Plasmodium(Apicomplexa) of the skylark (Alauda arvensis)

2009·4.2 MB·English

by  Jean-Marc Chavatte

Plasmodium (Apicomplexa)
of the skylark (Alauda arvensis)
Jean-Marc CHAVATTE
Virginie GRÈS
Georges SNOUNOU
Alain CHABAUD
Irène LANDAU
Muséum national d’Histoire naturelle,
Parasitologie comparée et modèles expérimentaux, USM 307,
case postale 52, 57 rue Cuvier, F-75231 Paris cedex 05 (France)
[email protected]
Chavatte J.-M., Grès V., Snounou G., Chabaud A. & Landau I. 2009. — Plasmodium
(Apicomplexa) of the skylark (Alauda arvensis). Zoosystema 31 (2) : 369-383.
ABSTRACT
Plasmodium parasites were sought in 30 skylarks (Alauda arvensis) captured
in the Département des Landes (France) during the post-mating migration.
Parasite prevalence was low (6/30) while intra-specifi c diversity was high (14
species). Five species were morphologically indistinguishable from those found
in the magpie (Pica pica) from the Paris region: Plasmodium dorsti, P. bioccai,
KEY WORDS P. ghadiriani, P. dherteae, and P. relictum quentini n. subsp. Two species had been
Apicomplexa, described in other birds: P. rouxi and P. hexamerium. Th e species Plasmodium
Plasmodium,
alaudae (Celli & Sanfelice, 1891) is redefi ned in this article. Finally, fi ve new
Alauda arvensis,
migratory gregarious species are described and named: P. reniai n. sp., P. coluzzii n. sp., P. caloti n. sp.,
bird, P. ginsburgi n. sp. and P. jeanriouxi n. sp., and one, Plasmodium sp. is described
Pica pica,
but not named. Th e pattern of infection in the skylark, a migratory gregarious
sedentary solitary bird,
new species. bird, is compared to that of the magpie, a solitary sedentary bird.
ZOOSYSTEMA • 2009 • 31 (2) © Publications Scientifi ques du Muséum national d’Histoire naturelle, Paris. www.zoosystema.com 369
Chavatte J.-M. et al.
RÉSUMÉ
Plasmodium (Apicomplexa) de l’alouette des champs (Alauda arvensis).
Trente alouettes (Alauda arvensis) dont certaines étaient porteuses de Plasmodium
ont été capturées dans le département des Landes au cours de leur migration
postnuptiale. La prévalence est faible (6/30) et la diversité intra-spécifi que
importante (14 espèces). Cinq espèces sont morphologiquement indistinguables de
MOTS CLÉS
Apicomplexa, celles de la pie de la région parisienne : Plasmodium dorsti, P. bioccai, P. ghadiriani,
Plasmodium, P. dherteae, P. relictum quentini n. subsp. ; deux sont connues d’autres oiseaux :
Alauda arvensis,
P. rouxi et P. hexamerium. Plasmodium alaudae (Celli & Sanfelice, 1891), est
oiseau grégaire
migrateur, redéfi ni ici. Enfi n, cinq espèces sont nouvelles : P. reniai n. sp., P. coluzzii n. sp.,
Pica pica, P. caloti n. sp., P. ginsburgi n. sp., P. jeanriouxi n. sp. et une Plasmodium sp. est
oiseau solitaire
décrite non nommée. Le parasitisme de l’alouette, oiseau grégaire et migrateur,
sédentaire,
espèces nouvelles. est comparé à celui de la pie, oiseau solitaire et sédentaire.
INTRODUCTION n. subsp. that was considered as P. relictum (Grassi &
Felleti, 1891) when it was observed in the magpie.
