 ± 0.41	1.26 ± 1.21
S2	0.02 ± 0	0.08 ± 0	0 ± 0	0.03 ± 0	0 ± 0	0.18 ± 0.03	0.36 ± 0.29
S3	0.06 ± 0	0.03 ± 0	0.04 ± 0	0 ± 0	0 ± 0	0.3 ± 0.15	0.57 ± 0.5

Table II. Average abundance score (calculated from the semi-quantitative classification of abundance 1=low, 2=medium, 3=high) per leaf (± s.d.) of the seven hydrozoan species collected in this study, for each sampling period

	Campanularia breviscyphia	Clytia hemisphaerica	Eudendrium simplex	Halecium pusillum	Obelia dichotoma	Plumularia obliqua	Sertularia perpusilla
September	0.14 ± 0.11	0.06 ± 0.02	0.04 ± 0	0.12 ± 0.13	0.04 ± 0	0.27 ± 0.24	1.13 ± 0.99
December	0.06 ± 0	0.03 ± 0	0.1 ± 0	0.06 ± 0	0 ± 0	0.58 ± 0.47	1 ± 0.99
March	1.2 ± 0.06	0 ± 0	0 ± 0	0 ± 0	0 ± 0	0.58 ± 0.54	0.5 ± 0.31
June	0.27 ± 0.23	0.05 ± 0	0.06 ± 0	0.03 ± 0	0 ± 0	0.77 ± 0.04	0.43 ± 0.31

Table III. Campanularia breviscyphia, ANOVA of average abundance score calculated from the semi-quantitative classification of abundance (1 = low, 2 = medium, 3 = high) per leaf according to the only significant descriptors

Predictors	Estimates	CI	p
(Intercept)	0.32	0.27–0.38	<0.001
S	−0.00	−0.07–0.07	0.925
pH condition 2	0.05	−0.02–0.12	0.147
pH condition 3	0.06	−0.01–0.14	0.079
SiteS:pH condition 2	−0.27	−0.37 – −0.17	<0.001
SiteS:pH condition 3	−0.16	−0.27 – −0.06	0.002
Observations	3858
R^2/adjusted R^2	0.025/0.023

Figure 2. Heatmap of the site*species associations among the hydrozoan species found at the Castello vent and control stations, calculated from the semi-quantitative classification of abundance (1 = low, 2 = medium, 3 = high)

Posidonia oceanica hydroids checklist update

Based on a detailed literature survey, we have documented at least 86 species of hydrozoans living on P. oceanica leaves, on rhizomes, or on both layers (Table IV), updating previous data reported by Boero (1981a), with an increase of 30% of the taxa if compared to the previous list that accounted for 66 species.

Table IV. List of the hydroid species recorded from Posidonia beds in the Mediterranean Sea updating previous data reported by Boero (1981a)

