J. Parasitol., 91(1), 2005, pp. 131–134
? American Society of Parasitologists 2005
HAEMOPROTEIDS OF THE AVIAN FAMILY DICRURIDAE (THE DRONGOS)
Amy F. Savage and Ellis C. Greiner*
Department of Pathobiology, College of Veterinary Medicine, University of Florida, Box 110880, Gainesville, Florida 32611. e-mail:
the presence of hematozoa and 1 species of Haemoproteus, i.e., Haemoproteus dicruri (De Mello, 1935). One species of drongo
occurs in Madagascar and has not been examined previously. Blood smears collected from wild-caught crested drongos, Dicrurus
forficatus, in Madagascar were examined using a compound microscope for the presence of hematozoa. A new species, Hae-
moproteus khani, is described in this study. This new species has circumnuclear gametocytes, in contrast to the halteridial H.
dicruri. In addition, H. dicruri is reported for the first time from the crested drongo and is redescribed. This is the first report of
hematozoa in drongos of Madagascar.
Dicrurids are a widespread avian family in Africa and Asia. Earlier surveys of this family in these areas have reported
The Dicruridae includes 20 species of birds, occurring in Af-
rica, India, and Australia (Langrand, 1990). The crested drongo
(Dicrurus forficatus) is the only member of the family on Mad-
agascar; it occurs there and on Anjouan in the Comoro Islands.
Dicrurids are common and can be found in a variety of habitats,
from forests to sparsely wooded terrain and plantations (Morris
and Hawkins, 1998). To date, 3 studies have examined birds
from Madagascar for hematozoa (Bennett and Blancou, 1974;
Greiner et al., 1996; Raharimanga et al., 2002).
As yet, only a single species of Haemoproteus has been re-
ported in the Dicruridae. Haemoproteus dicruri was first de-
scribed by De Mello (1935) from Dicrurus macrocercus and
later redescribed by Peirce (1984) from Dicrurus adsimilis.
Several authors have discussed host specificity in this genus
(Atkinson, 1986; Bennett and Peirce, 1988). For example, At-
kinson (1986) showed that Haemoproteus meleagridis, although
primarily observed in turkeys, was transmissible to other mem-
bers of the Phasianidae. The new Haemoproteus species de-
scribed in this study is distinct from H. dicruri and, to our
knowledge, is specific to the Dicruridae.
MATERIALS AND METHODS
All birds were mist-netted at field sites in Madagascar. Blood smears
were made either from toe clippings or from heart punctures. The slides
were air-dried and fixed in absolute methanol by the collecting orni-
thologists. Slides were either stained before shipment or shipped to the
University of Florida, where they were stained with Giemsa on arrival.
Slides were examined at ?100, ?160, and ?1,000 on a Zeiss compound
microscope for the presence of hematozoa. Blood parasites were drawn
with the aid of a drawing tube on a Nikon compound microscope. All
measurements, excepting parasite length, of erythrocytes and parasites
were performed as described in Bennett and Campbell (1972). Nuclear
displacement ratio (NDR) refers to the degree to which the host cell
nucleus is laterally displaced by the parasite. Nuclear displacement was
calculated as described in Savage and Greiner (2004). Parasite length
was determined by measuring a line drawn to bisect the gametocyte
along its longitudinal axis. Area was calculated using a drawing tube
and grid, as described in Forrester et al. (1977).
Haemoproteus khani n. sp.
(Figs. 1–6; Table I)
Immature gametocyte: Developmental stages halteridial, de-
veloping laterally in mature erythrocyte, with ends wrapping
Received 26 April 2004; revised 17 June 2004; accepted 18 June
* To whom correspondence should be addressed.
around erythrocyte nucleus (Figs. 1, 2). First circumnuclear
contact between parasite ends occurs adjacent to host cell nu-
cleus (Fig. 3), then parasite grows outward, filling remaining
host cell cytoplasm at maturity. Host–parasite complex at this
stage is 10 ?m2larger than the fully mature complex, but par-
asite has same area, indicating host cell atrophy as parasite ma-
Macrogametocyte (n ? 15): Circumnuclear at maturity (Fig.
