Skip to main content

Long-term changes in the benthic macroalgal flora of a coastal area affected by urban impacts (Conero Riviera, Mediterranean Sea)

Abstract

Seaweed communities are important coastal ecosystems representing good indicators of environmental variation related to climate change and other long-term changes. Long-term variation in the distribution of seaweed communities and individual seaweed species has been intensively investigated; however, long-term studies considering the whole seaweed flora of a geographical area have been infrequently produced, despite of their potential to unravel major changes. The macroalgal flora of a coastal area subjected to urban influences (Conero Riviera, Mediterranean Sea) was investigated comparing the contemporary flora with historical data available for three periods (1941–1946; 1964–1976; 1997–1999). The most evident change was the disappearance of 25–30 species that were present in 1941–1946 (and, in some cases, still in 1964–1976). Such losses are not recent and took place mainly in the years 1940–1960. A general environmental deterioration due to the urbanization of the area of Ancona is suggested as main cause of their disappearance; there is no evidence that their loss was related to climate change. Another major change was the introduction of 9 non-indigenous species, which were probably introduced from the Lagoon of Venice by maritime traffic. One of them, Melanothamnus japonicus, is now very abundant on the Conero Riviera. The results show that present floristic patterns may result from changes that took place at the time scale of many decades, which are rarely considered in studies on benthic vegetation. We suggest that future floristic studies of benthic macroalgae should be based on large-scale programs of DNA barcoding, in order to avoid overlooking invasive cryptic species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Accoroni S, Colombo F, Pichierri S, Romagnoli T, Marini M, Battocchi C, Penna A, Totti C (2012) Ecology of Ostreopsis cf. ovata blooms in the northern Adriatic Sea. Cryptogam Algol 33:191–198

    Google Scholar 

  • Artegiani A, Bregant D, Paschini E, Pinardi N, Raicich F, Russo A (1997) The Adriatic Sea general circulation. Part II: Baroclinic circulation structure. J Phys Oceanogr 27:1515–1532

    Google Scholar 

  • Battelli C (2016) Disappearance of Fucus virsoides J. Agardh from the Slovenian coast (Gulf of Trieste, northern Adriatic). Ann Ser Hist Nat 26:1–12

    Google Scholar 

  • Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F (2001) Predicting the consequences of anthropogenic disturbance: large–scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser 214:137–150

    Google Scholar 

  • Bertocci I, Arenas F, Cacabelos E, Martins GM, Seabra MI, Álvaro NV, Fernandes JN, Gaião R, Mamede N, Mulas M, Neto AI (2017) Nowhere safe? Exploring the influence of urbanization across mainland and insular seashores in continental Portugal and the Azorean Archipelago. Mar Pollut Bull 114:644–655

    CAS  PubMed  Google Scholar 

  • Biondi E, Casavecchia S, Pinzi M, Bagella S, Calandra R (2002) Excursion to the Conero regional natural park. Fitosociologia 39:5–32

    Google Scholar 

  • Blanfuné A, Boudouresque CF, Verlaque M, Thibaut T (2016) The fate of Cystoseira crinita, a forest–forming Fucale (Phaeophyceae, Stramenopiles), in France (North Western Mediterranean Sea). Estuar Coast Shelf Sci 181:196–208

    Google Scholar 

  • Blanfuné A, Boudouresque CF, Verlaque M, Thibaut T (2019) The ups and downs of a canopy–forming seaweed over a span of more than one century. Sci Rep 9. article 5250.

