Santiago Alarcon Et Al2012DipteraVectorsOfAvianHaemosporidianParasites

Biol. Rev. (2012), 87, pp. 928964. doi: 10.1111/j.1469-185X.2012.00234.
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Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy
Diego Santiago-Alarcon1,2, , Vaidas Palinauskas3 and Hinrich Martin Schaefer2
1 2
Biologa y Conservaci on de Vertebrados, Instituto de Ecologa, A.C., carretera antigua a Coatepec 351, Xalapa, C.P. 91070, M exico Department of Ecology and Evolutionary Biology, Faculty of Biology I, Hauptstr. 1, University of Freiburg, Freiburg 79104, Germany 3 Institute of Ecology, Nature Research Center, Akademijos 2, Vilnius 2100, LT-08412, Lithuania
ABSTRACT Haemosporida is a large group of vector-borne intracellular parasites that infect amphibians, reptiles, birds, and mammals. This group includes the different malaria parasites (Plasmodium spp.) that infect humans around the world. Our knowledge on the full life cycle of these parasites is most complete for those parasites that infect humans and, to some extent, birds. However, our current knowledge on haemosporidian life cycles is characterized by a paucity of information concerning the vector species responsible for their transmission among vertebrates. Moreover, our taxonomic and systematic knowledge of haemosporidians is far from complete, in particular because of insufcient sampling in wild vertebrates and in tropical regions. Detailed experimental studies to identify avian haemosporidian vectors are uncommon, with only a few published during the last 25 years. As such, little knowledge has accumulated on haemosporidian life cycles during the last three decades, hindering progress in ecology, evolution, and systematic studies of these avian parasites. Nonetheless, recently developed molecular tools have facilitated advances in haemosporidian research. DNA can now be extracted from vectors blood meals and the vertebrate host identied; if the blood meal is infected by haemosporidians, the parasites genetic lineage can also be identied. While this molecular tool should help to identify putative vector species, detailed experimental studies on vector competence are still needed. Furthermore, molecular tools have helped to rene our knowledge on Haemosporida taxonomy and systematics. Herein we review studies conducted on Diptera vectors transmitting avian haemosporidians from the late 1800s to the present. We also review work on Haemosporida taxonomy and systematics since the rst application of molecular techniques and provide recommendations and suggest future research directions. Because human encroachment on natural environments brings human populations into contact with novel parasite sources, we stress that the best way to avoid emergent and reemergent diseases is through a program encompassing ecological restoration, environmental education, and enhanced understanding of the value of ecosystem services. Key words: Haemosporida, malaria, Plasmodium, Haemoproteus, Leucocytozoon, Diptera, Culicidae, Ceratopogonidae, Hippoboscidae, Simuliidae, insect vector. CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (1) Haemosporidian parasites and their vectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (2) Methods for the study of haemosporidian parasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. Diptera vectors transmitting avian haemosporidian parasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (1) Family Culicidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (a) Taxonomic issues for parasites transmitted by Culicidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (2) Family Hippoboscidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (a) Taxonomic issues for parasites transmitted by Hippoboscidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 929 929 930 931 931 943 943 945
* Address for correspondence (Tel: +55 228 842 1800 ext. 4135; Fax: +55 228 818 60 09; E-mail: diego.santiago@inecol.edu.mx; onca77@gmail.com).
Biological Reviews 87 (2012) 928964 2012 The Authors. Biological Reviews 2012 Cambridge Philosophical Society
Avian haemosporidian vectors and taxonomy

(3) Family Simuliidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (a) Taxonomic issues for parasites transmitted by Simuliidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (4) Family Ceratopogonidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Advances since the rst application of molecular methods (PCR) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Future directions in understanding the ecology and evolution of haemosporidian parasites . . . . . . . . . . . . . . . . (1) A current limitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (2) The dynamic nature of haemosporidian transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (3) Taxonomy and systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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III. IV.
V. VI. VII.
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I. INTRODUCTION (1) Haemosporidian parasites and their vectors Vector-borne parasites of the order Haemosporida (Phylum Apicomplexa) are commonly found in amphibians, reptiles, birds, and mammals (Valki unas, 2005). Avian haemosporidian parasites have a cosmopolitan distribution and are divided into four genera: Plasmodium, Haemoproteus, Fallisia and Leucocytozoon (Atkinson & van Riper, 1991; Valki unas, 2005). The four genera of haemosporidian parasites have similar life cycles with differences during the asexual phase in the peripheral blood of their vertebrate host. Plasmodium and Fallisia can undergo asexual reproduction in the peripheral blood of the host (i.e. merogony), whereas this is not the case in the other parasite genera (Valki unas, 2005). Plasmodium species are considered to be highly virulent, particularly in immunologically nave hosts (van Riper et al., 1986; Atkinson et al., 1995, 2000; Yorinks & Atkinson, 2000; Palinauskas et al., 2008, 2009, 2011). Leucocytozoon is known to be highly pathogenic in poultry such as turkeys and ducks (Valki unas, 2005). Haemoproteus was considered to be relatively benign without causing serious harm to their hosts (Atkinson, 1991; Bennett, 1993; Bennett, Peirce & Earl e, 1994), but more recent evidence demonstrates that Haemoproteus can have signicant impacts and some species are highly virulent and lethal (Nordling et al., 1998; Merino et al., 2000; Marzal et al., 2005; Valki unas, 2005). Avian haemosporidians use dipteran insect vectors during their sexual and sporogonic phases (Garnham, 1966; Valki unas, 2005; Martinsen, Perkins & Schall, 2008). Plasmodium species are known to be transmitted by several species of mosquitoes (Culicidae) from different genera (Garnham, 1966; Atkinson & van Riper, 1991; Valki unas, 2005; Kimura, Darbro & Harrington, 2010); Haemoproteus is known to be transmitted by several species of hippoboscid and ceratopogonid ies (Baker, 1957; Atkinson, 1991; Valki unas, Liutkevicius & Iezhova, 2002; Valki unas et al., 2010a); Leucocytozoon species are known to be transmitted by simuliid ies (Malmqvist et al., 2004; Valki unas, 2005; Hellgren, Bensch & Malmqvist, 2008) and ceratopogonid ies for the subgenus Akiba (Akiba, 1960; Morii, Kitaoka & Akiba, 1965; Morii & Kitaoka, 1968), and there is some evidence that Fallisia parasites are transmitted by mosquitoes (Gabaldon, Ulloa & Zerpa, 1985). However, insect vectors represent
the life-cycle stage of haemosporidian parasites that we least understand; further studies are needed into the ecological and evolutionary dynamics of these host-parasite-vector systems particularly the inclusion of blood-feeding dipterans from the families Ceratopogonidae, Simuliidae, and Hippoboscidae. There are three taxonomic issues relevant to a discussion of haemosporidian parasite genera and their vectors. First, the validity of the Plasmodium subgenera Novyella and Giovannolaia was questioned by Corradetti & Scanga (1965) and recently by Martinsen, Paperna & Schall (2006); there are several Plasmodium species whose subgeneric position is difcult to identify, particularly at low parasitemia. Second, the genus Haemoproteus was divided into two groups (the H. columbae group and the H. nettionis group) (Baker, 1963); these two groups later were named as the subgenera Haemoproteus and Parahaemoproteus (Bennett, Garnham & Fallis, 1965; Valki unas, 2005). They are well classied in terms of the vectors transmitting them and their morphological features, but it is currently unknown if they are monophyletic or paraphyletic (Outlaw & Ricklefs, 2011). Third, the genus Leucocytozoon was reclassied into two genera Leucocytozoon and Akiba (Bennett et al., 1965) because they were transmitted by different Diptera families, but recently they were reclassied as one genus with two subgenera (Valki unas, 2005). Leucocytozoon and Akiba, unlike Plasmodium and Haemoproteus, are apparently able to metabolize the whole haemoglobin molecule, and no pigment, i.e. haemozoin, is left undigested. We suggest that when taxonomic descriptions are expanded to include competent vector species and sporogonic morphological traits, many of the current taxonomic problems will be resolved. Because parasite species of the genus Plasmodium represent a constant threat to human health, most studies on haemosporidian parasites have been directed at species infecting humans (Escalante & Ayala, 1994; Escalante, Barrio & Ayala, 1995; Escalante et al., 1998; Hughes & Verra, 2001; Joy et al., 2003; Paul, Ariey & Robert, 2003; Rich et al., 2009; Prugnolle et al., 2010). This results in a high number of vector studies focusing on a few species (52 anopheline spp. worldwide; Enayati & Hemingway, 2010) of mosquitoes (Diptera: Culicidae) transmitting human malaria parasites (e.g. Dong, Manfredini & Dimopoulos, 2009; Muenworn et al., 2009; Muturi et al., 2009; Swain et al., 2009). Furthermore, there is abundant research on the control and
930 eradication of human malaria ranging from the simple use of mosquito nets (Lef` evre et al., 2009; Michalakis & Renaud, 2009; Enayati & Hemingway, 2010) to interrupting the cellular and molecular mechanics of parasite development in the mosquito vector (e.g. Ghosh & Jacobs-Lorena, 2009; Reininger et al., 2009), including the use of genetically modied mosquitoes (Rakov, Bevilacqua & Wyse, 2009; Enayati & Hemingway, 2010). The most recent review on the management of human malaria addresses advances in the control and attempted eradication of malaria, such as the development of new drugs, vaccines, transgenic mosquitoes, and better human infrastructural capacity (Enayati & Hemingway, 2010). Owing to this focus, the need to survey the biodiversity of haemosporidian parasites in other mammal and vertebrate groups and the vectors transmitting them has rarely been recognised, despite the fact that at least two of the human malaria types (Plasmodium vivax and Plasmodium falciparum) probably originated from wild monkeys (Escalante et al., 2005; Mu et al., 2005; Hayakawa et al., 2008; Rich et al., 2009; Prugnolle et al., 2010). The 52 known Anopheles species that vector human malaria around the world are not the only Diptera vectors biting humans. For example, Culex mosquitoes were believed to transmit strictly avian malaria, but an early, yet unconrmed, report showed that the mosquito Cx. bitaeniorhynchus is susceptible to mixed infections of human P. vivax, Plasmodium malariae, and P. falciparum (Williamson & Zain, 1937). It was shown that Culex lines forced to feed on either birds or mammals became adapted to the blood of the host from which they fed (Huff, 1965). Furthermore, many species from the genus Culicoides (Diptera: Ceratopogonidae) are pests of human populations around the world, transmitting many different parasites (e.g. viruses, haemoproteids, worms) to mammals, birds, and reptiles (Borkent, 2005), suggesting that haemosporidian parasites might jump across different vertebrate groups (e.g. Huff, 1929; Herman, 1938; Coggeshall, 1940; McGhee, 1951; Santiago-Alarcon et al., 2012). In sum, we argue that attention should be given to the broad range of haemosporidian parasites, their vectors, feeding habits, and the evolutionary and ecological interactions between these parasites and their vectors. The bias in research efforts directed to the study of Culicidae vectors is also observed in avian haemosporidian research (e.g. Valki unas, 2005; Kimura, Dhondt & Lovette, 2006; Kim, Tsuda & Yamada, 2009b; Njabo et al., 2009). This is because mosquito vectors are relatively easy to work with both in the laboratory and in the wild, and because research efforts focus on species of Culicidae due to their role in human malaria (Huff, 1927; Valki unas, 2005). Two problems result from this lack of knowledge: rst, because we do not know the sporogonic phase (i.e. insect vector) of the life cycle for most haemosporidian parasites, we lack knowledge on the species they interact with directly and indirectly. This limitation hinders progress in understanding the evolutionary ecology of the groupor as expressed by Huff (1938, p. 42) Many of the contradictions grew out of false generalizations based upon work with one species of mosquito or upon the