Bird Plasmodium form a highly varied group of parasites Plasmodium rouxi Sergent, Sergent & Catanei, 1928,
because of the large number of species, the extent parasite of the sparrow, Passer hispaniolensis (Tem-
of their host spectrum and their almost worldwide minck, 1820), was also observed, as was P. alaudae
distribution. In a previous article (Chavatte et al. 2007) (Celli & Sanfelice, 1891) which is re-defi ned and re-
we showed that the number of species parasitizing a described here. Five new species could be described:
single bird species can be high (14 in magpies) and this Plasmodium coluzzii n. sp., P. caloti n. sp., P. jeanriouxi
fact, generally unknown, should be taken into account n. sp., P. ginsburgi n. sp. and P. reniai n. sp. Finally,
when analysing ecological or molecular data. parasites observed in small numbers and whose
In this communication we present a morphologi- gametocytes could not be identifi ed, could not be
cal study of Plasmodium species from 30 skylarks attributed to a known species and have thus been
(Alauda arvensis Linnaeus, 1758) caught in France referred to as Plasmodium sp. in this article.
during their post-mating migration. Six showed Th e distribution of the Plasmodium species ob-
low-level infections. Th ree of these and one of the served in the skylarks is presented in Table 1.
negative birds were maintained in captivity for fi ve Th e traditional morphological identifi cation of
days. Th e negative skylarks remained negative dur- species as a prerequisite to molecular biology analysis
ing this period, while the parasitaemia of the other is considered more and more by authors as indis-
three birds increased. Th is study is based on the pensable to understand the relationships between
blood smears collected on the fi fth day of captivity species and their evolution (Valkiūnas 2005). Data
from these three skylarks, where Plasmodium were from sequencing parasite DNA amplifi ed from sky-
the only haematozoan species observed. lark blood samples will be presented in a separate
Six of the 14 species described or re-described in article and compared with those from the magpie
the magpie, Pica pica (Linnaeus, 1758) from the Paris (Chavatte et al. 2007).
region (Chavatte et al. 2007), were also observed in
the skylarks: P. hexamerium Huff , 1935, parasite of
Sialis sialis sialis (Linnaeus, 1758), P. dorsti Chavatte & MATERIALS AND METHODS
Landau, 2007, P. bioccai Chavatte & Landau, 2007,
P. ghadiriani Chavatte & Landau, 2007, P. dherteae Blood smear examination was carried out for
Chavatte & Landau, 2007 and P. relictum quentini 30 skylarks (Alauda arvensis) captured on 20
370 ZOOSYSTEMA • 2009 • 31 (2)
Plasmodium (Apicomplexa) of the skylark (Alauda arvensis)
October 1996 in the localities of Saint-Julien-en- TABLE 1. — Plasmodium Marchiafava & Celli, 1885 distribution in
Born (44°03’42’’N, 1°13’33’’W) and Messanges the Skylarks (Alauda arvensis Linnaeus, 1758).
(43°48’56’’N, 1°22’47’’W) in the Département
Bird number Plasmodium species
des Landes (France).
Th e material was collected, processed and stored 1 (738U) P. bioccai Chavatte & Landau, 2007
P. coluzzii n. sp.
as previously described (Chavatte et al. 2007). Al-
P. dorsti Chavatte & Landau, 2007
iquots of blood were stored in liquid nitrogen for
P. ginsburgi n. sp.
molecular studies. 2 (740U) P. alaudae (Celli & Sanfelice, 1891)
Since multiple parasite species are present, we P. coluzzii n. sp.
P. dorsti
have not adopted the designation of hapantotypes
P. jeanriouxi n. sp.
but rather selected for each of the species a holo-
P. relictum quentini n. subsp.
type consisting of a characteristic schizont that P. rouxi Sergent, Sergent & Catanei, 1928
was clearly delimited within a circle etched on the Plasmodium sp.
3 (741U) P. alaudae
smear slide with a diamond, and that was pho-
P. bioccai
tographed (Fig. 3D-J). Th ese types are deposited
P. caloti n. sp.
in the MNHN, in the collection of Parasitologie P. coluzzii n. sp.
comparée et Modèles expérimentaux, under the P. dherteae Chavatte & Landau, 2007
P. dorsti
numbers 61-66, drawer PXII, 440 LV.
P. ghadiriani Chavatte & Landau, 2007
P. hexamerium Huff, 1935
ABBREVIATIONS P. jeanriouxi n. sp.
RBC(s) red blood cell(s); P. relictum quentini n. subsp.
MNHN Muséum national d’Histoire naturelle, Paris. P. reniai n. sp.
P. rouxi
Plasmodium sp.
