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Table 2 A list of studies detecting co-infections by heterologous parasites in amphibians

From: Host–multiparasite interactions in amphibians: a review

Host

Life stage

Parasites

Consequences for hosts

Association between parasites

References

Field studies

 Rana catesbeiana

Larval

Rv (FV-3-like) + alveolate (species not specified)

Larval mortality

Not specified

[182]

 Lithobates sphenocephalus

 Anaxyrus boreas

Larval, metamorph

Rv + Echinostoma sp.

Not specified

Negative correlation between infection intensity of Rv and Echinostoma sp.

[8]

 Rana catesbeiana

 Alytes obstetricans

Larval and metamorph

Bd + Rv

Larval mortality

Bd and Rv infection intensities were not significantly correlated

[168]

 Ichthyosaura alpestris

 Ambystoma talpoideum

Not specified

Bd + Rv

Not specified

Not specified

[61]

 Rana catesbeiana

Larval and adult

 Lithobates sphenocephalus

Adult

 Anaxyrus terrestris

Adult

Bd + Rv

Not specified

Bd prevalence was higher in individuals that were positive for Rv

[61]

 Craugastor fitzingeri

Metamorph

Bd + Rv

Not specified

A positive association between Bd and Rv prevalence

[165]

 Cryptobranchus alleganiensis

Not specified

Bd + Rv

Tail lesions, fused toes, and healed abrasions on the body of co-infected animals

Not specified

[153]

 Eurycea bislineata

Adult

Bd + Rv

Not specified

No association between Bd and Rv prevalence

[159]

 Rana catesbeiana

 Lithobates clamitans

 Hyla versicolor, H. chrysoscelis

Juvenile

Bd + Rv

Bloating, swelling, discolouration, lacerations, and morphological abnormalities

Not specified

[160]

 Lithobates sylvaticus

 Pseudacris maculata, P. triseriata

 Lissotriton boscai

Adult

Bd + Rv

Not specified

Not specified

[154]

 Hypsiboas gladiator

Adult

Bd + Rv

Not specified

Rv infection intensity was marginally associated with the probability of Bd infection

[164]

 Rhinella manu

 Pristimantis spp.

 Rana catesbeiana

Larval and adult

Bd + Rv

Not specified

No association

[61]

 Lithobates sphenocephalus

 Lithobates sylvaticus

Larval, juvenile and adult

Bd + Rv

No visible signs of Bd and Rv infections were observed

Not specified

[155]

 Notophthalmus viridescens

Adult

Bd + Rv

An individual collected alive showed small red tail lesions, another individual found dead in the field

Not specified

[163]

 Lithobates clamitans

Larval

Bd + Rv

Not specified

Not specified

[163]

 Pelophylax caralitanus

Not specified

Bd + Rv

Not specified

Not specified

[215]

 Pseudacris regilla

Larval, metamorph

Bd + Rv

Not specified

A positive correlation between Bd and Rv infection intensity

[8]

 Telmatobius marmoratus

Adult

Bd + Rv

Not specified

No association

[164]

 Rana catesbeiana

Adult

Bd + Rv

Not specified

Higher Bd infection intensity in co-infected individuals

[166]

 Lithobates sphenocephalus

 Alytes obstetricans

Metamorph

Bd + Rv (CMTV-like)

Isolated from a dead individual collected in the field

Not specified

[154]

 Bufo spinosus

Metamorph

Bd + Rv (CMTV-like)

Isolated from a dead individual collected in the field

Not specified

[154]

 Hyla molleri

Adult

Bd + Rv (CMTV-like)

Not specified

Not specified

[154]

 Xenopus laevis

Adult

Bd + Rv (FV-3)

Euthanized after live capture

Not specified

[157]

 Bufo bufo

Metamorph

Bd + Rv (FV-3-like)

Not specified

Not specified

[156]

 Rana muscosa

Larval

Bd + Rv (FV-3-like)

Mass mortality in larval population associated with both parasites

Not specified

[158]

 Boana pulchella

Adult

Bd + Amphibiocystidium sp.

Not specified

Not specified

[216]

 Eleutherodactylus cooki

Adult

Bd + Carios sp.

Male-biased co-infections due to male parental care: nesting sites are highly infested by ticks, and also suitable for Bd persistence

Not specified

[100]

 Boana pulchella

Adult

Bd + Valentines rwandae

Seasonal variability in prevalence, with distinct peaks for the two parasites

No association

[217]

 Lissotriton helveticus

Adult

Bd + Rv + Dermocystidium sp.

Isolated from a dead individual collected in the field

Not specified

[218]

 Rana aurora

Larval

Bd + ciliates + flagellates + Ribeiroia sp. + other macroparasites

Bd-infected tadpoles had significantly lower parasite species richness than those not infected

Diverse macroparasite fauna negatively influenced Bd prevalence

[198]

 Pseudacris regilla

Larval, metamorph

Bd + Alaria sp.

Not specified

Infection intensities negatively correlated between Bd and Alaria sp.

[24]

 Pseudacris regilla

Larval, metamorph

Bd + Echinostoma sp.

Not specified

Infection intensities negatively correlated between Bd and Echinostoma sp.

[24]

 Rana catesbeiana

Larval, metamorph

Bd + Echinostoma sp.

Not specified

Infection intensities negatively correlated between Bd and Echinostoma sp.

[8]

 Pseudacris regilla

 Anaxyrus boreas

Larval, metamorph

Ribeiroia ondatrae + Echinostoma sp.

Not specified

A positive correlation between infection intensity of macroparasites

[8]

 Taricha torosa

 Pseudacris regilla

Studies on captive populations

 Rana catesbeiana

Larval, juvenile

Rv + Myxosporidium (most likely Sphaerospora sp.)

R. catesbeiana tadpole showed symptoms like oedema and erythema

Not specified

[69]

 Lithobates clamitans

 Rana catesbeiana

Larval

Bd + Myxidium sp.

Not specified

Not specified

[219]

 Dendrobates auratus

Adult

Bd + Rv + Aeromonas hydrophila

Gross changes e.g., sloughing skin, proliferative ulcerations, and swollen and pale liver, were observed in dead animals

Not specified

[161]

 Phyllobates terribilis

 Pyxicephalus adspersus

 Rhacophorus dennysi

  1. Bd: Batrachochytrium dendrobatidis; CMTV-like: common midwife toad virus-like virus; FV-3: Frog virus-3 virus; FV-3-like: Frog virus 3-like virus; Rv: Ranavirus