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Biological Invasions in the Aegean Sea: Temporal Trends, Pathways, and Impacts

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The Aegean Sea Environment

Abstract

The Aegean Sea is highly impacted by biological invasions with 209 alien species being reported until the end of 2019, of which 149 are considered as established. Among these, the most abundant group is Pisces, followed by Mollusca, Crustacea, Annelida, and Macrophyta. There is an increasing trend of new species introductions in the Aegean Sea, reaching 60 new introductions between 2010 and 2019. The most common pathway of introduction in the Aegean Sea is “unaided” introduction from neighboring ecoregions, i.e., natural dispersal across the Aegean borders, without human agency. Most of these species are Lessepsian immigrants, introduced through the Suez Canal, and initially recorded in the Levantine Sea. The second most common pathway in the Aegean is “transport-stowaway,” i.e., introduction through ballast waters, hull fouling, or with angling/fishing equipment. All other pathways are of much lower importance for the Aegean Sea. The most invasive species in the region are the fish Siganus rivulatus, Siganus luridus, Fistularia commersonii, Lagocephalus sceleratus, and Pterois miles; the macroalgae Caulerpa cylindracea, Codium fragile, Stypopodium schimperi, Asparagopsis taxiformis, and Womersleyella setacea; the crab Callinectes sapidus; and potentially the molluscs Conomurex persicus, Pinctada imbricata radiata, Dendostrea cf. folium, and Fulvia fragilis.

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Acknowledgments

Stelios Katsanevakis was supported by the Hellenic Foundation for Research and Innovation (H.F.R.I.) under the “First Call for H.F.R.I. Research Projects to support Faculty members and Researchers and the procurement of high-cost research equipment grant” (Project ALAS – “ALiens in the Aegean – a Sea under siege” [108]; Project Number: HFRI-FM17-1597).

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Correspondence to Stelios Katsanevakis .

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Annex 1

Annex 1

Alien species in the Aegean Sea, sorted by the year of first record in the Aegean. Their taxonomic, establishment success, and pathway of introduction in the Aegean are also provided. Pathways: UNA unaided, TS transport-stowaway, TC transport-contaminant, COR corridor, REL release in nature, EC escape from confinement, UNK unknown

Taxonomic group

Species

Establishment success

Pathway

Year of first record

Macroalgae/Rhodophyta

Hypnea cornuta (Kützing) J. Agardh

Established

TS

1894

Chordata/Ascidiacea

Ascidiella aspersa (Müller, 1776)

Established

UNK

1901

Chordata/Ascidiacea

Ciona robusta Hoshino and Tokioka, 1967 (as Ciona intestinalis (Linnaeus, 1767))

Established

TS

1901

Macroalgae/Rhodophyta

Lophocladia lallemandii (Montagne) Schmitz

Established

TS

1908

Tracheophyta

Halophila stipulacea (Forsskål) Ascherson

Established

CORR

1923

Chordata/Pisces

Siganus rivulatus Forsskål, 1775

Established

UNA

1925

Macroalgae/Ochrophyta

Cutleria multifida (Turner) Greville

Established

TS

1932

Chordata/Pisces

Sargocentron rubrum (Forsskål, 1775)

Established

UNA

1940

Cnidaria/Scyphozoa

Cassiopea andromeda (Forsskål, 1775)

Established

UNA

1942

Chordata/Pisces

Hemiramphus far (Forsskål, 1775)

Established

UNA

1943

Chordata/Pisces

Stephanolepis diaspros Fraser-Brunner, 1940

Established

UNA

1943

Chordata/Pisces

Equulites klunzingeri (Steindachner, 1898)

Casual

UNA

1946

Chordata/Pisces

Parexocoetus mento (Valenciennes, 1846)

Established

UNA

1946

Crustacea/Decapoda

Callinectes sapidus Rathbun, 1896

Established

TS

1947

Chordata/Pisces

Upeneus moluccensis (Bleeker, 1855)

Established

UNA

1947

Chordata/Pisces

Lagocephalus guentheri Miranda Ribeiro, 1915

Established

UNA

1952

Foraminifera

Coscinospira hemprichii Ehrenberg, 1839

Established

UNA, TS

1955

Annelida

Ficopomatus enigmaticus (Fauvel, 1923)