REVIEW OF THE LITERATURE
Two species were mainly reported from the skylark lected, and we designate as lectotype of P. alaudae
(Garnham 1966; Bennett et al. 1982; Valkiūnas the specimen depicted by Celli & Sanfelice (1891:
2005): P. alaudae (Celli & Sanfelice, 1891) and pl. 3 fi g. 16).
P. subpraecox (Grassi & Feletti, 1892). It is necessary
to clarify the taxonomic status of these species.
Plasmodium subpraecox, has been mentioned in SYSTEMATICS
the skylark and described in the little owl, Athene
noctua (Scopoli, 1769) (Grassi & Feletti 1892: Family PLASMODIIDAE Mesnil, 1903
fi g. 8), and in Passer hispaniolensis (Grassi & Feletti
1892: fi g. 7). Th e fi rst accurate re-description Genus Plasmodium Marchiafava & Celli, 1885
was made by Giovannola (1939), his description
and drawings made from the little owl were quite REMARKS
concordant with those of Grassi & Feletti (1892). All the Plasmodium parasites were found within
Th us, Athene noctua, and not the skylark, is the erythrocytes, and except for a few rings none were
type host of P. subpraecox. A closely related but not seen in reticulocytes. Th e infected RBC were at
identical species (P. caloti n. sp.) was noted in the times deformed, rounded or discoloured by certain
skylark and is described below. In 1891, Celli & parasites, but the deformability observed was not
Sanfelice described a Plasmodium in the skylark more pronounced than that observed in other birds
with some forms that develop rapidly while others such as the magpie (Chavatte et al. 2007) or the
more slowly. When examining their drawings, it is sparrow (Landau et al. 2003). On the other hand,
clear that multiple species were represented. Here the red blood cell nucleus was often slightly tilted
we re-describe this species from the birds we col- even by parasites that did not truly displace it.
ZOOSYSTEMA • 2009 • 31 (2) 371
Chavatte J.-M. et al.
For the known Plasmodium species, only the main ETYMOLOGY. — Th is species is dedicated to the memory
characters are briefl y described. of Alberto Coluzzi.
Molecular biology studies (Martinsen et al. 2007) DISTRIBUTION. — Known only from the type locality,
evidenced that some of the avian Plasmodium Saint-Julien-en-Born, Landes, France.
sub-genera created by Corradetti et al. (1963) are
HOST. — Alauda arvensis (type host).
polyphyletic and until the situation is clarifi ed we
prefer not to use them. DESCRIPTION
Th e young schizonts cover ¹⁄ to ⅓ of the slightly
enlarged RBC, where the median or sub-median
Plasmodium bioccai Chavatte & Landau, 2007 nucleus is tilted sideways. Th e RBC rounds up as
(Fig. 1A) the schizonts mature, pushing the host nucleus to
the edge of the cell, and often the parasites are found
MATERIAL EXAMINED. — France. Landes, Saint-Julien- in RBCs without nucleus. Th roughout schizont
en-Born, 44°03’42’’N, 1°13’33’’W, blood smears of
maturation, chromatin occurs as a peripheral crown
A. arvensis number 738U, 25.X.1996 (MNHN P2-XXV,
in which one distinguishes granules and little nuclei
1-23); 741U, 25.X.1996 (MNHN P2-XXV, 44-64).
around a clear vacuolated centre. Th e pigment in
DISTRIBUTION. — Seine-Saint-Denis, France (Chavatte the more mature stages forms rough aggregates of
et al. 2007); new record for the Landes, France.
agglomerated granules. Th e most characteristic stage
HOSTS. — Pica pica (type host); new record for Alauda is round in a rounded enucleate RBC, with the
arvensis. parasite nuclei tightly packed around a clear sinuous
centre. Fully mature stages were not seen, and the
REMARKS number of nuclei is estimated to exceed 30.