  • Borja Á, Fontán A, Muxika I (2013) Interactions between climatic variables and human pressures upon a macroalgae population: Implications for management. Ocean Coast Manag 76:85–95

    Google Scholar 

  • Bottalico A, Boo GH, Russo C, Boo SM, Perrone C (2014) Parviphycus albertanoae sp. nov. (Gelidiales, Rhodophyta) from the Mediterranean Sea. Phycologia 53:243–251

    Google Scholar 

  • Bottalico A, Russo C, Furnari G, Perrone C (2015) Parviphycus bompardii sp. nov. and P. albertanoae (Gelidiales, Rhodophyta), two species misidentified as Gelidiella ramellosa in the Mediterranean Sea. Phytotaxa 219:155–164

    Google Scholar 

  • Bulleri F, Airoldi L (2005) Artificial marine structures facilitate the spread of a non–indigenous green alga, Codium fragile ssp. tomentosoides, in the North Adriatic Sea. J Appl Ecol 42:1063–1072

    Google Scholar 

  • Bulleri F, Chapman MG (2004) Intertidal assemblages on artificial and natural habitats in marinas on the north–west coast of Italy. Mar Biol 145:381–391

    Google Scholar 

  • Cacabelos E, Martins GM, Thompson R, Prestes ACL, Azevedo JMN, Neto AI (2016) Factors limiting the establishment of canopy–forming algae on artificial structures. Estuar Coast Shelf Sci 181:277–283

    Google Scholar 

  • Casado-Amezúa P, Araújo R, Bárbara I, Bermejo R, Borja A, Díez I, Fernández C, Gorostiaga JM, Guinda X, Hernández I, Juanes JA, Peña V, Peteiro C, Puente A, Quintana I, Tuya F, Viejo RM, Altamirano M, Gallardo T, Martínez B (2019) Distributional shifts of canopy-forming seaweeds from the Atlantic coast of Southern Europe. Biodivers Conserv 28:1151–1172

    Google Scholar 

  • Cecere E, Cormaci M, Furnari G (1991). The marine algae of Mar Piccolo, Taranto (Southern–Italy): a re–assessment. Bot Mar 34:221–228.

  • Cecere E, Saracino OD, Petrocelli A (2002) Sui primi studi delle macroalghe marine bentoniche della costa marchigiana. Biol Mar Mediterr 9:517–518

    Google Scholar 

  • Cormaci M, Furnari G (1999) Changes of the benthic algal flora of the Tremiti Islands (southern Adriatic) Italy. Hydrobiologia 398–399:75–79

    Google Scholar 

  • Cozzi S, Giani M (2011) River water and nutrient discharges in the Northern Adriatic Sea: current importance and long–term changes. Cont Shelf Res 31:1881–1893

    Google Scholar 

  • Curiel D, Marzocchi M, Bellemo G (1996) First report of fertile Antithamnion pectinatum (Ceramiales, Rhodophyceae) in the north Adriatic Sea (Lagoon of Venice, Italy). Bot Mar 39:19–22

    Google Scholar 

  • Curiel D, Bellemo G, La Rocca B, Scattolin M, Marzocchi M (2002) First report of Polysiphonia morrowii Harvey (Ceramiales, Rhodophyta) in the Mediterranean Sea. Bot Mar 45:66–70

    Google Scholar 

  • Curiel D, Bellemo G, Scattolin M, Marzocchi M (2006) First report of Lomentaria hakodatensis (Lomentariaceae, Rhodophyta) from the lagoon of Venice (Adriatic Sea, Mediterranean). Acta Adriat 47:65–72

    Google Scholar 

  • Di Camillo CG, Cerrano C (2015) Mass mortality events in the NW Adriatic Sea: phase shift from slow– to fast–growing organisms. PLoS ONE 10:e0126689. https://doi.org/10.1371/journal.pone.0126689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Camillo CG, Bosato S, Cerrano C (2014) Reproductive ecology of Epizoanthus arenaceus (Delle Chiaje, 1823) (Cnidaria: Anthozoa) from the North Adriatic Sea. J Exp Mar Biol Ecol 461:144–153

    Google Scholar 

  • Díez I, Muguerza N, Santolaria A, Ganzedo U, Gorostiaga JM (2012) Seaweed assemblage changes in the eastern Cantabrian Sea and their potential relationship to climate change. Estuar Coast Shelf Sci 99:108–120

