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Impact of anthropogenous environmental factors on the marine ecosystem of trophically transmitted helminths and hosting seabirds: Focus on North Atlantic, North Sea, Baltic and the Arctic seas Cover

Impact of anthropogenous environmental factors on the marine ecosystem of trophically transmitted helminths and hosting seabirds: Focus on North Atlantic, North Sea, Baltic and the Arctic seas

Helminthologia
Volume 60 (2023): Issue 4 (December 2023)
By:   
Open Access
|Dec 2023
Figures & tables

Figures & Tables

Table 1.

Marine digenean species (Trematoda) determined in seabirds of the North Atlantic, the Barent Sea, as well as the Baltic and the North Sea. Only those species are listed for which at least one intermediate and one final host are known.

DigeneaFirst intermediate hostSecond intermediate hostFinal host
Gymnophallidae
Gymnophallus deliciosus?Blue Mussel (Mytilus edulis)16European Herring Gull (Larus argentatus)15
Gymnophallus bursicolaUnknown18Mytilus edulis18

  • Common Eider (Somateria mollissima)18

  • Velvet scoter (Melanitta fusca)30

Gymnophallus choledochusBivalvia: Cestoderma edule12Polychaeta1 (Hediste diversicolor, Arenicola marina etc.)12 or alternatively Cestoderma spec.12Common Eider (Somateria mollissima)3, 26
Parvatrema spec.Unknown2Littorina saxatilis2,11, Littorina obtusata2,11

  • Common Eider (Somateria mollissima)3

  • Long-tailed Duck (Clangula hyemalis)10

  • Velvet Scoter (Melanitta fusca)10

  • Common Scoter (Melanitta nigra)10

Microphallidae
Microphallus triangulusLittorina saxatilis2,5,20, Littorina obtusata2,5None2Common Eider (Somateria mollissima)3
Microphallus pygmaeusLittorina saxatilis2,5,11,20, Littorina obtusata2,5,11, Littorina littorea2Littorina spec.24

  • Common Eider (Somateria mollissima)3,20

  • Great Black-backed Gull (Larus marinus)4

  • European Herring Gull (Larus argentatus)4,15

Microphallus pseudopygmaeusLittorina saxatilis2,5,11,20, Littorina obtusata2,5,11, Onoba aculeus2, Margarites helicinus2, Margarites groenlandicus2,20, Lacuna vincta2None2

  • Common Eider (Somateria mollissima)3,19

  • Glaucous Gull (Larus hyperboreus)27

Microphallus piriformesLittorina saxatilis2,5,11,20, Littorina obtusata2,5,11None2

  • Common Eider (Somateria mollissima)3

  • Great Black-backed Gull (Larus marinus)4,

  • European Herring Gull (Larus argentatus)4,15

Microphallus similisLittorina saxatilis2,11, Littorina obtusata2,11, Littorina littorea2Crustacea: Carcinus maenas2, Hyas araneus2

  • Great Black-backed Gull (Larus marinus)4

  • European Herring Gull (Larus argentatus)4,15

Maritrema arenariaLittorina saxatilis2,11Crustacea: Semibalanus balanoides2

  • Great Black-backed Gull (Larus marinus)4

  • European Herring Gull (Larus argentatus)4

  • Glaucous Gull (Larus hyperboreus)3

Opisthorchidae
Cryptocotyle linguaLittorina littorea2, Littorina saxatilis2,11, Littorina obtusata2,11Pisces (Ammodytes tobianus, Gadus spec., Sprattus sprattus, Salmo spec., Pleuronectiformes)2,17,23

  • Common Guillemot (Uria aalge)4

  • Brünnich’s Guillemot (Uria lomvia)4,6

  • Black-legged Kittiwake (Rissa tridactyla)4,6

  • Great Black-backed Gull (Larus marinus)4

  • European Herring Gull (Larus argentatus)4,15

  • Glaucous Gull (Larus hyperboreus)3,27

  • Northern Fulmar (Fulmarus glacialis)21

Cryptocotyle concavumHydrobia ventrosa8, Hydrobia ulvae9Pisces (Platichtys flesus9, Pomatoschistus microps10, Pungitius pungitius10, Gasterosteus aculeatus10)