D. Santiago-Alarcon and others

study of one species under only one type of biological habitat. Second, from a practical point of view, human encroachment into natural habitats brings us into contact with novel haemosporidian parasite species (e.g. Chasar et al., 2009), transmitted by unknown vectors, some of which are likely to have exible host preferences (e.g. Lef` evre et al., 2009; Santiago-Alarcon et al., 2012). Thus, it is important to know the range of haemosporidians that can enter the bloodstream of humans, even if they do not develop into a disease. (2) Methods for the study of haemosporidian parasites Avian haemosporidian research involved mainly traditional microscopy methods and experimental approaches during the last 100 years (see Garnham, 1966, and Valki unas, 2005, for reviews). This eld has expanded greatly during the last decade due to the wide application of molecular techniques (e.g. Bensch et al., 2000; Perkins & Schall, 2002; Ricklefs & Fallon, 2002; Perkins, Sarkar & Carter, 2007; Martinsen et al., 2008; Santiago-Alarcon et al., 2010). It has become clear that a combination of microscopy and molecular techniques produces more reliable results than each technique in isolation (Valki unas et al., 2006, 2008a, 2009a; Hellgren et al., 2007). Furthermore, microscopy techniques have improved to the extent that we are able to excise single parasite cells out of a blood smear (Palinauskas et al., 2010), allowing us to assign condently a morphologically identied parasite species to a set of DNA sequences (Palinauskas et al., 2010). These methodological improvements will soon enable us to delineate the genetic diversity (i.e. parasite DNA lineages) associated with morphologically determined haemosporidian parasite species (Martinsen et al., 2006; Hellgren et al., 2007; Palinauskas et al., 2007; Valki unas et al., 2007a, b, 2010a, b; Kri zanauskien e et al., 2010), and to obtain a better understanding of the taxonomy, systematics, and evolutionary ecology of this diverse group of parasites. Molecular methods can be applied to determine the ecological interactions of Haemosporida parasites with both their vertebrate and invertebrate hosts (Hellgren et al., 2008). Recently, the polymerase chain reaction (PCR) has been used to determine vector host preferences (Alcaide et al., 2009), and to detect haemosporidian sporogonic stages in vectors salivary glands (e.g. Ishtiaq et al., 2008; Njabo et al., 2009). Ishtiaq et al. (2008) found a broad range of mosquito species to be potential transmitters of related or identical parasite lineages and speculated that culicine and anopheline mosquitoes could probably also act as vectors of Haemoproteus parasites. These conclusions await detailed experimental conrmation. Hellgren et al. (2008) used blood meals of wild-caught blackies (Diptera: Simuliidae) for molecular identication of haemosporidians and of bird hosts, and found that blacky species were closely associated with different bird host groups. Njabo et al. (2009) tested Coquillettidia mosquitoes blood meals for malaria parasites in Cameroon and concluded that they might be major vectors of avian malaria parasites. Note that the taxonomic resolution differs between molecular and morphological studies (genetic

lineages when using DNA sequences versus morphospecies when using microscopy), which might lead to different conclusions. For example, a cophylogenetic analysis is likely to show a different cospeciation history between parasites and their hosts when using genetic lineages (which would be more like a cophylogeographic history) compared with morphological species. In addition, microscopy studies carry a risk of clumping cryptic species together (e.g. Sehgal et al., 2006; Valki unas et al., 2010b). Field and laboratory experimental infection studies were used to identify Diptera vectors transmitting haemosporidian parasites from the end of the 19th Century to the end of the 20th Century (e.g. Huff, 1927; Atkinson, Greiner & Forrester, 1983). Emphasis changed dramatically in recent years, however, and now most studies use the PCR method to identify vector feeding preferences (e.g. Imura et al., 2010) and sporogonic stages in salivary glands (e.g. Valki unas et al., 2010a). Whereas experimental infection studies can provide denitive statements about vectorial capacity, PCR studies can only identify natural putative vectors for the haemosporidian parasites under study, leaving unclear the vectorial capacity, as PCR methods cannot prove that the life cycle of the parasite will be completed. Thus, ideally a combination of both experimental infection and PCR methods should be used in order to determine the natural vectors of haemosporidian parasites. This review aims (i ) to review the work that has been done on dipteran vectors transmitting avian haemosporidian parasites since the early 1900s; (ii ) to review the work done on the taxonomy and systematics of avian haemosporidians since the rst application of molecular techniques; and (iii ) to integrate this knowledge in order to suggest areas where additional research is needed.
931 for human malaria research. Despite that, they remain convenient model organisms for investigations into the general biology of Plasmodium spp. and their close relatives, including questions of the evolution of haemosporidians. The list of discoveries and achievements using avian malarial models includes new antimalarial drugs (Davey, 1951; Coatney et al., 1953), the rst cultivation methods of tissue and erythrocytic stages in vitro (Trager, 1950; Ball & Chao, 1961), and the rst steps in the development of an antimalarial vaccine (McGhee, Singh & Weathersby, 1977). Ball (1964) described a technique for the cultivation of the sporogonic cycle of Plasmodium relictum: it was possible to grow P. relictum in vitro from the gametocyte stage to infective Sporozoites. At the beginning of the 20th Century many studies attempted to survey the different genera and species of mosquitoes in order to identify possible competent vectors for Plasmodium parasites (Huff, 1927, 1932a, 1965; Reichenow, 1932; Raffaele, 1934; Herman, 1937; Coggeshall, 1940; Laird, 1941; Hurlbut & Hewitt, 1942; Jeffrey, 1944; Manwell, 1947; Micks, 1949; Corradetti & Scanga, 1965; Niles, Fernando & Dissanaike, 1965; Garnham, 1966). Such experimental infections often used canaries as a model system, and vector competence was tested mostly using mosquitoes from the genera Culex and Aedes (Huff, 1927; Herman, 1938; Manwell, 1940; Laird, 1941; Jeffrey, 1944; Micks, 1949). Some researchers used other bird species, such as ducks, pheasants, pigeons, and chickens, in experimental infections in response to the high mortality and infection refraction of some bird species to some Plasmodium parasites (Coatney, 1938; Laird, 1941; Jeffrey, 1944; Micks, 1949; Becker, 1961). By 1907 it was proven that mosquitoes of two genera Culex and Aedes were vectors of several avian malaria parasites (Ross, 1898; Koch, 1899; Ruge, 1901; Daniels, 1899; Sergent & Sergent, 1907). Subsequently, additional species of Culex and Aedes and other genera were recognized as competent vectors in the transmission of avian malaria. By 1918 it was known that bird Plasmodium could be transmitted by seven mosquito species of three genera [Culex, Aedes, and Culiseta (as Theobaldia) (Huff, 1927)]. Huff (1927) investigated vector susceptibility of another nine mosquito species and two new genera (Psorophora and Anopheles) infected with three Plasmodium spp. From these, only two new species (Culex territans and Cx. salinarius) were added to the list of susceptible vectors of which only Cx. salinarius was competent at transmitting Plasmodium cathemerium (Huff, 1927). Reichenow (1932) discovered that mosquitoes of the genus Culiseta transmit Plasmodium circumexum. Corradetti & Scanga (1965) successfully transmitted Plasmodium polare using Culiseta longiareolata. Niles et al. (1965) described Coquillettidia (as Mansonia) crassipes as a natural vector of Plasmodium gallinaceum. Mayne (1928) showed for the rst time that malaria vectors of the genus Anopheles, which were considered only to transmit human malaria, might also transmit avian malaria. Later Coggeshall (1940) in experiments with Plasmodium lophurae proved that Anopheles quadrimaculatus is capable of transmitting parasites other than human malarias (i.e. Plasmodium falciparum, P. vivax, and P. malariae). All these
II. DIPTERA VECTORS TRANSMITTING AVIAN HAEMOSPORIDIAN PARASITES (1) Family Culicidae By the end of the 1800s it was believed that there was only one species of avian malaria parasite; this subsequently was proved incorrect (Huff, 1927; Herman, 1938). R. Ross rst discovered the involvement of a mosquito in the transmission of an avian Plasmodium parasite in 1897 (Ross, 1898; Cox, 2010 reviewed the history of this discovery); the involvement of an Aedes mosquito was rst described by Koch (1899) (Aedes communis; Huff, 1927, 1932a). Since then, bird malaria parasites attracted the attention of researchers as an experimental model for the investigation of human malaria; they were so used by many laboratories until the discovery of rodent malaria parasites in 1948 (Killick-Kendrick, 1974) and the successful infection of the Aotus trivirgatus monkey with human malaria parasites in 1966 (Young, Porter & Johnson, 1966). Rodent and monkey malaria parasites are closer to human malaria in numerous ways (Mulligan & Sinton, 1933); hence bird haemosporidians became less attractive
