Blood parasites in some birds from eastern plains of Colombia

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Blood Parasites in Some Birds from Eastern Plains of Colombia

Vol. 96(8): 1173-1176, November 2001

Oscar A Rodríguez, Nubia E Matta⁺

Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Calle 181a No. 28-54 Int. 1, Apto 403, Bogotá, Colombia

A total of 315 birds representing 75 species (23 families) from Villavicencio and San Miguel (Meta, Colombia) were examined for haematozoa. Fifty birds (15.9%) harbored blood parasites. Microfilariae were the most common haematozoans encountered, followed by species of the genera Haemoproteus, Plasmodium and Trypanosoma. This survey included 15 new host-parasite records and 8 species of birds that were examined for haematozoa for the first time. The prevalence registered in this research was similar to others recorded in the Neotropical region, but in sharp contrast with the prevalence of blood parasites in other major land masses.

Key words: birds - haematozoa - Colombia

Although the ornithological fauna of Colombia is among the most diverse of the world, the blood parasites of this avifauna have had only limited study. Blood parasites of Colombian birds have been recorded in a few small surveys, carried out by Renjifo et al. (1952), Bennett and Borrero (1976) and Ayala et al. (1977). The purpose of this study was to record the prevalence of blood parasites in some birds from the eastern plains of Colombia, giving new directions for research into the epizootiology of hematozoan infections in Colombian birds. This report summarizes and briefly discusses the results of this survey and compares the obtained results with those previously recorded by Renjifo et al. (1952).

Birds were collected from two sites in the Meta Department, eastern plains of Colombia, from June to September 1999. The first was in the Jardín Botánico de Villavicencio: (73°39' W; 4°0.9' N), at an elevation of 640 m above sea level, with a mean annual temperature of 26°C and an annual rainfall close to 2,500-3,000 mm. The area is a second growth tropical rainforest and contained patches of 20-30 m tall forest. The second site was in Fundación Yamato; San Miguel, (71° 31' W; 4°31' N). The area is about 130 m above sea level, with an annual temperature of 28.7°C and an annual rainfall of 2,000 mm. The vegetation is dominated by dry savanna and gallery forests.

The birds were mist-netted. Three thin smears from each of 315 birds were made from blood obtained by toenail clip. Smears were fixed in 100% methanol and stained with Giemsa stain pH 7.2. In order to determine the prevalence of haematozoa each smear was scanned double blind, under low magnification for 10 min and under oil immersion for 20 min.

The 315 birds, represented 75 species, 23 families and 7 orders. Fifty birds (15.9%) were infected with parasites of one or more genera of haematozoa (Table I). This is higher than the 10.5% prevalence reported by White et al. (1978) for the Neotropical region, but clearly lower than the 36.9% recorded for North America (Greiner et al. 1975). The 75 species of birds examined included 8 species that were examined for blood-parasites for the first time; 15 new host-parasites records were established from this sample (Table I).

Table I

The most common blood parasites found were microfilariae, which occurred in 26 birds, 17 species (8.2 %) representing 48.2% of the total infection. The proportion of microfilariae infections in the sample is exceptionally high, substantially higher than any other region, a feature that agrees with other studies in the Neotropics. The next most frequently found parasites were members of the genus Haemoproteus (6.7%) followed by Plasmodium (0.6%), Trypanosoma (0.9%) and others (0.6%).