    Google Scholar 

  • Eriksson BK, Johansson G, Snoeijs P (2002) Long–term changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak Coast. J Phycol 38:284–296

    Google Scholar 

  • Falace A, Alongi G, Cormaci M, Furnari G, Curiel D, Cecere E, Petrocelli A (2010a) Changes in the benthic algae along the Adriatic Sea in the last three decades. Chem Ecol 26:77–90

    Google Scholar 

  • Falace A, Alongi G, Spagnolo A, Fabi G (2010b) Segnalazione di macroalghe non–indigene nel porto di Ancona (medio Adriatico). Biol Mar Medit 17:300–301

    Google Scholar 

  • Falace A, Tamburello L, Guarnieri G, Kaleb S, Papa L, Fraschetti S (2018) Effects of a glyphosate–based herbicide on Fucus virsoides (Fucales, Ochrophyta) photosynthetic efficiency. Environ Pollut 243:912–918

    CAS  PubMed  Google Scholar 

  • Felline S, Del Coco L, Kaleb S, Guarnieri G, Fraschetti S, Terlizzi A, Fanizzi FP, Falace A (2019) The response of the algae Fucus virsoides (Fucales, Ochrophyta) to Roundup solution exposure: A metabolomics approach. Environ Pollut 254. article 112977

  • Fernández C (2011) The retreat of large brown seaweeds on the north coast of Spain: the case of Saccorhiza polyschides. Eur J Phycol 46:352–360

    Google Scholar 

  • Fruzzetti VME, Segato D, Ruggeri P, Vita A, Sakellariadi E, Scarpelli G (2011) Fenomeni di instabilità della falesia del Monte Conero: ruolo dell’assetto strutturale. Incontro Annuale dei Ricercatori di Geotecnica 2011—IARG 2011 Torino, 4–6 July 2011

  • Gargiulo MG, De Masi F, Tripodi G (1992) Sargassum muticum (Yendo) Fensholt (Phaeophyta, Fucales) is spreading in the lagoon of Venice (Northern Adriatic Sea). Giorn Bot Ital 126:259

    Google Scholar 

  • Guiry MD, Guiry GM (2019) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. https://www.algaebase.org. Accessed 12 Feb 2020

  • Hind KR, Starko S, Burt JM, Lemay MA, Salomon AK, Martone PT (2019) Trophic control of cryptic coralline algal diversity. Proc Nat Acad Sci US 116:15080–15085

    CAS  Google Scholar 

  • Irving AD, Balata D, Colosio F, Ferrando GA, Airoldi L (2009) Light, sediment, temperature, and the early life–history of the habitat–forming alga Cystoseira barbata. Mar Biol 156:1223–1231

    Google Scholar 

  • IUCN 2016. The IUCN Red List of Threatened Species. Version 2015–4. https://www.iucnredlist.org

  • Iveša L, Djakovac T, Devescovi M (2016) Long–term fluctuations in Cystoseira populations along the west Istrian Coast (Croatia) related to eutrophication patterns in the northern Adriatic Sea. Mar Pollut Bull 106:162–173

    PubMed  Google Scholar 

  • Kautsky N, Kautsky H, Kautsky U, Waern M (1986) Decreased depth penetration of Fucus vesiculosus (L.) since the 1940's indicates eutrophication of the Baltic Sea. Mar Ecol Prog Ser 28:1–8

    Google Scholar 

  • Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean sea. Trends Ecol Evol 25:250–260

    PubMed  Google Scholar 

  • Lima FP, Ribeiro PA, Queiroz N, Hawkins SJ, Santos AM (2007) Do distributional shifts of northern and southern species of algae match the warming pattern? Glob Chang Biol 13:2592–2604

    Google Scholar 

  • Lin SM, Tseng LC, Put OA, Bolton J, Liu LC (2018) Long–term study on seasonal changes in floristic composition and structure of marine macroalgal communities along the coast of Northern Taiwan, southern East China Sea. Mar Biol 165:1–17

