A citizen science-based survey of avian mortality focusing on haemosporidian infections in wild passerine birds

Abstract

Background Haemosporidioses are common in birds and their manifestations range from subclinical infections to severe disease, depending on the involved parasite and bird species. Clinical haemosporidioses are often observed in non-adapted zoo or aviary birds, whereas in wild birds, particularly passerines, haemosporidian infections frequently seem to be asymptomatic. However, a recent study from Austria showed pathogenic haemosporidian infections in common blackbirds due to high parasite burdens of Plasmodium matutinum LINN1, a common parasite in this bird species, suggesting that virulent infections also occur in natural hosts. Based on these findings, the present study aimed to explore whether and to what extent other native bird species are possibly affected by pathogenic haemosporidian lineages, contributing to avian morbidity. Methods Carcasses of passerine birds and woodpeckers were collected during a citizen science-based survey for avian mortality in Austria, from June to October 2020. Tissue samples were taken and examined for haemosporidian parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon by nested PCR and sequencing the mitochondrial cytb barcode region, histology, and chromogenic in situ hybridization applying genus-specific probes. Results From over 160 dead bird reportings, 83 carcasses of 25 avian species were submitted for investigation. Overall haemosporidian infection rate was 31%, with finches and tits prevailing species counts and infections. Sequence analyses revealed 17 different haplotypes (4 Plasmodium, 4 Haemoproteus, 9 Leucocytozoon), including 4 novel Leucocytozoon lineages. Most infected birds presented low parasite burdens in the peripheral blood and tissues, ruling out a significant contribution of haemosporidian infections to morbidity or death of the examined birds. However, two great tits showed signs of avian malaria, suggesting pathogenic effects of the detected species Plasmodium relictum SGS1 and Plasmodium elongatum GRW06. Further, exo-erythrocytic tissue stages of several haemosporidian lineages are reported. Conclusions While suggesting generally little contribution of haemosporidian infections to mortality of the investigated bird species, the findings indicate a possible role of certain haemosporidian lineages in overall clinical manifestation, either as main causes or as concurrent disease agents. Further, the study presents new data on exo-erythrocytic stages of previously reported lineages and shows how citizen science can be used in the field of haemosporidian research. Graphic abstract

A widespread survey of avian haemosporidia in deceased wild birds of Japan: the hidden value of personally collected samples

“…The vast majority of birds belonged to the order Passeriformes (84 birds), followed by Charadriiformes (12), Anseriformes (9), Columbiformes (8), and Gaviiformes (7). Birds were found across 23 prefectures of Japan, from the northernmost Hokkaido to the southernmost Okinawa Prefectures.…”

“…However, freezing is generally known to distort the tissue and may create artifacts, and therefore, frozen samples are not suitable for histopathological observations and preparations of impression smears. In a recent study, bird carcasses were collected in Austria through a citizen science project [ 12 ]. The study aimed to assess avian mortality and its relationship to avian haemosporidian infection through histopathological examinations, and hence, citizen scientists were advised to store the birds in a cool place until the birds are picked up.…”

Exo-erythrocytic development of Plasmodium matutinum (lineage pLINN1) in a naturally infected roadkill fieldfare Turdus pilaris

“…Plasmodium matutinum (pLINN1) lineage is common in wild birds in Austria [ 4 , 13 ] and pathogenic for local endemic birds in New Zealand [ 12 , 52 ], where it was probably introduced together with their Turdus host species. The same lineage was recently reported to cause lethal malaria in captive African penguins Spheniscus demersus and Lovebirds Agapornis roseicolli in Italy [ 37 , 53 ], and Atlantic puffins Fratercula arctica in Switzerland [ 54 ].…”

“…However, information on an important part of the life cycle of malaria parasites and related haemosporidians (Haemosporida)–the exo-erythrocytic development–still remains at an early stage. This is particularly true for wild birds due to the difficulties in accessing these stages for research, which requires animal dissection, direct investigation of organs and application of histologic techniques [ 3 , 4 ].…”

“…However, most experimental studies deal with non-adapted host-parasite associations, which could bias the understanding of the true virulence of the same pathogen in natural populations. Information on the exo-erythrocytic development of haemosporidian parasites in naturally infected birds would be a valuable supplement to experimental observations, but currently remains insufficient in wildlife [ 4 , 12 , 13 ]. This study provides first information on a natural infection with Plasmodium matutinum (genetic lineage pLINN1) in a wild fieldfare ( Turdus pilaris ).…”