  • Black-headed Gull (Chroicoceohalus ridibundus)10

  • Black-legged Kittiwake (Rissa tridactyla)4,6

  • Northern Fulmar (Fulmarus glacialis)21

Diplostomidae
Diplostomum nordmanniGastropoda7Pisces7Black-legged Kittiwake (Rissa tridactyla)4,6
Notocotylidae
Notocotylus spec.Littorina saxatilis2,11, Littorina obtusata2,11, Skeneopsis planorbis2None2

  • Seaducks13

  • European Herring Gull (Larus argentatus)4,15

  • Oystercatcher (Haematopus ostralegus)14

Renicolidae
Renicola spec.Littorina saxatilis2,11, Littorina obtusata2,11, Littorina littorea2

  • Mytilus edulis2

  • Littorina spp.2

  • Common Eider (Somateria mollissima)3

  • Common Gull (Larus canus)10

  • Velvet Scoter (Melanitta fusca)10

  • Long-tailed Duck (Clangula hyemalis)10

  • Cormorant (Phalacrocorax carbo)10

  • Shelduck (Tadorna tadorna)10

  • Manx Shearwater (Puffinus puffinus)25

Himasthlidae
Himasthla spec.Littorina saxatilis2,11, Littorina obtusata2,11, Littorina littorea2Mytilus edulis2

  • Great Black-backed Gull (Larus marinus)4

  • European Herring Gull (Larus argentatus)4,15

  • Glaucous Gull (Larus hyperboreus)3

Echinochasmidae
Mesorchis pseudoechinatusunknownPisces29

  • Black-legged Kittiwake (Rissa tridactyla)28

  • Cormorant (Phalacrocorax carbo)29

Data from:

1 Frank, 1969;

2 Galaktionov & Bustnes, 1999;

3 Kuklin, 2015;

4 Kuklin, 2017;

5 Sergievsky et al., 1997;

6 Kuklin et al., 2020;

7 Faltýnková et al., 2014;

8 Probst & Kube, 1999;

9 Zander et al., 1984;

10 Reimer, 2002;

11 Galaktionov, 1996;

12 Magalhães et al., 2020;

13 Galaktionov & Bustnes, 1996;

14 Borgsteede et al., 1988;

15 Kuklin, 2011;

16 Ching, 1991;

17 Heuch et al., 2011;

18 Galaktionov et al., 2015;

19 Galaktionov et al., 2021;

20 Galaktionov et al., 2019;

21 Kuklin et al., 2019;

22 O’Connell & Fives, 2004;

23 Groenwold et al., 1996;

24 Thieltges et al., 2006a;

25 De Matos et al., 2020;

26 Thieltges et al., 2006b;

27 Sagerup et al., 2009;

28 Kuklin & Kuklina, 2022;

29 Kanarek et al., 2003.

Table 2.

Cestodes determined in seabirds of the North Atlantic, the Barent Sea as well as the Baltic Sea and the North Pacific. In addition, intermediate hosts are named as far as known.

Cestoda (Tapeworms)Intermediate hostsFinal host
Dilepididae
Alcataenia armillarisCrustacea, Euphausiids of the genus Thysanoessa6

  • Common Guillemot (Uria aalge)2,3

  • Brünnich’s Guillemot (Uria lomvia)2,3,5,10

  • Black-legged Kittiwake (Rissa tridactyla)3,5,10

Alcataenia dominicanaCrustacea, Euphausiids of the genus Thysanoessa6

  • Black-legged Kittiwake (Rissa tridactyla)3,10

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Glaucous Gull (Larus hyperboreus)4,7,22