932 studies showed that Plasmodium parasites are able to use many vector species during the transmission cycle, and that some vectors are capable of feeding on different vertebrate hosts, some of which are not closely related. At present, more than 20 species of anopheline mosquitoes are known in which sporogony of avian malaria parasites is completed (Valki unas, 2005). Species of the genus Anopheles susceptible to avian malaria belong to three subgenera: Anopheles, Nyssorhynchus and Cellia (as Myzomyia) (Huff, 1965). Anopheles mosquitoes are known to be viable vectors of P. cathemerium, P. gallinaceum, P. lophurae, P. fallax, and P. relictum (Huff, 1965; Valki unas, 2005). There was no evidence until 1937 that mosquitoes of Culex and Aedes could be vectors of human malaria parasites. Williamson & Zain (1937) fed Cx. bitaeniorhynchus on patients with mixed infections of P. vivax and P. falciparum, and of P. malariae and P. falciparum. Sporozoites of all tested malaria species developed in the salivary glands of laboratory-bred Culex mosquitoes, but the infectivity of the sporozoites was not tested on human subjects. Warren & Wharton (1963) showed that subspecies of P. cynomolgi form Oocysts in Culex, Aedes and Mansonia mosquitoes. However, the development of Oocysts does not mean that the insects were able to transmit malaria parasites. Even though there was no conrmation that P. falciparum and P. vivax were able to complete their life cycle after Culex transmission, it remains possible that culicines are competent vectors for human Plasmodium species. In reptiles, Klein, Young & Telford (1987a) demonstrated that Cx. erraticus is a competent vector for P. oridense, a lizard parasite. Ayala (1971) showed that P. mexicanum (a lizard malaria parasite) completed its sporogonic cycle in two sandy species [Lutzomyia vexator (as Lutzomyia vexatrix occidentis, but subspecies not recognized to date) and Lutzomyia stewarti ]. Later, Lutzomyia vexator was conrmed to be a competent vector for P. mexicanum by Klein et al. (1987b). Petit et al. (1983) showed that Plasmodium agamae developed partially (the Oocysts developed sporozoites, but these never reached the salivary glands) in Culicoides nubeculosus (Ceratopogonidae). Table 1 shows the results of experimental and natural infections of Culicidae vectors for different avian Plasmodium species (see also Huff, 1965, for a comprehensive review of mosquitoes susceptibility to species of avian Plasmodium). There are very few studies testing the ability of avian Plasmodium parasites to develop in bloodsucking vectors other than Culicidae. There could be other vector families transmiting Plasmodium parasites, such as in some lizard Plasmodium species as described above. Species of Culicidae have a heterogeneous specicity for malaria parasites. Some Culicidae species are competent for only a small number of Plasmodium species, whereas others seem to be generalists (Huff, 1927, 1932a; Herman, 1938; Laird, 1941; Jeffrey, 1944; Manwell, 1947). For example, Coggeshall (1940) showed that An. quadrimaculatus (a vector of human Plasmodium parasites in the US) can be infected by both a monkey parasite (P. cynomolgi ) and an avian parasite (P. lophurae). Furthermore, specicity of a parasite can be altered by articial selection that increases or

decreases susceptibility of the vector to infection (Huff, 1929; Trager, 1942; Micks, 1949), and adaptation of an avian parasite (P. lophurae) to a mammal host has been observed following a few infectious injections (as few as four infectious passages) of infected avian cells into infant mice at different time steps (McGhee, 1951). Moreover, it is also possible to modify the host range of species of Culicidae under experimental conditions; for instance, Culex apicalis is known naturally to feed on cold-blooded vertebrates, but is able to utilize canary blood under experimental conditions (Herman, 1938). This suggests that it is possible for vectors to feed on alternative suboptimal hosts, providing an opportunity for parasites to switch hosts across distantly related vertebrates (e.g. Santiago-Alarcon et al., 2012). The time frame and stability of a vector-parasite-vertebrate interaction could lead to tight coevolution, and thus, to a specic interaction. However, such specic interactions could vary according to geographical location, producing a mosaic of coevolutionary interactions, where the parasite, vector, or vertebrate host may change depending on local environmental conditions (Huff, 1938; Thompson, 2005). Ecological factors such as spatial heterogeneity and phenology may be important in determining which parasite species are transmitted by which vectors (Huff, 1938; Applegate & Beaudoin, 1969). Even when a vector is experimentally susceptible to a Plasmodium parasite, if in nature they do not have overlapping niches they will never meet unless a change in environmental conditions allow them to come into contact. The genetic variation within haemosporidian parasites might be another factor determining the specicity or generality of an insect vector. A parasite with a larger spectrum of genetic lineages could be more likely to be transmitted by a larger array of vector species, whereas a parasite with low genetic variation is likely to be transmitted only by vectors to which it is already adapted. Environmental conditions, especially temperature, may also be important factors for the development of different malarial parasites in mosquitoes. Grassi (1900) showed that temperatures as low as 15.5 and 17.5 C for nine days were lethal for P. vivax and P. falciparum, suggesting that mosquitoes exposed to such conditions immediately after feeding would not develop an infection. By contrast, Sergent (1919) showed that exposure of P. relictum to 12 C for 6 h immediately after vector feeding did not interfere with the development of the parasite and sporozoites were formed. James (1926) reported that oocysts and sporozoites of P. vivax are able to resist temperatures of 45.5 C for three weeks, or below freezing temperature for six days. Chao & Ball (1961) showed that temperatures as low as 4 C are not immediately lethal to P. relictum infecting Culex tarsalis, even if exposure to the cold temperature occured as soon as 15 min after biting and continued for 48 h. Oocysts can be exposed to temperatures as low as 4 C for 23 days and will still retain the ability to develop after the host is returned to benecial conditions (Ball & Chao, 1961). Taken together, these studies suggest that there is considerable variation in the ability of Plasmodium species to withstand low temperatures.
Table 1. Experimental studies demonstrating full or partial (part of the life cycle has not been demonstrated experimentally) vectorial competence of different species of Culicidae transmitting parasites of the genera Plasmodium and Fallisia. Information not obtained from the primary literature was acquired from Garnham (1966) and Valki unas (2005)
PCR method
Parasite species Region India, USA Germany, Algeria, USA, Columbia Algeria USA USA USA USA India India India India Philippines Germany Algeria Sporozoite Sporozoite NA Oocyst Oocyst Sporozoite Sporozoite Sporozoite Sporozoite Germany NA NA NA NA NA NA Algeria, USA Algeria USA USA USA USA USA India + + + + + + Sporozoite Sporozoite + NA +
Vector species
Proven experimentally
Proven natural vector
Most advanced developmental stage observed in vector PCR on PCR on whole vector blood unengorged meal vectors PCR on thoracic parts of vectors
References
Plasmodium relictum
Culex quinquefasciatus (as Cx. pipiens fatigans in old literature) Cx. pipiens
Cx. hortensis Cx. territans Cx. salinarius Cx. tarsalis NA + + Sporozoite Sporozoite Oocyst Oocyst Oocyst Sporozoite Oocyst NA NA Sporozoite Oocyst Oocyst Sporozoite + + + + + +
+ +
Cx. stigmatosoma
Cx. bitaeniorhynchus
Ross (1898), Daniels (1899), Huff (1927), and Rosen & Reeves (1954) Ruge (1901), Sergent & Sergent (1907), Neumann (1908), Huff (1927), Tate & Vincent (1934), and Hunninen (1951, 1953) Sergent & Sergent (1918) Huff (1927) Huff (1927) Huff (1932a), Herman et al. (1954), and Rosen & Reeves (1954) Herman et al. (1954) and Rosen & Reeves (1954) Russell & Mohan (1942) and Singh & Mohan (1955) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942) Nono (1932) Reichenow (1932) Sergent & Sergent (1918) Koch (1899)
Cx. gelidus Cx. theileri Cx. whitmorei Lutzia fuscanus (as Cx. fuscanus in old literature) Culiseta annulata (as Theobaldia annulata in old literature) Cs. longeareolata (as Theobaldia spathipaopos in old literature) Aedes communis (as Cx. nemorosus in old literature) Ae. aegypti
Ae. mariae Ae. dorsalis Ae. vexans Anopheles crucians An. freeborni An. quadrimaculatus An. subpictus
Sergent & Sergent (1907, 1918) and Huff (1927) Sergent & Sergent (1918) Rosen & Reeves (1954) Rosen & Reeves (1954) Hunninen (1951) Hunninen (1951) Hunninen (1951, 1953) Mayne (1928)
933
934
Table 1. (Cont.)
PCR method PCR on thoracic parts of vectors References + + + Most advanced developmental stage observed in vector Region Panama USA USA USA USA, Japan USA Japan Japan USA USA USA USA Brazil Philippines France, India, USA, Nigeria, Japan France, India, USA, Japan France Brazil India India India India India India India Sporozoite Oocyst Oocyst Oocyst Oocyst Oocyst Sporozoite Oocyst Oocyst NA NA Oocyst Oocyst Oocyst Sporozoite PCR on whole PCR on vector blood unengorged vectors meal
Parasite species + NA NA NA NA NA NA + + + +
Vector species
P. cathemerium
An. albimanus Cx. salinarius Cx. territans Cx. pipiens
Cx. quinquefasciatus
Hunninen (1951, 1953) Huff (1927) Huff (1927) Huff (1927) and Herman (1938) Huff (1927), Tanaka (1946), and Micks & McCollum (1953) Huff (1932a) Tanaka (1946) Tanaka (1946) Huff (1927) Herman (1938) Herman (1938) Micks & McCollum (1953) Barreto (1943) Nono (1932)
P. gallinaceum
Cx. tarsalis Cx. bitaeniorhynchus Cx. tritaeniorhynchus Ae. aegypti Ae. sollicitans Cs. melanura (as Cs. melaneum in Valki unas, 2005) An. quadrimaculatus An. norestensis Lutzia fuscanus (as Culex fuscanus in old literature) Ae. aegypti
Ae. albopictus NA
Sporozoite
Ae. geniculatus Ae. lepidus Ae. pseudotaeniatus Ae. pseudalbopictus Ae. scutellaris Ae. unilineatus Ae. vittatus Ae. chrysolineatus Armigeres kuchingensis NA NA
+ + + + + + + + +
Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite
Brumpt (1935, 1936), Russell & Mohan (1942), Cantrell & Jordan (1949), Okpala (1958), Weathersby (1962), Huff (1965), and Kim et al. (2009a) Brumpt (1935, 1936), Russell & Mohan (1942), Cantrell & Jordan (1945), and Weathersby (1962) Roubaud et al. (1939) Paraense (1945) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942) Russell & Mohan (1942)
Table 1. (Cont.)
PCR method
Parasite species + + + + + + + + + + Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Oocyst Sporozoite Oocyst Sporozoite Oocyst Oocyst Oocyst Sporozoite Sporozoite Oocyst Sporozoite Sporozoite Oocyst Sporozoite Sporozoite Oocyst Oocyst Oocyst NA Sporozoite NA NA Oocyst Oocyst Sporozoite USA USA India India India Japan Mexico India USA USA Japan Sri Lanka USA USA Italy USA + India USA USA USA + + India USA USA USA USA USA Nigeria Japan Japan India USA India, USA + + NA NA NA NA + + + + + + + + NA NA NA NA NA NA
Vector species
Proven experimentally Region
Most advanced developmental stage observed in vector References
PCR on PCR on whole vector blood unengorged meal vectors
PCR on thoracic parts of vectors
Ar. obturbans Ae. triseriatus Ae. campestris Ae. cantator Ae. stimulans Ae. atropalpus Ae. stokesi Ae. japonicus Ae. togoi Ae. albolatoralis Ae. canadensis Ae. jamesi
Ae. pallirostris Ae. trivittatus Ae. vexans Cs. inornata (as Theobaldia innorata in old literature) An. quadrimaculatus
Russell & Menon (1942) Cantrell & Jordan (1945) Cantrell & Jordan (1945) Cantrell & Jordan (1945) Cantrell & Jordan (1945) Trembley (1946) Okpala (1958) Weathersby (1962) Weathersby (1962) Russell & Menon (1942) Cantrell & Jordan (1949) Russell & Menon (1942) and Cantrell & Jordan (1945) Russell & Mohan (1942) Cantrell & Jordan (1945) Cantrell & Jordan (1945) Cantrell & Jordan (1945) Haas & Akins (1947) and Cantrell & Jordan (1949) Eyles (1960) Eyles (1960) Russell & Mohan (1942) Russell & Menon (1942) Russell & Menon (1942) Weathersby (1962) Vargas & Beltran (1941) Russell & Menon (1942) Cantrell & Jordan (1945) Huff (1965) Kim et al. (2009a) Niles et al. (1965) Cantrell & Jordan (1945) Huff (1937) and Manwell (1940, 1947) Corradetti et al. (1962)
P. matutinum
An. freeborni An. albimanus Ar. aureolineatus Ar. annulipalpis Ar. magnus Ar. subalbatus Cx. quinquefasciatus Cx. mimeticus Cx. salinarius Cx. tarsalis Cx. pipiens pallens Coquillettidia crassipes (as Mansonia crassipes in old literature) Cq. perturbans (as M. perturbans in Valki unas, 2005) Cx. pipiens [as Cx. fatigans (quinquefasciatus) in Huff, 1937] Cx. stigmatosoma
935
Table 1. (Cont.)