Established

TS

1959

Chordata/Pisces

Alepes djedaba (Forsskål, 1775)

Established

UNA

1960

Mollusca/Bivalvia

Pinctada imbricata radiata (Leach, 1814)

Established

REL

1961

Crustacea/Stomatopoda

Erugosquilla massavensis (Kossmann, 1880)

Established

UNA

1963

Annelida

Notomastus aberans Day, 1957

Established

UNA

1964

Annelida

Paradyte cf. crinoidicola (Potts, 1910)

Casual

UNA

1964

Chordata/Pisces

Siganus luridus (Rüppell, 1829)

Established

UNA

1964

Foraminifera

Amphistegina lobifera (Larsen, 1976)

Established

UNA

1967

Crustacea/Copepoda

Arietellus pavoninus (G. O. Sars, 1905)

Established

UNA, TS

1967

Bryozoa

Crisularia serrata (Lamarck, 1816)

Unknown

TS

1967

Bryozoa

Microporella coronata (Audouin, 1826)

Questionable

TS

1967

Macroalgae/Ochrophyta

Pylaiella littoralis (Linnaeus) Kjellman

Questionable

TS

1967

Chordata/Ascidiacea

Styela plicata (Lesueur, 1823)

Established

TS

1968

Bryozoa

Amathia verticillata (delle Chiaje, 1822)

Established

TS

1969

Mollusca/Gastropoda

Nerita sanguinolenta Menke, 1829

Casual

UNA

1969

Crustacea/Cirripedia

Amphibalanus eburneus (Gould, 1841)

Unknown

TS

1970

Crustacea/Cirripedia

Balanus trigonus Darwin, 1854

Established

TS

1970

Chordata/Pisces

Saurida lessepsianus Russell, Golani, and Tikochinski, 2015

Established

UNA

1971

Mollusca/Bivalvia

Brachidontes pharaonis (P. Fischer, 1870)

Established

UNA, TS

1975

Mollusca/Gastropoda

Bursatella leachii (De Blainville, 1817)

Established

UNA, TS

1975

Annelida

Lysidice collaris Grube, 1870

Established

UNA

1975

Annelida

Protodorvillea biarticulata Day, 1963

Established

TS

1975

Annelida

Sigambra parva (Day, 1963)

Established

TS

1975

Annelida

Axionice medusa (Savigny in Lamarck, 1818)

Established

UNA

1976

Annelida

Dodecaceria capensis Day, 1961

Established

TS

1976

Annelida

Hydroides elegans (Haswell, 1883)

Established

TS

1976

Macroalgae/Rhodophyta

Hypnea spinella (C. Agardh) Kützing

Established

TS

1979

Macroalgae/Rhodophyta

Ceramium bisporum Ballantine

Casual

TS

1980

Macroalgae/Rhodophyta

Chondria collinsiana Howe

Questionable

TS

1980

Macroalgae/Rhodophyta

Sarconema scinaioides Børgesen

Casual

EC

1980

Cnidaria/hydrozoa

Clytia linearis (Thornely, 1900)

Established

UNA

1981

Macroalgae/Ochrophyta

Padina boryana Thivy

Questionable

UNA

1981

Chordata/Pisces

Apogonichthyoides pharaonis (Bellotti, 1874)

Established

UNA

1982

Mollusca/Gastropoda

Conomurex persicus (Swainson, 1821)

Established

UNA, TS

1983

Chordata/Pisces

Pempheris rhomboidea Kossmann and Rauber, 1877

Established

UNA

1983

Annelida

Polycirrus twisti Potts, 1928

Established

UNA

1983

Crustacea/Decapoda

Thalamita poissonii (Audouin, 1826)

Established

UNA

1983

Mollusca/Bivalvia

Mya arenaria Linnaeus, 1758

Established

TS, TC

1984

Mollusca/Gastropoda

Crepidula fornicata (Linnaeus, 1758)

Established

TC, TS

1985

Mollusca/Bivalvia

Petricolaria pholadiformis Lamarck, 1818

Established

TS

1985

Chordata/Pisces

Atherinomorus forskalii (Rüppell, 1838)

