Evidence of Warm Welcome From the Cymodocea nodosa (<em>Tracheophyta, Alismatales</em>) Meadow in the Seas of Taranto (Southern Italy, Mediterranean Sea)

The collection of photo shoots during the systematic monitoring activities is useful to witness the ecological role of marine phanerogams as hosts for a rich variety of organisms in coastal and transitional waters. Cymodocea nodosa is present in the Taranto seas. In the Mar Piccolo, it reached high covers in short times, up to 100%, due to the bettering of the environmental conditions. The most recent observations showed that it offers welcoming towards several vertebrates and invertebrates, native and non-indigenous, as well as to micro and macroalgae. The NPPR funded activities will make these observations more robust and structural.

Keywords:

biodiversity

;

Cymodocea nodosa

;

ecosystem services

;

ITINERIS

;

LTER

;

Mar Piccolo of Taranto

;

Mediterranean Sea

;

non-indigenous species

;

NBFC

Subject:

Environmental and Earth Sciences - Ecology

Marine phanerogams are paramount for the structuring and functioning of marine coastal ecosystems. They are emblematic primary producers, protect shoreline from erosion, support high biodiversity offering food, refuge and nursey areas to invertebrates and vertebrates, such as fish and even migrant birds [1,2,3,4]. Their value in terms of ecosystem services, only in the Caribbean, was estimated at about 255 billion $ per year [5]. Marine phanerogams’ abundance is a sign of excellent environmental conditions. So, they have been included among the primary species for the definition of priority habitat within the Habitat Directive (92/43/EEC), and used as bioindicators in the formulation of biotic indices for the assessment of the Good Environmental Status (GES) in coastal and transitional water systems, according to Water Framework Directive (2000/60/EC) and Marine Strategy Framework Directive (2008/56/EC) [6,7,8].

Cymodocea nodosa (Ucria) Ascherson is a plastic marine phanerogam, able to flourish into pristine environments, as well as to survive in stressed ones [9,10]. It is widely distributed into the Mediterranean coastal and transitional water systems, from East to West [9,11]. The articulated rhizome-root component with the dense slender leaves forms a robust grid, which stabilizes the substrate and welcomes the vagile fauna. Grazers find food also on the rich epiphytic community and often spawn among the shoots [2,3,12]. A value of about 3 million € per year was recently assessed for the commercial fish community housed by the C. nodosa meadows at Canary Islands [13]. Seahorses are joint guests of this marine plant [14,15], so as it earned the folk name of “seahorse grass” [16].

Cymodocea nodosa is present with a dense meadow along the south-eastern coast of the Mar Grande of Taranto [F. Rubino personal communication], where it sexually reproduces [E. Cecere personal communication]. Diving observations showed that it hosts a varied fauna from native seahorses Hyppocampus hippocampus (Linnaeus, 1758) and H. guttulatus (Cuvier 1829) to non-indigenous mollusks, such as Pinctada radiata (Leach, 1814) (Figure 1a,b).

In the Mar Piccolo, a transitional water system located in the Ionian Sea, after a consistent thinning in the 1980s and the 1990s, due to the presence of high eutrophication, C. nodosa is now flourishing again [17]. It is widely distributed along the basin coast, and in some zones, the meadow reaches a cover up to 100% [18], a sign of a high status, according to the MaQI index [6] (Figure 2).

The seasonal systematic observations carried out on the Mar Piccolo macrobenthos, mainly phytobenthos, since 2011, within the framework of long-term ecological research (LTER) activities, currently funded by the NRRP Project ITINERIS, allowed a visual assessment of the progressive recover of the meadow [17]. In addition, the activities performed within the framework of the Project “MIA Natura 2000”, funded through POR PUGLIA FESR-FSE 2014/2020, led to the quantitative evaluation of the meadow’s density as well as the structural descriptors [18]. The phenological monitoring is now continued within the National Recovery and Resilience Plan (NRRP), with the Project “National Biodiversity Future Center”. The diving observations carried out in these years, for the collection of benthos samples, brought also to light the close relations of C. nodosa with the fauna and flora living in the basin.