PCR method
936
Parasite species + + + + Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite USA Italy Italy Italy USA + NA NA
Vector species
Proven experimentally Region References
Most advanced developmental stage observed in vector
P. subpraecox P. giovannolai P. fallax
Cx. tarsalis Cx. pipiens Cx. pipiens Ae. albopictus
Ae. aegypti
P. polare
+ + + + + + + + Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Oocyst Sporozoite Sporozoite Sporozoite USA USA USA USA USA USA USA USA USA Italy Canada Canada NA NA NA + + +
NA +
Corradetti et al. (1962) Raffaele (1932) Corradetti et al. (1963a, b) Huff et al. (1950) and Huff (1965) Huff et al. (1950) and Huff (1965) Huff et al. (1950) Huff et al. (1950) Huff et al. (1950) Huff et al. (1950) Huff (1965) Corradetti & Scanga (1965) Meyer & Bennett (1976) Meyer & Bennett (1976)
P. lophurae
Ae. atropalpus Ae. triseriatus An. quadrimaculatus Cx. quinquefasciatus Cx. tarsalis Cs. longiareolata Cs. morsitans Cq. perturbans (as M. perturbans in Valki unas, 2005) Ae. aegypti
Ae. albopictus
Ae. atropalpus An. quadrimaculatus
P. durae
P. garnhami P. circumexum + + + + + + NA + +
Cx. pipiens Cx. restuans Cx. antennatus Cx. pipiens Cx. univittatus Cx. pipiens Cx. tarsalis Cs. annulata Oocyst Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Oocyst Sporozoite NA Sporozoite Sporozoite Sporozoite Sporozoite NA
+ NA NA NA + +
+ NA NA NA
USA USA Africa Africa Africa Egypt USA Germany, Italy USA Italy Canada Sri Lanka Canada USA
Cs. melanura Cs. longiareolata Cs. morsitans
Cq. crassipes Cq. perturbans Ae. sollicitans
Coggeshall (1940) and Jeffrey (1944) Laird (1941), Jeffrey (1944), and Huff et al. (1947) Laird (1941) Coggeshall (1940), Hurlbut & Hewitt (1942), and Jeffrey (1944) Coggeshall (1940) Laird (1941) Valki unas (2005) Valki unas (2005) Valki unas (2005) Garnham (1966) Huff (1965) Reichenow (1932) and Corradetti et al. (1964) Herman (1938) Corradetti et al. (1964) Meyer et al. (1974) and Meyer & Bennett (1976) Niles et al. (1965) Meyer & Bennett (1976) Herman (1938)
Table 1. (Cont.)
PCR method
Parasite species
Vector species
Proven natural vector References
P. vaughani Sporozoite Sporozoite Sporozoite Sporozoite
P. rouxi
Cx. pipiens Cs. morsitans Cq. perturbans Cx. pipiens
+ + +
+ +
Corradetti & Scanga (1972) Williams & Bennett (1978) Williams & Bennett (1978) Huff (1932a) and Manwell (1947)
P. kempi
P. elongatum + Oocyst Sporozoite USA USA NA
Cx. tarsalis Cx. territans Cx. pipiens Cx. restuans Cx. tarsalis Ae. triseriatus Cx. pipiens Oocyst Oocyst Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite
+ + + + +
NA NA +
Italy Canada Canada Algeria, USA USA USA USA USA USA USA USA, Italy
Cx. restuans Cx. tarsalis
P. hermani
Cx. territans Cx. salinarius Cx. quinquefasciatus Cx. salinarius Cx. nigripalpus Oocyst Oocyst Oocyst Sporozoite Sporozoite USA USA Italy USA USA
+ +
+ +
P. juxtanucleare
Cx. restuans Wyeomyia vanduzeei Cx. gelidus Cx. quinquefasciatus Cx. pipiens Cx. pseudovishnui Cx. sitiens NA NA NA NA NA + NA + + Sporozoite Sporozoite NA NA NA NA Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite + + + + + +
+ + + + + + +
USA USA Malaysia Brazil Japan Malaysia Malaysia
+ + +
Fallisia neotropicalis Plasmodium lineage LIN1p
Cx. tritaeniorhynchus Cx. annulus Aedeomyia squamipennis Cx. sitiens
Huff (1932a) Huff (1932a) Christensen et al. (1983) Christensen et al. (1983) Christensen et al. (1983) Huff (1930) and Micks (1949) Huff (1927), and Raffaele (1934), and Micks (1949) Micks (1949) Huff (1932a) and Huff & Shiroishi (1962) Huff (1927) Huff (1927) Raffaele (1934) Nayar et al. (1981b) Young et al. (1977), Forrester et al. (1980), and Nayar et al. (1981b, 1982) Nayar et al. (1981a) Nayar et al. (1980, 1981b) Bennett et al. (1966) Paraense (1944) Akiba (1959) Bennett et al. (1966) Bennett et al. (1966) and Bennett & Warren (1966) Bennett et al. (1966) Bennett et al. (1966) Gabaldon et al. (1985) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008)
Cx. annulirostris
Plasmodium lineage LIN2
Ae. hebrideus
Malaysia Malaysia Venezuela New Caledonia New Caledonia Vanuatu
937
938
Table 1. (Cont.)
PCR method
Parasite species + NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA Cameroon Cameroon Cameroon + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
Vector species
Most advanced developmental stage observed in vector PCR on vector blood meal
PCR on whole unengorged vectors
References Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Ishtiaq et al. (2008) Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2009) Njabo et al. (2011)
Plasmodium lineage LIN3p
Ae. notoscriptus
Cx. annulirostris
P. juxtanucleare lineage LIN4p Haemoproteus lineage LIN5h
An. farauti Cx. quinquefasciatus
Ae. vigilax
Cq. xanthogaster
Haemoproteus lineage LIN6h
An. farauti Ae. hebrideus Ae. alternans
Ae. vexans
Verrallina lineata Ae. aegypti
Cx. sitiens
Cx. annulirostris
Cx. quinquefasciatus
Ae. vigilax
Plasmodium lineage PlasCoq1 Plasmodium lineage PlasCoq2
Cq. aurites Cq. spp. Cq. aurites
New Caledonia New Caledonia Vanuatu New Caledonia New Caledonia New Caledonia Vanuatu Vanuatu New Caledonia New Caledonia Vanuatu New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia Cameroon Cameroon Cameroon
Plasmodium lineage PlasCoq3
Cq. spp. Cq. metallica Cx. spp.
Table 1. (Cont.)
PCR method
Parasite species Region
Vector species
Most advanced developmental stage observed in vector PCR on PCR on whole vector blood unengorged meal vectors PCR on thoracic parts of vectors
References
Haemoproteus lineage PlasCoq6
Plasmodium lineage PlasCoq7 Plasmodium lineage PlasCoq8 Plasmodium lineage PlasCoq9 Plasmodium lineage PlasCoq10 Plasmodium lineage PlasCoq11 Plasmodium lineage PlasCoq12 Plasmodium lineage PlasCoq13 Plasmodium lineage PlasCoq14 Plasmodium lineage PlasCoq15 Plasmodium lineage PlasCoq16
Plasmodium lineage PV3 Plasmodium lineage PV11
Plasmodium lineage PV12
Haemoproteus lineage HaemK1 Haemoproteus lineage HaemK2 Haemoproteus lineage HaemK3 Plasmodium lineage Rinshi-1
Plasmodium lineage Rinshi-2 Plasmodium lineage Rinshi-3
Plasmodium lineage Rinshi-7 Plasmodium lineage Rinshi-8
Cq. aurites Cx. spp. Cq. aurites Cq. spp. Cq. aurites Cx. spp. Cq. spp. Cx. spp. Cx. spp. Cx. spp. Cx. spp. Cx. spp. Cx. spp. Cq. spp. Cq. spp. Mansonia uniformis Cx. spp. Cq. spp. Cx. spp. Cq. aurites Cx. spp. Ae. mcintoshi Cq. aurites Cq. pseudoconopas Cq. metallica Cq. spp. Cq. spp. Cx. spp. Cx. spp. Cx. pipiens pallens Cx. sasai Cx. sasai Cx. pipiens pallens Cx. pipiens molestus Cx. sasai Lt. vorax Cx. pipiens pallens Cx. pipiens pallens NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Cameroon Japan Japan Japan Japan Japan Japan Japan Japan Japan
+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+ + + + + +
+ + + + +
+ + + + + + + + + + + + + + + + + + + + + + + + + + + + +
Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2009, 2011) Njabo et al. (2011) Njabo et al. (2009, 2011) Njabo et al. (2009) Njabo et al. (2009) Njabo et al. (2009) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Njabo et al. (2011) Kim et al. (2009b) Kim et al. (2009a) Kim et al. (2009a) Kim et al. (2009b) Kim et al. (2009b) Kim et al. (2009a) Kim et al. (2009b) Kim et al. (2009b) Kim et al. (2009b)
939
Table 1. (Cont.)