Hydrozoa species	Synonyms and notes	Main references	Hydrozoa species	Synonyms and notes	Main references
Bougainvillidae			Halopterididae
Bougainvillia muscus (Allman, 1863)	Bougainvillia ramosa (Van Beneden, 1844)	1, 2	Antennella secundaria (Gmelin, 1791)	Sertularia secundaria Gmelin, 1791	2, 3, 6, 10, 31
Pachycordyle napolitana Weissmann, 1883	Cordylophora neapolitana (Weissmann, 1883)	2, 3	Halopteris diaphana (Heller, 1868)	Antennella diaphana (Heller, 1868)	2, 3, 33
Pachycordyle pusilla (Motz-Kossowska, 1905)	Cordylophora pusilla Motz-Kossowska, 1905	2–9, 49
			Hebellidae
Eudendriidae			Hebella scandens (Bale, 1888)	Hebella cylindrata? Marktanner-Turneretscher, 1890; Hebella calcarata (Agassiz, 1862)	12, 22, 34–37
Eudendrium capillare Alder, 1856		2, 3	Hebella sp.		2
Eudendrium glomeratum Picard, 1952		2, 10	Scandia gigas (Pieper, 1884)	Lafoea gigas Pieper, 1884; Hebella gigas (Pieper, 1884)	2, 3, 10, 12
Eudendrium racemosum (Cavolini, 1785)	Sertolara racemosa Cavolini, 1785	1
Eudendrium ramosum (Linnaeus, 1758)	Tubularia ramosa Linnaeus, 1758	2, 3, 10	Kirchenpaueriidae
Eudendrium simplex Pieper, 1884*	Eudendrium motzkossowskae Picard, 1952	2–4, 8	Kirchenpaueria halecioides (Alder, 1859)	Ventromma halecioides (Alder, 1859)	38, 39
			Kirchenpaueria pinnata (Linnaeus, 1758)	Kirchenpaueria echinulata (Hincks, 1868)	1–3, 7–9, 14, 19, 22, 40
Hydractiniidae
Clava nana Motz-Kossowska, 1905	taxon inquirendum	4, 6	Lafoeidae
Podocoryna areolata (Alder, 1862)	Podocoryne areolata (Alder, 1862); Hydractinia areolata Alder, 1862	11	Filellum serpens (Hassall, 1848)	Campanularia serpens Hassal, 1848; Grammaria serpens (Hassall, 1848)	2, 3, 10
Stylactis fucicola (M. Sars, 1857)	Podocoryna fucicola M. Sars, 1857; Hydractinia fucicola (Sars, 1857)	7	Lafoea dumosa (Fleming, 1820)	Lafoea fruticosa (Sars, 1851)	1, 6, 22, 28, 34, 41
Stylactis inermis Allman, 1872	Hydractinia inermis (Allman, 1872)	2, 3, 6, 10, 12
			Laodiceidae
Oceaniidae			Laodicea undulata (Forbes & Goodsir, 1853)	Thaumantias undulata Forbes & Goodsir, 1853	1, 41
Merona cornucopiae (Norman, 1864)	Tubiclava cornucopiae (Norman, 1864)	2, 3
Rhizogeton nudus Broch, 1910	Clava multicornis (Forskål, 1775)	3	Lovenellidae
			Campalecium torreyi (Motz-Kossowska, 1911)	as Campalecium medusiferum Torrey, 1902	2, 8, 9, 22, 32, 34
Pandeidae
Amphinema dinema (Péron & Lesueur, 1810)	Oceania dinema Péron & Lesueur, 1810	2, 3	Plumulariidae
			Plumularia obliqua (Johnston, 1847)*	Monotheca obliqua (Johnston, 1847)	39, 42, 43
Cladocoryniidae			Plumularia posidoniae (Picard, 1952)	Monotheca posidoniae Picard, 1952	1–3, 7, 8, 10, 12, 14, 19, 21, 22, 27, 28, 31, 45, 50, 51
Cladocoryne floccosa Rotch, 1871		2, 3, 10, 13, 14	Plumularia setacea (Linnaeus, 1758)	Sertularia setacea Linnaeus, 1758	7, 21
Cladonematiidae			Sertularellidae
Cladonema radiatum Dujardin,1843	Stauridium radiatum (Dujardin,1843)	15, 16	Sertularella ellisii (Deshayes & Milne Edwards, 1836)	Sertularia ellisii Deshayes & Milne-Edwards, 1836	1, 12, 28
Staurocladia portmanni Brinckmann, 1964		13, 17, 18	Sertularella fusiformis (Hincks, 1861)	Sertularia fusiformis Hincks, 1861	12
			Sertularella gaudichaudi (Lamouroux, 1824)	Sertularia gaudichaudi Lamouroux, 1824	1–3, 10, 35, 50, 51
Corynidae			Sertularella ornata Broch, 1933	Sertularella fusiformis f. ornata Broch, 1933	1, 28
Coryne epizoica Stechow, 1921		13	Sertularella polyzonias (Linnaeus, 1758)	Sertularia polyzonias Linnaeus, 1758	2, 3
Coryne muscoides (Linnaeus, 1761)	Tubularia muscoides (Linnaeus, 1761)	19	Sertularella rugosa? (Linnaeus, 1758)	Sertularia rugosa Linnaeus, 1758	2
Coryne pintneri Schneider, 1897		2, 3, 8, 13, 19
Coryne pusilla Gaertner, 1774		2, 3, 20	Sertulariidae
			Amphisbetia distans (Lamouroux, 1816)	Sertularia distans Lamouroux, 1816	6, 7, 22, 27, 40, 46
Pennariidae			Dynamena disticha (Bosc, 1802)	Sertularia disticha Bosc, 1802	2, 3, 22, 38, 40, 49
Pennaria disticha Goldfuss, 1820	Halocordyle disticha (Goldfuss, 1820)	21	Dynamena pumila (Linnaeus, 1758)	Sertularia pumila (Linnaeus, 1758)	47, 48
			Salacia desmoides (Torrey, 1902)	Dynamena desmoides (Torrey, 1902)	7, 12, 49
Tubulariidae			Sertularia perpusilla Stechow, 1919*		1–3, 6–8, 10, 12, 14, 15, 19, 20, 22, 28, 31, 38, 42, 44, 49, 50, 51
Ectopleura larynx (Ellis & Solander, 1786)	Tubularia larynx Ellis & Solander, 1786	22
Ectopleura wrighti Petersen, 1979	as Ectopleura larynx (Wright, 1863)	13	Syntheciidae
			Synthecium evansi (Ellis & Solander, 1786)	Sertularia evansi (Ellis & Solander, 1786)	22, 50
Zancleidae
Zanclea costata Gegenbaur, 1857	Mnestra parasites Krohn, 1853	2, 18	Campanulariidae
			Campanularia breviscyphia Sars, 1857*	Campanularia asymmetrica (Stechow, 1919); Orthopyxis asymmetrica Stechow, 1919	1–3, 6, 7, 14, 19, 20, 22, 31, 49, 50
Aglaopheniidae			Campanularia hincksii Alder, 1856	Campanularia alta Stechow, 1919	2, 6, 8–10, 12, 21, 22, 28, 34, 35, 41, 49
Aglaophenia elongata Meneghini, 1845		22	Campanularia volubilis (Linnaeus, 1758)	Sertularia volubilis Linnaeus, 1758	6, 9, 12, 27, 38, 39, 43
Aglaophenia harpago Von Schenck, 1965		2, 3, 6, 8, 23, 24, 49, 50	Clytia hemisphaerica (Linnaeus, 1767)*	Medusa hemisphaerica Linnaeus, 1767; Campanularia johnstoni Alder, 1856; Clytia johnstoni (Alder, 1856); Phialidium hemisphaericum (Linnaeus, 1767)	1–3, 6, 7, 10, 19, 20, 27, 28, 31, 40, 49, 50, 51
Aglaophenia kirchenpaueri (Heller, 1868)	Plumularia kirchenpaueri (Heller, 1868)	22	Clytia linearis (Thornely, 1900)	Obelia linearis Thornely, 1900; Clytia gravieri (Billard, 1904); Campanularia gravieri Billard, 1904; Campanularia linearis (Thornely, 1900)	2, 3, 8–10, 31
Aglaophenia octodonta (Heller, 1868)	Plumularia octodonta (Heller, 1868)	25, 26	Clytia noliformis (McCrady, 1859)	Campanularia noliformis McCrady, 1859	2, 3, 8, 9, 22
Aglaophenia picardi Svoboda, 1979		2, 10, 12, 14, 25, 26	Clytia paulensis (Vanhöffen, 1910)	Campanularia paulensis Vanhöffen, 1910	2, 3, 8, 9, 12, 22, 31, 39, 41, 43
Aglaophenia pluma (Linnaeus, 1758)	Plumularia pluma (Linnaeus, 1758)	26–29	Gonothyraea loveni (Allman, 1859)	Laomedea loveni Allman, 1859	1, 6, 15, 22, 47
Aglaophenia tubiformis Marktanner-Turneretscher, 1890		12, 30	Laomedea angulata Hincks, 1861	Campanularia angulata (Hincks, 1861)	6, 7, 14, 15, 22, 27, 43, 44, 46, 51
			Laomedea calceolifera (Hincks, 1871)	Campanularia calceolifera Hincks, 1871	6–8, 10, 14, 15, 22, 27, 37
Campanulinidae			Laomedea flexuosa Alder, 1857	Campanularia flexuosa (Alder, 1857)	5, 22, 43, 46
Lafoeina tenuis G.O. Sars, 1874	Lafoeina vilaevelebiti Hadzi, 1917	1–3, 8, 9	Obelia dichotoma (Linnaeus, 1758)*	Sertularia dichotoma Linnaeus, 1758; Campanularia dichotoma (Linnaeus, 1758); Laomedea dichotoma (Linnaeus, 1758)	1–3, 6–9, 15, 22, 28, 35, 39, 43, 51
			Obelia geniculata (Linnaeus, 1758)	Sertularia geniculata Linnaeus, 1758; Campanularia geniculata (Linnaeus, 1758)	1, 2, 7, 15, 21, 27, 38, 40, 49
Haleciidae			Obelia longissima (Pallas, 1766)	Sertularia longissima Pallas, 1766	52
Halecium delicatulum Coughtrey, 1876		10, 49	Orthopyxis caliculata (Hincks, 1853)	Campanularia caliculata Hincks, 1853	21, 53, 54
Halecium lankesterii (Bourne, 1890)	Haloikema lankesterii Bourne, 1890	2	Orthopyxis crenata (Hartlaub, 1901)	Campanularia crenata (Hartlaub, 1901)	2, 3, 6, 7, 22
Halecium mediterraneum Weissmann, 1883		1–3, 6, 12	Orthopyxis everta Clarke, 1876	Campanularia everta Clarke, 1876	2
Halecium nanum Alder, 1859		2, 3, 19	Orthopyxis integra (MacGillivray, 1842)	Campanularia integra MacGillivray, 1842	5, 6, 8, 9, 12, 22, 37, 38
Halecium petrosum Stechow, 1919		12
Halecium pusillum (M. Sars, 1857)*	Eudendrium pusillum M. Sars, 1857	1–3, 6–9, 49
Halecium tenellum Hincks, 1861		2, 3, 12, 31
Hydrodendron mirabile (Hincks, 1866)	Ophiodes mirabilis Hincks, 1866	7, 32