Species of Haematozoa - Haemoproteus columbae Kruse 1890 was found in Columbina passerina and Zenaida auriculata. Macro and microgametocytes were found in both columbids Scardafella squammata and Leptotila verreauxi. Features such as shape, pigment granules and length were very similar to those described for H. columbae. Other features did show some differences: width (4.5-5 µm), nuclear displacement ratio (NDR = 0.3-0.2) and a grossly erythrocyte hypertrophy. These results do not agree with the constancy of morphological characters observed in H. columbae by Bennett and Pierce (1990). H. thraupi was found in the thraupiids Ramphocelus carbo, Tangara cyanicollis and Thraupis episcopus. With the exceptions of H. columbae and H. thraupi cited above, which were sufficiently numerous and characteristic to leave little doubt as to their identity, all other haemoproteid infections had parasitemia so low that species identification was not possible. In Vireo olivaceus 1-6 infected cells were found per 20,000 RBC. The parasites encountered were similar to H. vireonis as described by Bennett et al. (1986) but a diagnosis based on a few gametocytes can not be made with certainty. Plasmodium infections included the subgenus Novyella in Turdus nudigenis and Plasmodium (Haemamoeba), probably relictum, in Cyclarhis gujanensis. An unidentified parasite was found in the trochilid Phaethornis hispidus. It consisted of a small inclusion body in the erythrocyte and it could have been the earliest invasive merozoites of either Haemoproteus or Plasmodium. In the absence of mature forms even a generic diagnosis was not possible. Trypomastigotes were found in Elaenia chi-riquensis and V. olivaceus, however, only one to three specimens were found in each bird. Since, microfilariae can only be identified when associated with the adult filarial worms and no adult was collected, the parasites could not be further identified. In R. carbo a possible blood stage of He-patozoon was observed in erythrocytes. Finally, this survey showed absence of the genus Leucocytozoon.

Distribution by avian host - The largest number of birds were Passeriformes (253), followed by Apodiformes (22) and Coraciiformes (14). All other orders were represented in small number. Blood parasites occurred with greater frequency in certain families of birds than in others (Table I). The Vireonidae (70% primarily with Haemoproteus) was the most frequently parasitized family, followed by the Columbidae (50% with Haemoproteus). Other families (Thraupidae, Alcedinidae) had an intermediate prevalence. A number of families showed low parasite prevalence, including the Pipridae and Tyrannidae. All the other families had low prevalence levels: however, all were represented by one to three blood samples.

Even though the Neotropical region possesses the most diverse and richest avifauna of the world, this study indicated a low prevalence of blood parasites (15.9%), but represented a similar value to that recorded elsewhere in Central and South America (White et al. 1978, Bennett et al. 1980): it is far lower than that recorded for North America (Greiner et al. 1975). Furthermore, the low number of double infections (4 individuals) found in this study, agrees with other reports from the Neotropics (Bennett & Sousa 1980). Our results, in contrast to about 30% double infection of the total infected in North America, presumably indicate a low intensity of parasite attack in Colombia.

The distribution of the different genera of haematozoans among the avian hosts is very interesting. As noted by White et al. (1978) and Woodworth-Lynas et al. (1989), the haematozoans most frequently found in Neotropical birds are haemoproteids, followed by microfilariae and plasmodiids. Our Colombian sample closely approximates this general pattern, but microfilariae were more common than Haemoproteus, a finding similar to that recorded by Bennett et al. (1991) for Bolivia.

The number of birds infected with trypanosomes and microfilariae is comparatively higher than that seen elsewhere; these differences, as suggested by Bennett et al. (1991), could be explained by differences in vector composition and distribution patterns, compared to the rest of the world. Furthermore, the apparent absence of Leucocytozoon suggests a lack of suitable ornithophilic simuliid vectors for transmission of the parasite. The absence of members of Leucocytozoon can not be attributed to a lack of inocula, because North American migrant birds harboring the parasite, overwinter in the Neotropics (White et al. 1978).

It was possible to observe distribution trends among the different host families. The families with the highest prevalence in this study were essentially the same as those in other studies in the Neotropics (White et al. 1978), and the Neartic (Greiner et al. 1975). It would appear that some aspect or habit of these birds enhances parasitism by haematozoans. A possible interpretation is that certain families are inherently more susceptible to infection by blood parasites. It could also be interpreted that birds of these families have behavioral patterns (i.e. roosting sites) which bring them into more frequent contact with vectors. Bennett et al. (1980) made an interesting observation: families more closely related to the Caribbean and North America avifauna (i.e. Columbidae, Icteridae, Vireonidae), include the highest prevalence values, while those of presumed Neotropical origin (Trochilidae and Tyrannidae) have the lowest.

