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