Established

UNA

1986

Macroalgae/Ochrophyta

Colpomenia peregrina Sauvageau

Established

TS

1986

Bryozoa

Crepidacantha poissoni (Audouin, 1826)

Unknown

TS

1986

Annelida

Desdemona ornata Banse, 1957

Casual

TS

1986

Mollusca/Gastropoda

Rapana venosa (Valenciennes, 1846)

Casual

UNA

1986

Foraminifera

Heterostegina depressa d’Orbigny, 1826

Established

UNA

1988

Crustacea/Copepoda

Paracartia grani (G. O. Sars, 1904)

Established

TS

1988

Macroalgae/Rhodophyta

Womersleyella setacea (Hollenberg) Norris

Established

TS

1988

Annelida

Branchiomma luctuosum (Grube, 1869)

Established

TS

1989

Annelida

Chaetozone corona Berkeley and Berkeley, 1941

Established

TS

1989

Ctenophora

Mnemiopsis leidyi (Agassiz, 1865)

Established

UNA

1990

Cnidaria/hydrozoa

Sertularia marginata (Kirchenpauer, 1864)

Established

TS

1990

Mollusca/Gastropoda

Acteocina mucronata (Philippi, 1849)

Casual

UNA

1991

Macroalgae/Chlorophyta

Caulerpa racemosa var. lamourouxii f. requienii (Montagne) Weber van Bose

Established

UNA

1991

Annelida

Prionospio pulchra Imajima, 1990

Casual

TC

1991

Macroalgae/Rhodophyta

Asparagopsis taxiformis (Delile) Trevisan de Saint-Léon

Established

UNA

1992

Macroalgae/Chlorophyta

Codium fragile (Suringar) Hariot

Established

TS

1992

Chordata/Pisces

Pteragogus trispilus Randall, 2013

Established

UNA

1992

Mollusca/Bivalvia

Anadara transversa (Say, 1822)

Established

TS

1993

Echinodermata

Ophiactis savignyi (Müller and Troschel, 1842)

Casual

UNA

1993

Mollusca/Gastropoda

Smaragdia souverbiana (Montrouzier, 1863)

Established

UNA

1993

Foraminifera

Spiroloculina antillarum d’Orbigny, 1839

Established

UNA

1993

Mollusca/Gastropoda

Cerithiopsis tenthrenois (Melvill, 1896)

Casual

UNA

1994

Mollusca/Gastropoda

Melibe viridis (Kelaart, 1858)

Established

UNA, TS

1994

Crustacea/Decapoda

Penaeus pulchricaudatus Stebbing, 1914

Established

UNA

1995

Chordata/Pisces

Planiliza haematocheila (Temminck and Schlegel, 1845)

Established

UNA

1995

Chordata/Pisces

Sphyraena chrysotaenia Klunzinger, 1884

Established

UNA

1995

Macroalgae/Chlorophyta

Caulerpa cylindracea Sonder

Established

UNA

1996

Chordata/Ascidiacea

Diplosoma listerianum (Milne Edwards, 1841)

Established

TS

1996

Bryozoa

Hippopodina sp. A as Hippopodina feegeensis (Busk, 1884)

Established

TS

1996

Mollusca/Bivalvia

Malleus regula (Forsskål in Niebuhr, 1775)

Established

UNA

1996

Mollusca/Gastropoda

Mnestia girardi (Audouin, 1826)

Established

UNA

1996

Macroalgae/Ochrophyta

Stypopodium schimperi (Buchinger ex Kützing) Verlaque and Boudouresque

Established

UNA

1996

Mollusca/Bivalvia

Fulvia fragilis (Forsskål in Niebuhr, 1775)

Established

TS

1997

Annelida

Spirorbis marioni Caullery and Mesnil, 1897

Established

TS

1997

Crustacea

Paradella dianae (Menzies, 1962)

Established

TS

1997

Crustacea/Decapoda

Alpheus rapacida (de Man, 1908)

Casual

UNA

1998

Mollusca/Gastropoda

Bulla arabica Malaquias and Reid, 2008

Established

TS

1998

Crustacea/Decapoda

Charybdis (Goniohellenus) longicollis Leene, 1938

Established

UNA

1999

Crustacea/Decapoda

Ixa monodi Holthuis and Gottlieb, 1956

Established

UNA

1999

Crustacea/Decapoda

Metapenaeopsis aegyptia Galil and Golani, 1990

Established

UNA

1999

Annelida

Leiocapitellides analis Hartmann-Schröder, 1960

Casual

UNA

2000

Crustacea/Decapoda

Portunus segnis (Forsskål, 1775)

