Blood Parasites in Birds From the Lowlands of Northern Colombia

Caribbean Journal of Science, Vol. 43, No. 1, 87-93, 2007
Copyright 2007 College of Arts and Sciences
University of Puerto Rico, Mayagüez
Blood Parasites in Birds From the Lowlands of Northern Colombia
AURORA LONDOÑO 1,3 ,PAULO C. PULGARIN-R 2,4 , AND SILVIA BLAIR 1
1 Grupo Malaria, Laboratorio 610, Facultad de Medicina, Universidad de Antioquia. Calle 62, No. 52-59.
Medellín, Colombia
2 Instituto de Biología, Universidad de Antioquia, AA. 1226, Medellín, Colombia. E-mail: pulgarinrpc@yahoo.com.mx
3 Current address: Instituto Potosino de Investigación Científica y Tecnológica. P.C. 78216,
San Luis Potosí—México
4 Corresponding author
ABSTRACT.— Blood samples from 302 wild and domesticated birds (75 species, 24 families) from two zones
of lowlands in northern Colombia (Urabá Gulf and Lower Cauca) were examined for haematozoa. Microscopic
observation of blood smears stained with Giemsa revealed twenty-eight individuals of 16 species
(9.3% of all birds) infected with parasites of at least one genus. Plasmodium spp. accounted for 5.6% of the
infections, followed by Haemoproteus spp. (2.6%), Leucocytozoon spp. (0.3%) and unidentified microfilariae
(1.0%). This survey reports four species examined for the first time and four new records of hosts of haematozoa.
In agreement with previous studies in the Neotropics, the prevalence of blood parasites was low in
comparison to other regions of the world.
KEYWORDS.—Birds, blood parasites, Colombia, Haemoproteus, Leucocytozoon, microfilariae, Plasmodium
INTRODUCTION
Bird-blood parasite interactions have
been the subject of numerous ecological
and evolutionary studies (Hamilton and
Zuk 1982, Cooper 1989, Bishop and Bennett
1992, Ricklefs 1992, Bennett et al. 1993, Tella
et al. 1999, Martin et al. 2001, Fallon et al.
2003a,b). However, information about
prevalence and distribution of avian haematozoa
from many areas of the word is
scarce, especially from tropical regions
(White et al. 1978, Young et al.1993). In Colombia
only seven short surveys have been
conducted in the last fifty two years (1952-
2004) (Rengifo et al. 1952, Ayala and Varela
1975, Bennett and Borrero 1976, Ayala et al.
1977, Rodriguez and Matta 2001, Valkiunas
et al. 2003, Matta et al. 2004). The great majority
of these studies was carried out in the
eastern plains and in the western and eastern
Colombian Andes (See Figure 1). To
provide additional knowledge of birdparasite
relationships in the country, in this
pilot investigation we examined wild and
domestic birds for haematozoa in the lowlands
of northern Colombia. This work is
included in a project of Grupo Malaria
87
aimed to study new host-parasite relationships
in the genus Plasmodium, in the hope
of establishing new models to investigate
the disease, so we were also interested in
other hosts of Plasmodium than wild birds,
which is the reason for the inclusion of domesticated
birds in the survey. We compared
our results with those of other studies
in Colombia and elsewhere in the
Neotropics.
MATERIALS AND METHODS
Wild and domesticated birds were captured
between September 2001 and May
2002 in three localities of the lowlands of
northern Colombia in the department of
Antioquia. Two sites were in the Urabá
Gulf and one in the Lower Cauca (Fig. 1):
Site 1. El Tres, c. 8 km SE of Turbo
municipality (08°3038.5N, 76°3910.2W).
We sampled a small fragment (c. 2.5 ha) of
15-25 m tall gallery forest surrounded by
deforested areas, croplands and small
populated villages.
Site 2. Punta de Piedra, c. 15 km N of Turbo
municipality (08°1106.4N, 76°4347.4W).

88
A. LODOÑO ET AL.
FIG. 1. Studies for haematozoa in Colombian birds. Numbers 1, 2, 3 refer to localities in the text.