    Google Scholar 

  • Mancuso FP, Strain EMA, Piccioni E, De Clerck O, Sarà G, Airoldi L (2018) Status of vulnerable Cystoseira populations along the Italian infralittoral fringe, and relationships with environmental and anthropogenic variables. Mar Pollut Bull 129:762–771

    CAS  PubMed  Google Scholar 

  • McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919

    CAS  PubMed  Google Scholar 

  • Méndez-Sandín M, Fernández C (2016) Changes in the structure and dynamics of marine assemblages dominated by Bifurcaria bifurcata and Cystoseira species over three decades (1977–2007). Estuar Coast Shelf Sci 175:46–56

    Google Scholar 

  • Montanari A, Mainiero M, Coccioni R, Pignocchi G (2018) Catastrophic landslide of medieval Portonovo (Ancona, Italy). Geol Soc Am GSA Bull 128:1660–1678. https://doi.org/10.1130/B31472.1

    Article  Google Scholar 

  • Munda IM (2000) Long–term marine floristic changes around Rovinj (Istrian coast, North Adriatic) estimated on the basis of historical data from Paul Kuckuck's field diaries from the end of the 19th century. Nova Hedwigia 71:1–36

    Google Scholar 

  • Orlando-Bonaca M, Rotter A (2018) Any signs of replacement of canopy–forming algae by turf–forming algae in the northern Adriatic Sea? Ecol Indic 87:272–284

    Google Scholar 

  • Orlando-Bonaca M, Mannoni PA, Poloniato D, Falace A (2013) Assessment of Fucus virsoides distribution in the Gulf of Trieste (Adriatic Sea) and its relation to environmental variables. Bot Mar 56:451–459

    Google Scholar 

  • Orlando-Bonaca M, Lipej L, Bonanno G (2019) Non–indigenous macrophytes in Adriatic ports and transitional waters: trends, taxonomy, introduction vectors, pathways and management. Mar Pollut Bull 145:656–672

    CAS  PubMed  Google Scholar 

  • Perkol-Finkel S, Airoldi L (2010) Loss and recovery potential of marine habitats: an experimental study of factors maintaining resilience in subtidal algal forests at the Adriatic Sea. PLoS ONE 5:e10791

    PubMed  PubMed Central  Google Scholar 

  • Perrone C, Bottalico A, Boo GH, Boo SM, Miller KA, Freshwater DW (2019) Gelidium adriaticum sp. nov. and Gelidium carolinianum sp. nov. (Gelidales, Rhodophyta) from the Mediterranean Sea. Phycologia 58:359–373

    Google Scholar 

  • Petrocelli A, Antolić B, Bolognini L, Cecere E, Cvitković I, Despalatović M, Falace A, Finotto S, Iveša L, Mačić V, Marini M, Orlando-Bonaca M, Rubino F, Trabucco B, Žuljević A (2019) Port baseline biological surveys and seaweed bioinvasions in port areas: what's the matter in the Adriatic Sea? Mar Pollut Bull 147:98–116

    CAS  PubMed  Google Scholar 

  • Pezzolesi L, Peña V, Le Gall L, Gabrielson PW, Kaleb S, Hughey JR, Rodondi G, Hernandez-Kantun JJ, Falace A, Basso D, Cerrano C, Rindi F (2019) Mediterranean Lithophyllum stictiforme (Corallinales, Rhodophyta) is a genetically diverse species complex: implications for species circumscription, biogeography and conservation of coralligenous habitats. J Phycol 55:473–492

    PubMed  Google Scholar 

  • Pierpaoli I (1941) 1° Manipolo di alghe Anconetane. Alghe nella vita e nella pesca: 5–22.

  • Pierpaoli I (1946) Rilievi sulla flora algologica anconetana. Nuovo Giorn Bot Ital, n.s. LII:14–20.