Alcataenia larinaCrustacea, Euphausiids of the genus Thysanoessa1,6

  • Atlantic Puffin (Fratercula arctica)1

  • Black Guillemot (Cephus grille)1

  • Black-legged Kittiwake (Rissa tridactyla)1,3,5,10

  • Great Black-backed Gull (Larus marinus)1,3

  • European Herring Gull (Larus argentatus)1,3

  • Glaucous Gull (Larus hyperboreus)4

  • Northern Fulmar (Fulmarus glacialis)1,21

Alcataenia longicervicaCrustacea, Euphausiids of the Genus Thysanoessa20

  • Common Guillemot (Uria aalge)20

  • Brünnich’s Guillemot (Uria lomvia)20

Neovalipora spec.Pisces8Brünnich’s Guillemot (Uria lomvia)3,10
Paricterotaenia porosaChironomus spec.9

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Black-legged Kittiwake (Rissa tridactyla)10

Paricterotaenia sternina?European Herring Gull (Larus argentatus)3
Anomotaenia microcantha

  • 1. Crustacea16

  • 2. Pisces16

  • Black-legged Kittiwake (Rissa tridactyla)3,10

  • European Herring Gull (Larus argentatus)3

  • Common Gull (Larus canus)16

  • Glaucous Gull (Larus hyperboreus)5,22

Lateriporus teresAmphipoda (Amphitoe rubricata)4Common Eider (Somateria mollissima)4,20
Hymenolepididae
Microsomacanthus ductilisGammaridae12

  • Common Guillemot (Uria aalge)3,

  • Brünnich’s Guillemot (Uria lomvia)5,10

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Black-legged Kittiwake (Rissa tridactyla)10

  • Common Gull (Larus canus)16

  • Glaucous Gull (Larus hyperboreus)22

  • Common Eider (Somateria mollissima)20

Microsomacanthus diorchisGammaridae12

  • Common Eider (Somateria mollissima)4,20

  • Black-legged Kittiwake (Rissa tridactyla)10

Microsomacanthus microsomaGammaridae12 (Gammarus setosus)20

  • Common Eider (Somateria mollissima)4,20

  • European Herring Gull (Larus argentatus)17

  • Long-tailed Duck (Clangula hyemalis)16

  • Velvet Scoter (Melanitta fusca)16

  • Northern Fulmar (Fulmarus glacialis)21

Microsomacanthus jaegerskioeldiGammaridae12Common Eider (Somateria mollissima)4,20
Fimbriarioides intermedia

  • Copepoda18, Ostracoda18,

  • Semibalanus balanoides4

  • Balanus balanoides20

Common Eider (Somateria mollissima)4,20
Laricanthus lateralis?European Herring Gull (Larus argentatus)3
Nadejdolepsis nutidulans?Black-legged Kittiwake (Rissa tridactyla)3,5,10
Wardium cirrosaNereidae13

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Glaucous Gull (Larus hyperboreus)4

  • Common Gull (Larus canus)16

  • Northern Fulmar (Fulmarus glacialis)21

Wardium fryeiNereidae15

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Glaucous Gull (Larus hyperboreus)4

Wardium fusaCrustacea (Branchiopoda14)

  • Great Black-backed Gull (Larus marinus)3

  • Purple Sandpiper (Calidris maritima)4

Wardium manubriatumCrustacea (Branchiopoda14)Black-legged Kittiwake (Rissa tridactyla)10
Aploparaksis crassirostrisOligochaeta19European Herring Gull (Larus argentatus)3
Diphyllobotriidae
Diphyllobotrium dendriticum

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Cormorant (Phalacrocorax carbo)16

Tetrabothriidae
Tetrabothrius erostris

  • 1. Planktonic Crustacean6

  • 2. Arctic cod? (Boreogadus saida)5

  • Brünnich’s Guillemot (Uria lomvia)5,10

  • Great Black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Black-legged Kittiwake (Rissa tridactyla)3,10

