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SHORT COMMUNICATION |
nas1,3,5
1 Institute of Ecology, Vilnius University, Akademijos 2, Vilnius 21, LT-08412, Lithuania;
2 Department of Biology, San Francisco State University, 1600 Holloway Ave., San Francisco, California, 94132, USA;
3 Center for Tropical Research, Institute of the Environment, University of California, Los Angeles, 1365 Hershey Hall, P.O. Box 95 1496, Los Angeles, California 90095-1496, USA;
4 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095-1606, USA
5 Corresponding author (email: gedvalk{at}ekoi.lt)
ABSTRACT:
Birds from three National Parks (Bwindi Impenetrable, Kibale, and Queen Elizabeth) in western Uganda were surveyed during the dry season in July 2003 and investigated for hematozoa by microscopic examination of stained blood films. Of 307 birds examined, representing 68 species of 15 families and four orders, 61.9% were found to be infected with blood parasites. Species of Haemoproteus (15.3% prevalence), Plasmodium (20.5%), Leucocytozoon (40.1%), Trypanosoma (11.4%), Hepatozoon (2.6%), Atoxoplasma (0.3%), and microfilariae (3.9%) were recorded. Except for Haemoproteus spp. infections, the overall prevalence of hematozoa belonging to all genera was significantly higher in this study than was previously reported in Uganda. Thirty-six species of birds were examined for blood parasites for the first time and 112 new host-parasite associations were identified. Eighty-one were at the generic and 31 at the specific level of the hematozoa. Hepatozoon and Atoxoplasma spp. were detected for the first time in Uganda.
Key words: Atoxoplasma, avian hematozoa, Haemoproteus, Hepatozoon, Leucocytozoon, microfilariae, Plasmodium, Trypanosoma, Uganda.
Although numerous surveys have been conducted on the hematozoa of sub-Saharan African birds (Bennett et al., 1992a; Valkinas, 2005), some areas of the Ethiopian zoogeographical region remain insufficiently studied. Relatively little is known about blood parasites of wild birds from Uganda, a country of particular interest because of its diverse endemic avifauna that is threatened by severe deforestation (Sekercioglu, 2002). Hoare (1932) sampled 17 bird species in Uganda and reported a Plasmodium sp. infection in only one specimen of the common stonechat (Saxicola torquata). Two extensive studies were carried out on blood parasites of wild birds on the Entebbe Peninsula (EP) in Uganda (Bennett et al., 1974, 1977). Of 1,998 birds investigated, 31% were found to be infected with blood parasites. Interestingly, Haemoproteus spp. represented 91% of all detected infections of hemosporidian parasites. The prevalences of infections of birds with species of Plasmodium, Leucocytozoon, Trypanosoma, and microfilariae were recorded to be less than 2% for the representatives of each genus. However, these blood parasites are common in other countries of sub-Saharan Africa (Bennett et al., 1992a). Dranzoa et al. (1999) reported an unidentified species of Haemoproteus (76% prevalence) and Plasmodium (29%) in the rock pigeon (Columba livia) in Kampala. The distribution of avian blood parasites in other regions of Uganda has not yet been investigated. Our objectives here were to further study the avian hematozoa of Uganda by providing the first documentation on the occurrence and peculiarities of distribution of these parasites in western regions of this country.
