Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns
ABSTRACT Recent developments in microscopic and molecular tools have allowed the implementation of new approaches for assessing parasitic infections in wildlife populations. This is particularly important for the noninvasive detection and quantification of endoparasites in live animals. Here, we com...
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Wiley
2024-11-01
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| Series: | Ecology and Evolution |
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| Online Access: | https://doi.org/10.1002/ece3.70564 |
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| author | Sofía Capasso Manuel Parejo José Manuel Reyes‐González Juan G. Navedo Ricardo Morán‐López José A. Masero Jorge S. Gutiérrez |
| author_facet | Sofía Capasso Manuel Parejo José Manuel Reyes‐González Juan G. Navedo Ricardo Morán‐López José A. Masero Jorge S. Gutiérrez |
| author_sort | Sofía Capasso |
| collection | DOAJ |
| description | ABSTRACT Recent developments in microscopic and molecular tools have allowed the implementation of new approaches for assessing parasitic infections in wildlife populations. This is particularly important for the noninvasive detection and quantification of endoparasites in live animals. Here, we combined copromicroscopic (Mini‐FLOTAC) and molecular (qPCR) techniques to detect the infection of the macroparasite Ligula intestinalis (Cestoda, Pseudophyllidea) in fresh droppings of Gull‐billed Terns Gelochelidon nilotica (Charadriiformes, Laridae) breeding in southwestern Spain. Additionally, we sequenced the cytochrome b gene in parasite isolates from Gull‐billed Terns (definitive host) and Common Bleak Alburnus alburnus (second intermediate host) sampled around tern colonies to explore potential genetic differences between the isolates. The qPCR test showed a higher prevalence (18%; in 13/73 samples) than Mini‐FLOTAC (9%; in 8/88 samples), indicating that qPCR was more sensitive for diagnostic purposes than fecal flotation alone. Although the agreement between both techniques was substantial (84.2%) mainly due to the large number of uninfected samples, only Mini‐FLOTAC allowed us to quantify parasite shedding. When combining techniques, the prevalence of infection did not differ between adults and chicks, suggesting frequent trophic transmission from parents to their offspring via food provisioning. Phylogenetic analyses identified four haplotypes in the isolates from Gull‐billed Terns and Bleak, all of which were placed within a European clade composed of tapeworms recovered exclusively from phylogenetically derived cyprinid fish. This, combined with the short lifespan of mature tapeworms, suggests that Gull‐billed Terns became infected after consuming infected fish around their breeding colonies rather than on their West African wintering grounds. Altogether, our results represent the first record of L. intestinalis in Gull‐billed Terns and the first molecular characterization of the parasite in the Iberian Peninsula. This integrative coprodiagnostic protocol can be applied to other host–parasite systems, allowing researchers to study helminth infections in wild populations using a noninvasive approach. |
| format | Article |
| id | doaj-art-12c0bfa4aed94f9ebd813b06c2365a50 |
| institution | OA Journals |
| issn | 2045-7758 |
| language | English |
| publishDate | 2024-11-01 |
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| series | Ecology and Evolution |
| spelling | doaj-art-12c0bfa4aed94f9ebd813b06c2365a502025-08-20T01:58:19ZengWileyEcology and Evolution2045-77582024-11-011411n/an/a10.1002/ece3.70564Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed TernsSofía Capasso0Manuel Parejo1José Manuel Reyes‐González2Juan G. Navedo3Ricardo Morán‐López4José A. Masero5Jorge S. Gutiérrez6Departamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias Universidad de Extremadura Badajoz SpainABSTRACT Recent developments in microscopic and molecular tools have allowed the implementation of new approaches for assessing parasitic infections in wildlife populations. This is particularly important for the noninvasive detection and quantification of endoparasites in live animals. Here, we combined copromicroscopic (Mini‐FLOTAC) and molecular (qPCR) techniques to detect the infection of the macroparasite Ligula intestinalis (Cestoda, Pseudophyllidea) in fresh droppings of Gull‐billed Terns Gelochelidon nilotica (Charadriiformes, Laridae) breeding in southwestern Spain. Additionally, we sequenced the cytochrome b gene in parasite isolates from Gull‐billed Terns (definitive host) and Common Bleak Alburnus alburnus (second intermediate host) sampled around tern colonies to explore potential genetic differences between the isolates. The qPCR test showed a higher prevalence (18%; in 13/73 samples) than Mini‐FLOTAC (9%; in 8/88 samples), indicating that qPCR was more sensitive for diagnostic purposes than fecal flotation alone. Although the agreement between both techniques was substantial (84.2%) mainly due to the large number of uninfected samples, only Mini‐FLOTAC allowed us to quantify parasite shedding. When combining techniques, the prevalence of infection did not differ between adults and chicks, suggesting frequent trophic transmission from parents to their offspring via food provisioning. Phylogenetic analyses identified four haplotypes in the isolates from Gull‐billed Terns and Bleak, all of which were placed within a European clade composed of tapeworms recovered exclusively from phylogenetically derived cyprinid fish. This, combined with the short lifespan of mature tapeworms, suggests that Gull‐billed Terns became infected after consuming infected fish around their breeding colonies rather than on their West African wintering grounds. Altogether, our results represent the first record of L. intestinalis in Gull‐billed Terns and the first molecular characterization of the parasite in the Iberian Peninsula. This integrative coprodiagnostic protocol can be applied to other host–parasite systems, allowing researchers to study helminth infections in wild populations using a noninvasive approach.https://doi.org/10.1002/ece3.70564Cestodafecal egg countfish‐eating birdshelminthsmini‐FLOTACreal‐time qPCR |
| spellingShingle | Sofía Capasso Manuel Parejo José Manuel Reyes‐González Juan G. Navedo Ricardo Morán‐López José A. Masero Jorge S. Gutiérrez Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns Ecology and Evolution Cestoda fecal egg count fish‐eating birds helminths mini‐FLOTAC real‐time qPCR |
| title | Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns |
| title_full | Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns |
| title_fullStr | Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns |
| title_full_unstemmed | Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns |
| title_short | Noninvasive Methods Unveil the Trophic Transmission of the Tapeworm Ligula intestinalis in Gull‐Billed Terns |
| title_sort | noninvasive methods unveil the trophic transmission of the tapeworm ligula intestinalis in gull billed terns |
| topic | Cestoda fecal egg count fish‐eating birds helminths mini‐FLOTAC real‐time qPCR |
| url | https://doi.org/10.1002/ece3.70564 |
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