  • Glaucous Gull (Larus hyperboreus)5,22

Tetrabothrius cylindraceus

  • 1. Planktonic crustacean6

  • 2. Arctic cod? (Boreogadus saida)5

  • Black-legged Kittiwake (Rissa tridactyla)10

  • European Herring Gull (Larus argentatus)16

Tetrabothrius jaegerskioeldi

  • Common Guillemot (Uria aalge)3

  • Brünnich’s Guillemot (Uria lomvia)10

Tetrabothrius morschtini

  • Black-legged Kittiwake (Rissa tridactyla)5,10

  • Glaucous gull (Larus hyperboreus)5

Tetrabothrius immerinus

  • Great black-backed Gull (Larus marinus)3

  • European Herring Gull (Larus argentatus)3

  • Black-legged Kittiwake (Rissa tridactyla)3,10

Tetrabothrius bassaniAtlantic Gannet (Morus bassani)23

Data from:

1 Muzzaffar et al., 2007;

2 Hoberg, 1984;

3 Kuklin, 2017;

4 Kuklin, 2015;

5 Galaktionov, 1996;

6 Hoberg, 1996;

7 Sagerup et al., 2000;

8 Ortega-Olivares & Garcia-Varela, 2018;

9 Krasnoshchekov & Tomilovskaia, 1978;

10 Kuklin et al., 2020;

11 de Marval et al., 2013;

12 Kuklin & Maslich, 2011;

13 Greben et al., 2019;

14 Maksimova, 1990;

15 Bondarenko, 1997;

16 Reimer, 2002;

17 Kuklin, 2011;

18 McDonald, 1996;

19 Jarecka, 1961;

20 Galaktionov et al., 2021;

21 Kuklin et al., 2019;

22 Sagerup et al., 2009;

23 Mendes et al., 2013.

Table 3.

Acanthocephalans determined in seabirds of the North Sea, the Barent Sea and the Baltic Sea, as well as their intermediate hosts.

AcanthocephalaIntermediate hostsFinal hosts
Polymorphidae
Corynosoma strumosumSpinulogammarus ochotensis5, Gammarus setosus7

  • Common Eider (Somateria mollissima)7

  • Brünnich’s Guillemot (Uria lomvia)1

  • Black-legged Kittiwake (Rissa tridactyla)1

  • Glaucous Gull (Larus hyperboreus)13

  • Cormorant (Phalacrocorax carbo)4

  • Northern Fulmar (Fulmarus glacialis)8

Polymorphus phippsiGammarus setosus7, Gammarus oceanicus3,7

  • Common Eider (Somateria mollissima)2,7

  • Black-legged Kittiwake (Rissa tridactyla)7

  • Glaucous Gull (Larus hyperboreus)13

  • Arctic Terns (Sterna paradisea)7

  • Brünnich’s Guillemot (Uria lomvia)7

  • Black Guillemot (Cepphus grille)7

  • Northern Fulmars (Fulmarus glacialis)14

Polymorphus magnusGammarus spec.4

  • Purple Sandpiper (Calidaris maritima)2

  • Common Scoter (Melanitta nigra)4

  • Long-tailed Duck (Clangula hyemalis)4

  • Steller’s Eider (Polysticta stelleri)4

Polymorphus minutusGammarus spec.10Common Eider (Somateria mollissima)9
Proficollis botulusDecapoda: Carcinus maenas6,11, Hyas araneus7, Pagurus pubescens7

  • Common Eider (Somateria mollissima)2,7,11,12,

  • Purple Sandpiper (Calidaris maritima)2

Data from:

1 Kuklin et al., 2020;

2 Kuklin, 2015;

3 Kuklin & Maslich, 2011;

4 Reimer, 2002;

5 Skorobrekhova & Nikishin, 2019;

6 Neal & Pizzolla, 2008;

7 Galaktionov et al., 2021;

8 Kuklin et al., 2019;

9 Garbus et al., 2018;

10 Hynes & Nicholas, 1957;

11 Camphuysen et al., 2002;

12 Thieltges et al., 2006b;

13 Sagerup et al., 2009;

14 Mallory et al., 2008.

Table 4:

Nematodes determined in seabirds of the North Atlantic, Barent Sea and the Baltic Sea as well as their intermediate hosts.