PCR method
940
Parasite species + + + + + + + + + + + NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan + + + + + + + + + + + + Japan + Japan + Japan Panama Panama Panama Panama Panama Panama Panama Panama Panama Japan + + + + + + + + + + + + + + + + + + + + + + + + +
Vector species
Most advanced developmental stage observed in vector PCR on vector blood meal References
Plasmodium lineage Yacho-1 Plasmodium lineage PAN1 Plasmodium lineage PAN2 Plasmodium lineage PAN3 Plasmodium lineage PAN4 Plasmodium lineage PAN5 Plasmodium lineage PAN6 Plasmodium lineage PAN7 Plasmodium lineage PAN8 Plasmodium lineage PAN9 Plasmodium lineage mosquito5
Kim et al. (2009b) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Gager et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2008) Ejiri et al. (2009) Ejiri et al. (2009) Ejiri et al. (2009) Ejiri et al. (2009) Ejiri et al. (2009) Ejiri et al. (2009)
Cx pipiens pallens Ad. squamipennis Cx. ocossa Cx. ocossa Ad. squamipennis Ad. squamipennis Ad. squamipennis Cx. ocossa Ad. squamipennis Ad. squamipennis Cx. quinquefasciatus Plasmodium lineage mosquito9 Cx. quinquefasciatus Plasmodium lineage Lt. fuscanus mosquito13 Plasmodium lineage Ae. albopictus mosquito17 Plasmodium lineage Cx. mosquito24 quinquefasciatus Plasmodium lineage Cx. mosquito111 quinquefasciatus Plasmodium lineage Cx. mosquito132 quinquefasciatus Plasmodium lineage Cx. mosquito227 quinquefasciatus Plasmodium lineage Ma. sp. mosquito290 Plasmodium lineage Lt. vorax mosquitoZ34 Plasmodium lineage Cx. pipiens mosquitoS33 Plasmodium lineage Lt. vorax mosquitoZ74 Plasmodium lineage Lt. vorax mosquitoZ73 Plasmodium lineage Cx. pipiens mosquitoZ64 Plasmodium lineage Lt. vorax mosquitoZ83
Table 1. (Cont.)
PCR method
Parasite species
Vector species
Most advanced developmental stage observed in vector PCR on vector blood meal
References
Plasmodium lineage CXPIP01 Plasmodium lineage CXPIP02 Plasmodium lineage CXPIP03 Plasmodium lineage CXPIP04 Plasmodium lineage CXPIP05 Plasmodium lineage CXPIP06 Plasmodium lineage CXPIP07 Plasmodium lineage CXRES01 Plasmodium lineage CXRES02 Plasmodium lineage CXRES03 Plasmodium lineage CXRES04 Plasmodium lineage CXRES05 Plasmodium lineage E1 Plasmodium lineage SEIAUR01/F1
Plasmodium lineage LINN1
P. vaughani lineage SYAT05
Plasmodium lineage TUMIG3
Plasmodium lineage PADOM11
Cx. pipiens Cx. pipiens Cx. pipiens Cx. pipiens Cx. pipiens Cx. pipiens Cx. pipiens Cx. restuans Cx. restuans Cx. restuans Cx. restuans Cx. restuans Cx. restuans Ae. canadensis Cx. pipiens Cx. restuans Cx. pipiens Cx. restuans Cx. pipiens Cx. restuans Cx. pipiens Cx. restuans Cx. restuans NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA USA
+ + + + + + + + + + + + + + + + + + + + + + +
+ + + + + + + + + + + + + + + + + + + + + + +
Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010) Kimura et al. (2010)
These parasite lineages belong to the genus Haemoproteus, which are supposed to be exclusively transmitted by louse ies (Diptera: Hippoboscidae) and biting midges (Diptera: Ceratopogonidae) (see Tables 2 and 4). Proven natural vector = sporogonic cycle is completed in vector and transmission of parasites to avian host was conducted either by vector bites, by injection of a slurry of triturated infected vectors, or by salivary glands containing Sporozoites; a complete merogonic cycle was observed. Only vectors naturally present in the study area were used in experiments. Proven experimentally = laboratory [including polymerase chain reaction (PCR) studies] and/or eld experiments have been conducted on vector competence, experiments could have been conducted using vector species not occurring at the study site (i.e. unnatural vectors), and in some cases complete life cycle has not been proved. NA, not available.
941
942 Initial studies on vector specicity showed that it was not possible to identify broad patterns of infection because of the paucity of knowledge on genetic variation. The fact that large numbers of Plasmodium sporozoites develop in an insect vectors salivary glands, or that large parasite inoculums are used to infect birds, does not mean that the parasite will be successfully transmitted or that an infection will develop in the vertebrate host (Huff, 1927, 1929; Laird, 1941; Jeffrey, 1944; Micks, 1949). Vector susceptibility depends on the parasite strain used during experimental infections (Manwell, 1940; Micks, 1949). Some authors described parasites of the same species with no difference in morphology as having distinct physiological characteristics (Huff, 1927, 1929, 1932a, 1938). For example, P. elongatum was not able to infect Culex pipiens in a study by Reichenow (1932), but it did develop in 30% of C. pipiens when an Italian strain of this parasite was used (Raffaele, 1934). Furthermore, Huff (1927) demonstrated that some individuals and/or varieties of the same competent vector species have different efciencies at transmitting P. cathemerium (Huff, 1927, 1929, 1938) indicating the presence of intraspecic variation in vectorial capacity (see also Tate & Vincent, 1934). Similarly, a more susceptible Ae. aegypti strain was selected by Trager (1942) for P. lophurae infection and a Cx. pipiens strain for P. elongatum by Micks (1949). Thus, differences in vector susceptibility could be explained by both vector and parasite genetic diversity. Recent ndings using molecular approaches suggest that there could be more than 1000 avian haemosporidian strains (Bensch, Hellgren & P erez-Tris, 2009), whereas only about 220 morphological species of avian haemosporidians have been described (Valki unas, 2005; Valki unas et al., 2010a). Clearly, vertebrate host-parasite-vector interactions will have a geographical component that must be taken into account when making epidemiological and model predictions. Natural immunity of mosquitoes and vertebrate hosts to malaria has received considerable attention. Manwell (1938) proved that immunity of a susceptible species of mosquito might be due to its inheritance. Weathersby (1965) described a parabiotic twinning method to determine immune mechanisms of susceptible and refractory mosquitoes to malaria infections. This involved pairing two mosquitoes (one of a susceptible and one of a refractory species) using a tiny capillary glass, so that haemolymph could be shared between the two species. Using this method it was shown that there were enough nutritive elements for development of ookinetes and early oocyst stages of P. gallinaceum in refractory Cx. pipiens, but due to some antagonistic action oocysts appeared distorted in immune mosquitoes, while in Ae. aegypti mosquitoes oocyst development was successful (Weathersby & McCall, 1968). It was proven later that the innate immunity of Cx. pipiens mosquitoes to P. gallinaceum infection is due to antagonistic (antiblastic) factors in mosquito haemolymph and not to the lack of metabolites or required substances (Weathersby & McCroddan, 1982). However, it now appears that these innate immunity mechanisms are not generalisable across species. Alavi et al. (2003) injected P. berghei ookinetes into Ae. aegypti haemocoel without successful development

of the initial stages of oocysts. Inhibitory agents such as the peritrophic membrane barrier, oxygen free radicals, melanization and others act throughout the development of parasites to block their transmission stages (Billingsley & Rudin, 1992; Sinden, 2002). Sinden, Alavi & Raine (2004) commented that the refractoriness of mosquitoes may depend on the level of inhibitory barriers at each developmental stage and that only when all inhibiting mechanisms fail to block development can the insect be considered a competent or viable vector. Recently, it was discovered that the mid-gut microbiota (bacteria) plays a critical role in the vectorial capacity to sustain Plasmodium infections; mosquitoes with a normal associated microbiota had a lower infection rate compared to microbe-free mosquitoes (Dong et al., 2009). This suggests that within-vector microbe interactions represent a natural immunological barrier to infection, resulting from the modulation of the mosquitos immune genes by the mid-gut microbial ora (Dong et al., 2009). Results of studies on parasite specicities and vector and vertebrate immunities support Huff, Marchbank & Shiroishis (1959) hypothesis that infectivity of the parasite is the result of various factors such as individual variability of the immune response, behavioral traits of the host, genetic diversity of the host and parasite populations, and coevolutionary history between parasites and hosts. To evaluate the effect of malaria parasites on invertebrate hosts, studies have measured the longevity of infected mosquitoes or ight performance variables (ight speed, length of initial ight or longest ight). Huff (1965) stated that the age of the adult mosquito and its nutritional state might affect its susceptibility to parasite infection. Initial studies showed no apparent reduction in vitality or longevity of anopheline mosquitoes infected with P. vivax even when females were heavily infected (King, 1929; DeBuck, 1936). These results were corroborated by other studies (Mayne, 1920; Wenyon, 1926; Boyd, 1940; Ragab, 1958). Freier & Friedman (1987) stated that the relationship of P. gallinaceum to Ae. aegypti was that of a commensal rather than parasitic, however this is at odds with evidence cited below reporting negative tness consequences of parasite infection in Culex and Anopheles spp. It remains to be investigated whether variation in tolerance of mosquitoes to infection depends on the specic species and strains used. By contrast, Buxton (1935) showed that infection with P. relictum led to an increase in mortality in Culex fatigans (now Cx. quinquefasciatus) and this was corroborated by Maier (1973), who showed a correlation between increased death rate in Cx. pipiens fatigans (now Cx. quinquefasciatus) and infection with P. cathemerium. The greatest mortality occurred during the period of ookinete penetration of the midgut (Maier, 1973). Gad, Maier & Piekarski (1979) observed higher mortality in An. stephensi during the rst three days after infection with Plasmodium berghei. A detailed study by Klein et al. (1982) using Plasmodium cynomolgi and An. dirus showed that mortality peaks coincided with oocyst rupturing and later with penetration of salivary gland cells by sporozoites. A positive correlation between the severity of infection and a reduction in ight capability was reported by Schiefer, Ward & Eldridge (1977) who suggested that

