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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

U. Schwantes
U. Schwantes
   | Dec 31, 2023
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Article Category: Review
Published Online: Dec 31, 2023
Page range: 300 - 326
Received: Dec 31, 2022
Accepted: Sep 21, 2023
DOI: https://doi.org/10.2478/helm-2023-0034
Keywords
© 2023 U. Schwantes et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

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).
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).
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).

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

Nematoda Intermediate host Final hosts
Acuariidae
Stegophorus stellapolaris Unknown (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 crassicauda Unknown

Brünnich’s Guillemot (Uria lomvia)1

Black-legged Kittiwake (Rissa tridactyla)1
Cosmocephalus obvelatus Brünnich’s Guillemot (Uria lomvia)1
Paracuaria adunca Amphipoda (i.e. Gammarus duebeni)5

Glaucous Gull (Larus hyperboreus)2, 17

Northern Fulmar (Fulmarus glacialis)11

Black-legged Kittiwake (Rissa tridactyla)20
Streptocara formosensis Common Eider (Somateria mollissima)16
Streptocara crassicauda Gammaridae6

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 laricola Common Gull (Larus canus)3
Raphidascaididae
Hysterothylacium aduncum Sandeels (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 anseri None3

Common Eider (Somateria mollissima)2

Long-tailed Duck (Clangula hyemalis)3

Common Scoter (Melanitta nigra)3

Velvet Scoter (Melanitta fusca)3
Amidostomum acutum Common Eider (Somateria mollissima)15

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 hosts Final host
Dilepididae
Alcataenia armillaris Crustacea, 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 dominicana Crustacea, 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 larina Crustacea, 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 longicervica Crustacea, Euphausiids of the Genus Thysanoessa20

Common Guillemot (Uria aalge)20

Brünnich’s Guillemot (Uria lomvia)20
Neovalipora spec. Pisces8 Brünnich’s Guillemot (Uria lomvia)3,10
Paricterotaenia porosa Chironomus 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 teres Amphipoda (Amphitoe rubricata)4 Common Eider (Somateria mollissima)4,20
Hymenolepididae
Microsomacanthus ductilis Gammaridae12

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 diorchis Gammaridae12

Common Eider (Somateria mollissima)4,20

Black-legged Kittiwake (Rissa tridactyla)10
Microsomacanthus microsoma Gammaridae12 (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 jaegerskioeldi Gammaridae12 Common 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 cirrosa Nereidae13

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 fryei Nereidae15

Great Black-backed Gull (Larus marinus)3

European Herring Gull (Larus argentatus)3

Glaucous Gull (Larus hyperboreus)4
Wardium fusa Crustacea (Branchiopoda14)

Great Black-backed Gull (Larus marinus)3

Purple Sandpiper (Calidris maritima)4
Wardium manubriatum Crustacea (Branchiopoda14) Black-legged Kittiwake (Rissa tridactyla)10
Aploparaksis crassirostris Oligochaeta19 European Herring Gull (Larus argentatus)3
Diphyllobotriidae
Diphyllobotrium dendriticum

1. Copepoda11, 16

2. Pisces11

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 bassani Atlantic Gannet (Morus bassani)23

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

Seabirds species Number of helminth species identified Geographic area Authors
Common Guillemot 7 Murman coast Kuklin 2017
Brünnich's Guillemot 8 Murman coast Kuklin 2017
6 Novaya Zemlya Kuklin et al. 2020
Black-legged Kittiwakes 24 Murman coast Kuklin 2017
11 Murman coast Kuklin & Kuklina 2022
5 Novaya Zemlya Kuklin et al. 2020
Great Black-backed Gull 30 Murman coast Kuklin 2017
European Herring Gull 38 Murman coast Kuklin 2017
Northern Fulmar 14 Murman coast Kuklin et al. 2019
Common Eider 13 North sea Thieltges et al. 2000
10 Franz Josef Land Galaktionov et al. 2021
Velvet Scoter 60 Southern Baltic + literature Rolfes 2023
Great Cormorant 9 Southern Baltic sea Kanarak et al. 2003

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.

Digenea First intermediate host Second intermediate host Final host
Gymnophallidae
Gymnophallus deliciosus ? Blue Mussel (Mytilus edulis)16 European Herring Gull (Larus argentatus)15
Gymnophallus bursicola Unknown18 Mytilus edulis18

Common Eider (Somateria mollissima)18

Velvet scoter (Melanitta fusca)30
Gymnophallus choledochus Bivalvia: Cestoderma edule12 Polychaeta1 (Hediste diversicolor, Arenicola marina etc.)12 or alternatively Cestoderma spec.12 Common Eider (Somateria mollissima)3, 26
Parvatrema spec. Unknown2 Littorina 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 triangulus Littorina saxatilis2,5,20, Littorina obtusata2,5 None2 Common Eider (Somateria mollissima)3
Microphallus pygmaeus Littorina saxatilis2,5,11,20, Littorina obtusata2,5,11, Littorina littorea2 Littorina spec.24

Common Eider (Somateria mollissima)3,20

Great Black-backed Gull (Larus marinus)4

European Herring Gull (Larus argentatus)4,15
Microphallus pseudopygmaeus Littorina saxatilis2,5,11,20, Littorina obtusata2,5,11, Onoba aculeus2, Margarites helicinus2, Margarites groenlandicus2,20, Lacuna vincta2 None2

Common Eider (Somateria mollissima)3,19

Glaucous Gull (Larus hyperboreus)27
Microphallus piriformes Littorina saxatilis2,5,11,20, Littorina obtusata2,5,11 None2

Common Eider (Somateria mollissima)3

Great Black-backed Gull (Larus marinus)4,

European Herring Gull (Larus argentatus)4,15
Microphallus similis Littorina saxatilis2,11, Littorina obtusata2,11, Littorina littorea2 Crustacea: Carcinus maenas2, Hyas araneus2

Great Black-backed Gull (Larus marinus)4

European Herring Gull (Larus argentatus)4,15
Maritrema arenaria Littorina saxatilis2,11 Crustacea: Semibalanus balanoides2

Great Black-backed Gull (Larus marinus)4

European Herring Gull (Larus argentatus)4

Glaucous Gull (Larus hyperboreus)3
Opisthorchidae
Cryptocotyle lingua Littorina littorea2, Littorina saxatilis2,11, Littorina obtusata2,11 Pisces (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 concavum Hydrobia ventrosa8, Hydrobia ulvae9 Pisces (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 nordmanni Gastropoda7 Pisces7 Black-legged Kittiwake (Rissa tridactyla)4,6
Notocotylidae
Notocotylus spec. Littorina saxatilis2,11, Littorina obtusata2,11, Skeneopsis planorbis2 None2

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 littorea2 Mytilus edulis2

Great Black-backed Gull (Larus marinus)4

European Herring Gull (Larus argentatus)4,15

Glaucous Gull (Larus hyperboreus)3
Echinochasmidae
Mesorchis pseudoechinatus unknown Pisces29

Black-legged Kittiwake (Rissa tridactyla)28

Cormorant (Phalacrocorax carbo)29

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

Acanthocephala Intermediate hosts Final hosts
Polymorphidae
Corynosoma strumosum Spinulogammarus 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 phippsi Gammarus 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 magnus Gammarus 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 minutus Gammarus spec.10 Common Eider (Somateria mollissima)9
Proficollis botulus Decapoda: Carcinus maenas6,11, Hyas araneus7, Pagurus pubescens7

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

Purple Sandpiper (Calidaris maritima)2
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