NematodaIntermediate hostFinal hosts
Acuariidae
Stegophorus stellapolarisUnknown (pisces)7

  • Common Guillemot (Uria aalge)9

  • Brünnich’s Guillemot (Uria lomvia)1,9

  • Razorbill (Alca torda)18

  • Little Auk (Alle alle)18

  • Common Eider (Somateria mollissima)10

  • European Herring Gull (Larus argentatus)9

  • Common Gull (Larus canus)9

  • Black-legged Kittiwake (Rissa tridactyla)1

  • Glaucous Gull (Larus hyperboreus)17

  • Arctic Skua (Stercorarius parasiticus)9

  • Long-tailed Skua (Stercorarius longicaudus)9

  • European Storm-petrel (Hydrobates pelagicus)9

  • Northern Fulmar (Fulmarus glacialis)9,11

Stegophorus crassicaudaUnknown

  • Brünnich’s Guillemot (Uria lomvia)1

  • Black-legged Kittiwake (Rissa tridactyla)1

Cosmocephalus obvelatusBrünnich’s Guillemot (Uria lomvia)1
Paracuaria aduncaAmphipoda (i.e. Gammarus duebeni)5

  • Glaucous Gull (Larus hyperboreus)2, 17

  • Northern Fulmar (Fulmarus glacialis)11

  • Black-legged Kittiwake (Rissa tridactyla)20

Streptocara formosensisCommon Eider (Somateria mollissima)16
Streptocara crassicaudaGammaridae6

  • Common Eider (Somateria mollissima)2

  • Common Scoter (Melanitta nigra)3

  • Velvet Scoter (Melanitta fusca)3

  • Glaucous Gull (Larus hyperboreus)17

Anisakidae
Anisakis spec.

  • 1. Krill crustaceans (Euphausiacea)4

  • 2. Pisces4 (Gadus morhua8 Sprattus sprattus12, Sardina pilchardus13, Engraulis encrasicolus13)

    or

    Cephalopods12

  • Brünnich’s Guillemot (Uria lomvia)1

  • Black-legged Kittiwake (Rissa tridactyla)1

  • Northern Fulmar (Fulmarus glacialis)11

Contracaecum spec.

  • 1. Copepoda / Amphipoda

  • 2. Pisces

  • Common Scoter (Melanitta nigra)3

  • European Herring Gull (Larus argentatus)3

  • Common Gull (Larus canus)3

  • Black-legged Kittiwake (Rissa tridactyla)1

  • Brünnich’s Guillemot (Uria lomvia)1

  • Cormorant (Phalacrocorax carbo)3

  • European Shag (Phalacrocorax aristotelis)19

  • Northern Fulmar (Fulmarus glacialis)11

Capillariidae
Capillaria contorta

  • European Herring Gull (Larus argentatus)3

  • Common Gull (Larus canus)3

  • Black-legged Kittiwake (Rissa tridactyla)1

Capillaria laricolaCommon Gull (Larus canus)3
Raphidascaididae
Hysterothylacium aduncumSandeels (Ammodytes tobianus, Hyperoplus lanceolatus)14, Clupeidae (Sprattus sprattus)12

  • Brünnich’s Guillemot (Uria lomvia)1

  • Northern Fulmar (Fulmarus glacialis)11

  • Glaucous Gull (Larus hyperboreus)17

Cyatholaimidae
Seuratia spec.