For several years, starting from 2014, it was common to see specimens of the fan mussel Pinna nobilis (Linnaeus 1758) among the shoots of C. nodosa [19] (Figure 3). The big bivalve mollusk shows a marked preference for this phanerogam in transitional waters, mainly due to the close bonds produced among the rhizomes, the sediments, and the byssus filaments [20,21,22,23]. Also of paramount importance is the protective effect of leaves against the hydrodynamics, which fosters the mollusk’s larvae settlement [23]. In Spain, in the transitional system of the Ebro River (NW Mediterranean), the highest density of P. nobilis specimens were measured in zones where the C. nodosa meadow reached a covering of 80-100% [21]. In the Venice Lagoon (Adriatic Sea, northern Italy), the fan mussel density was the highest at the highest cover of the phanerogam, and it was preferably located at the border of the meadow, where the filtering activity can be enhanced [23]. Unfortunately, Figure 3 represents an historical relic, since starting from 2018, P. nobilis underwent mass mortality in the Taranto seas, due to an infection of the protozoic parasite Haplosporidium pinnae [24]. This caused its disappearance from the basin, as already observed all around the Mediterranean Sea [25].

The Mar Piccolo of Taranto, like most of the transitional water systems, is subject to a high degree of biological pollution. At the moment, 22 non-indigenous invertebrates and 16 seaweeds have been recorded in the basin ([26], A. Petrocelli unpublished data). Generally, marine non-indigenous species (NIS) are considered a serious menace for the native communities, especially when they have a markedly invasive behavior, since they can cause strong alteration of ecosystem functions, reduction of biodiversity, damages to the economic activities [27,28]. Caulerpa cylindracea Sonder considerably spread along most of the coastal zone of the Mediterranean Sea in 1990s and 2000s, with a negative impact on both biodiversity and structure of the invaded ecosystems.

Within a mixed meadow of C. nodosa and Nanozostera noltei (Hornemann) Tomlinson & Posluszny (as Zostera noltii Hornemann) in the Tyrrhenian Sea, this invasive NIS considerably reduced the shoot density of the former [29] and altered the density of its flowering plants [30]. However, if the ecology of native species and NIS is significantly different, no interaction between the species can establish [28]. In the Mar Piccolo, no NIS caused serious damage to benthic populations to date [26]. Concerning seaweeds, the only species with an invasive behavior is Hypnea corona Huisman & Petrocelli, which is spreading into the basin since 2000, becoming the dominant species in summer, but without any evident disruption for both the icrophytobenthic communities and the native fauna [26]. Mixed communities with native species of seaweeds and invertebrates, and even C. nodosa, are observed in the basin (Figure 4a). Among NIS invertebrates, 7 molluscan species were recorded in the Mar Piccolo. The grazer Bursatella leachii Blainville 1817 and the carnivorous Melibe viridis (Kelaart, 1858) are frequently present in the C. nodosa meadow both in the Mar Piccolo and Mar Grande of Taranto [31] (Figure 4b), as reported also for other coastal Mediterranean environments [32,33,34,35,36]. Both species surely find refuge among the dense shoots, as well as their preferred meal. The former is primarily drawn to the rich epiphytic communities (e.g. diatoms, cyanobacteria) and the detritus, but sometimes does not mind associated seaweeds [35]. The latter finds several preys, such as microalgae herbivores, filter feeders, ectoparasites [12].

Once again, the effectiveness of LTER activities in the study of biodiversity in the Mar Piccolo of Taranto is made evident. The continuous monitoring and the availability of historical observations allow to follow the population development of species worth of protection (e.g., Pinna nobilis, Cymodocea nodosa). The NIS fate and every possible new introduction are continuously under surveillance. New technologies, such as the remote sensing and the eDNA, joined to the field activities and the classical taxonomy will surely lead to a more and more deep knowledge. In Italy, finally there was an awareness of this. The funding of the National Biodiversity Future Center can be an initial step and the fulfillment of its main task “conserve, restore, monitor and enhance Italian and Mediterranean biodiversity” is on track.

Author Contributions

Conceptualization, G.D., A.P.; methodology, G.D and F.R.; investigation, G.D., A.P., F.R.; resources, G.D. and F.R.; data curation, A.P.; writing—original draft preparation, A.P.; writing—review and editing, E.C., G.D., A.P., F.R.; visualization, A.P.; supervision, A.P., F.R.; project administration, A.P.; funding acquisition, A.P., F.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by POR PUGLIA FESR-FSE 2014/ 2020—Axis VI, Action 6.5.; under the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 1.4 - Call for tender No. 3138 of 16 December 2021, rectified by Decree n. 3175 of 18 December 2021 of Italian Ministry of University and Research funded by the European Union – NextGenerationEU, Project code CN_00000033, Concession Decree No. 1034 of 17 June 2022 adopted by the Italian Ministry of University and Research, CUP B83C22002930006 Project title “National Biodiversity Future Center - NBFC”; under the NRRP, Mission 4 Component 2 Investment 3.1, code IR_0000032, CUP B53C22002150006 Project title “ITINERIS”. The APC was funded by POR PUGLIA FESR-FSE 2014/ 2020—Axis VI, Action 6.5.