4), lightly staining blue with Giemsa. Nucleus commonly in-
distinct, light pink when visible. Margins smooth or slightly
irregular, but not amoeboid. Fully developed host cell–parasite
complex area ? 130.5 ?m2, 8% larger than uninfected eryth-
rocytes. Host cell nucleus displaced slightly, NDR ? 0.81. Av-
erage parasite area ? 109.3 ?m2, host cell nucleus reduced from
22.4 to 18.0 ?m2. Parasite length ? 28.8 ?m. Infected cells
slightly increased in length. When visible, parasite nucleus ?
10.4 ?m2(9.5% of parasite). Refractile granules located ran-
domly through parasite, sometimes clumped. Pigment granules
vary in size, generally moderately large and ovoid, occasionally
smaller. Pigment white or yellow. Average number ? 13. No
volutin observed. Parasite develops in mature erythrocytes.
Microgametocyte (n ? 11): Same morphological character-
istics as described above, with gender staining associated dif-
ferences (Figs. 5, 6). Parasite stains pale pink or clear, com-
monly noticed only because of pigment granules. Parasite nu-
cleus pink when observed, average area ? 24.1 ?m2, 22.1% of
Type host: Dicrurus forficatus, Linnaeus, 1766.
Basis of description: Parasites are described from a blood
smear taken from an adult D. forficatus. Hapantotype: blood
smear SG-604 collected by Steven M. Goodman on 10 Decem-
ber 1995 in Andohahela, Madagascar, at 120 m. Accession
G463732 to the International Reference Centre for Avian He-
matozoa, Queensland Museum, South Brisbane, Queensland,
Australia. Parahapantotype: blood smear SG-605 collected by
Steven M. Goodman on 10 December 1995 in Andohahela,
Madagascar, at 120 m. Accession to IPM-11 to Institut de Pas-
teur de Madagascar.
Distribution: It is presumed that this parasite will be found
throughout the range of this species of drongo on Madagascar
and perhaps the Comoro Islands.
Etymology: The parasite is named in recognition of the sig-
132THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 1, FEBRUARY 2005
approaching circumnuclear. 3. Immature H. khani macrogametocyte that has become circumnuclear. 4. Mature H. khani macrogametocyte. 5–6.
Mature H. khani microgametocytes. 7. Haemoproteus dicruri macrogametocyte. 8–9. Haemoproteus dicruri microgametocytes.
Haemoproteids of the Dicruridae. 1. Immature Haemoproteus khani macrogametocyte. 2. Immature H. khani macrogametocyte
TABLE I. Morphometric parameters of the haemoproteids of Dicruridae (means in ? or ?2, followed by standard deviations in parentheses).*
Area (host–parasite complex)
Macrogametocyte nucleus area
Microgametocyte nucleus area
RBC nucleus length
RBC nucleus width
RBC nucleus area
n ? 26
n ? 16
n ? 12
n ? 16
* RBC, red blood cells; NDR, nucleus displacement ratio.
SAVAGE AND GREINER—BLOOD PARASITES OF DRONGOS 133
nificant body of work produced by Razul Khan, particularly his
efforts in the study of hematozoa.
This is the first circumnuclear haemoproteid recorded from
the Dicruridae. The parasite has a characteristic development in
that the ends generally connect first adjacent to the host cell
nucleus margin and then grow together and outward from there.
(Figs. 7–9; Table I)
Macrogametocyte: Halteridial gametocyte infecting mature
erythrocytes (Fig. 7). Gametocyte fully displaces host cell nu-
cleus laterally to erythrocyte margin (NDR ? 0.01). Ends of
parasite do not wrap around erythrocyte nucleus, do not cross
the plane created by the far side of the erythrocyte nucleus.