Th is species is comparable to that described in the Gametocytes are large and round and are often
magpie. Th e parasites lie in a rounded, prematurely found in RBCs devoid of nuclei.
hypertrophied and non-discoloured RBC with a
condensed ellipsoid nucleus displaced to one of the DIFFERENTIAL DIAGNOSIS
edges. Th e schizonts are regular in shape, rounded Plasmodium coluzzii n. sp. should be compared to
or approximately oval with smooth contours. Th e P. bioccai, a parasite described in the magpie and found
chromatin, initially as granular masses of variable in the skylark. Th e two species diff er by the smaller
sizes, progressively fragments into distinct nuclei. Th e size of the schizonts of P. coluzzii n. sp. where the
pigment is fi ne, loosely assembled in irregular rows, immature forms have dispersed and diff use chromatin,
though agglomerated in some areas. Two mature features that contrast with the well-defi ned nuclei
schizonts were observed with 26 nuclei dispersed that can be observed even in the young schizonts
in the cytoplasm. Th e gametocytes lead to the same of P. bioccai. Th e RBC nuclei, present in P. bioccai,
RBC modifi cation as do the schizonts. are often absent in P. coluzzii n. sp.
Some schizonts similar to those of P. coluzzii n. sp.
had been observed in the magpie studied by Chavatte
Plasmodium coluzzii Chavatte & Landau, n. sp. et al. (2007), but the paucity in the numbers observed
(Fig. 1B) had not allowed to distinguish the species.
TYPE MATERIAL. — Holotype: France. Landes, Saint-
Julien-en-Born, 44°03’42’’N, 1°13’33’’W, blood smear Plasmodium dorsti Chavatte & Landau, 2007
of A. arvensis number 741U, 25.X.1996 (MNHN 440LV (Fig. 1C)
PXIII, 61) (Fig. 3I).
Paratypes: same data as holotype, blood smears of
A. arvensis number 738U, 25.X.1996 (MNHN P2-XXV, MATERIAL EXAMINED. — France. Landes, Saint-Julien-
1-23); 740U, 25.X.1996 (MNHN P2-XXV, 24-43); en-Born, 44°03’42’’N, 1°13’33’’W, blood smears of
741U, 25.X.1996 (MNHN P2-XXV, 44-64). A. arvensis number 738U, 25.X.1996 (MNHN P2-XXV,
372 ZOOSYSTEMA • 2009 • 31 (2)
Plasmodium (Apicomplexa) of the skylark (Alauda arvensis)
A A A A A B
1 2 3 4 5 1
B B B B B B
2 3 4 5 6 7
C C C C D D
1 2 3 4 1 2
D D D D D E
3 4 5 6 7 1
E E E E E E
2 3 4 5 6 7
FIG. 1. — A, Plasmodium bioccai Chavatte & Landau, 2007; A1-A3, schizonts; A4, microgametocyte; A5, macrogametocyte; B, P. coluzzii
Chavatte & Landau, n. sp.; B-B, schizonts; B, B, macrogametocyte; B, microgametocyte; C, P. dorsti Chavatte & Landau, 2007;
1 4 5 7 6
C, C, schizonts; C, microgametocyte; C, macrogametocyte; D, P. ginsburgi Chavatte & Landau, n. sp.; D-D, schizonts; D, micro-
1 2 3 4 1 5 6
gametocyte; D, macrogametocyte; E, P. relictum quentini Chavatte & Landau, n. subsp.; E-E, schizonts; E, microgametocyte;
7 1 5 6
E, macrogametocyte. Scale bar: 10 μm.
7
ZOOSYSTEMA • 2009 • 31 (2) 373
Chavatte J.-M. et al.
1-23); 740U, 25.X.1996 (MNHN P2-XXV, 24-43); mass in which nuclei are yet to be diff erentiated.
741U, 25.X.1996 (MNHN P2-XXV, 44-64). Th e older schizonts occupy nearly the whole of
the RBC, whose nucleus is consequently found
DISTRIBUTION. — Seine-Saint-Denis, France (Chavatte
et al. 2007); new record for the Landes, France. in a notch. Th e parasite chromatin is still highly
granular and covers the whole of the schizont,
HOSTS. — Pica pica (type host); new record for Alauda except for one or two central vacuolated areas, and
arvensis.
progressively condenses to form nuclei. Th e rough
pigment is assembled and is often associated with
REMARKS a white vacuole. Fully mature schizonts could not
Th e examined specimens are closely similar to be observed, but we evaluate the number of nuclei
P. dorsti from the magpie. Th is large species lies to exceed 30.
in a little or non-enlarged RBC whose nucleus is Gametocytes are ellipsoid and contain numerous
pushed to one of the extremities. Th e schizonts that little vacuoles.
