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Roger Jovani Æ Luisa Amo Æ Elena Arriero Oliver Krone Æ Alfonso Marzal Æ Peter Shurulinkov

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Roger Jovani Æ Luisa Amo Æ Elena Arriero

Oliver Krone Æ Alfonso Marzal Æ Peter Shurulinkov

Gustavo Tomas Æ Daniel Sol Æ Jana Hagen Pilar Lopez Æ Jose Martın Æ Carlos Navarro Jordi Torres
Double gametocyte infections in apicomplexan parasites of birds and reptiles

Abstract The simultaneous occurrence of male and female gametocytes inside a single host blood cell has been suggested to enhance apicomplexan transmission [’’double gametocyte infection (DGI) hypothesis’’]. We did a bibliographic search and a direct screen of blood smears from wild birds and reptiles to answer, for the first time, how common are these infections in the wild. Taking these two approaches together, we report here cases of DGIs in Plasmodium, Haemoproteus, Leucocy- tozoon and Hepatozoon, and cases of male–female DGIs in Haemoproteus of birds and reptiles and in Leucocy- tozoon of birds. Thus, we suggest that DGIs and male–

female DGIs are more widespread than previously thought, opening a new research avenue on apicom- plexan transmission.

In Plasmodium and related apicomplexan parasites, the occurrence of two or more gametocytes inside a single host blood cell recently attracted the attention of researchers for their potential to enhance parasite transmission between vertebrate hosts (Jovani 2002). In these microparasites, transmission occurs when the gametocytes contained in the host blood cells are in- gested within the bloodmeal of a suitable vector. Once in the vector, male and female gametes differentiate from

male and female gametocytes, respectively, and at least

R. Jovani (&)

Department of Applied Biology,

Estacion Biologica de Donana (CSIC), Avda.

Maria Luisa s/n, 41013 Sevilla, Spain


Tel.: +34-954-232340

Fax: +34-954-621125

L. Amo Æ E. Arriero Æ G. Tomas Æ P. Lopez Æ J. Martın

Department of Evolutionary Ecology,

Museo Nacional de Ciencias Naturales (CSIC),

Jose Gutierrez Abascal 2, 28006 Madrid, Spain

O. Krone Æ J. Hagen

Institute for Zoo and Wildlife Research,

P.O. Box 601103, 10252 Berlin, Germany

A. Marzal Æ C. Navarro

Department of Animal Biology,

Facultad de Ciencias, Universidad de Extremadura,

06071 Badajoz, Spain

P. Shurulinkov

Institute of Zoology, 1 Tzar Osvoboditel Blvd.,

1000 Sofia, Bulgaria

D. Sol

Department of Biology, McGill University,

1205 avenue Docteur Penfield, Montreal, Quebec,

H3A 1B1, Canada

J. Torres

Laboratory of Parasitology, Facultat de Farmacia,

Universitat de Barcelona, Av. Joan XXIII s/n,

08028 Barcelona, Spain

one of the mobile male gametes must search for and fertilize one of the immobile female gametes contained in the same bloodmeal. Gametocytes are normally alone within single host blood cells (e.g. erythrocytes), but they are also found in couples (double gametocyte infections, DGIs) or in trios (TGIs) within a given blood cell.

Female gametes are very small compared with the bloodmeal volume ingested by the vector; and male gametes do not seem to have any searching mechanism to find the female gamete (Gaillarg et al. 2003). Thus, it seems logical that some mechanism operating while in the vertebrate host could have evolved to increase the proximity of gametocytes and thus gametes when on the bloodmeal; and two non-mutually exclusive hypotheses have been proposed. Jovani (2002) proposed that male– female DGIs (i.e. one blood cell infected by one male and one female gametocyte) might reduce the time needed for male gametes to encounter female gametes, facilitating parasite transmission between vertebrate hosts. Gaillard et al. (2003) recently proposed that ery- throcytes infected by gametocytes could adhere among them in peripheral host capillaries, enhancing the probability of gamete encounter once in the vector bloodmeal.