References: 1 (Repetto et al. 1977); 2 (Boero 1981a); 3 (Boero 1981b); 4 (Motz-Kossowska 1905); 5 (Lo Bianco 1909); 6 (Stechow 1919); 7 (Picard 1952); 8 (Boero & Fresi 1986); 9 (Puce et al. 2009); 10 (Roca et al. 1991); 11 (Yamada 1961); 12 (Peña Cantero & García Carrascosa 2002); 13 (Brinckmann-Voss 1970); 14 (Piraino & Morri 1990); 15 (Rossi 1971); 16 (Morri & Bianchi 1976); 17 (Brinckmann 1964); 18 (Brinckmann-Voss 1987); 19 (Boero et al. 1985); 20 (García Rubies 1992); 21 (Brahim et al. 2010); 22 (Gili 1986); 23 (Svoboda 1979); 24 (Von Schenck 1965); 25 (Svoboda & Cornelius 1991); 26 (Medel & Vervoort 1995); 27 (Stechow 1923); 28 (Broch 1933); 29 (Riedl 1966); 30 (Marktanner-Turneretscher 1890); 31 (Fresi et al. 1982); 32 (Motz-Kossowska 1911); 33 (Schuchert 1997); 34 (Picard 1951b); 35 (Rossi 1961); 36 (Schmidt 1973); 37 (Marinopoulos 1979); 38 (Galea 2007); 39 (Isinibilir et al. 2015); 40 (El Beshbeeshy 1995); 41 (Ramil & Vervoort 1992); 42 (Billard 1936); 43 (Yilmaz et al. 2020); 44 (Picard and Le Roch 1949); 45 (Picard 1951a); 46 (Redier 1962a); 47 (Redier 1962b); 48 (El Beshbeeshy 1994); 49 (Roca 1987); 50 (Relini Orsi et al. 1977); 51 (Morri et al. 1991); 52 (Morri & Bianchi 1982); 53 (Brahim et al. 2014); 54 (Brahim et al. 2015).

