Marine Crustaceans as Potential Hosts and Vectors for Metazoan Parasites



Fig. 14.1
Marine helminth parasites in intermediate hosts. (a) L3 larvae of Anisakis simplex in the haemocoel of Paraeuchaetha norvegica (Copepoda). (b) Hysterothylacium aduncum in a hyperiid Amphipoda. (c) Amphipod Crustacea hosting a Pomphorhynchus larva. (d) Anisakis sp. in a decapod Crustacea. (e) Nematodes and Crustacea in the stomach content of fish. (f) Fish liver with Anisakis sp. larvae. Photos (a), (b): Klimpel et al. (2004); (d): Klimpel (private property); (c), (e), (f): Möller (private property)



The phylum Acanthocephala comprises approximately 1,150 species which are exclusively parasitic (Verweyen et al. 2011). The adults live in the intestine wall of their vertebrate hosts. The marine life cycle involves one or two intermediate hosts with a benthic association (Marcogliese 1995). The eggs, which contain the acanthor larvae, will be released into the water column with the faeces of the final host. Detritus-feeding zooplankton organisms (e.g. Amphipoda) acquire the parasites by oral ingestion (Fig. 14.1c). The acanthor larvae enter the body cavity by penetrating the intestinal wall and reach the acanthella stage. Paratenic hosts (e.g. fish) and final hosts (fish, birds, seals, whales) get infected by preying upon the intermediate hosts. In general, Amphipoda serve as main intermediate hosts for marine Acanthocephala (Taraschewski 2005). According to the literature, human pathogenetic species seems to be restricted to terrestrial habitats. Nevertheless, it cannot be excluded that the consumption of marine Acanthocephala in fish food can cause allergic reactions as known from anisakid nematodes (Audicana and Kennedy 2008).



14.4 Marine Crustacea in the Life Cycle of Helminth Parasites


Data from 52 peer-reviewed publications have been taken into consideration in order to assess the role of marine crustacean as potential hosts for helminth parasites (Tables 14.114.4). A total of 69 different parasites belonging to the Trematoda (n = 28), Cestoda (n = 18), Nematoda (n = 10) and Acanthocephala (n = 13) where reported among the crustacean subgroups Copepoda, Euphausiacea, Amphipoda, Decapoda, Mysidacea, Isopoda and Cirripedia (Tables 14.114.3). The Acanthocephala have been proven to be parasites of 38 different hosts in three subgroups Euphausiacea, Amphipoda and Decapoda, whereas the Nematoda were reported from 91 different Crustacea in all subgroups. Parasites of the Cestoda and Trematoda have been proven from a total of 27 and 32 crustacean hosts, respectively (Figs. 14.2 and 14.3).


Table 14.1
Reported marine crustacean intermediate hosts of Digesnea and the respective references




































































































































































Host

Parasite

References

Copepoda

Acartia clausi

Hemiurus communis

Marcogliese (1995)

A. tonsa

Brachyphallus crenatus

Køie (1992)

Acartia sp.

Lecithaster gibbosus a, Lecithaster confusus

Hunninen and Cable (1943), Køie (1989), Marcogliese (1995)

Centropages abdominalis

Lecithaster sp.

Køie (1989)

C. hamatus

Lecithaster gibbosus a

Køie (1989)

Oithona similis

Lecithocladium excisum

Køie (1991), Marcogliese (1995), Reimer et al. (1975)

Pseudocalanus elongatus

Lecithaster gibbosus a

Køie (1989)

P. minutus

Lecithaster sp.

Køie (1989)

Tigriopus brevicornis

Lecithochirium furcolabiatum

Marcogliese (2002)

Calanoida indet.

Derogenes varicus, Hemiurus luehei, Lecithaster gibbosus, Lecithocladium excisum

Køie (1989, 1991), Marcogliese (1995), Reimer et al. (1975), Svendsen (1990)

Harpacticoida indet.

Derogenes varicus

Marcogliese (2002)

Euphausiacea

Euphausia pacifica

Paronatrema sp.

Marcogliese (1995)

E. similis

Neonotoporus trachuri, Pseudopecoelus japonicus

Marcogliese (1995)

Nyctiphanes simplex

Paronatrema sp.

Gómez-Gutiérrez et al. (2010)

Euphausiacea indet.