Established

UNA

2000

Chordata/Pisces

Fistularia commersonii (Rüppell, 1835)

Established

UNA

2001

Foraminifera

Planogypsina acervalis (Brady, 1884)

Established

UNK

2001

Chordata/Pisces

Callionymus filamentosus Valenciennes, 1837

Established

UNA

2003

Chordata/Pisces

Etrumeus golani Di Battista, Randall and Bowen, 2012

Established

UNA

2003

Chordata/Pisces

Lagocephalus suezensis Clark and Gohar, 1953

Established

UNA

2003

Annelida

Pseudonereis anomala (Gravier, 1900)

Established

TS

2003

Chordata/Pisces

Sphyraena flavicauda Rüppell, 1838

Established

UNA

2003

Annelida

Spirobranchus tetraceros (Schmarda, 1861)

Established

TS

2003

Chordata/Pisces

Tylosurus crocodilus Péron and Lesueur, 1821

Casual

UNA

2003

Chordata/Pisces

Upeneus pori Ben-Tuvia and Golani, 1989

Established

UNA

2003

Ctenophora

Beroe ovata Mayer, 1912

Unknown

UNA

2004

Mollusca/Gastropoda

Goniobranchus annulatus (Eliot, 1904)

Established

UNA, TS

2004

Crustacea/Decapoda

Myra subgranulata Galil and Golani, 1990

Established

UNA

2004

Crustacea/Decapoda

Percnon gibbesi (H. Milne Edwards, 1853)

Established

UNA

2004

Chordata/Pisces

Petroscirtes ancylodon Rüppell, 1838

Established

UNA

2004

Chordata/Pisces

Tylerius spinosissimus (Regan, 1908)

Established

UNA

2004

Crustacea/Decapoda

Calappa pelii Herklots, 1851

Casual

UNK

2005

Crustacea/Decapoda

Coleusia signata (Paulson, 1875)

Established

UNA

2005

Mollusca/Gastropoda

Haminoea cyanomarginata Heller and Thompson, 1983

Established

UNA, TS

2005

Chordata/Pisces

Lagocephalus sceleratus (Gmelin, 1788)

Established

UNA

2005

Annelida

Pseudopolydora paucibranchiata (Okuda, 1937)

Established

TS

2005

Echinodermata

Synaptula reciprocans (Forsskål, 1775)

Established

UNA

2005

Macroalgae/Rhodophyta

Botryocladia madagascariensis G. Feldmann

Established

TS

2006

Annelida

Caulleriella viridis (Langerhans, 1881)

Questionable

TS

2006

Macroalgae/Rhodophyta

Melanothamnus harveyi (Bailey) Díaz-Tapia and Maggs

Established

TS

2006

Foraminifera

Miliolinella fichteliana d’Orbigny, 1839

Established

UNA

2006

Annelida

Timarete punctata (Grube, 1859)

Casual

TS

2006

Chordata/Pisces

Torquigener flavimaculosus Hardy and Randall, 1983

Established

UNA

2006

Mollusca/Bivalvia

Chama asperella Lamarck, 1819

Established

TS

2007

Mollusca/Gastropoda

Ergalatax junionae Houart, 2008

Established

UNA

2007

Annelida

Glycinde bonhourei Gravier, 1904

Casual

UNA

2007

Annelida

Linopherus canariensis Langerhans, 1881

Casual

TC

2007

Annelida

Neanthes agulhana (Day, 1963)

Casual

TS

2007

Mollusca/Bivalvia

Crassostrea/Magallana sp./spp.