Parasite length ? 16.1 ?m. Host–parasite complex slightly larg-
er than uninfected erythrocytes, area ? 128 ?m2. Parasite ?
106.3 ?m2, occupying 98% of host cell cytoplasm and 83% of
host–parasite complex. Macrogametocyte stains light blue with
Giemsa, parasite nucleus stains pink. Parasite nucleus usually
central, commonly against host cell nucleus. Refractile granules
sometimes noticeably rodlike, 11 per parasite.
Microgametocyte: As described above, with normal sexual
differences (Figs. 8, 9). Microgametocyte nucleus boundaries
Type host: Dicrurus forficatus, Linnaeus, 1766.
Type locale: Andohahela, Madagascar (24?37.6?S, 46?45.9?E).
Basis of description: Parasites are described from a blood
smear taken from an adult D. forficatus. Blood smear SG-604
collected by Steven M. Goodman on 10 December 1995 in
Andohahela, Madagascar, at 120 m. Accession G463733 to the
International Reference Centre for Avian Hematozoa, Queens-
land Museum, South Brisbane, Queensland, Australia. Blood
smear SG-605 collected by Steven M. Goodman on 10 Decem-
ber 1995 in Andohahela, Madagascar, at 120 m. Accession to
IPM-11 to Institut de Pasteur de Madagascar.
Distribution: On the basis of the existing reports, it is pre-
sumed that this parasite will be found throughout the range of
This is a new host record for H. dicruri. De Mello (1935)
originally described this parasite from a black drongo (D. ma-
crocercus); later, Peirce (1984) redescribed it from a fork-tailed
drongo (D. adsimilis). The former investigator described an
ovoid, convex parasite with rod-shaped pigment granules. He
referred to lightly staining microgametocytes with indistinct nu-
clei and displaced erythrocyte nuclei (De Mello, 1935). Peirce
(1984) also described a pale microgametocyte with an indistinct
nucleus. In addition, he reported the displacement of the host
cell nucleus and that the parasite does not wrap around the host
cell nucleus. In this study, we describe the same traits. We ob-
served a parasite that does not wrap around the erythrocyte
nucleus, displaces the host cell nucleus, and stains lightly with
an often indistinct parasite nucleus. Although Peirce (1984) did
not describe rod-shaped pigment granules in the text, they are
visible in the accompanying micrographs, showing both round
and rod-shaped refractile granules. We also noted that the pig-
ment granules are not always rod-shaped, and rounder granules
are common. Furthermore, we observed that the parasite oc-
cupies more than 90% of the host cell cytoplasm. This is slight-
ly more than observed by Peirce (1984); it is unknown whether
this is a result of host-induced variation or those observed in
this study were more mature parasites. The morphometric pa-
rameters of H. dicruri reported here are intended to add to the
current knowledge of this species and variation therein, as well
as document a new host record. More importantly, these param-
eters are provided as a means by which to compare H. dicruri
and the new species, H. khani in the same species of host.
Haemoproteus dicruri was differentiated from H. khani n.
sp. largely by its length, NDR, and its tendency not to envelop
the erythrocyte nucleus. Haemoproteus dicruri seemed to have
a more rigid morphology, being almost more rodlike. In con-
trast, H. khani n. sp. causes little displacement of the host cell
nucleus and grows around it. Haemoproteus khani n. sp. be-
came circumnuclear as it grew into mature gametocytes and is
approximately 12-? longer at maturity than H. dicruri. The
NDR of 0.01 associated with H. dicruri recorded in this study
readily supported the morphology observed, i.e., a host cell
nucleus completely displaced laterally. In comparison, H. khani
n. sp. has an NDR of 0.81, indicating only minor displacement
by the gametocyte.