fi ll three-quarters of the RBC, are elongated with
irregular shapes and contours. Th e oldest schizonts DIFFERENTIAL DIAGNOSIS
observed had 26 nuclei. In contrast to what is Plasmodium ginsburgi n. sp. can be distinguished
observed in the magpie, RBCs in the skylark, are from P. bioccai by its shape and that of the RBC
neither deformed nor discoloured. which is ellipsoid and elongated in the former and
rounded in the latter. Th ese species also diff er by
their pigment, which is gathered and rough in the
Plasmodium ginsburgi Chavatte & Landau, n. sp. former and fi ner and more dispersed in the latter.
(Fig. 1D) Schizont maturation and nucleus formation diff er
between the two species: the chromatin remains
TYPE MATERIAL. — Holotype: France. Landes, Saint- diff use until the late stages in P. ginsburgi n. sp.
Julien-en-Born, 44°03’42’’N, 1°13’33’’W, blood smear
in contrast to the early formation of individual
of A. arvensis number 738U, 25.X.1996 (MNHN 440LV
nuclei in P. bioccai. Finally, the number of nuclei
PXIII, 65) (Fig. 3H).
Paratypes: same data as holotype, blood smears of exceeds 30 in P. ginsburgi n. sp. but is around 24
A. arvensis number 738U, 25.X.1996 (MNHN P2- to 30 in P. bioccai.
XXV, 1-23). Th e ellipsoid elongate P. ginsburgi n. sp. with a
high number of nuclei is comparable to Plasmo-
ETYMOLOGY. — Th is species is dedicated to Hagai
Ginsburg. dium maior Raff aele, 1930, a parasite of Passer
hispaniolensis and P. domesticus (Linnaeus, 1758).
DISTRIBUTION. — Known only from the type locality, Th e schizonts illustrated by Raff aele (1930) are
Saint-Julien-en-Born, Landes, France.
comparable to those observed here: the ellipsoid
HOST. — Alauda arvensis (type host). schizonts are large even in young forms, they fi ll
the RBC whose globular nucleus is pushed to one
DESCRIPTION of the extremities. However, the two species diff er
This large species lies in an enlarged ellipsoid by the chromatin that remain diff use throughout
RBC where extremities are often narrower and a large portion of P. ginsburgi n. sp. maturation
sometimes discoloured. Th e RBC nucleus is dense whereas it is gathered up in a few large massed in
and sub-globular and is pushed towards one of the P. maior, and by the rough pigment amassed around
extremities. Th e young and sub-mature schizonts a vacuole that contrasts to the pigment distributed
are irregular in form and are disposed transversally in several masses in P. bioccai. Raff aele had not de-
in the middle part of the RBC whose nucleus is scribed any mature forms, but in the re-description
tilted. Th ey comprise a blue cytoplasmic area scat- (Landau et al. 2003), it was noted that 20 to 24
tered with vacuoles, a rather rough pigment, and merozoites are formed, a number inferior to that
a highly granular and abundant diff use chromatin estimated for P. ginsburgi n. sp.
374 ZOOSYSTEMA • 2009 • 31 (2)
Plasmodium (Apicomplexa) of the skylark (Alauda arvensis)
Plasmodium relictum quentini these very same diff erential characters, we consider
Chavatte & Landau, n. subsp. that in these two hosts they represent a vicariant
(Fig. 1E) form of the P. relictum described in the sparrow.
We designate it as P. relictum quentini n. subsp.
Plasmodium relictum – Chavatte & Landau 2007 (parasite (= P. relictum sensu Chavatte & Landau 2007,
of Pica pica).
parasite of Pica pica).
TYPE MATERIAL. — Holotype: France. Landes, Saint-
Julien-en-Born, 44°03’42’’N, 1°13’33’’W, blood smear
of A. arvensis number 740U, 25.X.1996 (MNHN 440LV Plasmodium reniai Chavatte & Landau, n. sp.
PXIII, 62) (Fig. 3E).
