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Costs of Avian Malaria in Austral-Papuan Avifauna

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Costs of Avian Malaria in Austral-Papuan Avifauna Association of Avian Veterinarians Australasian Committee Ltd. Annual Conference 2016 pp 67-71 Costs of Avian Malaria in Australo-Papuan Avifauna Lee Peacock BSc (Vet) BVSc (Hons)1, Anders Gonçalves da Silva PhD2, Rohan Clarke PhD3 1. PhD Candidate Monash University 2. University of Melbourne 3. Monash University Clayton VIC 3800 Parkville. VIC. 2010. Wellington Rd. And Blackburn Rd. [email protected] Clayton. VIC. 3800 Introduction factors. These parasites are thus not detected evenly throughout their distribution; instead a mosaic pat- Avian malarial parasites are represented by a large tern nested within a general trend of higher diversity diversity of haemosporida within Plasmodiidae and and prevalence at lower altitudes and latitudes is ob- Haemoproteidae families. Other closely related hae- served (Mendes et al., 2005; Wood et al., 2007; Clark mosporida from Leukocytozoidae and Garniidae also et al., 2016). Large-scale migratory movements of infect birds and are often discussed under the um- avian hosts and near life-long infections mean these brella of avian malaria. Each family differs in life-cy- parasites can move within their avian hosts well be- cle, host and vector specificity, distribution, and yond current transmission zones, effectively expand- pathogenicity. ing their distribution. Avian malarial infections are described as acute, Avian malaria is associated with island bird extinc- chronic and abortive (Valkiunas 2004b; Valkiunas tions and can impose significant restrictions to avi- 2011). The acute phase is distinguished by a rising an distributions ( Warner 1968; van Riper III et al., parasitaemia, occurring after a latent or prepatent 1982). This is in stark contrast to evidence reveal- period following inoculation. This acute phase is ing avian hosts successfully completing large-scale often associated with the most overt clinical signs movements while infected (Bensch et al., 2007). including lethargy, dyspnoea, seizures, and death Some avian families, including penguins (Sphenis- (Valkiunas 2004c). Survivors of the acute phase go cidae) have shown particular susceptibility to avian on to carry the infections chronically at relatively low malaria, however this is not consistent for all species intensities and near life-long infections can occur and populations. The introduction of a known vec- (Bishop et al., 1938). Chronic avian malaria is asso- tor of Plasmodium relictum, Culex quinquefasciatus, ciated with a variety of costs. In addition to mortal- to the Galapagos Islands exposed the naïve island ity these include effects on investment in reproduc- avifauna to avian malaria (Whiteman et al., 2005). tion (Marzal et al., 2005) and immunity (Loiseau et Despite exposure evidenced by serological and mo- al., 2011; Dunn et al., 2013), sexual ornaments and lecular testing, clinical signs and parasitaemia were signaling (Hõrak et al., 2001; Bosholn et al., 2016), rarely observed in Galapagos Penguins (Palmer et and lifespan (Asghar et al., 2015). Abortive infections al., 2013). Predicting the effects of avian malaria in a are those detected with PCR without evidence of host is thus not a simple task. It is clear that the out- completing reproduction within the vertebrate host comes of infection with avian malaria are multifac- or vector and the outcomes of such infections can torial and dependent on a range of broad concepts range from minimal clinical signs to death ( Olias et such as host immunity and tolerance, exposure al., 2011; Cannell et al., 2013; Levin et al., 2013; Dim- dynamics, and parasite virulence. Costs are detect- itrov et al., 2015). ed disproportionately less frequently in wild popu- lations, possibly due to a sample bias towards less The distribution of avian malaria spans both transmis- affected individuals or through removal of affected sion and non-transmission zones. Transmission is the individuals by predation ( Bennett et al., 1993; Valki- result of complex interactions between avian hosts, unas 2004a). Much of what is known of avian malar- vectors, malarial organisms, and local environmental ia comes from the northern hemisphere, and of all www.aavac.com.au© 67 the continents, Australia stands out for its paucity of malarial organisms in north eastern Australia is de- avian malaria investigations (Clark et al., 2014). scribed, and baseline expectations of effects in natu- rally infected populations are determined. The Australian continent is expansive and provides an unbroken land bridge between the tropics and Sample and Data Collection temperate zones. Frequent continental avian move- ments connect avian populations on the mainland Birds were captured, sampled and released from and nearby