negative effects on vectors were due to decreases in levels of available carbohydrates, which are crucial for ight. A recent publication by Ferguson & Read (2002) questioned why the impact of malarial parasites on their invertebrate host is still unresolved. They used a meta-analysis to show that malaria parasites reduce vector survival, but showed this effect to be due to the use of unnatural vector-parasite combinations in experimental studies, to the length of the experiment (e.g. experiments that end before the invasion of salivary glands by sporozoites are less likely to nd tness effects or behavioural changes in infected mosquitoes), and to the lack of standardized experimental conditions. Despite avian Plasmodium being the best understood genus of haemosporidian parasites in terms of their transmission vectors, there are still many Plasmodium species for which the vector species is unknown, and even for well-studied Plasmodium parasites new vectors previously believed to be unsuitable are still found (Huff, 1965; Garnham, 1966; Valki unas, 2005). If we add to the lack of knowledge on competent vectors the fact that the outcome depends on local environmental conditions and geographic origin (i.e. subspecies, strains or lineages) both of the parasites and hosts, then the inherent difculty in making denitive statements about the specicity of haemosporidian genera to particular Diptera families becomes clear. Studies on haemosporidian parasites and vector competence and susceptibility would benet greatly from the inclusion of a geographic coevolutionary framework (Thompson, 2005) in their design (e.g. Kimura, Dhondt & Lovette, 2006). (a) Taxonomic issues for parasites transmitted by Culicidae Corradetti & Scanga (1965) stressed difculties with the identication of the systematic position of Plasmodium polare. They described P. polare as falling between the subgenera Giovannolaia and Novyella; the nal reason for placement of P. polare in the subgenus Giovannolaia was the quantity of cytoplasm. There were also difculties with attributing Plasmodium octamerium to the subgenus Giovannolaia (Manwell, 1968). It was pointed out (Manwell, 1968) that this parasite is similar to species of the subgenus Novyella in the morphology of its blood stages. P. octamerium was attributed to the subgenus Novyella in the Garnham collection of malaria parasites (Garnham & Duggan, 1986). However, after examination of the type material, P. octamerium was placed in the subgenus Giovannolaia by Valki unas (2005), reverting to Manwells (1968) original systematic position. Strictly speaking, P. octamerium belongs to a group of species (together at least with P. dissanaike), whose subgeneric position is difcult to identify, particularly at low parasitemia. (2) Family Hippoboscidae The oldest record of transmission of a haemosporidian parasite by hippoboscid ies was by Arag ao (1908) working with Haemoproteus columbae (Adie, 1915). This parasite infects the common pigeon Columba livia. By 1906 a y from the genus Lynchia was implicated in the transmission of H. columbae,
943 the rst studies used the species Lynchia maura (originally described as Olfersia maura, now Pseudolynchia canariensis) and Lynchia brunea lividicolor (originally described as Olfersia lividicolor, now Pseudolynchia canariensis) (Sergent & Sergent, 1906; Adie, 1915). The role of these ies in transmission was conrmed by later observers, including Wenyon (1926), Huff (1932b), Coatney (1933, 1935), and Mohammed (1958). By 1911 it was believed that H. columbae developed up to the ookinete stage in the insect vector and proceeded no further; hence, researchers thought that the ookinete was the stage inoculated into the pigeon (Minchin, 1912, cited in Adie, 1915). A few years later the complete development of the parasite in Lynchia ies was demonstrated (Adie, 1915). Unlike mosquitoes and ceratopogonid vectors, both males and females of hippoboscid ies take blood meals, are susceptible to infection, and are able to transmit the parasite; moreover, infection rates of Lynchia ies can be up to 100% (Adie, 1915). Rendtorff, Jones & Coatney (1949) conducted experiments on H. columbae using P. canariensis as vector; they found that vectors feeding on birds with patent infections developed sporozoites only if the bird was infected for 25 days or longer; birds with patent infections of less than 25 days most likely had immature gametocytes, which precluded the development of the sexual and sporogonic stages in the vector. Early studies working on host specicity of Haemoproteus parasites suffered from taxonomic confusion and lack of knowledge on genetic variability. Baker (1957) noted that many hippoboscid species used in earlier studies were synonyms of P. canariensis, and that this y was the only known vector of H. columbae at that time. Subsequently, he demonstrated that Ornithomya avicularia was also susceptible to infections with a Haemoproteus sp. parasite similar to H. columbae (Baker, 1957). However, it was not possible to infect uninfected C. livia pigeons with the Haemoproteus sp. parasites obtained from the wood pigeon Columba palumbus via infectious bites of O. avicularia (Baker, 1957, 1963). This led to the suggestion that Haemoproteus parasites acquired from C. palumbus were from a subspecies or lineage unable to develop in C. livia (Baker, 1963). This parasite was able to develop in P. canariensis but at a low rate (two out of 73 ies were successfully infected) (Baker, 1966b). Baker (1966a) showed that the C. palumbus parasite was a different species (named H. palumbis) unable to develop in C. livia. A subsequent experiment showed that H. columbae was unable to develop in C. palumbus, and although it was able to infect O. avicularia, the oocysts appeared degenerated and no sporozoites were observed (Baker, 1968). This series of experiments suggests that there is strong host specicity of these parasites, in particular for the vertebrate host (Baker, 1968). However, Rashdan (1998a) showed that H. columbae could successfully infect two other dove species Streptopelia senegallus and S. turtur through either injection of infected salivary glands or infectious bites of P. canariensis. The course of infection of H. columbae in the new hosts was the same in S. senegallus but a longer pre-patent period and lower parasitemia was observed in S. turtur compared to C. livia (Rashdan, 1998a). P. canariensis was able to feed and survive normally on the Streptopelia
944 doves (Rashdan, 1998a). Furthermore, P. canariensis was able to successfully transmit Haemoproteus turtur to both S. senegallus and S. turtur, but was unable to transmit this parasite to C. livia, even by inoculation of infected tissue (i.e. salivary glands or macerated lungs; Rashdan, 1998b). These studies suggest that host specicity of haemosporidian parasites cannot be evaluated based on phylogenetic relationships, at least not below the family taxonomic rank. Table 2 lists all experimental vector studies for Haemoproteus parasites. The hippoboscid y O. avicularia is not only involved in the transmission of H. palumbis, but is also a competent vector for Trypanosoma avium (Baker, 1956, 1957). It has been suggested that hippoboscid ies can act as a bridge in the transmission of Haemoproteus species across different vertebrate hosts due to their plastic feeding preferences (when the preferred host is absent or in low numbers, these ies will use alternative hosts; Greiner, 1975). Host-generalist insect vectors are potentially capable of transmitting parasites from different genera, and can act as reservoirs and vectors of introduced and expanding parasites (Perkins et al., 2008). A study analyzing the ecology of hippoboscid ies feeding on mourning doves (Zenaida macroura) recorded Microlynchia pusilla and Stilbometopa podopostyla ies as natural vectors of H. sacharovi and suggested that some Culicoides (Ceratopogonidae) species could act as supplementary vectors in the transmission of this dove parasite, although no experimental evidence was provided (Greiner, 1975). When a parasite species is transmited by different vectors, their population may show less uctuations over time within a given area compared to parasites specializing on a single vector both due to the alternative pathways (i.e. vector species) and because some vectors can act as reservoirs. On the other hand, use of an abundant vector species would compensate for the narrow host preferences of a specialized parasite. Such patterns are likely to vary as a geographic mosaic; a parasite species that is a vector generalist in one location may be a vector specialist in another. For example, P. relictum is mostly transmitted by Cx quinquefasciatus in Hawaii, whereas Cx. pipiens, Cx. restuans and Ae. canadensis are its vectors in Eastern USA (LaPointe, Goff & Atkinson, 2005; Kimura et al., 2010). The other bird species used intensively in studies of Haemoproteus parasites transmitted by hippoboscid ies is the California quail (Lophortyx californica) (Tarshis, 1955). Tarshis (1952, 1954) developed eld methods for the collection and transport of hippoboscid ies from wild-trapped California quail. This bird is parasitized by H. lophortyx, which is successfully transmitted by Stilbometopa impressa, and has an average infection prevalence of 63% (Tarshis, 1955). The prepatent period in naturally infected S. impressa ies was determined to be 2144 days and for experimentally infected ies the prepatent period was 44 days or longer, depending on the temperature at which ies were maintained (Tarshis, 1955). These experiments were later criticized because aviaries were used with mesh sizes that did not exclude Ceratopogonid vectors (Valki unas, 2005; Mullens et al., 2006); thus, Culicoides ies could not be eliminated as competent vectors of H. lophortyx (see Section II.4).

Table 2. Experimental studies demonstrating full or partial vectorial competence of different species of Hippoboscidae ies transmitting parasites of the genus Haemoproteus
Arag ao (1908), Rendtorff et al. (1949), and Rashdan (1998a) Baker (1957, 1963, 1966a, b, 1968) Baker (1966a, b) Rashdan (1998b) Huff (1932b) Valki unas et al. (2010a) Levin et al. (2011) England Sporozoite + Sporozoite + See Table 1 for denitions of experimental and natural vectors. H. turtur H. sacharovi H. multipigmentatus H. iwa P. canariensis P. canariensis P. canariensis Microlynchia galapagoensis Olfersia spinifera + + + + + Haemoproteus columbae Pseudolynchia canariensis + H. palumbis Ornithomya avicularia + Sporozoite Sporozoite Sporozoite None None England Egypt USA Ecuador (Galapagos) Ecuador (Galapagos) USA, Egypt, Brazil + +
PCR method
Parasite species
Vector species
Region
PCR on whole PCR on vector blood unengorged vectors meal
References

Few studies have been conducted on the seasonal dynamics of hippoboscid vectors, limiting our understanding of the transmission cycle of the Haemoproteus parasites transmitted by these ies. For example, Klei & DeGiusti (1975) showed that intensity of infection and prevalence of H. columbae in pigeon populations from Detroit was higher in the autumn and winter seasons and lower in spring. This was explained by the higher number of ies in late summer and during the autumn, in contrast to patterns observed in other populations exposed to less seasonal habitats. (a) Taxonomic issues for parasites transmitted by Hippoboscidae The genus Haemoproteus was divided into two groups (H. columbae group and H. nettionis group) (Baker, 1963); later these two groups were named as Haemoproteus and Parahaemoproteus (Bennett et al., 1965). Haemoproteus contains H. columbae (type species), H. sacharovi and H. multipigmentatus (Valki unas et al., 2010a), H. lophortyx was considered to belong to this subgenus, but has recently been placed in the subgenus Parahaemoproteus; hippoboscid ies transmit these parasites. The features of the Haemoproteus group are: (i ) the invertebrate host is a hippoboscid y; (ii ) sporogony occurs relatively slowly with the production of expanding oocysts, giving rise to several hundred sporozoites, having one end more pointed than the other; (iii ) exoerythrocytic merogony occurs in the vascular endothelium without the production of compartmentalized cytomeres. The second group, Parahaemoproteus, has strikingly different features. It was originally described by Wenyon (1926), who stated that unpigmented schizonts occurred in masses in the lung, liver, and kidneys of infected birds. Sporogony of Parahaemoproteus has been described in detail by Fallis & Wood (1957) and Fallis & Bennett (1961a) in Canadian birds and was shown to occur in species of Culicoides (Ceratopogonidae). The Parahaemoproteus group may thus be dened as including parasites of birds that (i ) undergo sporogony in species of Culicoides, with the production of small, non-expanding oocysts containing few sporozoites, with tapered ends, and (ii ) mostly present exoerythrocytic schizogony in large compartmentalized foci in the organs. Parahaemoproteus danilewskii (Kruse, 1890a, b) is the type species. Nowadays, these two groups are recognized as the subgenera H . (Haemoproteus) and H . (Parahaemoproteus) (Valki unas, 2005), and this division is supported by molecular phylogenetic studies (Martinsen et al., 2008; SantiagoAlarcon et al., 2010), but it is still unclear whether they are sister or paraphyletic subgenera (Outlaw & Ricklefs, 2011). (3) Family Simuliidae Before the 1930s only speculations about the life cycle of Leucocytozoon parasites were available (Schaudinn, 1904), and the vector responsible for transmitting the parasite Leucocytozoon smithi in turkeys, which caused high mortalities in farms across the USA was unknown. During an outbreak of L. smithi in 1930 in Nebraska, healthy turkeys were injected with blood preparations derived from heavily infected turkeys, but the infections could not be maintained beyond