We sampled a dry forest patch (c. 2 ha)
surrounded by secondary forest remnants,
croplands and villages. Sites 1 and 2
are at 70 m a.s.l with annual mean temperature
of 28°C, and annual rainfall of
200 cm.
Site 3. El 16, S of Zaragoza municipality
(07°3044N, 74°5114W), east bank of
Nechí river at 55 m a.s.l, with a mean annual
temperature of 28°C and annual rainfall
of 307.5 cm. We worked on a c. 10 ha
fragment with secondary and mature forest
(25-30 m tall), close to Tafur marsh and San
Nicolas watershed.
Wild birds were mist-netted between 06:
00 h and 13:00 h, and domestic birds were
captured by hand between 14:00 and 17:00
h in rural housing near the mist-netting
sites. Two or three blood smears per bird
were taken from a drop of blood from the
brachial vein using capillary tubes. Smears
were fixed in 100% methanol after air drying,
and then were stained with Giemsa
(pH 7.0 for 40 min) on the same day. Blood
films were first examined under low power
(10× and 20×) for microfilariae and trypanosomes,
covering all regions of the
smear, and then under oil immersion

BLOOD PARASITES OF COLOMBIAN BIRDS 89
(100×), counting smaller haematozoa in 100
microscopic fields (which exceeds the minimum
number of erythrocytes required for
this kind of diagnosis) (Godfrey et al. 1987).
To avoid wrong determination of Plasmodium
spp. and Haemoproteus spp. due to
similarities in their sexual forms, Plasmodium
spp. was identified by the presence of
both schizonts and round or enlarged gametocytes
in the blood smear, while infections
by Haemoproteus spp. are characterized
by the presence only of enlarged
(halteridium) or round gametocytes in peripheral
blood. AL and SB independently
analyzed all blood smears with similar results.
The collection of samples was kept at
the Malaria Group in the Faculty of Medicine
of University of Antioquia. Finally,
comparisons of percentages of parasitism
were made by 2 test (EpiInfo version 6.1),
and values of p < 0.05 were considered as
significantly different. Our nomenclature of
birds follows the South American Check
list Committee (SACC, Remsen et al. 2004).
RESULTS
In total, 302 birds (75 species of 24 families)
were examined for blood parasites
(Table 1). From the municipality of Turbo
(sites 1 and 2), blood smears of 140 wild
birds (20 families and 52 species) and 50
domesticated birds (5 families and 5 species)
were examined. From the municipality
of Zaragoza (site 3), we examined
smears of 63 wild birds of 32 species (11
families) and 49 domesticated birds of two
species (two families). Among wild birds,
the families Tyrannidae and Thamnophilidae
were the most frequent. Twenty-eight
birds (9.3%) of 16 species harbored at least
one genus of parasite. Plasmodium, present
in 5.6% of all birds, was the most frequent
haematozoa, followed by Haemoproteus
(2.6%), Leucocytozoon (0.3%) and microfilariae
(1.0%) (Table 1). Parasites were
most frequent in passerine birds (81.2% of
all infected). None of the seven Nearctic-
Neotropical migratory songbirds harbored
parasites (Table 1).
To our knowledge, four species were examined
for haematozoa for the first time
(Sakesphorus canadensis, Myrmotherula fulviventris,
Myiodinastes chrysocephalus and Formicivora
grisea) (sensu White et al. 1978,
Woodworth-Lynas 1989, Bennett et al. 1991,
Young et al. 1993 and all the former Colombian
studies). New host-parasite records include
White-fringed Antwren (Formicivora
grisea) with Plasmodium spp., Buff-throated
Foliage-gleaner (Automolus ochrolaemus)
with Leucocytozoon spp., Tawny-throated
Leaftosser (Sclerurus mexicanus) and the Bicolored
Wren (Campylorhynchus griseus)
with microfilariae. Only two species: the
Tawny-throated Leaftosser and the Bananaquit
(Coereba flaveola) had multiple infections
in both zones (Table 1).
Comparison of total prevalence showed
a pattern similar to other reports in Neotropics.
Also non significant differences
were observed between prevalence of haematozoa
in wild and domesticated birds.