The hypothesis proposed by Gaillard et al. (2003) agrees with the discovered pattern of aggregated distri- bution of erythrocytes infected by malaria gametocytes,

Table 1 Some examples of published data on the occurrence of multiple gametocyte infections in apicomplexan parasites. DGI Double gametocyte infection

Host Parasite Observation Reference

Columba livia Haemoproteus columbae

DGIs in 17 of 30 host individuals infected, with 14–97 DGIs in each individual host

Graczyk et al. (1994)

H. columbae A photograph of a male–female DGI Bennett and Peirce (1990)

H. columbae A photograph of a male–female DGI, a photograph of a TGI

Mushi et al. (1999)

Haemoproteus spp A photograph of a female–female DGI Tsai et al. (1986)

Geochelone denticulate

H. geochelonis Drawings and photographs of male–female

DGIs; text: ‘‘quite common’’

occurrence of DGIs

Lainson and Naiff (1998)

Birds Haemoproteus, Plasmodium, Leucocytozoon spp

Drawings of: immature DGIs from

20 Haemoproteus spp,

one immature TGI in H. kairullaevi,

one male–female DGI

in H. bennetti, one male–male DGI in H. ortalidum,

two immature DGIs in P. octamerium and P. columbae,

one immature DGI and one male–female DGI

in L. caulleryi

Valkiunas (1997)

Caiman c. crocodiles Hepatozoon caimani Photographs of DGIs and TGIs, sex unknown

Lainson et al. (2003)

Homalopsis buccata Hepatozoon spp Photograph of a DGI, sex unknown Salakij et al. (2002)

both in human blood (Gaillard et al. 2003) and in the vector bloodmeal (Pichon et al. 2000). The ‘‘DGI hypothesis’’ relies on the assumption that DGIs, and especially male–female DGIs, are widespread in nature, but this is currently unconfirmed (Jovani 2002). The goal of this note is to show that DGIs are widespread among in vivo apicomplexan parasites of wild populations of birds and reptiles. Moreover, we also report the occur- rence of other multiple gametocyte infections (MGIs, i.e. more than one gametocyte inside a single erythrocyte), because they inform us that the needed process to pro- duce a DGI does occur in a given host–parasite system, i.e. the entrance and growth into a given erythrocyte of more than one gametocyte.

We first systematically searched in the parasite liter- ature for cases of MGIs. Information regarding this kind of infection is little likely to appear in the title, abstract, or keywords of a publication. Consequently, we were forced to search our files for papers on apicomplexan infections; and then we accurately revised each paper for any mention of MGIs. Our survey found any reference on the possible relevance of MGIs for any aspect of the biology of the parasite. Indeed, some papers even con- tained photographs of DGIs, but without any mention in the text (e.g. Mushi et al. 1999). Despite this evident lack of attention of researchers for DGIs and MGIs as a whole, we found eight works with information on DGIs and TGIs (Table 1).

Moreover, from our own blood smear collection, we selected those blood samples of 11 bird and four reptile species infected by some apicomplexan parasites. These blood smears were collected from wild hosts in Germany and Spain during the period 1996–2002 (see Table 1). On each smear, we actively searched for MGIs on a portion equivalent to ca. 2,000 erythrocytes for Haemoproteus and Hepatozoon infections and ca. 25,000 erythrocytes for Leucocytozoon infections, recording when possible

the sex for mature gametocytes involved in a MGI. MGIs were found in most of the parasite–host associa- tions we examined (Table 2).