Between 12 July and 25 July 2003 (the dry season), blood smears of 307 birds (55 males, 52 females, and 200 of unidentified sex) of 68 species belonging to 15 families and four orders were collected for the presence of blood parasites (Table 1
). All birds sampled are known to be year-round residents. Among these birds were 18 specimens of <1 yr old (young birds), 288 specimens of >1 yr old (adult birds), and one specimen of unidentified age. The sex and age of each bird was determined according to Stevenson and Fanshawe (2002). Birds were caught with mist nets between daybreak (6:00 AM) and dusk (5:00 PM). They were ringed, bled, and released. None of them were recaptured. The blood was taken by puncturing the brachial vein. Three blood films were prepared from each bird. Blood films were air dried within 5–10 sec after their preparation. In humid environments, we used a battery-operated fan to aid in the drying of the blood films. Slides were fixed in methanol in the field and then stained with Giemsa in the laboratory. Blood films were examined for 10–15 min at low magnification (400x) and then at least 100 fields were studied at high magnification (1,000x). Intensity of infection was estimated as a percentage by actual counting of the number of parasites per 1,000 red blood cells or per 10,000 red blood cells if infections were light (i.e., <0.1%), as recommended by Godfrey et al. (1987). Species of Trypanosoma and hemosporidian parasites were identified according to the reviews by Baker (1976) and Valkinas (2005), in which illustrations of all species of parasites mentioned in this article are given.
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In BINP, the study site situated along a mountain ridge consisted of dense, moist, evergreen, montane forest close to mountain marshes and secondary growth vegetation along permanent small, clean streams. The annual mean temperature range is 7–15 C minimum to 20–27 C maximum; annual precipitation lies in the range 1,130–2,390 mm. In KNP, the study site was moist evergreen forest with permanent small, clean streams. The forest is a mixture of pure forest stands and successional grassland, swamp forests, and secondary forests. The mean annual precipitation is approximately 1,740 mm. The annual mean temperature ranges between 16.2 C and 23.3 C. In QENP, the study site was located on a peninsular separating the Kazinga Channel from Lake Edward. The habitat was a mixture of open dry grassland and small patches of secondary bushes. Permanent streams were not present. The mean annual precipitation is approximately 1,000 mm. The annual mean temperature ranges between 18.0 C and 28.0 C (Sekercioglu, 2002; Zhou et al., 2004).
Prevalences of infections were compared by Yates corrected 
2 test. A P
0.05 was considered significant.
The overall prevalence of blood parasites was 61.9% (Table 1
). Species of Haemoproteus, Plasmodium, Leucocytozoon, Trypanosoma, Hepatozoon, Atoxoplasma, and microfilariae were recorded. A number of the infections (40.5% of all positive birds) were mixed infections with parasites from two to four genera present in the infected birds. Over 80% of all recorded infections were light (<0.1%) and could be regarded as chronic. There was no significant difference in the prevalence or intensity of hematozoa between males or females or between young or adult birds.
Identification of species of hemosporidians was possible when the intensity of infection was >0.01% and when fully grown parasites were present in blood films. Fifteen species of hematozoa were identified (Table 2). Representative blood slides were deposited in the Institute of Ecology, Vilnius University, Vilnius, Lithuania.
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). It is worth noting that species of Leucocytozoon were not seen and species of Plasmodium and Trypanosoma were not prevalent in QENP, but these parasites were frequently recorded in both BINP and KNP. This is probably because the former is much drier and has no permanent streams and thus limits mosquito (Culicidae) activity and habitat for immature simuliid flies (Simuliidae). The mosquitoes and simuliid flies are vectors of avian Plasmodium and Leucocytozoon spp., respectively (Valkinas, 2005). These blood-sucking dipterans also transmit avian trypanosomes (Baker, 1976).
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Sample sizes of the little greenbul (Andropadus virens) and olive sunbird (Nectarinia olivacea) were sufficient to compare prevalences of blood parasites in different species of avian hosts at the same study sites. There was no significant difference in the overall prevalence of infection and the prevalence of Leucocytozoon spp. and microfilarial infections between these bird species in KNP. The species of Haemoproteus, Plasmodium, and Trypanosoma were significantly more prevalent in the olive sunbird than in the little greenbul at this study site (P=0.05, P<0.01, and P<0.05, respectively). It is probable that the olive sunbird is an attractive host for vectors of these hematozoa.