It is important to compare this survey with the results of Renjifo et al. (1952), in nearby localities of the same region. Although the prevalence obtained in our study is lower than that obtained by these authors (Table II), the avian hosts studied were different. These authors also analyzed different organs, which did not allow a direct comparison and discussion. Nevertheless, there are some trends in the distribution of haemotropic parasites. In both studies microfilariae were widely distributed among the avian families, with very similar prevalence values (Table II). The greatest difference observed was the low prevalence of the genus Plasmodium, compared with the higher value obtained by Renjifo et al. (1952) (Table II). A suitable hypothesis for these differences, could be attributed to the reduction of adequate environments for the development of the ornithophilic vectors (i. e. breeding sites). Both the urban growth and the use of savanna for cattle ranches, can be possible explanations for this reduction. It is necessary to explore this, and other possible hypotheses, that may explain the trends of distribution of blood parasites in avian hosts.

Table II

Identification of blood parasites using morphology of blood stages was not possible when the parasitaemias were very low, indicating the need for the development of others diagnostic techniques.

To Robert Adlard (Queensland Museum), CJ Marinkelle (Centro de Investigaciones en Microbiología y Parasitología Tropical, Universidad de los Andes) and Gary F Stiles (Instituto de Ciencias Naturales, Universidad Nacional de Colombia) for sharing their knowledge in parasitology and ornithology respectively. To L Garcia for his comments and valuable suggestions.

Table I | Table II

This study was supported by DIB-UN.

⁺Corresponding author. Fax: [phone]. E-mail: [e-mail]

Received 24 April 2001

Accepted 6 August 2001

References

• Ayala S, Ramakka JM, Ramakka VF, Varela CE 1977. Haemoproteus, Plasmodium, and Hippoboscid ectoparasites of Colombian wild doves. Rev Inst Med Trop São Paulo 19: 411-416.
• Bennett GF, Borrero JI 1976. Blood parasites of some birds from Colombia. J Wildl Dis 12: 454-458.
• Bennett GF, Pierce MA 1990. The haemoproteid parasites of the pigeons and doves (family Columbidae). J Nat Hist 24: 311-325.
• Bennett GF, Sousa O 1980. Blood parasites of some birds from São Paulo, Brazil. Mem Inst Oswaldo Cruz 75: 117-134.
• Bennett GF, Caines JR, Woodworth-Iynas CB 1986. Avian Haemoproteidae. 24. The haemoproteids of the new world passeriform families Formicariidae, Furnariidae, Mimidae and Vireonidae. Can J Zool 65: 317-321.
• Bennett GF, Garvin M, Bates JM 1991. Avian hematozoa from west-central Bolivia. J Parasitol 77: 207-211.
• Bennett GF, Witt H, White EM 1980. Blood parasites of some Jamaican birds. J Wildl Dis 16: 29-38.
• Greiner EC, Bennett GF, White EM, Coombs RF 1975. Distribution of the avian haematozoa of North America. Can J Zool 53: 1762-1787.
• Renjifo S, Sanmartin C, Zulueta J 1952. A survey of the blood parasites of vertebrates in eastern Colombia. Acta Trop 9: 151-169.
• White EM, Greiner EC, Bennett GF, Herman CM 1978. Distribution of the hematozoa of Neotropical birds. Rev Biol Trop 26: 43-102.
• Woodworth-Lynas CB, Caines JR, Bennett GF 1989. Prevalence of avian haematozoa in São Paulo State, Brazil. Mem Inst Oswaldo Cruz 84: 515-526.

Publication Dates

• Publication in this collection
  08 Jan 2002
• Date of issue
  Nov 2001

History

• Accepted
  06 Aug 2001
• Received
  24 Apr 2001