Both parasites discussed in this study stained in a similar
manner, and it was often easy to overlook the microgametocytes
unless the refractile granules were observed. Care should be
taken when examining blood smears with few mature gameto-
cytes, and NDR as well as any indication of encircling the host
cell nucleus should be used to differentiate between these spe-
This is the first report of hematozoa in the dicrurids of Mad-
agascar. The data presented in this study represent a new host
record for H. dicruri and the description of H. khani n. sp. The
Dicruridae are widespread geographically and have been ex-
amined several times, but this is the first report of a circum-
nuclear parasite in this family. Because no circumnuclear par-
asites have been described from drongos elsewhere, it is pos-
sible that H. khani n. sp. is limited to the drongos of Madagas-
car, although there are no data supporting or refuting this
observation. Further investigations of this family, as well as the
identification of the vector for these parasites are needed before
this can be determined. In addition, transmission studies for
these 2 species would allow a better understanding of the var-
iation in developmental morphologies of the circulating stages.
The authors wish to gratefully acknowledge Steven M. Goodman of
the Field Museum of Natural History and WWF–Madagascar and Ar-
istide Andrianarimisa for the collection of samples in the field. Also,
the authors recognize Garry Foster, Donald Forrester, and Ramiro Isaza
for their critical comments on this manuscript. In addition, the authors
thank Carter Atkinson for providing workspace.
134 THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 1, FEBRUARY 2005
ATKINSON, C. T. 1986. Host specificity and morphometric variation of
Haemoproteus meleagridis Levine, 1961 (Protozoa: Haemosporina)
in gallinaceous birds. Canadian Journal of Zoology 64: 2634–2638.
BENNETT, G. F., AND J. BLANCOU. 1974. A note on the blood parasites
of some birds from Madagascar. Journal of Wildlife Diseases 10:
———, AND A. G. CAMPBELL. 1972. Avian Haemoproteidae. I. Descrip-
tion of Haemoproteus fallisi n. sp. and a review of the haemopro-
teids of the family Turdidae. Canadian Journal of Zoology 50:
———, AND M. A. PEIRCE. 1988. Morphological form in the avian
Haemoproteidae and an annotated checklist of the genus Haemo-
proteus Kruse, 1890. Journal of Natural History 22: 1683–1696.
DE MELLO, I. F. 1935. New haemoproteids of some Indian birds. Pro-
ceedings of the Indian Academy of Science (B) 2: 469–475.
FORRESTER, D. J., E. C. GREINER, AND G. F. BENNETT. 1977. Avian Hae-
moproteidae. 7. A review of the haemoproteids of the family Ci-
coniidae (storks) and descriptions of Haemoproteus brodkorbi sp.
nov. and H. peirci sp. nov. Canadian Journal of Zoology 55: 1268–
GREINER, E. C., M. S. PUTNAM, AND S. M. GOODMAN. 1996. Blood
parasites from birds in the Re ´serve Naturelle Inte ´grale d’ Andrin-
gitra, Madagascar. Fieldiana: Zoology 85: 142–143.
LANGRAND, O. 1990. Guide to the birds of Madagascar. Yale University
Press, New Haven, Connecticut, 303 p.
MORRIS, P., AND F. HAWKINS. 1998. Birds of Madagascar. A photographic
guide. Yale University Press, New Haven, Connecticut, 298 p.
PEIRCE, M. A. 1984. Haematozoa of Zambian birds VIII. Redescription
of Haemoproteus dicruri from Dicrurus adsimilis (Dicruridae).
Journal of Natural History 18: 789–791.
RAHARIMANGA, V., F. SOULA, M. J. RAHERILALAO, S. M. GOODMAN, H.
SADONE`S, A. TALL, M. RANDRIANARIVELOJOSIA, L. RAHARIMALALA,
J.-B. DUCHEMIN, F. ARIEY, AND V. ROBERT. 2002. He `moparasites
des oiseaux sauvages a ` Madagascar. Archives de Institut Pasteur
de Madagascar 68: 90–99.
SAVAGE, A. F., AND E. C. GREINER. 2004. Hematozoa of the avian family
Brachypteraciidae (the Ground-rollers). Journal of Parasitology [In