Acknowledgments

Giovanni Squitieri (www.officinadellimmagine.eu) is acknowledged for his participation in all the underwater activities and for the photo documentation produced. We acknowledge also the contribution of Giuseppe Portacci for sampling activities and photo provided.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

Terrados, J.; Borum, J. Why are seagrasses important? – Goods and services provided by seagrass meadows. In European seagrasses: An introduction to monitoring and management; Borum, J., Duarte, C.M., Krause-Jensen, D., Greve, T.M., Eds.; The M&MS project: EU, 2004; pp. 8–10. [Google Scholar]
Tuya, F.; Haroun, R.; Espino, F. Economic assessment of ecosystem services: Monetary value of seagrass meadows for coastal fisheries. Ocean Coast. Manag. 2014, 96, 181–187. [Google Scholar] [CrossRef]
Jiménez-Ramos, R.; Egea, L.G.; Vergara, J.J.; Brun, F.G. Factors modulating herbivory patterns in Cymodocea nodosa meadows. Limnol. Oceanogr. 2021, 66, 2218–2233. [Google Scholar] [CrossRef]
do Amaral Camara Lima, M.; Bergamo, T.F.; Ward, R.D.; Joyce, C.B. A review of seagrass ecosystem services: Providing nature-based solutions for a changing world. Hydrobiologia 2023, 850, 2655–2670. [Google Scholar] [CrossRef]
Shayka, B.F.; Hesselbarth, M.H.; Schill, S.R.; Currie, W.S.; Allgeier, J.E. The natural capital of seagrass beds in the Caribbean: Evaluating their ecosystem services and blue carbon trade potential. Biol. Letters 2023, 19, 20230075. [Google Scholar] [CrossRef] [PubMed]
Sfriso, A.; Facca, C.; Ghetti, P.F. Validation of the Macrophyte Quality Index (MaQI) set up to assess the ecological status of Italian marine Transitional environments. Hydrobiologia 2009, 617, 117–141. [Google Scholar] [CrossRef]
Orlando-Bonaca, M.; Francé, J.; Mavrič, B.; Grego, M.; Lipej, L.; Flander-Putrle, V.; Šiško, M.; Falace, A. A new index (MediSkew) for the assessment of the Cymodocea nodosa (Ucria) Ascherson meadow's status. Mar. Environ. Res. 2015, 110, 132–141. [Google Scholar] [CrossRef] [PubMed]
Sfriso, A.A.; Sciuto, K.; Mistri, M.; Munari, C.; Juhmani, A.S.; Buosi, A.; Sfriso, A. Where, when, how and what seagrass to transplant for long lasting results in transitional water systems: The cases of Cymodocea nodosa, Zostera marina, Zostera noltei and Ruppia cirrhosa. Front. Mar. Sci. 2023, 10, 1299428. [Google Scholar] [CrossRef]
Orfanidis, S.; Papathanasiou, V.; Gounaris, S.; Theodosiou, T. Size distribution approaches for monitoring and conservation of coastal Cymodocea habitats. Aquatic Conserv. Mar. Freshw. Ecosyst. 2009, 20, 177–188. [Google Scholar] [CrossRef]
Papathanasiou, V.; Orfanidis, S.; Brown, M.T. Cymodocea nodosa metrics as bioindicators of anthropogenic stress in N. Aegean, Greek coastal waters. Ecol. Indic. 2016, 63, 61–70. [Google Scholar] [CrossRef]
Chefaoui, R.M.; Assis, J.; Duarte, C.M.; Serrão, E.A. Large-scale prediction of seagrass distribution integrating landscape metrics and environmental factors: The case of Cymodocea nodosa (Mediterranean–Atlantic). Estuar. Coast 2016, 39, 123–137. [Google Scholar] [CrossRef]
Manousis, T.; Galinou-Mitsoudi, S. Great molluscan diversity associated with a limited Cymodocea nodosa (Ucria) Ascherson, bed in Thermaikos Gulf, North Aegean Sea, Greece. Xenophora Taxon. 2022, 35, 20–42. [Google Scholar]
