Haemosporidian Parasites of White-Breasted Waterhens (Amaurornis phoenicurus), with a Report and Molecular Characterization of Haemoproteus gallinulae in Thailand
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Sites and Sample Collection
2.2. Staining and Microscopic Examination
2.3. DNA Extraction and Mitochondrial Cytochrome b Gene Amplification
2.4. Phylogenetic Analyses of the Partial Cytochrome b Gene Sequences
2.5. Statistical Analysis
3. Results
3.1. Morphological Characterization of Haemoproteus gallinulae de Mello, 1935 from Amaurornis phoenicurus in Thailand
3.2. Phylogenetic Relationships between Haemosporidian Parasites
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Valkiunas, G. Avian Malaria Parasites and Other Haemosporidia, 1st ed.; CRC Press: Boca Raton, FL, USA, 2004. [Google Scholar]
- Sol, D.; Jovani, R.; Torres, J. Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 2003, 135, 542–547. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Longoria, L.; Palinauskas, V.; Ilgūnas, M.; Valkiūnas, G.; Hellgren, O. Differential gene expression of Plasmodium homocircumflexum (lineage pCOLL4) across two experimentally infected passerine bird species. Genomics 2020, 112, 2857–2865. [Google Scholar] [CrossRef] [PubMed]
- Marzal, A.; Reviriego, M.; Hermosell, I.G.; Balbontín, J.; Bensch, S.; Relinque, C.; Rodríguez, L.; Garcia-Longoria, L.; de Lope, F. Malaria infection and feather growth rate predict reproductive success in house martins. Oecologia 2013, 171, 853–861. [Google Scholar] [CrossRef]
- Coon, C.A.C.; Garcia-Longoria, L.; Martin, L.B.; Magallanes, S.; de Lope, F.; Marzal, A. Malaria infection negatively affects feather growth rate in the house sparrow Passer domesticus. J. Avian Biol. 2016, 47, 779–787. [Google Scholar] [CrossRef]
- Palinauskas, V.; Žiegytė, R.; Ilgūnas, M.; Iezhova, T.A.; Bernotienė, R.; Bolshakov, C.; Valkiūnas, G. Description of the first cryptic avian malaria parasite, Plasmodium homocircumflexum n. sp., with experimental data on its virulence and development in avian hosts and mosquitoes. Int. J. Parasitol. 2015, 45, 51–62. [Google Scholar] [CrossRef]
- Gulliver, E.; Hunter, S.; Howe, L.; Castillo-Alcala, F. The pathology of fatal avian malaria due to Plasmodium elongatum (GRW6) and Plasmodium matutinum (LINN1) infection in New Zealand kiwi (Apteryx spp.). Animals 2022, 12, 3376. [Google Scholar] [CrossRef]
- Schumm, Y.R.; Metzger, B.; Neuling, E.; Austad, M.; Galea, N.; Barbara, N.; Quillfeldt, P. Year-round spatial distribution and migration phenology of a rapidly declining trans-Saharan migrant—Evidence of winter movements and breeding site fidelity in European turtle doves. Behav. Ecol. Sociobiol. 2021, 75, 152. [Google Scholar] [CrossRef]
- Zehtindjiev, P.; Križanauskienė, A.; Bensch, S.; Palinauskas, V.; Asghar, M.; Dimitrov, D.; Scebba, S.; Valkiūnas, G. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J. Parasitol. 2012, 98, 657–665. [Google Scholar] [CrossRef]
- Round, P. Checklist of the Birds of Thailand. Available online: https://www.thaibirding.com/book_reviews/roundlist.htm (accessed on 13 July 2020).