Syncoelium filiferum

Marcogliese (1995)

Amphipoda

Calliopius laeviusculus

Microphallus papillorobustus

Zander et al. (1994)

Gammarus duebeni

Microphallus claviformes, M. papillorobustus

Zander et al. (1994)

G. finmarchicus

Maritrema subdolum, Microphallus papillorobustus, Podocotyle atomon

Zander et al. (1994)

G. insensibilis

Microphallus papillorobustus

Brown et al. (2003)

G. locusta

Levinseniella brachysoma, Maritrema subdolum, Microphallus papillorobustus, Podocotyle atomon

Zander et al. (2002)

G. oceanicus

Levinseniella brachysoma, Maritrema subdolum, Microphallus claviformes, M. papillorobustus, Podocotyle atomon

Zander et al. (2002)

G. salinus

Maritrema subdolum, Microphallus claviformes, M. papillorobustus, Levinseniella brachysoma, Podocotyle atomon

Zander et al. (2002)

G. tigrinus

Microphallus claviformes, M. papillorobustus, Maritrema subdolum

Zander et al. (1994)

G. zaddachi

Levinseniella brachysoma, Maritrema subdolum, Microphallus claviformes, M. papillorobustus, Podocotyle atomon

Zander et al. (2002)

Paracalliope novizealandiae

Maritrema novaezealandensis a

Fredensborg and Poulin (2005), Leung and Poulin (2006)

Decapoda

Farfantepenaeus aztecus

Opecoeloides fimbriatus

Feigenbaum (1975)

F. duorarum

Microphallus sp., Opecoeloides fimbriatus

Feigenbaum (1975)

Hemigrapsus crenulatus

Maritrema novaezealandensis, Microphallus sp.

Martorelli et al. (2004)

H. penicilliatus

Levinseniella conicostoma, Maritrema laricola, M. setoenesis, Microphalloides japonicus, Probolocoryphe asadai, Microphallus macrorchis

Blakeslee et al. (2009), McDermott (2011)

H. sanguineus

Maritrema jebuensis, M. setoenensis, Microphalloides japonicus, Probolocoryphe asadai, Microphallus capellae

Blakeslee et al. (2009), Chung et al. (2010), McDermott (2011)

H. sexdentatus

Maritrema novaezealandensis, Microphallus sp.

Koehler and Poulin (2010)

Hippolyte inermis

Opecoeloides collumbellae

Jousson and Bartoli (2000)

Idotea balthica

Maritrema subdolum, Podocotyle atomon

Zander et al. (2002)

I. chelipes

Maritrema subdolum, Microphallus claviformes, M. papillorobustus, Levinseniella brachysoma, Podocotyle atomon

Zander et al. (2002)

I. granulosa

Maritrema subdolum

Zander et al. (2000)

Penaeus setiferus

Opecoeloides fimbriatus

Feigenbaum (1975)


aExperimental infection



Table 14.2
Reported marine crustacean intermediate hosts of Cestoda and the respective references










































































































































Host

Parasite

References

Copepoda

Acartia clausi

Bothriocephalus scorpii

Solonchenko (1985)

Calanus finmarchicus

Aporhynchus norvegicus, Scolex pleuronectis

Klimpel et al. (2003), Marcogliese (1995)

Eurytemora affinis

Bothriocephalus scorpii

Marcogliese (1995)

Mesochra sp.

Prochristianella hispida a

Palm (2004)

Tigriopus californicus

Lacistorhynchus tenuis, Parachristianella monomegacantha, Prochristianella hispida a

Palm (2004)

Calanoida indet.

Bothriocephalus barbatus, B. gregarius b, Grillotia erinaceus

Marcogliese (1995)

Harpacticoida indet.

Lacistorhynchus dollfusi

Marcogliese (1995)

Euphausiacea

Euphausia pacifica

Nybelinia surmenicola

Marcogliese (1995)

E. recurva

Pseudonybelinia odontocantha

Marcogliese (1995)

E. similis

Echinobothrium sp., Tetrarhynchobothrium sp.

Marcogliese (1995)

Meganyctiphanes norvegica

Aporhynchus norvegicus

Klimpel et al. (2003)

Nyctiphanes simplex

Echinobothrium sp., Tetrarhynchobothrium sp.