The symbol * indicates the species recorded in this study.

Discussion and conclusion

The present study provides information on the composition and structure of the hydrozoan epiphytic community in Posidonia oceanica meadows and on the phenology of this seagrass exposed to a natural acidification gradient due to volcanic CO₂ emissions. The results indicated that P. oceanica shoot density and plant phenology in the studied stations of the vent systems showed significant differences among pH conditions, consistently with the results of previous studies (Hall-Spencer et al. 2008; Donnarumma et al. 2014; Garrard et al. 2014; Mecca et al. 2020). Our observations confirm that Posidonia has higher levels of shoot density and shorter leaves in the stations characterized by the highest emission of bubbles, and where extremely low and high fluctuating pH conditions occur. The higher density, however, compensates for the shorter leaves with the consequence that the space/surface potentially available for epiphyte colonization (L.A.I.) is higher than in the control stations. As regards the hydrozoans, our results show that these organisms have the ability to withstand low pH values in all the periods considered, and relevant colonization by hydroids in P. oceanica subjected to ocean acidification, have been also observed in other studies both around Ischia (Donnarumma et al. 2014; Mecca et al. 2020) and in the Panarea Island (Gaglioti et al. 2019). This can be explained by the fact that the species found all belong to chitinous and not-calcifying forms and, in addition, being small organisms and living on the leaf surface and within the leaf canopy, hydroids can probably benefit from an attenuation of the negative effects of pH due to the plant’s photosynthesis activity (Hendriks et al. 2014). However, a further aspect to consider for hydroids abundance in our sites is that they could be also favoured by the reduced competition for substratum with the calcareous forms of many other epiphytes. In fact, in the studied samples, we observed a strong reduction or disappearance of calcareous organisms in the most acidified stations (e.g., coralline algae, spirorbid polychaetes, bryozoans) (Di Meglio 2016). This pattern was indeed observed also in previous studies on both natural and artificial/mimic P. oceanica shoots at the Castello vents (Martin et al. 2008; Donnarumma et al. 2014; Nogueira et al. 2017), as well as in the Posidonia meadows of other vent’s systems both around Ischia (Mecca et al. 2020), in the Aeolian Islands (Gaglioti et al. 2019), and also in shoots sampled inside special in situ mecosoms the FOCE systems (Cox et al. 2015, 2017). Tolerance to low pH conditions it is particularly evident in the more common observed hydrozoan species such as S. perpusilla and P. obliqua. Furthermore, hydroids are among the first colonizers of marine hard substrata with several species that grow on a limited range of surface types (Boero 1987; Boero & Hewitt 1992; Puce et al. 2005, 2007) and with several hydroid species that are obligate epiphytes of Posidonia leaves (Boero 1981a, 1987).