(Fig. 2A)
Paratypes: same data as holotype, blood smears of A. arven-
sis number 740U, 25.X.1996 (MNHN P2-XXV, 24-43);
741U, 25.X.1996 (MNHN P2-XXV, 44-64). TYPE MATERIAL. — Holotype: France. Landes, Saint-
Julien-en-Born, 44°03’42’’N, 1°13’33’’W, blood smear
ETYMOLOGY. — Th is subspecies is dedicated to Jean- of A. arvensis number 741U, 25.X.1996 (MNHN 440LV
Claude Quentin. PXIII, 64) (Fig. 3G).
Paratypes: same data as holotype. Blood smears of
DISTRIBUTION. — Seine-Saint-Denis, France (Chavatte A. arvensis number 741U, 25.X.1996 (MNHN P2-
et al. 2007) and type locality, Saint-Julien-en-Born, XXV, 44-64).
Landes, France.
ETYMOLOGY. — Th is species is dedicated to Laurent
HOSTS. — Alauda arvensis (type host); Pica pica. Rénia.
DESCRIPTION DISTRIBUTION. — Known only from the type locality,
Saint-Julien-en-Born, Landes, France.
Th e schizonts lie in an enlarged and often rounded
and sometimes discoloured RBC, whose condensed HOST. — Alauda arvensis (type host).
and sub-globular nuclei is pushed to the periphery.
Th e schizont’s 12 to 18 nuclei are dense, rounded DESCRIPTION
and well delimited. Initially peripheral and slightly Th e parasite lies in a non-deformed, non-hypertro-
protruding towards the outside, the nuclei are then phied RBC whose nucleus is slightly displaced by the
distributed to the interior of the schizont. Th e larger parasite forms. Th e young schizonts have 2 to
cytoplasm is clear with a few white sharp-edged 6 nuclei, and are crescent-shaped and found at the
vacuoles. Th e pigment is most often central with apex of the RBC, generally attached to its edge. Th eir
the fi ne grains gathered up. Th e gametocytes are cytoplasm is abundant, vacuolated and the nuclei
rounded and induce the same alterations in the though of irregular shape are clearly distinguished
RBC as the schizonts. individually. As they develop, the schizonts extend
along one of the RBC borders, keeping contact with
TAXONOMIC STATUS RBC membrane and separated from its nucleus by
Th e specimens studied are identical to the species a band of erythrocytic cytoplasm. Th roughout its
described from the magpie (Chavatte et al. 2007) development, the schizont retains a curved shape,
where it was identifi ed to P. relictum. However, this larger on the top of the RBC and narrower along
parasite presented some minor diff erences with the host nucleus. Th e number of nuclei is estimated
respect to the P. relictum re-described (Landau to be around 30, though no fully mature schizonts
et al. 2003), in Passer domesticus, namely, a more could be observed.
pronounced RBC deformation, and crown of Gametocytes are elongated and have roughly the
nuclei that are more regular and protuberant than same shape and position as the schizonts.
those in the sparrow. Th e authors opted then to
designate these parasites as P. relictum, as these DIFFERENTIAL DIAGNOSIS
diff erences are rather minor. However, since both Th e closest species is P. golvani Chavatte & Landau,
the parasites of the lark and the magpie display 2007, parasite of the magpie.
ZOOSYSTEMA • 2009 • 31 (2) 375
Chavatte J.-M. et al.
Th is parasite is distinguished from the one in illustrated by Grassi & Feletti in Athene noctua
the magpie by its general shape which is thinner (Grassi & Feletti 1892: fi g. 8). Th ese authors have
and more elongated. Moreover, and in contrast to also recorded it in Alauda arvensis and in Passer
P. reniai n. sp., P. golvani shows a long thin protru- hispaniolensis.
sion along the RBC nucleus, its young forms have According to these authors the number of mero-
few nuclei and these are arranged in two rows in zoites is 5 to 12. In a re-description of this species,
the mature forms. Giovannola (1939), enumerated 10 to 12 mero-
zoites in the mature schizont, and from his illustra-
tions one can note a few similarities with P. caloti
Plasmodium caloti Chavatte & Landau, n. sp. n. sp.: defi ned outlines, cytoplasmic abundance,
(Fig. 2B) and a rather peripheral location of the nuclei in
mature schizonts. On the other hand, the parasite
TYPE MATERIAL. — France. Landes, Saint-Julien-en-Born, described here produces an average of 8 merozoites
44°03’42’’N, 1°13’33’’W, blood smear of A. arvensis
and leads to a much more pronounced hypertrophy
number 741U, 25.X.1996 (MNHN 440LV PXIII, 63)
of the RBC.