Gómez-Gutiérrez et al. (2010)

Thysanoessa inermis

Nybelinia surmenicola

Shimazu (1975)

T. longipes

Nybelinia surmenicola, Pelichnibothrium caudatum

Marcogliese (1995), Shimazu (1975)

T. raschii

Nybelinia surmenicola

Shimazu (1975)

Euphausiacea indet.

Nybelinia surmenicola

Shimazu (1975)

Decapoda

Callianassa sp.

Parachristianella monomegacantha

Palm (2004)

Callichirus islagrande

Prochristianella hispida

Palm (2004)

Callinectes sapidus

Polypocephalus sp.

Hutton (1964)

Farfantepenaeus aztecus

Parachristianella dimegacantha, Prochristianella hispida

Feigenbaum (1975)

F. brasiliensis

Mecistobothrium penaeus, Parachristianella monomegacantha, P. heteromegacantha, Polypocephalus sp., Prochristianella hispida

Feigenbaum (1975), Hutton (1964)

F. duorarum

Parachristianella dimegacantha, P. monomegacantha, Polypocephalus sp., Prochristianella hispida

Feigenbaum (1975), Hutton (1964)

F. setiferus

Polypocephalus sp.

Hutton (1964)

Penaeus setiferus

Prochristianella hispida

Feigenbaum (1975)

Sicyonia dorsalis

Polypocephalus sp.

Hutton (1964)

Solenocera atlantidis

Polypocephalus sp.

Hutton (1964)

Squilla empusa

Polypocephalus sp.

Hutton (1964)

Trachypeneus constrictus

Polypocephalus sp.

Hutton (1964)

T. similis

Polypocephalus sp.

Hutton (1964)

Xiphopenaeus kroyeri

Polypocephalus sp.

Hutton (1964)


aExperimental infection

bNomen nudum



Table 14.3
Reported marine crustacean intermediate hosts of Nematoda and the respective references



















































































































































































































































































Host

Parasite

References

Copepoda

Acartia bifilosa

Hysterothylacium sp.

Lick (1991)

A. longiremis

Hysterothylacium sp.a

Lick (1991)

A. tonsa

Anisakis simplex a, Hysterothylacium aduncum a

Køie (1993, 2001)

Acartia sp.

Contracaecum osculatum a

Køie and Fagerholm (1995)

Calanus finmarchicus

Hysterothylacium sp.

Lick (1991), Marcogliese (1995), Svendsen (1990)

Calanus sp.

Hysterothylacium sp.

Lick (1991)

Centropages hamatus

Contracaecum osculatum a

Køie and Fagerholm (1995)

C. typicus

Hysterothylacium sp.

Svendsen (1990)

Euchoeta sp.

Hysterothylacium sp.

Lick (1991)

Eurytemora affinis

Hysterothylacium sp.

Lick (1991)

Microsetella norvegica

Hysterothylacium sp.a

Lick (1991)

Oithona similis

Anisakis simplex a

Køie (2001)

Paracalanus parvus

Contracaecum osculatum a

Køie and Fagerholm (1995)

Paraeuchaeta norvegica

Anisakis simplex

Klimpel et al. (2004)

Pseudocalanus elongatus

Hysterothylacium sp.

Lick (1991)

Pseudocalanus sp.

Hysterothylacium sp.

Lick (1991)

Temora longicornis

Contracaecum osculatum a, Hysterothylacium sp. a

Køie and Fagerholm (1995), Lick (1991)

Calanoida indet.

Hysterothylacium aduncum

Hurst (1984), Køie (1993), Marcogliese (1995), Svendsen (1990)

Harpacticoida indet.

Hysterothylacium aduncum a

Klimpel et al. (2004), Køie (1993)

Cirripedia

Balanus sp.

Anisakis simplex a, Contracaecum osculatum a

Køie (2001), Køie and Fagerholm (1995)

Mysidacea

Erythrops erythrophthalma

Hysterothylacium sp.

Lick (1991)

Mesopodopsis slabberi

Anisakis sp., Hysterothylacium sp., Pseudoterranova decipiens

Lick (1991)

Mysis gaspensis

Paracuaria adunca

Jackson et al. (1997)

M. mixta

Hysterothylacium sp.