  • Pinedo S, Zabala M, Ballesteros E (2013) Long–term changes in sublittoral macroalgal assemblages related to water quality improvement. Bot Mar 56:461–469

    Google Scholar 

  • Piñeiro-Corbeira C, Barreiro R, Cremades J (2016) Decadal changes in the distribution of common intertidal seaweeds in Galicia (NW Iberia). Mar Environ Res 113:106–115

    PubMed  Google Scholar 

  • Piñeiro-Corbeira C, Verbruggen H, Díaz-Tapia P (2019) Molecular survey of the red algal family Rhodomelaceae (Ceramiales, Rhodophyta) in Australia reveals new introduced species. J Appl Phycol. In press

  • QGIS Development Team, 2017. QGIS geographic information system. Open Source Geospatial Foundation Project. https://qgis.osgeo.org

  • Rindi F, Guiry MD (2004) A long–term comparison of the benthic algal flora of Clare Island, County Mayo, western Ireland. Biodivers Conserv 13:471–492

    Google Scholar 

  • Rodríguez-Prieto C, De Clerck O, Huisman JM, Lin SM (2019) Characterisation of Nesoia latifolia (Halymeniaceae, Rhodophyta) from Europe with emphasis on cystocarp development and description of Nesoia mediterranea sp. nov. Phycologia 58:393–404

    Google Scholar 

  • Romagnoli T, Solazzi A (2003) Evoluzione dei popolamenti fitobentonici lungo la Riviera del Conero dal 1941 al 2000. Quad. Ist. Ric. Pesca Marittima, n.s. 1:63–84.

  • Sales M, Ballesteros E (2010) Long–term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur J Phycol 45:404–412

    Google Scholar 

  • Sánchez N, Vergés A, Peteiro C, Sutherland JE, Brodie J (2014) Diversity of bladed Bangiales (Rhodophyta) in western Mediterranean: recognition of the genus Themis and descriptions of T. ballesterosii sp. nov., T. hiberica sp. nov and Pyropia parva sp. nov. J Phycol 50:908–929

    PubMed  Google Scholar 

  • Savoie AM, Saunders GW (2015) Evidence for the introduction of the Asian red alga Neosiphonia japonica and its introgression with Neosiphonia harveyi (Ceramiales, Rhodophyta) in the Northwest Atlantic. Mol Ecol 24:5927–5937

    PubMed  Google Scholar 

  • Sfriso A, Curiel D (2007) Check–list of seaweeds recorded in the last 20 years in Venice lagoon and a comparison with the previous records. Bot Mar 50:22–58

    Google Scholar 

  • Solazzi A (1964) Primi dati sulle alghe della scogliera «I Travi» di Portonovo (Ancona). Giorn Bot Ital 71:253–257

    Google Scholar 

  • Solazzi A (1966–67) Studio ecologico sulla vegetazione algale bentonica (macrofite) della riviera del Monte Conero (Ancona). Mem Biogeog Adriat 7:159–192.

  • Solazzi A (1967) Nereia filiformis Zan. nuova specie per la costa marchigiana Atti Ist Ven Sci Lett Arti 223–226.

  • Solazzi A (1976) Le alghe della costa marchigiana. Giorn Bot Ital 110:419–425

    Google Scholar 

  • Strain EMA, Van Belzen J, Van Dalen J, Bouma TJ, Airoldi L (2015) Management of local stressors can improve the resilience of marine canopy algae to global stressors. PLoS ONE 10:e0120837

    PubMed  PubMed Central  Google Scholar 

  • Tesi T, Langone L, Giani M, Ravaioli M, Miserocchi S (2013) Source, diagenesis, and fluxes of particulate organic carbon along the western Adriatic Sea (Mediterranean Sea). Mar Geol 337:156–170

    CAS  Google Scholar 

  • Thibaut T, Pinedo S, Torras X, Ballesteros E (2005) Long–term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North–western Mediterranean). Mar Pollut Bull 50:1472–1489