(Fig. 3D).
Paratypes: same data as holotype, blood smears of Plasmodium caloti n. sp. and P. alaudae diff er by
A. arvensis number 741U, 25.X.1996 (MNHN P2- the following features: the larger size of P. caloti
XXV, 44-64). n. sp., its more or less central position in a con-
siderably enlarged RBC with a displaced nucleus,
ETYMOLOGY. — Th is species is dedicated to the memory
of Jacques Calot. contrasts with the small size of the apically located
P. alaudae where infected RBCs are not modifi ed
DISTRIBUTION. — Known only from the type locality, nor their nuclei displaced.
Saint-Julien-en-Born, Landes, France.
HOST. — Alauda arvensis (type host).
Plasmodium alaudae (Celli & Sanfelice, 1891)
DESCRIPTION (Fig. 2C)
Th e average sized parasite is found in a rounded
highly hypertrophied RBC that is sometimes dis- MATERIAL EXAMINED. — France. Landes, Saint-Julien-
en-Born, 44°03’42’’N, 1°13’33’’W, blood smears of
coloured and whose nucleus is off -centre though
A. arvensis number 740U, 25.X.1996 (MNHN P2-
not in close contact with the cell edge. Among the
XXV, 24-43); 741U, 25.X.1996 (MNHN P2-XXV,
small or medium sized (<10 nuclei) Plasmodium 44-64).
species of the skylark, P. caloti n. sp. is the only one
where RBCs are modifi ed to this extent. DISTRIBUTION. — Italy (Celli & Sanfelice 1891); new
record for the Landes, France.
In general the shape of the immature and nearly
mature schizonts is rounded, their contours regular HOSTS. — Pica pica (type host); new record for Alauda
and the nuclei, usually 8 in number, are dense and arvensis.
are predominantly found at the periphery. As they
near maturity, these nuclei can bulge slightly to the REDESCRIPTION
outside. Th e abundant and homogeneous cytoplasm Th e parasites are small in size, and are found located
is pink coloured and contains a small number of at the apex of non-modifi ed RBCs where nuclei
vacuoles. Th e pigment is fi ne and agglomerated. are not displaced or only a little. Th e schizonts
Gametocytes are rounded like the schizonts and are compact and rounded, and the nuclei, eight
lie in rounded RBCs. in number, are dense roughly round with a clear
centre. Th e cytoplasm is relatively abundant with
DIFFERENTIAL DIAGNOSIS a few dispersed vacuoles and two granules of black
Plasmodium caloti n. sp. should be compared pigment. Th e gametocytes have not been identifi ed
to P. subpraecox, a parasite described briefl y and but are probably elongated.
376 ZOOSYSTEMA • 2009 • 31 (2)
Plasmodium (Apicomplexa) of the skylark (Alauda arvensis)
A A A A A A A
1 2 3 4 5 6 7
A B B B B B
8 1 2 3 4 5
B B C C C C C
6 7 1 2 3 4 5
C C D D D D D
6 7 1 2 3 4 5
E E E E E F F
1 2 3 4 5 1 2
FIG. 2. — A, Plasmodium reniai Chavatte & Landau, n. sp.; A1-A6, schizonts; A7, microgametocyte; A8, macrogametocyte; B, P. caloti
Chavatte & Landau, n. sp.; B-B, B, B, schizonts; B, macrogametocyte; C-C, P. alaudae (Celli & Sanfelice, 1891), schizonts;
1 4 6 7 5 1 7
D, P. ghadiriani Chavatte & Landau, 2007; D-D, schizonts; D, microgametocyte; D, macrogametocyte; E, P. rouxi Sergent, Sergent &
1 3 4 5
Catanei, 1928; E-E, schizonts; E, macrogametocyte; F, F, P. dherteae Chavatte & Landau, 2007, schizonts. Scale bar: 10 μm.