945 28 days (Skidmore, 1931, see also Johnson et al., 1938). Turkey lice (Eomenacanthus stramineum) and the y Stomoxys calcitrans (Muscidae) were suggested as possible vectors, but experiments did not validate this (Skidmore, 1931). Finally, Simulium meridionale (referred as S. occidentale) was observed feeding on infected turkeys; macerated ies were prepared in saline solution and injected into healthy turkeys, infections developed on the 12th day and parasites were observed in the blood even >70 days after infection (Skidmore, 1931). Future outbreaks that killed large numbers of turkeys in the USA prompted further studies that concluded that S. jenningsi (as S . nigroparvum) and S. venustum [now a species group with some recognized cytospecies (the use of cellular level traits such as chromosomal inversions to differentiate closely realted species)] could vector L. smithi in turkeys and L. anatis (= L. simondi ) in ducks (Johnson et al., 1938). Due to the economic losses generated in the poultry industry by L. smithi infections and to the vectorial capacity of many simuliids to transmit human and domestic animal parasites, largescale aerial treatments to control blacky populations were conducted in some areas of the United States (Kissam, Noblet & Garris, 1975), and efforts to establish laboratory colonies of several simuliid species were made (Edman & Simmons, 1985; Lacoursi` ere & Boisvert, 1987), in order to facilitate indepth studies of L. smithi (e.g. Steele, Noblet & Noblet, 1992). Blackies were bred in captivity since the early 1900s because of their involvement in the transmission of Onchocerca parasites (Blacklock, 1926), but were difcult to maintain successfully (Johnson et al., 1938). With the discovery of their involvement in the transmission of L. smithi, further attempts to culture these insects in the laboratory were made. Davies (1953) was able to keep S. venustum and Simulium decorum in captivity for up to 63 days. During his studies he measured y mortality and found that ies with a partial blood meal survived better than those that took a full blood meal. Furthermore, ies that fed on ducks infected with Leucocytozoon were less viable than those that fed on uninfected ducks, but both survived less than ies that did not take a blood meal at all (Davies, 1953). This study suggests that ies pay a tness cost even when feeding on uninfected hosts, and such costs increase when large blood meals or infected blood is ingested (see also Desser & Yang, 1973; Allison, Desser & Whitten, 1978). Once the vector family was identied, work on other simuliids was conducted. Johnson et al. (1938) described the different stages of L. smithi in both turkeys and in S. nigroparvum; however, they were not able to identify oocysts in the insects gut wall and some developmental stages in the internal organs of turkeys. Starting in the 1950s more in depth studies on the developmental stages, in particular the sporogonic cycle, of Leucocytozoon parasites were conducted. Desser & Fallis (1967) provided a detailed description of the sporogony of L. simondi in Simulium rugglesi ; this y species was recorded attacking 14 different bird species around Lake Michigan, with a clear preference for ducks (Barrow, Kelker & Miller, 1968). The complete life cycle of L. sakharof was recorded using Simulium angustitarse feeding on rooks (Corvus
946 frugilegus; Baker, 1970). The parasite L. bonasae (= L. lovati ), a parasite infecting ruffed grouse (Bonasa umbellus), was experimentally transmitted to grouse chicks obtained from wild broods via injection of infected salivary glands of the simuliids S. latipes and S. aureum; S. venustum ies were unable to produce viable infections in this model (Fallis & Bennett, 1958). In this same study, the infected salivary gland suspension used to inoculate grouse chicks was used to inoculate ducklings and white-crowned sparrows (Zonotrichia leucophrys), neither of which developed L. bonasae infection. Furthermore, grouse chicks and heavily infected ducklings with L. simondi were kept in proximity, and no cross infection was detected; the ies feeding on grouse and duckings were different and seemed to have different parasite afnities (Fallis & Bennett, 1958). Nonetheless, further experimental studies proved that different species of simuliids could be competent for more than one Leucocytozoon species, successfully transmitting the parasite to different bird species (Fallis & Bennett, 1962). Even S. venustum, which is not ornithophilic, was a suitable vector for the bird parasites L. fringillinarum and L. simondi when forced to feed experimentally on birds (Fallis & Bennett, 1962; Desser & Yang, 1973), but S. venustum rarely feeds on ducks under natural conditions (Fallis & Bennett, 1961b). Fallis (1964) provided an extensive list of simuliids and their feeding habits from which it is clear that many species of blackies feed habitually on both mammals and birds (e.g. Simulium aureosimile, S. latipes, S. mexicanum, S. meridionale). Moreover, many simuliids have exible host preferences, which might depend on host availability (Fallis, 1964) and potentially provides opportunities for parasites to jump across species and vertebrate groups. For example, Simulium veracruzanum is implicated in the transmission of Onchocerca nematodes from cows and horses to man (Fallis, 1964). If cross infections are rare, parasite jumps could instantly isolate parasite populations, eventually leading to genetic divergence and/or to a new emergent disease. Experimental studies of simuliids transmitting Leucocytozoon parasites are listed in Table 3. More recently, molecular techniques have been used to untangle the host-parasite-vector relationships. Using engorged vectors it is possible to extract the DNA of the blood meal and amplify specic sections of DNA to identify the vertebrate host, and the haemosporidian parasite genera when the blood meal is infected. By using this method it has been possible to determine that black ies have some degree of host specicity (Hellgren et al., 2008). Moreover, the Leucocytozoon lineages that specic simuliid species transmit are closely related, implying an ecological restriction in terms of the vertebrate host spectrum that Leucocytozoon parasites are able to infect due to the specic host preferences of simuliids (Malmqvist et al., 2004; Hellgren et al., 2008). Care must be taken in the conclusions drawn from molecular studies, however, because: (i ) vectors can switch their feeding choices depending on availability in a specic year or site, and many species have broad host preferences (see Fallis, 1964), (ii ) only parasite genera can be identied when using DNA sequences, unless parasite lineages have been previously attached to morphological species identied

from blood smears prepared from the same sample used for molecular analysis, and (iii ) identication of parasites in blood meals does not indicate vector competencefor this, experimental infections must be performed. (a) Taxonomic issues for parasites transmitted by Simuliidae The genus Leucocytozoon was named by Berestneff (1904) from a malaria-like parasite present in the blood of little owls (Athena noctua), which previously had been named Haemamoeba danilewskyi by Ziemann (1898). The type species is now named L. danilewskyi and is transmitted by Simulium aureum. Bennett et al. (1965) reclassied the family into two genera Leucocytozoon and Akiba, but it was later reclassied in one genus with two subgenera (Valki unas, 2005). The subgenus Leucocytozoon is dened as including those unpigmented haemosporidian parasites that exhibit sporogonic development in ornithophilic simuliids, with the production of small, non-expanding oocysts. The subgenus Akiba is diagnosed as: unpigmented haemosporidian parasites, of which sporogony occurs in Culicoides (see discussion at the end of Section II.4), with the production of small non-expanding oocysts containing sporozoites with tapered ends. The type species is Leucocytozoon (Akiba) caulleryi described from chickens; no other species of the subgenus is at present recognized with certainty. (4) Family Ceratopogonidae Ceratopogonidae is a vector family recognized by their broad host preferences and their capacity to transmit a diverse array of parasites, ranging from viruses (50% are known from the genus Culicoides), larial nematodes, and protozoa (Borkent, 2005). Ceratopogonidae, specically the genus Culicoides, was the last Diptera family to be implicated in the transmission of haemosporidian parasites. Fallis & Wood (1957) investigated potential vectors from four different y families (Simuliidae, Hippoboscidae, Culicidae, and Ceratopogonidae) and showed that ies from the genus Culicoides (most likely Culicoides downesi ) were responsible for the transmission of Haemoproteus nettionis in ducks. Following this discovery further investigations of Culicoides spp. were carried out (Fallis & Bennett, 1961a). Fallis & Bennett (1960) gave a detailed description of the sporogonic development of Haemoproteus canachites (= Haemoproteus mansoni ) in Culicoides sphagnumensis; some stages were even similar to those of Leucocytozoon parasites. The experimental infections were conducted using two grouse species as vertebrate hosts, and attempts to infect ducks, sparrows, and pigeons with H. mansoni were unsuccessful, indicating some degree of specicity of this parasite (Fallis & Bennett, 1960). Such specicity may also depend on the feeding behaviour of Culicoides vectors; different species feed at different times, in different habitats, at different height levels within forests, and some species have specic bird host preferences (Fallis & Bennett, 1961a). Subsequent investigations showed that Haemoproteus meleagridis (= H. mansoni ) infecting wild turkeys successfully completed sporogony in several species of Culicoides (Table 4), with Culicoides edeni being the most important in Florida (Atkinson et al.,
Table 3. Experimental studies demonstrating full or partial vectorial competence of different species of Simuliidae ies transmitting parasites of the genus Leucocytozoon
PCR method
Parasite species + Sporozoite [Skidmore (1931) did not observe any developmental stage] Sporozoite USA USA USA USA Canada Canada Canada Sporozoite Sporozoite Sporozoite Sporozoite Ookynete +
Vector species
References Skidmore (1931) and Pinkovsky et al. (1981)
Leucocytozoon smithi
Simulium meridionale (as S . occidentale in the old literature) + + + + + + + + + +
S. jenningsi (as S . nigroparvum in the old literature) S. slossonae
Johnson et al. (1938)
S. congareenarum
L. lovati (= L. bonasae)
S. latipes
S. aureum
Noblet et al. (1975) and Pinkovsky et al. (1981) Noblet et al. (1972, 1975) and Pinkovsky et al. (1981) Fallis & Bennett (1958, 1961b, 1962) Fallis and Bennett (1958, 1962) Fallis & Bennett (1958)
L. dubreuili (= L. mirandae)
S. venustum (mammalophilic) S. rugglesi S. croxtoni S. quebecense P. hirtipes S. japonicum S. uchidai S. aureum S. latipes S. croxtoni + + + + + + + + Ookynete Sporozoite Sporozoite None None None Sporozoite Sporozoite Sporozoite Sporozoite + + + + + +
Canada Canada Canada Japan Japan Japan Canada Canada Canada Canada
+ + +
+ + +
L. fringillinarum + +
Prosimulium decemarticulatum Cnephia ornithophilia S. quebecense S. aureum + + + + + + + +
Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite
Canada Canada Canada Canada Canada
S. latipes
S. croxtoni
Fallis & Bennett (1958) Fallis & Bennett (1962) Fallis & Bennett (1962) Sato et al. (2009) Sato et al. (2009) Sato et al. (2009) Fallis & Bennett (1961b) Fallis & Bennett (1961b) Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b) Khan & Fallis (1970) Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b, 1962)
947
Table 3. (Cont.)