Differences were observed at the level of
genus of parasite when separating wilds
from domesticated and comparing with
data filtered from White et al. 1978; Plasmodium
spp. was significantly more abundant
in our sample of domesticated (p = 0.0012)
and Haemoproteus spp. was lower in our
sample of wild birds (p = 0.0317). No significant
differences for prevalence of infected
birds were observed between Turbo
(sites 1 and 2) and Zaragoza (site 3). In
Turbo, Haemoproteus was the most frequent
genus of parasite, being present in seven of
14 infected wild birds, and Plasmodium was
the most common in domesticated species
(5 of 5). In Zaragoza, Plasmodium was the
most frequent in both domestic and wild
birds, and Haemoproteus was not found. The
birds infected with Haemoproteus spp. had
relatively high parasitaemia (more than 2
gametocytes/100 erythrocytes), while in
those infected with Plasmodium spp. the
parasitaemia was lower and in the remaining
infections, only one to three parasites
were seen in the smears.
DISCUSSION
The prevalence of blood parasites (9.3%)
in our study was significantly low compared
with the nearest continental land
mass (37% in Neartic, p < 0.0001, White

90
A. LODOÑO ET AL.
TABLE 1. Blood parasites present in domesticated and wild birds in northwest Colombia.
Birds
Parasite genus
Family and species Examined Infected Plasmodium Haemoproteus Leucocytozoon Microfilariae
ANATIDAE
Cairina moschata 8 ab 3 2 b 1 a
PHASIANIDAE
Gallus gallus 74 ab 7 7 ab
COLUMBIDAE
Columbina talpacoti 1 a 1 1 a
FURNARIIDAE
Automolus ochrolaemus 4 b 1 1 be
Sclerurus mexicanus 1 b 1 1 b 1 be
THAMNOPHILIDAE
Formicivora grisea f 11 a 1 1 ae
COTINGIDAE
Pachyramphus
cinnamomeus 1 a 1 1 a
Pachyramphus rufus 1 a 1 1 a
Pachyramphus
polychopterus 1 a 1 1 a
TYRANNIDAE
Myiodynastes maculatus 1 a 1 1 a
Mionectes oleagineus 16 ab 1 1 ae
VIREONIDAE
Vireo olivaceus 1 a 1 1 a
TROGLODYTIDAE
Compylorhynchus griseus 1 a 1 1 ae
EMBERIZIDAE
Arremonops conirostris 2 a 1 1 a
COEREBIDAE
Coereba flaveola 4 ab 4 2 b 2 a
THRAUPIDAE
Ramphocelus dimidiatus 12 ab 2 2 a
Uninfected unlisted* 163
TOTAL 302 28 17 8 1 3
% Infected 9.3 5.6 2.6 0.3 1.0
a From Turbo.
b From Zaragoza.
e New record of host for the respective parasite.
f Species examined for haematozoa for the first time.
† Refers to boreal migratory birds.
*Uninfected species (the number of birds is in parenthesis, underlined species correspond to the domesticated
ones): Meleagridae: Meleagris gallopavo a (13); Numididae: Numida meleagirs a (1); Columbidae: Columba livia a (2),
Leptotila verreauxi a (1); Cuculidae: Crotophaga ani a (1); Trochilidae: Glaucis hirsutus a (3), Phaetornis longirostris ab
(9), Phaetornis anthophilus b (1), Heliothryx barroti b (1); Momotidae: Momotus momota a (1); Galbulidae: Galbula
ruficauda a (1); Ramphastidae: Pteroglossus torquatus b (1); Picidae: Colaptes punctigula a (1), Dryocopus lineatus a (1);
Dendrocolaptidae: Xyphorhyncus picus a (2), Xyphorhyncus guttatus a (1), Lepidocolaptes souleyetii a (1), Glyphorhynchus
spirurus b (2), Dendrocolaptes certhia b (1), Dendrocincla fuliginosa b (2); Furnariidae: Xenops minutus ab (2); Thamnophilidae:
Gymnopitys leucaspis ba (2); Sakesphorus canadensis bf (1), Myrmotherula fulviventris bf (1), Thamnophilus
doliatus a (2), Thamnophilus nigriceps a (1), Cercomacra tyrannina a (1); Pipridae: Manacus vitellinus ab (42), Pipra
erythrocephala ab (8), Pipra coronata b (2); Cotingidae: Schiffornis turdina b (2); Tyrannidae: Leptopogon amaurocephalus
a (1), Poecilotriccus sylvia a (5), Attila spadiceus a (2), Empidonax sp. a† (1), Terenotricus erithrurus b (2), Myiodinastes