Moreover, from a parasite survey conducted by Shurulinkov and Golemansky (2002, 2003), P.S. revised their own notes taken during blood smear inspection in a search for records of MGIs. Although not comparable with the other samples because it was not a systematic search for MGIs, it is of qualitative importance and also denotes the low reporting of these infections in publi- cations, although present in the researchers’ notes. A total of 15 DGIs were recorded from 11 birds infected by Haemoproteus of five bird–parasite assemblages (bird–parasite [number of birds with DGIs, total num- ber of DGIs]: Sylvia borin–H. belopolskyi [1, 3], Lanius minor–H. lanii [2, 2], Lanius collurio–H. lanii [2, 2], Acrocephalus arundinaceus–H. payevskyi [2, 3], Musci- capa striata–H. pallidus [4, 5]). Most of these DGIs were constituted by female gametocytes. However, H. pay- evskyi infecting A. arundinaceus showed a case of a male–female DGI. Moreover, two cases of DGIs were recorded in Plasmodium polare infecting one individual of Hirundo rustica. See Shurulinkov and Golemansky (2002, 2003) for the total numbers of species and indi- viduals examined.

Our results support the view that DGIs are wide- spread in a variety of host–parasite associations, including Plasmodium, Haemoproteus, and Leucocyto- zoon infections of birds and Haemoproteus and Hepa- tozoon parasites of reptiles. Moreover, we found male–female DGIs in Haemoproteus parasites of birds and reptiles and in Leucocytozoon of birds, validating the major assumption of the ‘‘DGI hypothesis’’. The widespread occurrence of DGIs, and particularly of male-female DGIs, opens a promising direction for future research on the transmission strategies of api- complexan parasites.

Table 2 Occurrence of DGIs, male–female (m-f)DGIs, and triple gametocyte infections (TGIs) in blood smears inspected for this study.

N Number of infected individual hosts inspected, or number of individual hosts with at least one D/TGI. Numbers in

Host Country N N DGIs N m-f DGIs N TGIs
Haemoproteus parasites

Buteo buteo Germany 8 3 (1, 1, 2) 0 0

Falco tinnunculus Germany 3 0 – 0

F. subbuteo Germany 7 0 – 0

Tyto alba Spain 4 1 (3) 0 0

Bubo bubo Spain 21 3 (1, 2, 2) 0 0

parentheses indicate the number of D/TGIs in each

Strix aluco Germany,


21 10 (1, 2, 2, 2, 3, 4, 10, 11, 13, 27) 1 (1) 4 (1, 1, 3, 15)

infected host. – Sex of parasite could not be determined

Parus caeruleus Spain 46 10 (1, 1, 1, 1, 1, 2, 2, 3, 4, 6) 0 0

Delichon urbica Spain 57 7 (1, 1, 1, 1, 1, 1, 2) 1 (1) 0

Lanius collurio Spain 11 0 – 1 (1)

Passer domesticus Spain 39 11 (1, 1, 1, 1, 2, 2, 2, 2, 2, 5, 6) 4 (1, 1, 1, 1) 0

Leucocytozoon parasites

B. bubo Spain 19 0 – 0

Athene noctua Spain 2 0 – 0

Strix aluco Spain 5 0 – 0

Parus caeruleus Spain 15 2 (1, 2) – 0

Hepatozoon parasites

P. caeruleus Spain 9 0 – 0

Lacerta lepida Spain 38 0 – 0

L. monticola Spain 105 5 (1, 1, 1, 2, 3) – 0

Podarcis muralis Spain 28 0 – 0

P. hispanica Spain 19 0 – 0

Acknowledgements The authors thank Juan A. Fargallo, Jesus Martınez, Marilo Romero, Alberto Lizarraga, Francisco Campos, Santiago Merino, Juan Moreno, Judith Morales for their fieldwork and Javier Caldera for allowing the collection of blood smears at the Wildlife Recuperation Centre of ‘‘Los Hornos’’. Grants and funds are as follows: R.J. (Telefonica Mobiles S.A.), L.A. (C.S.I.C.–Ventorrillo, BOS 2002–00598, BOS 2002–00547), E.A. (C.S.I.C.–Ventorrillo, 07 M/0137/2000), A.M. (Junta de Extrema- dura, FIC01A043), G.T. (Residencia de Estudiantes; FPI from Comunidad de Madrid, BOS2000–1125, BOS2001–0587). This study has been done according to the current laws of each country.

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