- Kumar, P.; Gupta, S.K. Diversity and abundance of wetland birds around Kurukshetra, India. Our Nat. 2009, 7, 212–217. [Google Scholar] [CrossRef] [Green Version]
- Bhaibulaya, M.; Indra-Ngarm, S.; Ananthapruti, M. Freshwater fishes of Thailand as experimental intermediate hosts for Capillaria philippinensis. Int. J. Parasitol. 1979, 9, 105–108. [Google Scholar] [CrossRef]
- Yoshino, T.; Uemura, J.; Endoh, D.; Kaneko, M.; Osa, Y.; Asakawa, M. Parasitic nematodes of anseriform birds in Hokkaido, Japan. Helminthologia 2009, 46, 117–122. [Google Scholar] [CrossRef] [Green Version]
- Jaafar, N.; Babjee, M.A. Parasites of the White-Breasted Waterhen (Amaurornis phoenicurus); Universiti Putra Malaysia: Serdang, Malaysia, 2011. [Google Scholar]
- Bennett, G.F. Avian Haemoproteidae. 14. The haemoproteids of the avian family Rallidae. Can. J. Zool. 1980, 58, 321–325. [Google Scholar] [CrossRef]
- Prompiram, P.; Kaewviyudth, S.; Sukthana, Y.; Rattanakorn, P. Study of morphological characteristic and prevalence of haemoproteus blood parasite in passerines in bung Boraphet. Thai J. Vet. Med. 2015, 45, 399–409. [Google Scholar]
- Valkiūnas, G.; Iezhova, T.A. Keys to the avian Haemoproteus parasites (Haemosporida, Haemoproteidae). Malar. J. 2022, 21, 269. [Google Scholar] [CrossRef] [PubMed]
- Godfrey, R.D., Jr.; Fedynich, A.M.; Pence, D.B. Quantification of hematozoa in blood smears. J Wildl. Dis. 1987, 23, 558–565. [Google Scholar] [CrossRef]
- Clark, P.; Boardman, W.; Raidal, S. Atlas of Clinical Avian Hematology; Wiley: Hoboken, NJ, USA, 2009. [Google Scholar]
- Waldenström, J.; Bensch, S.; Hasselquist, D.; Ostman, O. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J. Parasitol. 2004, 90, 191–194. [Google Scholar] [CrossRef]
- Hall, T.A. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT; Nucleic Acids Symposium Series; Information Retrieval Ltd.: London, UK, 1999; pp. 95–98. [Google Scholar]
- Rozas, J.; Ferrer-Mata, A.; Sánchez-DelBarrio, J.C.; Guirao-Rico, S.; Librado, P.; Ramos-Onsins, S.E.; Sánchez-Gracia, A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 2017, 34, 3299–3302. [Google Scholar] [CrossRef]
- Bensch, S.; Hellgren, O.; Pérez-Tris, J. Malavi MalAvi: A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol. Ecol. Resour. 2009, 9, 1353–1358. [Google Scholar] [CrossRef]
- Katoh, K.; Rozewicki, J.; Yamada, K.D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019, 20, 1160–1166. [Google Scholar] [CrossRef] [Green Version]
- Ronquist, F.; Huelsenbeck, J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19, 1572–1574. [Google Scholar] [CrossRef] [Green Version]
- Nylander, J.A.A. MrModelTest v2. Program Distributed by the Author: Evolutionary Biology Centre; Uppsala University: Uppsala, Sweden, 2004. [Google Scholar]
- Rambout, A. FigTree: Tree Figure Drawing Tool, Version 1.4.0. Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 18 September 2020).
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Jukes, T.H.; Cantor, C.R. Evolution of Protein Molecules; Academic Press: New York, NY, USA, 1969. [Google Scholar]
- Van Hoesel, W.; Marzal, A.; Magallanes, S.; Santiago-Alarcon, D.; Ibáñez-Bernal, S.; Renner, S.C. Management of ecosystems alters vector dynamics and haemosporidian infections. Sci. Rep. 2019, 9, 8779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davis, A.K.; Maney, D.L.; Maerz, J.C. The use of leukocyte profiles to measure stress in vertebrates: A review for ecologists. Funct. Ecol. 2008, 22, 760–772. [Google Scholar] [CrossRef]
- Gross, W.B.; Siegel, H.S. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 1983, 27, 972–979. [Google Scholar] [CrossRef] [PubMed]
- Maxwell, M.H. Avian blood leucocyte responses to stress. Worlds Poult. Sci. J. 1993, 49, 34–43. [Google Scholar] [CrossRef]