Established

EC/REL

2008

Macroalgae/Rhodophyta

Hypnea anastomosans Papenfuss, Lipkin and Silva

Established

UNA

2008

Annelida

Lepidonotus tenuisetosus (Gravier, 1902)

Casual

UNA

2008

Chordata/Ascidiacea

Phallusia nigra Savigny, 1816

Established

UNA

2008

Annelida

Polydora cornuta Bosc, 1802

Established

TS

2008

Chordata/Pisces

Scomberomorus commerson Lacepède, 1800

Established

UNA

2008

Mollusca/Bivalvia

Spondylus cf. spinosus Schreibers, 1793

Casual

TS

2008

Chordata/Pisces

Terapon theraps Cuvier, 1829

Casual

UNK

2008

Mollusca/Bivalvia

Chama pacifica Broderip, 1834

Established

UNA

2009

Mollusca/Gastropoda

Coryphellina rubrolineata O’Donoghue, 1929

Established

UNA

2009

Macroalgae/Rhodophyta

Laurencia caduciramulosa Masuda and Kawaguchi

Established

TS

2009

Crustacea/Decapoda

Macrophthalmus indicus Davie, 2012

Casual

UNA

2009

Crustacea/isopoda

Paracerceis sculpta (Holmes, 1904)

Established

TS

2009

Crustacea/Copepoda

Parvocalanus crassirostris (Dahl, 1894)

Established

UNK

2009

Chordata/Pisces

Pterois miles (Bennett, 1828)

Established

UNA

2009

Mollusca/Cephalopoda

Sepioteuthis lessoniana Férussac in Lesson, 1831 complex

Established

UNA

2009

Macroalgae/Rhodophyta

Asparagopsis armata Harvey

Casual

UNA

2010

Crustacea/Decapoda

Charybdis (Charybdis) hellerii (A. Milne-Edwards, 1867)

Established

UNA

2010

Mollusca/Bivalvia

Dendostrea cf. folium (Linnaeus, 1758)

Established

UNA, TS

2010

Chordata/Pisces

Lutjanus sebae (Cuvier, 1816)

Casual

EC

2010

Crustacea/Cirripedia

Megabalanus tintinnabulum (Linnaeus, 1758)

Casual

TS

2010

Mollusca/Bivalvia

Septifer cumingii (Dunker, 1855)

Established

UNA

2010

Crustacea/Decapoda

Atergatis roseus (Rüppell, 1830)

Established

UNA

2011

Crustacea/Decapoda

Carupa tenuipes Dana, 1851

Established

UNA

2011

Crustacea/Copepoda

Centropages furcatus (Dana, 1852)

Established

UNA

2011

Mollusca/Gastropoda

Cerithium scabridum Philippi, 1848

Established

UNA

2011

Crustacea/Decapoda

Gonioinfradens giardi (Nobili, 1905)

Established

UNA

2011

Crustacea/Amphipoda

Caprella scaura Templeton, 1836

Established

UNK

2012

Chordata/Pisces

Champsodon nudivittis (Ogilby, 1895)

Established

UNA

2012

Foraminifera

Euthymonacha polita (Chapman, 1900)

Casual

UNK

2012

Crustacea/isopoda

Paranthura japonica Richardson, 1909

Established

TS

2012

Crustacea/Decapoda

Penaeus aztecus Ives, 1891

Established

UNA

2012

Crustacea/Decapoda

Penaeus hathor (Burkenroad, 1959)

Established

UNA

2012

Mollusca/Gastropoda

Syrnola fasciata Jickeli, 1882

Established

UNA

2012

Macroalgae/Chlorophyta

Caulerpa taxifolia var. distichophylla (Sonder) Verlaque, Huisman and Procaccini

Established

UNA

2013

Mollusca/Gastropoda

Diodora funiculata (Reeve, 1850)

Established

TS

2013

Annelida

Leonnates persicus Wesenberg-Lund, 1949

Casual

UNA

2013

Mollusca/Gastropoda

Pyrunculus fourierii (Audouin, 1826)

Casual

UNA

2013

Macroalgae/Ochrophyta

Scytosiphon dotyi Wynne

Questionable

TS

2013

Crustacea/Decapoda

Xanthias lamarckii (H. Milne Edwards, 1834)

Casual

UNA

2013

Chordata/Pisces

Bregmaceros nectabanus Whitley, 1941

Established

UNA

2014

Porifera

Paraleucilla magna Klautau, Monteiro and Borojevic, 2004

Established

TC

2014

Mollusca/Gastropoda

Syphonota geographica (A. Adams and Reeve, 1850)