Based on a detailed literature survey, we have documented at least 86 species of hydrozoans living on P. oceanica leaves, on rhizomes, or on both layers (Table IV) updating previous data reported by Boero (1981a). According to Boero (1981a, 1981b) and our updated checklist, among the epiphytic hydroids on Posidonia leaves at 2–4 m depth (the range considered in this study) have been reported the species Campanularia breviscyphia, Eudendrium simplex, Sertularia perpusilla (superficial and intermediate-superficial species); Clytia hemisphaerica, Halecium pusillum, Plumularia obliqua (species of leaves at all depths). Therefore, the biodiversity level observed in our samples (7 species) is consistent with the number of hydroids species generally associated to shallow Posidonia stands. Knowledge of their bathymetric distribution began with the studies by Boero (1981a, 1981b), Balduzzi et al. (1981, 1984), and Boero et al. (1985) in P. oceanica meadows in the western Mediterranean Sea. Moreover, these results highlighted, as proposed by Boero (1981a), the mainly shallow distributions of the exclusive epiphytic hydroids on Posidonia leaves could be explained by an association with Posidonia leaves started long ago, before the rise in sea level after the Messinian crisis (over 5–6 million years ago) according to the Den Hartog’s theory (1973): Posidonia is a superficial plant that survives at greater depths owing to the Mediterranean Sea-level variations. Therefore, the distribution of the species strictly epiphytic of Posidonia leaves can be explained by their incapacity to tolerate the changes of physical-chemical conditions remaining within Posidonia optimal depths.

This association with the Posidonia leaves has been promoted by certain characteristics of hydroids such as rapid growth and asexual reproduction by stolonization (Philbert 1935; Von Schenck 1963). Moreover, the topographical/temporal separation between Posidonia and hard substrata has favoured the isolation of hydroid populations inhabiting Posidonia leaves leading to speciation among some of the Posidonia hydroids (Boero 1987). Furthermore, that association of hydroids with Posidonia leaves could be favoured by the good trophic conditions achieved in positions raised above the sea bottom also in shallow waters where water movement provides an equally high rate of water flow also over the rhizomes (Boero 1984). Adaptations by those species, probably, started because of the advantages of this substratum as great water flow around the near erect leaves and, since much of the space on Posidonia leaves is relatively free from epiphytes, showing a reduced competition for substratum (Boero 1987). On the other hand, hydroids have overcome the disadvantage as epiphytes of a living substratum with the rapid growth and turnover such as those of their host substratum. In fact, hydrozoan-Posidonia associated species have a rapid growth, and some species are able to pass from old leaves to new ones by stolonization (Philbert 1935; Von Schenck 1963). The hydrozoan epiphytic population of Posidonia is so typical and rich that its study can be an optimal tool for the evaluation of the conditions of the Posidonia meadows and its associated fauna. In addition, this study on the Castello vents confirms that these organisms represent some of the few “winner” organisms able to survive in view of the future scenario of ocean acidification in the global ocean.

Consent for publication

Being the corresponding author of the manuscript, I state that all authors agree to its submission and the Corresponding author has been authorized by the co-authors.

Ethical approval consent to participate

No animal testing was performed during this study.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent Authorities and are mentioned in the acknowledgements. The study is compliant with CBD and Nagoya protocols.

Acknowledgements

We wish to thank Dr Luigia Donnarumma for help in the morphological measures of Posidonia oceanica shoots, and Vincenzo Rando and Bruno Iacono for support in the field. Thanks are due to Martina Gaglioti for drawing the background map of the Castello in Figure 1. The scientific field collections of the Stazione Zoologica Anton Dohrn (Naples) around Ischia are authorized by the local managing Authority of the Marine Protected Area “Regno di Nettuno”, which include also the Castello vent’s area.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary material

Supplemental data for this article can be accessed here.