  • Brünnich’s Guillemot (Uria lomvia)1

  • Black-legged Kittiwake (Rissa tridactyla)10

Dioctophymatidae
Eustrongylides mergorum

  • 1. Oligochaeta7

  • 2. Pisces7

Brünnich’s Guillemot (Uria lomvia)1
Amidostomidae
Amidostomum anseriNone3

  • Common Eider (Somateria mollissima)2

  • Long-tailed Duck (Clangula hyemalis)3

  • Common Scoter (Melanitta nigra)3

  • Velvet Scoter (Melanitta fusca)3

Amidostomum acutumCommon Eider (Somateria mollissima)15

Data from:

1 Kuklin et al., 2020;

2 Kuklin, 2015;

3 Reimer, 2002;

4 Pravettoni et al., 2012;

5 Anderson & Wong, 1982;

6 Garkavi, 1949;

7 Leszek et al., 1999;

8 Heuch et al., 2011;

9 Nagasawa et al., 1998;

10 Galaktionov et al., 2021;

11 Kuklin et al., 2019;

12 Kleinertz et al., 2012;

13 Dessier et al., 2016;

14 Groenewold et al., 1996;

15 Thieltges et al., 2006b;

16 Borgsteede et al., 2005;

17 Sagerup et al., 2009;

18 Muzzafar & Jones, 2004;

19 Abollo et al., 2001;

20 Kuklin & Kuklina, 2022.

Fig. 1.

Left: Possible routes of helminth infections in marine aquaculture of fish when foraging on the bottom fauna is not prevented and the plant is not protected from seabirds with nets. Right: Possible additional routes of helminth infections when fishes, filter-feeders and kelp are farmed together (integrated multi-trophic aquaculture, IMTA). Likelihood of infection may be increased when first intermediate hosts (Littorina) populate on kelp and second intermediate hosts (mussels) are farmed close to farmed fishes to clear environmental input from fish-aquaculture (Parts of the graphics licensed from stock.adobe.com).

Fig. 2.

Illustration of the potential role of intestinal helminths as a sink for the trace elements cadmium (Cd) and Lead (Pb).

Some digenea, cestoda, or acanthocephala show higher concentration of trace elements than the hosts’ tissues. Clues are still missing today whether helminths are also able to accumulate and/or metabolise POPs in seabirds as shown for parasite host relationships of other vertebrates.

A: accumulation of Cd and Pb as well as POPs in seabirds’ tissues (muscle and liver) not infested with helminths; B: greater bioaccumulation of Cd, Pb, and hypothetically POPs, in helminths compared to the seabirds’ tissues (Parts of the graphics licensed from istockphoto.com).

Table 5.

Studies on the helminth population of individual seabird species and their geographical localization.

Seabirds speciesNumber of helminth species identifiedGeographic areaAuthors
Common Guillemot7Murman coastKuklin 2017
Brünnich's Guillemot8Murman coastKuklin 2017
6Novaya ZemlyaKuklin et al. 2020
Black-legged Kittiwakes24Murman coastKuklin 2017
11Murman coastKuklin & Kuklina 2022
5Novaya ZemlyaKuklin et al. 2020
Great Black-backed Gull30Murman coastKuklin 2017
European Herring Gull38Murman coastKuklin 2017
Northern Fulmar14Murman coastKuklin et al. 2019
Common Eider13North seaThieltges et al. 2000
10Franz Josef LandGalaktionov et al. 2021
Velvet Scoter60Southern Baltic + literatureRolfes 2023
Great Cormorant9Southern Baltic seaKanarak et al. 2003
DOI: https://doi.org/10.2478/helm-2023-0034 | Journal eISSN: 1336-9083 | Journal ISSN: 0440-6605
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Language: English
Page range: 300 - 326
Submitted on: Dec 31, 2022
Accepted on: Sep 21, 2023
Published on: Dec 31, 2023
Published by: Slovak Academy of Sciences, Institute of Parasitology
In partnership with: Paradigm Publishing Services
Publication frequency: Volume open
Keywords:
Helminths,
seabirds,
fisheries,
aquaculture,
climate change,
seawater acidification,
microplastic,
organic pollutants,
trace elements
Related subjects:
Life sciences,
Zoology,
Ecology,
Life sciences, other,
Medicine,
Clinical medicine,
Microbiology, virology and infection epidemiology

© 2023 U. Schwantes, published by Slovak Academy of Sciences, Institute of Parasitology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Volume 60 (2023): Issue 4 (December 2023)
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