The overall prevalence of hematozoa in this study was two times greater than had been formerly recorded in wild birds from the EP in southern Uganda (Bennett et al., 1974, 1977). We recorded a significantly greater prevalence of infection in western Uganda than had been previously detected around EP for Plasmodium spp. (1% prevalence was detected around the EP), Leucocytozoon spp. (2%), and Trypanosoma spp. (1%). However, the overall prevalence of Haemoproteus spp. infection was greater at EP (28%) than in our sites.
We sampled birds only during the dry season, whereas Bennett et al. (1974, 1977) sampled birds throughout the year over a period of 6 years. They found no significant differences in the overall prevalence of hematozoan infections in birds collected during wet and dry seasons or in different years. Thus, the prevalence of blood parasites in birds collected around EP was relatively stable. Therefore, the differences in prevalence of hematozoa around EP and in western Uganda during this study probably cannot be explained by differences due to the season of investigation. These differences are perhaps due to differences in the transmission of hematozoa in these different regions of Uganda.
There is presently no published information regarding the vectors that transmit the avian blood parasites of Uganda. In addition, few studies have reported on the vectors of the blood parasites of birds in sub-Saharan Africa (Fallis et al., 1973; Crewe, 1975; Huchzermeyer, 1993). The limited information concerning the insect vectors in Africa remains one of the main obstacles to understanding the dynamics of transmission of avian blood parasites in Uganda.
According to Bennett et al. (1974, 1977) and this study, blood parasites are present in birds at all study sites in Uganda. Because the resident year-round birds were infected at each study site, it is probable that the transmission of representatives of all recorded genera of blood parasites takes place throughout the country.
Atoxoplasma and Hepatozoon spp. have been frequently recorded in birds all over the world, including African countries (Levine, 1982; Bennett et al., 1992b). These parasites are reported for the first time in Ugandan birds in this study. Six of the eight recorded Hepatozoon spp. infections were found in the yellow-whiskered greenbul (Table 1). Because Hepatozoon spp. are transmitted among avian hosts by means of eating infected arthropods (Bennett et al., 1992b), investigations on the feeding behavior of the yellow-whiskered greenbul may be helpful to elucidate a possible invertebrate host of Hepatozoon spp. in Uganda.
In all, 36 species of birds (Table 1) were examined for hematozoa for the first time and 46 for the first time in Uganda during this study (Bennett et al., 1974, 1977, 1992a; Valkinas, 2005). Twelve new host records for Haemoproteus spp., 20 for Plasmodium spp., 25 for Leucocytozoon spp., 11 for Trypanosoma spp., three for Hepatozoon spp., one for Atoxoplasma spp., and nine for microfilariae are reported in this study (Table 1).
The diversity of hematozoa recorded in this work is typical for African birds and the most parasitized birds belong to families typically heavily infected in sub-Saharan Africa (Bennett et al., 1992a). The great majority of species of blood parasites recorded in this study (Table 2) are found throughout the Old World (Valkinas, 2005). The detection of these parasites in Ugandan birds is thus not unexpected. Further field studies, supplemented by experimental work on vectors, and studies on the epidemiology, virulence, and molecular phylogenetics of the parasites are needed to explain the peculiarities of the distribution of hematozoa and to determine their significance in Uganda and other sub-Saharan countries.
We wish to thank Christine Dranzoa and John Kasenene, Makerere University, Kampala, Uganda, for their advice and help in organizing our work in Uganda. Adam Freedman and Joseph Kamanyire are gratefully acknowledged for help in the field. We are grateful to the Uganda Wildlife Authority for the opportunity to perform this study, which was supported by the NATO Collaborative Linkage Grant and the Lithuanian State Science and Studies Foundation. R.N.M.S. was supported in part by a NIGMS MORE Institutional Research and Academic Career Development Award to UC Davis and San Francisco State University, grant K12GM00679. The research was also supported by the NSF-NIH Ecology of Infectious Diseases Program grant EF-0430146 awarded to R.N.M.S. and T.B.S.
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Received for publication 6 August 2004.
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