- Sacchi, L.; Prigioni, C. Haematozoa of Italian birds. II. First European record of Haemoproteus gallinulae de Mello, 1935. In Gallinula chloropus and Redescription (Apicomplexa Haemosporina); Atti della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale: Milano, Italy, 1986; Volume 127, pp. 27–32. [Google Scholar]
- Valkiūnas, G.; Santiago-Alarcon, D.; Levin, I.I.; Iezhova, T.A.; Parker, P.G. A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. J. Parasitol. 2010, 96, 783–792. [Google Scholar] [CrossRef] [PubMed]
- Bertram, M.R.; Hamer, S.A.; Hartup, B.K.; Snowden, K.F.; Medeiros, M.C.; Outlaw, D.C.; Hamer, G.L. A novel Haemosporida clade at the rank of genus in North American cranes (Aves: Gruiformes). Mol. Phylogenet. Evol. 2017, 109, 73–79. [Google Scholar] [CrossRef]
- Musa, S.; Mackenstedt, U.; Woog, F.; Dinkel, A. Untangling the actual infection status: Detection of avian haemosporidian parasites of three Malagasy bird species using microscopy, multiplex PCR, and nested PCR methods. Parasitol. Res. 2022, 121, 2817–2829. [Google Scholar] [CrossRef] [PubMed]
- Valkiūnas, G.; Ilgūnas, M.; Bukauskaitė, D.; Duc, M.; Iezhova, T.A. Description of Haemoproteus asymmetricus n. sp. (Haemoproteidae), with remarks on predictability of the DNA haplotype networks in haemosporidian parasite taxonomy research. Acta Trop. 2021, 218, 105905. [Google Scholar] [CrossRef]
- Levin, I.I.; Valkiūnas, G.; Iezhova, T.A.; O’Brien, S.L.; Parker, P.G. Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. J. Parasitol. 2012, 98, 847–854. [Google Scholar] [CrossRef]
- Levin, I.I.; Valkiūnas, G.; Santiago-Alarcon, D.; Cruz, L.L.; Iezhova, T.A.; O’Brien, S.L.; Hailer, F.; Dearborn, D.; Schreiber, E.A.; Fleischer, R.C.; et al. Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: Evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Int. J. Parasitol. 2011, 41, 1019–1027. [Google Scholar] [CrossRef] [PubMed]
- Beadell, J.S.; Gering, E.; Austin, J.; Dumbacher, J.P.; Peirce, M.A.; Pratt, T.K.; Atkinson, C.T.; Fleischer, R.C. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol. Ecol. 2004, 13, 3829–3844. [Google Scholar] [CrossRef]
- Silva-Iturriza, A.; Ketmaier, V.; Tiedemann, R. Profound population structure in the Philippine Bulbul Hypsipetes philippinus (Pycnonotidae, Aves) is not reflected in its Haemoproteus haemosporidian parasite. Infect. Genet. Evol. 2012, 12, 127–136. [Google Scholar] [CrossRef]
- Platonova, E.; Aželytė, J.; Iezhova, T.; Ilgūnas, M.; Mukhin, A.; Palinauskas, V. Experimental study of newly described avian malaria parasite Plasmodium (Novyella) collidatum n. sp., genetic lineage pFANTAIL01 obtained from South Asian migrant bird. Malar. J. 2021, 20, 82. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Tris, J.; Hellgren, O.; Krizanauskiene, A.; Waldenström, J.; Secondi, J.; Bonneaud, C.; Fjeldså, J.; Hasselquist, D.; Bensch, S. Within-host speciation of malaria parasites. PLoS ONE 2007, 2, e235. [Google Scholar] [CrossRef]
- Harl, J.; Himmel, T.; Valkiūnas, G.; Ilgūnas, M.; Nedorost, N.; Matt, J.; Kübber-Heiss, A.; Alic, A.; Konicek, C.; Weissenböck, H. Avian haemosporidian parasites of accipitriform raptors. Malar. J. 2022, 21, 14. [Google Scholar] [CrossRef]
- Harl, J.; Himmel, T.; Valkiūnas, G.; Weissenböck, H. The nuclear 18S ribosomal DNAs of avian haemosporidian parasites. Malar. J. 2019, 18, 305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Musa, S.; Mackenstedt, U.; Woog, F.; Dinkel, A. Avian malaria on Madagascar: Prevalence, biodiversity and specialization of haemosporidian parasites. Int. J. Parasitol. 2019, 49, 199–210. [Google Scholar] [CrossRef]
- Vanstreels, R.E.T.; Gardiner, C.H.; Yabsley, M.J.; Swanepoel, L.; Kolesnikovas, C.K.M.; Silva-Filho, R.P.; Ewbank, A.C.; Catão-Dias, J.L. Schistosomes and microfilarial parasites in Magellanic penguins. J. Parasitol. 2018, 104, 322–328. [Google Scholar] [CrossRef]