    CAS  PubMed  Google Scholar 

  • Thibaut T, Blanfuné A, Markovic L, Verlaque M, Boudouresque CF, Perret-Boudouresque M, Maćic V, Bottin L (2014) Unexpected abundance and long–term relative stability of the brown alga Cystoseira amentacea, hitherto regarded as a threatened species, in the north–western Mediterranean Sea. Mar Poll Bull 89:305–323

    CAS  Google Scholar 

  • Thibaut T, Blanfuné A, Boudouresque CF, Verlaque M (2015) Decline and local extinction of Fucales in the French Riviera: the harbinger of future extinctions? Mediterr Mar Sci 16:206–224

    Google Scholar 

  • Tolomio C (1993) First record of Grateloupia doryphora (Mont.) Howe (Rhodophyceae) from the Lagoon of Venice. Lav Soc Ven Sci Nat 5:220

    Google Scholar 

  • Totti C, Romagnoli T, Accoroni S, Coluccelli A, Pellegrini M, Campanelli A, Grilli F, Marini M (2019) Phytoplankton communities in the northwestern Adriatic Sea: interdecadal variability over a 30–years period (1988–2016) and relashionships with meteoclimatic drivers. J Mar Syst 193:137–153

    Google Scholar 

  • Trowbridge CD, Little C, Pilling GM, Stirling P, Miles A (2011) Decadal–scale changes in the shallow subtidal benthos of an Irish marine reserve. Bot Mar 54:497–506

    Google Scholar 

  • Verlaque M (1994) Inventaire des plantes introduites en Méditerranée: origines et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23

    Google Scholar 

  • Verlaque M, Ruitton S, Mineur F, Boudouresque CF (2015) CIESM atlas of exotic species of the Mediterranean macrophytes. CIESM Publishers, Paris

    Google Scholar 

  • Wolf MA, Sciuto K, Maggs CA, de Barros-Barreto MBB, Andreoli C, Moro I (2011) Ceramium Roth (Ceramiales, Rhodophyta) from Venice lagoon (Adriatic Sea, Italy): comparative studies of Mediterranean and Atlantic taxa. Taxon 60:1584–1595

    Google Scholar 

  • Wolf MA, Sciuto K, Andreoli C, Moro I (2012) Ulva (Chlorophyta, Ulvales) biodiversity in the North Adriatic Sea (Mediterranean, Italy): cryptic species and new introductions. J Phycol 48:1510–1521

    PubMed  Google Scholar 

  • Wolf MA, Buosi A, Juhmani ASF, Sfriso A (2018) Shellfish import and hull fouling as vectors for new red algal introductions in the Venice Lagoon. Estuar Coast Shelf Sci 215:30–38

    Google Scholar 

  • Wolf MA, Sciuto K, Betto VM, Moro I, Maggs CA, Sfriso A (2019) Updating Ceramium (Rhodophyta, Ceramiales) biodiversity in the North Adriatic Sea (Mediterranean): Ceramium rothianum sp. nov. and rediscovery of three forgotten species. Eur J Phycol 54:571–584

    CAS  Google Scholar 

  • Yesson C, Bush LE, Davies AJ, Maggs CA, Brodie J (2015) Large brown seaweeds of the British Isles: Evidence of changes in abundance over four decades. Estuar Coast Shelf Sci 155:167–175

    Google Scholar 

Download references

Funding

Funding was provided by Università Politecnica delle Marche (Grant No. RSA years 2011-2018).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabio Rindi.

Additional information

Communicated by Angus Jackson.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article belongs to the Topical Collection: Coastal and marine biodiversity.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rindi, F., Gavio, B., Díaz-Tapia, P. et al. Long-term changes in the benthic macroalgal flora of a coastal area affected by urban impacts (Conero Riviera, Mediterranean Sea). Biodivers Conserv 29, 2275–2295 (2020). https://doi.org/10.1007/s10531-020-01973-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-020-01973-z

Keywords

  • Climate change
  • Floristic losses
  • Habitat destruction
  • Long-term changes
  • Macroalgal floras
  • Non-indigenous species