Established

UNA

2014

Crustacea/Amphipoda

Bemlos leptocheirus (Walker, 1909)

Unknown

UNA

2015

Annelida

Branchiomma bairdi (McIntosh, 1885)

Established

TS

2015

Bryozoa

Celleporaria brunnea (Hincks, 1884)

Unknown

TS

2015

Bryozoa

Celleporaria vermiformis (Waters, 1909)

Established

TS

2015

Mollusca/Gastropoda

Cerithiopsis pulvis (A. Issel, 1869)

Casual

UNA

2015

Crustacea/isopoda

Cymodoce fuscina Schotte and Kensley, 2005

Casual

TS

2015

Crustacea/Decapoda

Dyspanopeus sayi (Smith, 1969)

Casual

TS

2015

Chordata/Ascidiacea

Herdmania momus (Savigny, 1816)

Established

UNA

2015

Annelida

Hydroides brachyacantha Rioja, 1941

Casual

TS

2015

Annelida

Hydroides dirampha Mörch, 1863

Established

TS

2015

Mollusca/Gastropoda

Rhinoclavis kochi (Philippi, 1848)

Established

UNA

2015

Mollusca/Gastropoda

Sticteulima sp. [cf. lentiginosa (A. Adams, 1861)]

Casual

UNA, TS

2015

Chordata/Ascidiacea

Symplegma brakenhielmi (Michaelsen, 1904)

Established

TS

2015

Bryozoa

Tricellaria inopinata d’Hondt and Occhipinti Ambrogi, 1985

Unknown

TS

2015

Echinodermata

Diadema setosum (Leske, 1778)

Established

UNA

2016

Mollusca/Bivalvia

Isognomon legumen (Gmelin, 1791)

Established

UNA

2016

Crustacea/isopoda

Mesanthura cf. romulea Poore and Lew-Ton, 1986

Unknown

TS

2016

Mollusca/Gastropoda

Oscilla galilae Bogi, Karhan and Yokeş, 2012

Casual

UNA

2016

Chordata/Pisces

Synchiropus sechellensis Regan, 1908

Established

UNA

2016

Mollusca/Gastropoda

Viriola sp.[cf. bayani] Jousseaume, 1884

Established

UNA

2016

Chordata/Pisces

Abudefduf sexfasciatus (Lacepède, 1801)

Casual

EC

2017

Chordata/Pisces

Acanthurus sohal (Forsskål, 1775)

Casual

CORR

2017

Chordata/Pisces

Scarus ghobban Forsskål in Niebuhr, 1775

Established

UNA

2017

Mammalia

Sousa plumbea (G. Cuvier, 1829)

Casual

UNA

2017

Crustacea/isopoda

Sphaeroma walkeri Stebbing 1905

Unknown

TS

2017

Cnidaria/Scyphozoa

Chrysaora cf. achlyos Martin, Gershwin, Burnett, Cargo and Bloom, 1997

Casual

TS

2018

Tracheophyta

Halophila decipiens Ostenfeld

Casual

TS

2018

Crustacea/Copepoda

Oithona davisae Ferrari F.D. and Orsi, 1984

Casual

UNA/TS

2018

Chordata/Pisces

Parupeneus forsskali (Fourmanoir and Guézé, 1976)

Established

UNA

2018

Chordata/Pisces

Lutjanus argentimaculatus (Forsskål, 1775)

Casual

UNA

2019

Chordata/Pisces

Pomadasys stridens (Forsskål, 1775)

Unknown

UNA

2019

Cnidaria/Scyphozoa

Rhopilema nomadica Galil, 1990

Established

UNA

2019

Chordata/Pisces

Vanderhorstia mertensi Klausewitz, 1974

Casual

UNA

2019

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Katsanevakis, S., Zenetos, A., Corsini-Foka, M., Tsiamis, K. (2020). Biological Invasions in the Aegean Sea: Temporal Trends, Pathways, and Impacts. In: Anagnostou, C.L., Kostianoy, A.G., Mariolakos, I.D., Panayotidis, P., Soilemezidou, M., Tsaltas, G. (eds) The Aegean Sea Environment. The Handbook of Environmental Chemistry, vol 129. Springer, Cham. https://doi.org/10.1007/698_2020_642

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