Volume 50, No. 1



Volumes > 38 (2010-->) Volumes 28-37 (2000-09) Volumes 18-27 (1990-99) Volumes 5-17 (1978-89)
a.k.a. Cormorant

Quick Search by author or article title:


No evidence of avian malaria in two Mediterranean endemic seabirds


Authors

LUCA ILAHIANE1*, FEDERICO DE PASCALIS2, DANILO PISU3, DAVID PALA4, FEDERICA FERRARIO5, MARCO CUCCO1, DIEGO RUBOLINI2, JACOPO G. CECERE6 & IRENE PELLEGRINO1

1University of Piemonte Orientale, Department of Sustainable Development and Ecological Transition (DiSSTE), 13100, Vercelli, Italy *(luca.ilahiane@uniupo.it)
2University of Milan, Department of Environmental Sciences and Policy, 20133, Milan, Italy
3Regione Pireddu Nieddu snc, 07040, Stintino, Italy
4Azienda Speciale Parco di Porto Conte, 07041, Alghero, Italy
5Ente Regionale per i Servizi all’Agricoltura e alle Foreste, ERSAF Lombardia, 20124, Milan, Italy
6Area BIO-AVM, Italian National Institute for Environmental Protection and Research ISPRA, 40064, Ozzano dell’Emilia, Italy


Received 23 August 2021, Accepted 22 October 2021

Date Published: 2022/04/15
Date Online: 2022/02/10


Download PDF

Citation

ILAHIANE, L., DE PASCALIS, F., PISU, D., PALA, D., FERRARIO, F., CUCCO, M., RUBOLINI, D., CECERE, J.G. & PELLEGRINO, I. 2022. No evidence of avian malaria in two Mediterranean endemic seabirds. Marine Ornithology 50: 13-17.


Key words: Aedes mariae, blood parasites, Calonectris diomedea, Haemoproteus, Haemosporidian, Hydrobates pelagicus, Leucocytozoon, Plasmodium


Abstract

In birds, pathogens and diseases, such as avian malaria, can have severe detrimental effects on individual fitness. Pathogen prevalence can vary across species and may differ between populations living in different localities, but screening can help to understand a disease's distribution and parasite-host interactions. Although seabirds generally exhibit low avian malaria infection patterns, blood parasites of several species and populations have never been investigated in detail. Using molecular techniques, we screened for blood parasites in two Mediterranean seabirds, the Scopoli's Shearwater Calonectris diomedea and the Mediterranean Storm Petrel Hydrobates pelagicus melitensis. In addition, we searched for and sampled potential vector insects at each seabird colony. DNA was extracted from blood samples (or whole specimens for vector insect species), and polymerase chain reaction was performed to assess the presence of Plasmodium, Haemoproteus, and Leucocytozoon, the most frequent infective protozoan genera. Our results showed no evidence of haemosporidians, either in the sampled species or in the vector insects. The low prevalence of parasites in these species could reflect the absence or rarity of the vector for transmission. Thus, extreme care must be taken when releasing individuals into the wild to avoid introducing infection into new seabird populations.


References

ASGHAR, M., HASSELQUIST, D., HANSSON, B., ZEHTINDJIEV, P., WESTERDAHL, H. & BENSCH, S. 2015. Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347: 436-438. doi:10.1126/science.1261121

ATKINSON, C.T., WOODS, K.L., DUSEK, R.J., SILEO, L. S. & IKO, W.M. 1995. Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111: S59-S69. doi:10.1017/s003118200007582x

BENSCH, S., HELLGREN, O. & PÉREZ‐TRIS, J. 2009. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9: 1353-1358. doi:10.1111/j.1755-0998.2009.02692.x

BENSCH, S., STJERNMAN, M., HASSELQUIST, D., HANNSON, B., WESTERDAHL, H. & PINHEIRO, R.T. 2000. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London. Series B: Biological Sciences 267: 1583-1589. doi:10.1098/rspb.2000.1181

BRIED, J., CÉLÉRIER, A., MAUREL, L. & BONADONNA, F. 2011. New haematological data in Cory's shearwater, Calonectris diomedea (Aves, Procellariiformes). Italian Journal of Zoology 78: 279-286. doi:10.1080/11250003.2010.544408

CAMPIONI, L., MARTÍNEZ-DE LA PUENTE, J., FIGUEROLA, J., GRANADEIRO, J.P., SILVA, M.C. & CATRY, P. 2018. Absence of haemosporidian parasite infections in the long-lived Cory's shearwater: evidence from molecular analyses and review of the literature. Parasitology Research 117: 323-329. doi:10.1007/s00436-017-5676-7

CLARK, N.J., CLEGG, S.M. & LIMA, M.R. 2014. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology 44: 329-338. doi:10.1016/j.ijpara.2014.01.004

DE PASCALIS, F., IMPERIO, S., BENVENUTI, A., CATONI, C., RUBOLINI, D. & CECERE, J.G. 2020. Sex-specific foraging behaviour is affected by wind conditions in a sexually size dimorphic seabird. Animal Behaviour 166: 207-218.