Lick (1991)

M. stenolepis

Paracuaria adunca, Pseudoterranova decipiens

Jackson et al. (1997)

Neomysis americana

Hysterothylacium sp., Paracuaria adunca, Pseudoterranova decipiens

Jackson et al. (1997), Lick (1991)

N. integer

Contracaecum osculatum a, Hysterothylacium aduncum, Hysterothylacium sp., Pseudoterranova decipiens

Klimpel and Rückert (2005), Køie and Fagerholm (1995), Lick (1991)

N. intermedia

Hysterothylacium sp.a

Lick (1991)

Praunus flexuosus

Paracuaria adunca

Jackson et al. (1997)

Amphipoda

Americorchestia megalophthalma

Pseudoterranova decipiens

Jackson et al. (1997)

Amphiporeia virginiana

Paracuaria adunca, Pseudoterranova decipiens

Jackson et al. (1997)

Calliopius laeviusculus

Hysterothylacium sp.

Zander et al. (1994)

Caprella septentrionalis

Anisakis sp., Hysterothylacium sp., Pseudoterranova decipiens

Lick (1991)

Echinogammarus obtusatus

Paracuaria adunca, Pseudoterranova decipiens, Tetrameres sp.

Jackson et al. (1997)

Eogammarus kygi

Hysterothylacium sp.

Moravec and Nagasawa (1986)

Gammarus duebeni

Hysterothylacium sp.

Lick (1991)

G. finmarchicus

Hysterothylacium sp.

Zander et al. (1994)

G. inaequicauda

Hysterothylacium sp.

Lick (1991)

G. lawrencianus

Ascarophis sp., Hysterothylacium sp., Paracuaria adunca, Pseudoterranova decipiens, Tetrameres sp.

Jackson et al. (1997), Lick (1991)

G. locusta

Ascarophis arctica, Hysterothylacium sp.

Lick (1991), Zander et al. (2002)

G. oceanicus

Ascarophis arctica, Hysterothylacium sp., Paracuaria adunca, Tetrameres sp.

Jackson et al. (1997), Lick (1991), Svendsen (1990), Zander et al. (2002)

G. salinus

Ascarophis arctica , Hysterothylacium sp.

Lick (1991), Zander et al. (2002)

G. zaddachi

Ascarophis arctica , Hysterothylacium sp.

Lick (1991), Zander et al. (2002)

Gammarus spp.

Hysterothylacium aduncum

Klimpel and Rückert (2005)

Hyperia galba

Hysterothylacium aduncum

Klimpel and Rückert (2005)

Themisto abyssorum

Ascarophis sp., Hysterothylacium aduncum

Jackson et al. (1997), Klimpel and Rückert (2005), Køie (1993), Marcogliese (1995)

T. gaudichaudii

Hysterothylacium aduncum

Klimpel and Rückert (2005)

Unciola irrorata

Hysterothylacium sp., Pseudoterranova decipiens

Lick (1991)

Isopoda

Edotia triloba

Hysterothylacium sp.

Lick (1991)

Idotea neglecta

Pseudoterranova decipiens

Lick (1991)

Idotea spp.

Hysterothylacium aduncum

Klimpel and Rückert (2005)

Jaera albifrons

Hysterothylacium sp.

Zander et al. (1994)

Euphausiacea

Euphausia krohnii

Anisakis sp.

Smith and Snyder (2005)

E. nana

Anisakis simplex, Anisakis sp.

Lick (1991)

E. pacifica

Anisakis simplex, Anisakis sp., Contracaecum osculatum, Hysterothylacium sp.

Lick (1991), Marcogliese (1995), Smith and Snyder (2005)

E. similis

Philometra sp.

Marcogliese (1995)

E. vallentini

Anisakis sp.

Hays et al. (1998)

Meganyctiphanes norvegica

Anisakis simplex, Hysterothylacium sp.

Hays et al. (1998), Lick (1991), Smith and Snyder (2005)

Nyctiphanes australis

Anisakis simplex

Marcogliese (1995)

N. couchii

Anisakis simplex, Hysterothylacium sp.

Hays et al. (1998), Lick (1991)

N. simplex

Anisakis simplex

Gómez-Gutiérrez et al. (2010)

Thysanoessa inermis

Anisakis simplex, Hysterothylacium sp.

Lick (1991), Marcogliese (1995), Smith (1971)

T. longicaudata

Anisakis simplex

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