1 4 5 1 2
ZOOSYSTEMA • 2009 • 31 (2) 377
Chavatte J.-M. et al.
TAXONOMIC STATUS Plasmodium alaudae must also be distinguished
Celli & Sanfelice (1891) described Haemoproteus from P. caloti n. sp. (see below).
alaudae (later trasferred to Plasmodium) in the blood
of the skylark. At that time the authors elected to
reserve Plasmodium to the parasites of humans. Th is Plasmodium ghadiriani Chavatte & Landau, 2007
species was considered to be composed of three (Fig. 2D)
types in the blood that were distinguished by the
time required for development. When the fi gures MATERIAL EXAMINED. — France. Landes, Saint-Julien-
en-Born, 44°03’42’’N, 1°13’33’’W, blood smears of
published by these authors are carefully examined
A. arvensis number 741U, 25.X.1996 (MNHN P2-XXV,
(Celli & Sanfelice 1891: pl. III), it became clear
44-64).
that they were in fact dealing with multiple species,
not an unexpected occurrence in skylarks: a large DISTRIBUTION. — Seine-Saint-Denis, France (Chavatte
et al. 2007); new record for the Landes, France.
species with schizonts of 22-30 nuclei where the
RBC nuclei are displaced or even expelled (Celli & HOSTS. — Pica pica (type host); new record for Alauda
Sanfelice 1891: fi gs 19-21), a smaller apical spe- arvensis.
cies with 8 or 9 nuclei that does not displace the
RBC nucleus or only little (same, fi gs 16, 17), a REMARKS
latero-apical species with 18 nuclei where the RBC Th is parasite is identical to that described in the
nuclei is unaff ected (same, fi g. 18), and fi nally a magpie. Th e schizonts are large and elongate and
very small species with 8 nuclei where the RBC is lie next to the laterally displaced nucleus of the
slightly rounded and its nucleus displaced (same, RBC that is often enlarged. Young schizonts char-
fi g. 15). For the most part these species could not be acteristically contain a few large chromatin masses
confi dently ascribed to a known species. However, that will fragment into smaller rounded nuclei.
the taxon H. alaudae could be retained for the form Th e older schizonts observed contained 17 nuclei,
depicted in Celli & Sanfelice’s plate III, fi gs 16, consistent with the 18 to 24 nuclei enumerated in
17, for the species described above in view of the the magpie parasite.
following similarities: small size, apical position,
number of nuclei = 8, and little or no displacement
of the nuclei in RBCs that are neither rounded nor Plasmodium rouxi
hypertrophied. Sergent, Sergent & Catanei, 1928
Gametocytes could not be linked with confi dence (Fig. 2E)
with the gametocytes observed for this species.
MATERIAL EXAMINED. — France. Landes, Saint-Julien-en-
Born, 44°03’42’’N, 1°13’33’’W, blood smears of A. arvensis
DIFFERENTIAL DIAGNOSIS
number 740U, 25.X.1996 (MNHN P2-XXV, 24-43);
Plasmodium alaudae, by virtue of the number of
741U, 25.X.1996 (MNHN P2-XXV, 44-64).
nuclei (8) in the schizont, could be compared to
Plasmodium vaughani merulae Corradetti & Scanga, DISTRIBUTION. — Algeria (Sergent et al. 1928); new
record for the Landes, France.
1972, a parasite of Turdus merula Linnaeus, 1758,
where 8 merozoites can be observed per schizont HOSTS. — Culex pipiens (Sergent et al. 1928) (type host);
albeit rarely. However, the absence of a bluish Serinus canaria (Sergent et al. 1928); Passer hispaniolensis
refractile globule in P. alaudae clearly distinguishes (Sergent et al. 1929); new record for Alauda arvensis.
it from P. vaughani.
Plasmodium alaudae is close to the rounded apical REMARKS
forms of P. ashfordi that also produce 7 or 8 nuclei Th e characters that allow to identify this species
on average. It diff ers with respect to the absence of to P. rouxi are: the small size of the schizont, the
the fan-shaped schizonts that characterise P. ashfordi, rectangular form, the presence of four nuclei, the
and by its denser and clearly delimited nature. two unequal pigment grains, and the absence of
378 ZOOSYSTEMA • 2009 • 31 (2)