DE PASCALIS, F., PALA, D., PISU, D. ET AL. 2021. Searching on the edge: dynamic oceanographic features increase foraging opportunities in a small pelagic seabird. Marine Ecology Progress Series 668: 121-132.

DROVETSKI, S.V., AGHAYAN, S.A., MATA, V.A. ET AL. 2014. Does the niche breadth or trade‐off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Molecular Ecology 23: 3322-3329. doi:10.1111/mec.12744

EMMENEGGER, T., BENSCH, S., HAHN, S. ET AL. 2020. Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long-distance migratory passerine. Ecology and Evolution 11: 753-762. doi:10.1002/ece3.7030

ESPARZA, B., MARTÍNEZ-ABRAÍN, A., MERINO, S. & ORO, D. 2004. Immunocompetence and the prevalence of haematozoan parasites in two long-lived seabirds. Ornis Fennica 81: 40-46.

FECCHIO, A., CLARK, N. J., BELL, J. A. ET AL. 2021. Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecology and Biogeography 30: 2393-2406. doi:10.1111/geb.13390

FRIDOLFSSON, A.K. & ELLEGREN, H 1999. A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology 30: 116-121. doi:10.2307/3677252

FURNESS, R.W. 2012. Seabird Ecology. Berlin/Heidelberg, Germany: Springer Science & Business Media.

GERING, E. & ATKINSON, C.T. 2004. A rapid method for counting nucleated erythrocytes on stained blood smears by digital image analysis. Journal of Parasitology 90: 879­-881. doi:10.1645/GE-222R

GÓMEZ-DÍAZ, E., NAVARRO, J. & GONZÁLES-SOLÍS, J. 2008. Ectoparasite community structure on three closely related seabird hosts: a multiscale approach combining ecological and genetic data. Ecography 31: 477-489. doi:10.1111/j.0906-7590.2008.05330.x

GONZÁLES-SOLÍS, J. & ABELLA, J. C. 1997. Negative record of haematozoan parasites on Cory's Shearwater Calonetris diomedea. Ornis Fennica 74: 153-153.

HELLGREN, O., WALDENSTRÖM, J. & BENSCH, S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90: 797-802. doi:10.1645/GE-184R1

HERNANDEZ-TRIANA, L.M., BRUGMAN, V.A., NIKOLOVA, N.I. ET AL. 2019. DNA barcoding of British mosquitoes (Diptera, Culicidae) to support species identification, discovery of cryptic genetic diversity and monitoring invasive species. Zookeys 832: 57-76. doi:10.3897/zookeys.832.32257

ILAHIANE, L., BOANO, G., PAVIA, M. ET AL. 2021. Completing the genetic puzzle of the reed warbler complex: insights from Italy. Bird Study 67: 1-8. doi:10.1080/00063657.2021.1927980

INUMARU, M., MURATA, K. & SATO, Y. 2017. Prevalence of avian haemosporidia among injured wild birds in Tokyo and environs, Japan. International Journal for Parasitology: Parasites and Wildlife 6: 299-309. doi: 10.1016/j.ijppaw.2017.09.007

JIA, T., HUANG, X., VALKIŪNAS, G. ET AL. 2018 Malaria parasites and related haemosporidians cause mortality in cranes: a study on the parasites diversity, prevalence and distribution in Beijing Zoo. Malaria journal 17: 1-11.  doi:10.1186/s12936-018-2385-3

JOHNSON, P.T. & HOVERMAN, J. T. 2012. Parasite diversity and coinfection determine pathogen infection success and host fitness. Proceedings of the National Academy of Sciences 109: 9006-9011.

KOVATS, R.S., CAMPBELL-LENDRUM, D.H., MCMICHEL, A.J., WOODWARD, A. & COX, J.S. 2001. Early effects of climate change: do they include changes in vector-borne disease? Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356: 1057-1068. doi:10.1098/rstb.2001.0894

LARCOMBE, S.D. & GAUTHIER-CLERC, M. 2015. Avian malaria is absent in juvenile colonial herons (Ardeidae) but not Culex pipiens mosquitoes in the Camargue, Southern France. Waterbirds 38: 387-395.

LE GOFF, G, GOODMAN, S.M., ELGUERO, E. & ROBERT, V. 2014. Survey of the Mosquitoes (Diptera: Culicidae) of Mayotte. PLoS One 9: e100696. doi:10.1371/journal.pone.0100696

MARIANO, P.N. & DANTAS, G.P.M. 2021. Low prevalence of Plasmodium and Haemoproteus in resident seabirds from oceanic islands off the Brazilian coast. Marine Ornithology 49: 97-100.