Casas, E.; Martín-García, L.; Otero-Ferrer, F.; Tuya, F.; Haroun, R.; Arbelo, M. Economic mapping and assessment of Cymodocea nodosa meadows as nursery grounds for commercially important fish species. A case study in the Canary Islands. One Ecosyst. 2021, 6, e70919. [Google Scholar] [CrossRef]
Pierri, C.; Cardone, F.; Corriero, G.; Lazic, T.; Quattrocchi, F.; Alabiso, G.; Gristina, M. Density decline in a Mediterranean seahorse population: Natural fluctuations or new emerging threats? Front. Mar. Sci. 2021, 8, 692068. [Google Scholar] [CrossRef]
Vivas, M.; Peñalver, J.; Oliver, J.A.; López Giraldo, J.D.; Mena, C. Population dynamics of the long-snouted seahorse (Hippocampus guttulatus Cuvier, 1829) in the Mar Menor coastal lagoon. J. Fish Biol. 2024, 104, 163–170. [Google Scholar] [CrossRef] [PubMed]
Borum, J.; Greve, T.M. The four European seagrass species. In European seagrasses: An introduction to monitoring and management; Borum, J., Duarte, C.M., Krause-Jensen, D., Greve, T.M., Eds.; The M&MS project: EU, 2004; pp. 1–7. [Google Scholar]
Petrocelli, A.; Cecere, E.; Rubino, F. Successions of phytobenthos species in a Mediterranean transitional water system: The importance of long term observations. Nat. Conserv. 2019, 34, 217–246. [Google Scholar] [CrossRef]
Petrocelli, A.; Cecere, E.; Fanelli, G.; Rubino, F.; Denti, G. Phenological monitoring of Cymodocea nodosa (Tracheophyta, Alismatales) in the transitional system Mar Piccolo of Taranto for the detection of anthropogenic impact. In Proceedings of the IEEE International Workshop on Metrology for the Sea, Valletta, Malta, 4–6 October 2023. [Google Scholar]
Rubino, F.; Cecere, E.; Petrocelli, A.; Casale, A.; Casale, V.; Passarelli, S. Recent observations of Pinna nobilis (Mollusca, Bivalvia) in the Mar Piccolo basin (Gulf of Taranto, Mediterranean Sea). Biol. Mar. Medit. 2015, 22, 107. [Google Scholar]
Zakhama-Sraieb, R.; Sghaier, Y.S.; Omrane, A.; Charfi Cheikhrouha, F. Density and population structure of Pinna nobilis (Mollusca, Bivalvia) in the Ghar El Melh lagoon (NE Tunisia). Bull. Inst. Natl. Sci. Technol. Mer 2011, 38, 65–71. [Google Scholar]
Prado, P.; Caiola, N.; Ibáñez, C. Habitat use by a large population of Pinna nobilis in shallow waters. Sci. Mar. 2014, 78, 555–565. [Google Scholar] [CrossRef]
Belando, M.D.; García-Muñoz, R.; Ramos, A.; Franco, I.; Bernardeau-Esteller, J.; García, P.; Ruiz, J.M. Distribution and abundance of Cymodocea nodosa meadows and Pinna nobilis populations in the Mar Menor coastal lagoon (Murcia, South East of Spain). PeerJ PrePrints 2015, 3, e1063v1. [Google Scholar] [CrossRef]
Silvestri, S.; Capra, V.; Cucchiaro, S.; Pivato, M.; Tarolli, P. Tides, topography, and seagrass cover controls on the spatial distribution of Pinna nobilis on a coastal lagoon tidal flat. J. Geophys. Res.-Biogeo. 2022, 127, e2021JG006667. [Google Scholar] [CrossRef]
Tiscar, P.G.; Rubino, F.; Paoletti, B.; Francesco, C.E.D.; Mosca, F.; Salda, L.D.; Hattab, J.; Smoglica, C.; Morelli, S.; Fanelli, G. New insights about Haplosporidium pinnae and the pen shell Pinna nobilis mass mortality events. J. Invertebr. Pathol. 2022, 190, 107735. [Google Scholar] [CrossRef] [PubMed]
Kersting, D.; Benabdi, M.; Čizmek, H.; Grau, A.; Jimenez, C.; Katsanevakis, S.; Öztürk, B.; Tuncer, S.; Tunesi, L.; Vázquez-Luis, 216 M.; Vicente, N.; Otero Villanueva, M. Pinna nobilis. In: The IUCN Red List of Threatened Species 2019; International Union for Conservation of Nature and Natural Resources; e.T160075998A160081499. [CrossRef]