chrysocephalus bf (1), Myiozetetes cayanensis ab (6), Elaneia frantzii a ? (1), Empidonax traillii ab† (1), Myiarchus tuberculifer
a (1); Troglodytidae: Thryothorus fasciatoventris a (1), Thryothorus leucotis a (1), Troglodytes aedon a (1), Microcerculus
marginatus ab (3); Emberizidae: Oryzoborus crassirostris b (1), Oryzoborus angolensis ab (7), Volatinia jacarina a (4);
Cardinalidae: Cyanocompsa cyanoides ab (2), Saltator coerulescens b (2), Saltator maximus a (1); Parulidae: Dendroica
petechia a† (1), Dendroica castanea a† (1), Vermivora peregrina a† (1), Oporornis philadelphia a† (1), Basileuterus fulvicauda a
(1), Seirus novoeborascensis a† (1); Thraupidae: Mitrospingus cassini a (1), Thraupis episcopus a (2).

BLOOD PARASITES OF COLOMBIAN BIRDS 91
et al. 1978, Rodriguez & Matta 2001). It was
also lower than prevalence in neighboring
regions like Caribbean islands and Panama
(ca 30%, p < 0.0001, Fallon et al. 2004 and
18%, p = 0.0008, Sousa and Herman 1982,
respectively). The total prevalence of haematozoa,
however, was not different from
other studies carried out in Colombia [Bennett
and Borrero (1976: 7.1%), Rodriguez
and Matta (2001:15.9%), Valkiunas et al.
(2003: 7.8%)], and other Neotropical countries
[Woodworth-Lynas and Bennett (1989:
8%), Young et al. (1993: 11%)]. Many reasons
have been proposed to explain the low
frequency of blood parasites in Neotropical
birds: the scarcity of vectors (Bennett and
Borrero 1976, White et al. 1978, Young et al.
1993), under-estimation of the infections by
failure in the methods to detection of parasitized
birds (Bennett et al. 1991, Fallon et al.
2003a) and the evolutionary history of Neotropical
birds (Ricklefs 1992, Tella et al.
1999). However parasitic relationships vary
widely according to host species or the geographical
regions, and therefore careful
analyses which reflect these dynamics are
needed (Fallon et al. 2003b).
It is important to consider the effect of
the diversity of host species and sampling
strategy on the prevalence. In 77% of the
examined species only one or two individuals
were captured, as a result of the
opportunistic sampling. Although a high
diversity would dilute the prevalence occurring
in susceptible species by disproportion
of non-susceptible species, it was ruled
out because the sample size of the dominant
species supports the reports of low
prevalence of blood parasites in Neotropical
birds. Three species (Gallus gallus, Manacus
vitellinus and Mionectes oleaginea) conform
44% of the sample, which mean they
are overrepresented. Two of these species
are known as susceptible to haematozoa (G.
gallus and M. vitellinus) (White et al. 1978,
Bishop and Bennett 1992), but their specific
prevalence wasn’t as high as in other parts
of the world, and didn’t generate an augment
in the general prevalence. Probably
the diversity allowed the equilibrium between
non-susceptible and overrepresented
susceptible species. The prevalence
by genera was affected by the sample size
of host species. In comparisons of prevalence
separating wild from domesticated
birds the total prevalence of haematozoa in
wilds was similar to the Neotropics (using
information filtrated from White et al.
1978), but some differences were observed
at the level of genera. In the case of infections
by Plasmodium spp., G. gallus had a
highest percentage of the infections which
is the source of augmented frequency of
this genus in our sample of domesticated
birds. This situation put Plasmodium spp. as
the most frequent parasite in our overall
sample, instead of Haemoproteus spp., as
had been observed in other studies reported
in Colombia (Rodriguez and Matta
2001, Valkiunas et al. 2003).