MARTÍNEZ-ABRAÍN, A., ESPARZA, B. & ORO, D. 2004. Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all? Ardeola 51: 225-232.

MASTRANTONIO, V., PORRETTA, D., BELLINI, R., NASCETTI, G. & URBANELLI, S. 2015. Molecular systematics and origin of the mediterranean sea rock-pool mosquitoes of the Aedes mariae (Diptera: Culicidae) complex. Annals of the Entomological Society of America 108: 593-599. doi:10.1093/aesa/sav031

MERINO, S. & MINGUEZ, E. 1998. Absence of haematozoa in a breeding colony of the Storm Petrel Hydrobates pelagicus. Ibis 140: 180-181. doi:10.1111/j.1474-919X.1998.tb04560.x

MERINO, S., MORENO, J., JOSÉ SANZ, J. & ARRIERO, E. 2000. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London. Series B: Biological Sciences 267: 2507-2510. doi:10.1098/rspb.2000.1312

PELLEGRINO, I., CURLETTI, G., LIBERATORE, F. & CUCCO, M. 2017. Cryptic diversity of the jewel beetles Agrilus viridis (Coleoptera: Buprestidae) hosted on hazelnut. European Zoological Journal 84: 465-472. doi:10.1080/24750263.2017.1362050

PELLEGRINO, I., ILAHIANE, L., BOANO, G. ET AL. 2021. Avian haemosporidian diversity on Sardinia: a first general assessment for the Insular Mediterranean. Diversity 13: 75. doi:10.3390/d13020075

PEREZ-RODRIGUEZ, A., DE LA HERA, I., FERNANDEZ-GONZALEZ, S. & PEREZ-TRIS, J. 2014. Global warming will reshuffle the areas of high prevalence and richness of three genera of avian blood parasites. Global Change Biology 20: 2406-2416. doi:10.1111/gcb.12542

QUILLFELDT, P., ARRIERO, E., MARTÍNEZ, J., MASELLO, J. F. & MERINO, S. 2011. Prevalence of blood parasites in seabirds-a review. Frontiers in Zoology 8: 1-11. doi:10.1186/1742-9994-8-26

QUILLFELDT, P., MARTINEZ, J., BUGONI, L., MANCINI, P. L. & MERINO, S. 2014. Blood parasites in noddies and boobies from Brazilian offshore islands-differences between species and influence of nesting habitat. Parasitology 141: 399-410. doi:10.1017/S0031182013001649

QUILLFELDT, P., MARTÍNEZ, J., HENNICKE, J. ET AL. 2010. Hemosporidian blood parasites in seabirds—a comparative genetic study of species from Antarctic to tropical habitats. Naturwissenschaften 97: 809-817. doi:10.1007/s00114-010-0698-3

RICKLEFS, R.E., DODGE GRAY, J., LATTA, S.C. & SVENSSON-COELHO, M. 2011. Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles. Journal of Avian Biology 42: 570-584. doi:10.1111/j.1600-048X.2011.05404.x

SOARES, L., ESCUDERO, G., PENHA, V.A.S. & RICKLEFS, R.E. 2016. Low prevalence of haemosporidian parasites in shorebirds. Ardea 104: 129-141. doi:10.5253/arde.v104i2.a8

STEFAN, L.M., GÓMEZ-DÍAZ, E., ELGUERO, E., PROCTOR, H.C., MCCOY, K.D. & GONZÁLEZ-SOLÍS, J. 2015. Niche partitioning of feather mites within a seabird host, Calonectris borealis. PLoS One 10: e0144728. doi:10.1371/journal.pone.0144728

TELLA, J.T., GAJÓN, A., GORTÁZAR, C. & OSÁCAR, J.J. 1998. High host specificity of Crataerina melbae (Diptera: Hippoboscidae) in a mixed colony of birds. Journal of Parasitology 84: 198-200.

VALKIŪNAS, G. 2005. Avian malaria parasites and other Haemosporidia. New York, USA: CRC Press.

VALKIŪNAS, G., ILGŪNAS, M., BUKAUSKAITE, D. & IEZHOVA, T. 2016. Description of Haemoproteus ciconiae sp. nov. (Haemoproteidae, Haemosporida) from the white stork Ciconia, with remarks on insensitivity of established polymerase chain reaction assays to detect this infection. Parasitology Research 115: 2609-2616. doi:10.1007/s00436-016-5007-4

VANSTREELS, R.E.T., DE ANGELI DUTRA, D., SANTOS, A.P., HURTADO, R., EGERT, L. & BRAGA, E.M. 2020. First report of avian malaria in a Manx shearwater (Puffinus puffinus). Parasitology International 78: 102148. doi:10.1016/j.parint.2020.102148

WALDENSTRÖM, J., BENSCH, S., HASSELQUIST, D. & ÖSTMAN, Ö. 2004. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90: 191-194. doi:10.1645/GE-3221RN


© Marine Ornithology 2022