islands (Griffioen and Clarke 2002), and communities in the north-western islands of TS and inter-continental migration further connects Austra- mainland FNQ in the years spanning 2006 and 2015. lia to Papua New Guinea and beyond into the North- Each bird was banded, provided with a unique ID, ern Hemisphere (Dingle 2008). Unsurprisingly, Aus- and blood was sampled. Blood and data from ap- tralia is host to a diverse population of avian malarial proximately 1000 birds were collected for this proj- organisms (Adlard et al., 2004; Beadall et al., 2004). ect. However studies of the effects and costs of these parasites in Australian avifauna are few. A single Aus- A broad approach was taken and numerous poten- tralian study has determined how the distribution tial indices were measured. These included: and diversity of avian malaria are associated with altitude, and simultaneously inferred costs by an as- $ Parasitaemia, prevalence, and infection in- sociation of avian species distributions with absence tensity: manual cell counts (parasites per of avian malaria and vectors (Zamora-Vilchis et al., 10,000 erythrocytes) and qPCR; 2012). Direct costs of avian malaria in Australian avi- $ Immunity investment: manual differential fauna are, however, limited to a handful of reports white cell counts (cells per 10,000 erythro- describing histological findings from sporadic mor- cytes); tality events of small groups or individuals (Peirce et $ Plasma biochemistry: Carotenoid concentra- al., 2004; Olias et al., 2011; Cannell et al., 2013). tion, VetScan VS2® Avian Reptile Profile Plus biochemistry profile (VetScan VS2® Chemis- Distributions of vector-borne diseases are not static try Analyzer, Abaxis, Inc.); and climate change is predicted to affect distribu- $ Visual signaling: plumage colour measured tions of avian malaria (Garamszegi 2011; Pérez-Ro- by photospectroscopy; and dríguez et al., 2014). Rising temperatures are ex- $ Body condition: body mass (scaled to skeletal pected to allow transmission at higher altitudes and size), body condition score (pectoral muscle latitudes, and evidence suggests changes are already mass). occurring (Loiseau et al., 2012; Atkinson et al., 2014). In Australia, avian malaria has been detected as far Results and Discussion south as Perth (Cannell et al., 2013), where it caused an outbreak in the local penguin population. It is Approximately 67% (n=900) of all birds sampled in unclear what role climate change had in aiding this TS were positive by PCR for avian malaria and a low- outbreak, but it is suggested that warmer than usual er prevalence, 37%, was detected in FNQ (n=104). ocean surface created ideal environments for vector Prevalence of malaria varied greatly between avian breeding. species, ranging from 0% to 98%, and infection in- tensity also differed significantly between species. There is no current understanding of the distributions Quick scans (scanning each slide for less than five of avian malaria lineages in Australian avifauna, nor minutes each) confirmed 69% of PCR positive birds, is there an understanding of host-parasite dynamics however the agreement increased as more time was for almost all the known malaria infecting Australian applied to each slide. The relationship between PCR/ avifauna. This project focuses on Australo-Papuan qPCR and microscopy agreement varied for different avifauna in tropical Far North Queensland (FNQ) avian hosts and malaria species. There was greatest and Torres Strait (TS) and includes data spanning agreement for Haemoproteus species, with agree- 10 years. This project is the first to investigate the ment reaching 100% for some avian species. The effects of avian malaria in an endemic transmission majority of malaria were haemoproteus lineages zone in wild Australian avifaunal populations. It in- and numerous novel lineages were detected. This is corporates ecological survey methods and veteri- consistent with previous work in northern and south nary tests and interpretation. By targeting tropical eastern Queensland (Adlard et al., 2004; Beadall et avian communities, the potential diversity of avian al., 2004). Prevalence was similar between dry and www.aavac.com.au© 68 wet seasons on Boigu Island, however infection in- References tensity was greatest in the wet season. Presumably this is associated with vector abundance, timing of Adlard, R.D., Peirce, M.A. and Lederer, R., 2004. Blood breeding, and other factors including seasonal mor- Parasites of birds from south-east Queensland. Emu. tality patterns. 104, 191-196. The communities from which these samples were Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, taken included active flying birds and so chronically Westerdahl H, Bensch S. 2015. Chronic infection. infected birds were expected to comprise the ma- Hidden costs of infection: chronic malaria
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