A handful of reasons besides the biology
of Neotropical birds could explain the percentage
of prevalence found in this work. A
direct relationship between high parasite
prevalence and wet season, breeding period
and hormonal conditions has been reported
(e.g. Young et al. 1993 and Deviche et
al. 2001 as examples). The low prevalence
of haematozoa in our sample of wild birds
may be a mixture of factors: one is that
most birds (67%) were caught during the
dry season, in the months of February and
early May, before the proliferation of mosquitoes;
the second is that only 18% of the
birds were breeding, therefore there were
fewer individuals susceptible to vector biting.
A good explanation for the low parasite
presence in domesticated birds is difficult
due to many factors involved in their
human habitat. A model proposing a relationship
between endemic zones for human
malaria and prevalence of avian malaria
was proposed by Gabaldon and Ulloa
(1980), in which is established that the bioclimatic
conditions of this zones facilitate
the infection of several families of birds, especially
marsh birds. From that view, the
low prevalence could come from a low
number of mosquitoes in the zones studied
as a result of ongoing control programs.
Since Turbo (Urabá) and Zaragoza (Nechí)
are endemic zones for human malaria, and
dengue fever is also frequent, spraying of
the surrounding forest is common to control
several mosquito species. Even so, Plas-

92
A. LODOÑO ET AL.
modium (60% of all infections) was the most
common protozoa in domesticated birds,
which makes the availability of vectors a
poor explanation of the phenomena, at
least it were species of mosquito resistant to
that kind of insecticide. We claim that biologic
factors (immunology, ecology, behavior,
to mention something) of Neotropical
birds more than sampling methods are accounting
for the observed prevalence of
blood parasites in the Neotropics.
Nevertheless, we cannot conclude unerringly
that there is a low frequency of
haematozoa in the lowlands of northern
Colombia. We have examined different
groups of birds with different life histories
at different seasons and with few samples
per bird species, which limits our possibilities
to do comparisons, a disadvantage of
our sampling method. Opportunistic sampling
has advantages only in unexplored
areas where information of both, biodiversity
of birds and blood parasites is unknown
and also leaves a wider possibility
to find new hosts of parasites. Groupdirected
studies, on the other hand, have
more advantages to establish prevalence.
For example the families Tyrannidae, Cotingidae
and Furnariidae (sensu Remsen et
al. 2004) are almost never infected in other
studies (like Bennett et al. 1991, Young et al.
1993), but had more infected species in our
work than in theirs (Table 1), and moreover
these families had an increased frequency
of parasites in family focused studies as
Matta et al. (2004). We suggest that without
statistically designed studies with broad
host samples from different seasons and at
the same localities, it is difficult to draw
conclusions regarding the level of prevalence
as such. It is better to carry out detailed
examinations of specific groups of
birds (Tella et al. 1999, Matta et al. 2004).
New analyses and additional data, including
biology of both vertebrate and invertebrate
host, life cycles, physiology and genetic
backgrounds are needed to resolve
many questions about bird-parasite interactions.
Although the parasites have not been
identified at the level of species, this short
exploration is the first from this part of Colombia,
and adds to our knowledge for
the bird-parasite relationships in South
America. Explorations with more refined
methods are required, because in 52 years
only eight studies (including ours), and
about 440 total species (c. 22% of the Colombian
avifauna) of birds have been examined.
Additional methods for haematozoa
identification are also necessary to
understand the ecological and evolutionary
relationships between hosts, parasites and
vectors occurring in the Neotropics.
Acknowledgments.—We are indebted to
Corantioquia and Corpourabá (entities that
regulate the use of regional natural resources)
for permission to catch birds in
their ecological jurisdiction, and to Servicio
de Erradicación de Malaria in Turbo and
Zaragoza for introducing us to the forests.
We thank Gabriel J. Colorado, Juan F. Díaz
and Ana M. Castaño for their collaboration
during field work. Lastly to Sylvia M. Fallon
and John T. Klicka for reviewing the
manuscript, and Luciane Willcox for providing
information about Brazilian blood
parasite studies.
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