- Palinauskas, V.; Žiegytė, R.; Iezhova, T.A.; Ilgūnas, M.; Bernotienė, R.; Valkiūnas, G. Description, molecular characterisation, diagnostics and life cycle of Plasmodium elongatum (lineage pERIRUB01), the virulent avian malaria parasite. Int. J. Parasitol. 2016, 46, 697–707. [Google Scholar] [CrossRef]
- Ejiri, H.; Sato, Y.; Kim, K.S.; Tamashiro, M.; Tsuda, Y.; Toma, T.; Miyagi, I.; Murata, K.; Yukawa, M. First record of avian Plasmodium DNA from mosquitoes collected in the Yaeyama Archipelago, southwestern border of Japan. J. Vet. Med. Sci. 2011, 73, 1521–1525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Haemosporidian Infection Status | ||
---|---|---|
Negative (n = 4) | Positive (n = 6) | |
WBC (×10³ cells/mm³) | 5.2 (3.9–6.6) | 7.2 (6.2–8.4) |
Heterophils (%) | 59.3 (54.0–67.0) | 64.8 (53.0–74.0) |
Lymphocytes (%) | 37.3 (23.0–44.0) | 31.3 (21.0–44.0) |
Monocytes (%) | 3.5 (1.0–10.0) | 3.8 (2.0–8.0) |
H:L ratio | 1.7 (1.2–2.9) | 2.3 (1.2–3.5) |
Measurements | Uninfected Erythrocyte | Macrogametocyte | Microgametocyte | |||
---|---|---|---|---|---|---|
(n = 28) | (n = 37) | (n = 28) | ||||
Range | Mean ± SD | Range | Mean ± SD | Range | Mean ± SD | |
Erythrocyte | ||||||
Length | 13.49–12.13 | 13.02 ± 0.38 | 12.59–15.92 | 14.29 ± 0.73 | 12.84–15.86 | 14.27 ± 0.78 |
Width | 8.14–6.52 | 7.28 ± 0.44 | 6.36–8.48 | 7.68 ± 0.54 | 6.80–8.54 | 7.65 ± 0.47 |
Area | 83.42–66.34 | 74.29 ± 4.97 | 74.42–101.11 | 86.99 ± 6.39 | 76.73–97.88 | 85.71 ± 5.88 |
Erythrocyte nucleus | ||||||
Length | 5.1–6.59 | 5.77 ± 0.35 | 5.00–6.46 | 5.66 ± 0.36 | 4.49–6.37 | 5.64 ± 0.44 |
Width | 2.67–3.72 | 3.02 ± 0.21 | 2.35–3.18 | 2.78 ± 0.19 | 2.22–3.21 | 2.78 ± 0.23 |
Area | 10.8–16.28 | 14.21 ± 1.17 | 11.58–16.16 | 13.58 ± 1.14 | 10.56–17.61 | 13.41 ± 1.64 |
NDR * | - | - | 0.11–0.92 | 0.48 ± 0.22 | 0.31–0.98 | 0.62 ± 0.16 |
Gametocyte | ||||||
Length | - | - | 12.22–15.27 | 13.61 ± 0.78 | 12.08–15.02 | 13.16 ± 0.80 |
Width | - | - | 2.16–5.30 | 3.66 ± 0.59 | 2.57–4.12 | 3.28 ± 0.38 |
Area | - | - | 41.12–67.75 | 56.19 ± 6.88 | 39.47–61.55 | 49.69 ± 5.34 |
Pigment granules | - | - | 13–40 | 29.89 ± 5.79 | 17–27 | 21.70 ± 2.70 |
Gametocyte nucleus | ||||||
Length | - | - | 2.08–5.26 | 3.33 ± 0.79 | 4.52–8.56 | 6.46 ± 0.94 |
Width | - | - | 1.92–4.03 | 2.86 ± 0.40 | 1.81–3.71 | 2.79 ± 0.46 |
Area | - | - | 5.16–12.45 | 8.14 ± 1.76 | 10.45–20.08 | 15.47 ± 2.78 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Prompiram, P.; Poltep, K.; Chaisilp, N.; Chakritbudsabong, W.; Buamas, S.; Rungarunlert, S. Haemosporidian Parasites of White-Breasted Waterhens (Amaurornis phoenicurus), with a Report and Molecular Characterization of Haemoproteus gallinulae in Thailand. Animals 2023, 13, 2006. https://doi.org/10.3390/ani13122006
Prompiram P, Poltep K, Chaisilp N, Chakritbudsabong W, Buamas S, Rungarunlert S. Haemosporidian Parasites of White-Breasted Waterhens (Amaurornis phoenicurus), with a Report and Molecular Characterization of Haemoproteus gallinulae in Thailand. Animals. 2023; 13(12):2006. https://doi.org/10.3390/ani13122006
Chicago/Turabian StylePrompiram, Phirom, Kanaporn Poltep, Nattarun Chaisilp, Warunya Chakritbudsabong, Supakit Buamas, and Sasitorn Rungarunlert. 2023. "Haemosporidian Parasites of White-Breasted Waterhens (Amaurornis phoenicurus), with a Report and Molecular Characterization of Haemoproteus gallinulae in Thailand" Animals 13, no. 12: 2006. https://doi.org/10.3390/ani13122006
APA StylePrompiram, P., Poltep, K., Chaisilp, N., Chakritbudsabong, W., Buamas, S., & Rungarunlert, S. (2023). Haemosporidian Parasites of White-Breasted Waterhens (Amaurornis phoenicurus), with a Report and Molecular Characterization of Haemoproteus gallinulae in Thailand. Animals, 13(12), 2006. https://doi.org/10.3390/ani13122006