Petrocelli, A.; Wolf, M.A.; Sciuto, K.; Sfriso, A.; Rubino, F.; Ricci, P.; Cecere, E. Long-term data prove useful to keep track of non-indigenous seaweed fate. Front. Environ. Sci. 2023, 11, 1075458. [Google Scholar] [CrossRef]
Ojaveer, H.; Galil, B.S.; Campbell, M.L.; Carlton, J.T.; Canning-Clode, J.; Cook, E.J.; Davidson, A.D.; Hewitt, C.L.; Jelmert, A.; Marchini, A.; et al. Classification of non-indigenous species based on their impacts: Considerations for application in marine management. PLoS Biol. 2015, 13, e1002130. [Google Scholar] [CrossRef] [PubMed]
Thomsen, M.S.; Wernberg, T.; Staehr, P.A.; Schiel, D. Ecological interactions between marine plants and alien species. In Marine Macrophytes as Foundation Species; Ólafsson, E., Ed.; CRC Press: Boca Raton, USA, 2016; pp. 226–258. [Google Scholar]
Ceccherelli, G.; Campo, D. Different effects of Caulerpa racemosa on two co-occurring seagrasses in the Mediterranean. Bot. Mar. 2002, 45, 71–76. [Google Scholar] [CrossRef]
Piazzi, L.; Balata, D.; Bulleri, F.; Gennaro, P.; Ceccherelli, G. The invasion of Caulerpa cylindracea in the Mediterranean: The known, the unknown and the knowable. Mar. Biol. 2016, 163, 1–14. [Google Scholar] [CrossRef]
Carriglio, D.; Fanelli, G.; Rubino, F. First record of the alien gastropod Melibe fimbriata (Opistobranchia: Tethyidae) in the Taranto seas (Mediterranean Sea). J. Mar. Biol. Ass. U.K. 2004, 84, 1067–1068. [Google Scholar] [CrossRef]
Mandic, M.; Macic, V.; Markovic, O. Spawning of alien nudibranch Melibe viridis (Kelaart, 1858) in south Adriatic Sea (Montenegro). Fresen. Environ. Bull. 2016, 25, 4566–4568. [Google Scholar]
Selfati, M.; Ouamari, N.E.; Crocetta, F.; Mesfioui, A.; Boissery, P.; Bazairi, H. Closing the circle in the Mediterranean Sea: Bursatella leachii Blainville, 1817 (Mollusca: Gastropoda: Anaspidea) has reached Morocco. BioInvasions Rec. 2017, 6, 129–134. [Google Scholar] [CrossRef]
Sghaier, Y.R.; Zakhama-Sraieb, R.; Hmida, A.B.; Charfi, F. An inventory of non-indigenous species (NIS) inside and outside three tourist marinas from the southern Mediterranean coast. J. Black Sea/Medit. Environ. 2019, 25, 29–48. [Google Scholar]
Pontes, M.; Ballesteros, M. Bursatella leachii Blainville, 1817 (Mollusca, Gastropoda, Heterobranchia), a successful global sea hare. OPK-Opistobranquis 2023, Available at https://opistobranquis.info/en/?p=42720.
Monnier, B.; Goirand-Mauberret, C.; André, S.; Pergent-Martini, C.; El Idrissi, O. First record of Bursatella leachii de Blainville, 1817 (Mollusca: Gastropoda: Aplysiidae) in Corsica (France, NW Mediterranean). Reg. Stud. Mar. Sci. 2024, 73, 103473. [Google Scholar] [CrossRef]

Figure 1. Associated fauna to Cymodocea nodosa shoots in the Mar Grande of Taranto: (a) the seahorse Hyppocampus guttulatus takes refuge within the meadow; (b) aggregated specimens of Pinctada radiata.

Figure 2. A dense meadow of Cymodocea nodosa onto the bottom of the Mar Piccolo basin (Photo credits: Gianni Squitieri).

Figure 3. Pinna nobilis among the leaves of Cymodocea nodosa in the Mar Piccolo of Taranto (Photo credits: Gianni Squitieri).

Figure 4. Alien organisms among Cymodocea nodosa shoots in the Mar Piccolo of Taranto: (a) Thalli of Hypnea corona intertwined with leaves (Photo credits: Giuseppe Portacci); (b) A specimen of Melibe viridis hidden within the dense meadow.

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