PCR method
948
Parasite species + Sporozoite Sporozoite Sporozoite Canada, USA Canada Canada + + + + +
Vector species
Proven natural vector References
P. decemarticulatum
C. ornithophilia
L. simondi
S. rugglesi
+ + + + Sporozoite Sporozoite Sporozoite Sporozoite Canada, USA Norway Canada Canada
+ + + +
Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b, 1962) Fallis & Bennett (1961b), Fallis et al. (1956), Barrow et al. (1968), and Desser & Fallis (1967) Fallis et al. (1951) Eide & Fallis (1972) Fallis & Bennett (1966) Desser & Yang (1973)
L. sakharof Sporozoite Sporozoite Sporozoite Canada England New Zealand
L. tawaki
S. innocens S. dogieli S. anatinum S. venustum (mammalophilic) S. aureum S. angustitarse Austrosimulium ungulatum + + + + + +
L. danilewskyi
L. neavei
L. berestnef
L. macleani L. toddi
L. schoutedeni
Leucocytozoon lineage lCAP1
A. australense A. dumbletoni S. aureum S. latipes P. decemarticulatum S. adersi S. nyasalandicum S. aureum P. decemarticulatum S. metatarsale S. aureum S. quebecense P. decemarticulatum S. adersi S. nyasalandicum S. vorax S. transiens S. silvestre Metacnephia lyra S. transiens Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite None None None None
+ + + + + + + + + + + + + + + + + + + +
+ + + + + + + + + + +
New Zealand New Zealand Canada Canada Canada Tanzania Tanzania Canada Canada China South Africa South Africa South Africa Tanzania Tanzania Tanzania Sweden Sweden Sweden Sweden
+ + + +
Fallis & Bennett (1961b) Baker (1970, 1971) Fallis et al. (1976), Allison et al. (1978), and Desser & Allison (1979) Fallis et al. (1974) Fallis et al. (1974) Khan (1975) Khan (1975) Khan (1975) Fallis et al. (1973) Fallis et al. (1973) Khan & Fallis (1971b) Khan & Fallis (1971b) Hong et al. (1990) Bennett et al. (1993) Bennett et al. (1993) Bennett et al. (1993) Fallis et al. (1973) Fallis et al. (1973) Fallis et al. (1973) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008)
Table 3. (Cont.)
PCR method
Parasite species Region
Proven Vector species experimentally
Most advanced developmental stage observed in vector PCR on PCR on whole vector blood unengorged meal vectors
References
Leucocytozoon lineage lCAP4 Leucocytozoon lineage lBRG1 Leucocytozoon lineage lBRG2 Leucocytozoon lineage lBRG3
Leucocytozoon lineage lHGR1
Leucocytozoon lineage lGRUS1 Leucocytozoon lineage lHelli1 Leucocytozoon lineage lHelli2 Leucocytozoon lineage lHelli3 Leucocytozoon lineage IMTUR1 Leucocytozoon lineage IMTUR2 Leucocytozoon lineage lSTUR1
S. transiens M. lyra M. lyra S. transiens M. lyra S. transiens M. lyra S. transiens M. lyra S. annulus S. usovae S. usovae S. usovae S. silvestre S. silvestre S. silvestre None None None None None None None None None None None None None None None None Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden Sweden
+ + + + + + + + + + + + + + + +
+ + + + + + + + + + + + + + + +
Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008) Hellgren et al. (2008)
See Table1 for denitions of experimental and natural vectors.
949
950
Table 4. Experimental studies demonstrating complete or partial vectorial competence of different species of Ceratopogonidae ies transmitting parasites of the genus Haemoproteus and Leucocytozoon (Akiba)
PCR method PCR on thoracic parts of vectors References Most advanced developmental stage observed in vector Region Japan Japan Sporozoite Sporozoite Proven natural vector + + PCR on whole PCR on vector blood unengorged vectors meal
Parasite species + +
Vector species
Leucocytozoon (Akiba) caulleryi
Culicoides arakawae
C. circumscriptus
Haemoproteus nettionis + + Sporozoite Sporozoite Sporozoite Sporozoite USA USA Canada USA + + + + + +
C. schultzei C. odibilis C. downesi Sporozoite Sporozoite Sporozoite Japan Japan Canada
+ + +
H. mansoni (= H. canachites, C. sphagnumensis H. meleagridis) C. edeni
C. hinmani
C. arboricola
H. velans
H. fringillae
C. haematopotus C. knowltoni C. scanloni C. nanus C. baueri C. paraensis C. sphagnumensis C. stilobezzioides C. crepuscularis C. stilobezzioides C. impunctatus Sporozoite Sporozoite Oocysts Oocysts Oocysts Oocysts Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite USA USA USA USA USA USA Canada Canada Canada Canada Russia
+ + + + + + +
+ + + +
H. handai (= H. desseri ) H. danilewskii + + + + + +
C. sphagnumensis C. nubeculosus C. crepuscularis
+ + +
Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite
Russia France Canada Canada Canada USA
C. stilobezzioides
C. sphagnumensis
C. edeni
Akiba (1960), Morii et al. (1965), and Morii & Kitaoka (1968) Morii et al. (1965) and Morii & Kitaoka (1968) Morii et al. (1965) Morii & Kitaoka (1968) Fallis & Wood (1957) and Sibley & Werner (1984) Fallis & Bennett (1960) Atkinson et al. (1983) and Atkinson (1988) Atkinson et al. (1983) and Atkinson (1988) Atkinson et al. (1983) and Atkinson (1988) Atkinson (1988) Atkinson (1988) Atkinson (1988) Atkinson et al. (1983) Atkinson et al. (1983) Atkinson et al. (1983) Khan & Fallis (1971a) Khan & Fallis (1971a) Fallis & Bennett (1961b) Fallis & Bennett (1961b) Valki unas (1997, 2005) and Valki unas & Iezhova (2004a) Valki unas (1997, 2005) Miltgen et al. (1981) Bennett & Fallis (1960) and Fallis & Bennett (1961b) Bennett & Fallis (1960) and Fallis & Bennett (1961b) Bennett & Fallis (1960) and Fallis & Bennett (1961b) Garvin & Greiner (2003)
Table 4. (Cont.)
PCR method
Parasite species
Vector species Region
References
H. parabelopolskyi H. lanii H. balmorali H. dolniki H. tartakovskyi H. lophortyx
C. knowltoni C. arboricola C. impunctatus C. impunctatus C. impunctatus C. impunctatus C. impunctatus C. bottimeri USA USA Russia Russia Russia Russia Russia USA
+ + + + + + + +
+ + + + +
Garvin & Greiner (2003) Garvin & Greiner (2003) Valki unas & Iezhova (2004b) Valki unas & Iezhova (2004a) Valki unas et al. (2002) Valki unas et al. (2002) Valki unas et al. (2002) Mullens et al. (2006)
Haemoproteus lineage CulHae1
Haemoproteus lineage CulHae2
Haemoproteus lineage CulHae3 Haemoproteus lineage CulHae4 + + + + + None None None None None None None None None + + + + Spain Spain Spain Spain Spain Spain Spain Spain Spain
C. circumscriptus C. kibunensis C. simulator C. truncorum C. kibunensis C. pictipennis C. simulator C. kibunensis Spain Spain Spain Spain Spain Spain Spain Spain
+ + + + + + + +
Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite None (parous eld-collected midges were triturated and injected into quail hosts) None None None None None None None None + + + + + + + + + + + + + + + + +
Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011)
C. circumscriptus C. festivipennis C. pictipennis C. simulator C. simulator
C. pictipennis
C. segnis
C. simulator
Haemoproteus lineage CulHae5 Haemoproteus lineage CulHae6 Haemoproteus lineage CulHae7 Haemoproteus lineage CulHae8 Haemoproteus lineage CulHae9
C. circumscriptus
951
952
Table 4. (Cont.)
PCR method PCR on thoracic parts of vectors +
Parasite species + + + + + + + + + + + + None None None None None None None None None None None None None Germany Spain Spain Spain Spain Spain Spain Spain Spain Germany Germany Germany Germany + + + + + + + + + + + + +
Vector species Region
PCR on whole PCR on vector blood unengorged vectors meal
References Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Martinez-de la Puente et al. (2011) Santiago-Alarcon et al. (2012) Santiago-Alarcon et al. (2012) Santiago-Alarcon et al. (2012) Santiago-Alarcon et al. (2012) Santiago-Alarcon et al. (2012)
C. simulator Haemoproteus lineage CulHae10 C. festivipennis C. festivipennis Plasmodium lineage CulPlas1 C. kibunensis C. pictipennis C. simulator C. truncorum Plasmodium lineage CulPlas2 C. festivipennis Haemoproteus lineage SYAT07 C. kibunensis Plasmodium lineage LINN1 C. pictipennis H. minutus C. pictipennis Haemoproteus lineage SYAT02 C. poperinghensis (Haemoproteus parabelopolskyi ) Haemoproteus lineage CCF2 C. semimaculatus
This is the only bird Leucocytozoon parasite that is so far known to be transmitted by Culicoides ies. These parasite lineages belong to the genus Plasmodium, which are supposed to be exclusively transmitted by mosquitoes (Diptera: Culicidae), mainly genus Culex (see Table 1). See Table 1 for denitions of experimental and natural vectors.

1983; Atkinson, 1988). Apparently, this parasite develops successfully only in Galliformes (Valki unas, 2005). Haemoproteus velans, a parasite of woodpeckers, has been successfully transmitted by C. sphagnumensis and C. stilobezzioides, and was initially placed in the subgenus Parahaemoproteus based on features of its sporogonic development (Khan & Fallis, 1971a). Haemoproteus danilewskyi was succesfully transmitted by C. crepuscularis, C. stilobezzioides, and C. sphagnumensis (Bennett & Fallis, 1960; Fallis & Bennett, 1961b). More recently, Garvin & Greiner (2003) added three new species to the list of competent vectors for H. danilewskii (Table 4). The blackcap (Sylvia atricapilla) is a migratory passerine that has been the subject of research from the perspective of the haemoproteid parasites infecting it. It is one of the few parasite-vector-vertebrate systems with considerable information available on parasite diversity (e.g. P erez-Tris et al., 2007; Kri zanauskien e et al., 2010; Santiago-Alarcon et al., 2011). Haemoproteus parabelopolskyi, a parasite specic to blackcaps, completes sporogony in Culicoides impunctatus in a population located in the Curonian Spit of the Baltic Sea (Valki unas & Iezhova, 2004a). Furthermore, C. impunctatus was also competent for Haemoproteus balmorali, H. dolniki, and H. tartakovskyi (Valki unas et al., 2002). In the same population, Valki unas & Iezhova (2004b) demonstrated experimentally that H. parabelopolskyi, H. fringillae, and H. lanii produced high mortalities in C. impunctatus ies, indicating high tness costs of parasitism for this vector species. H. lophortyx has been experimentally transmitted by Culicoides bottimeri (Mullens et al., 2006). This parasite was previously shown to be transmitted by hippoboscid ies (ORoke, 1930; Tarshis, 1955); however, their eld experiments were inconclusive because they used cages with a mesh size that did not exclude Culicoides vectors, which may explain some of their unusual results (e.g. long prepatent periods). Leucocytozoidae parasites of the subgenus Akiba are transmitted by Ceratopogonidae ies of the genus Culicoides. Mathis & L eger (1909) found an unpigmented parasite in the blood of domestic fowl, which they recognized as a species of Leucocytozoon, but later studies placed it in the genus Akiba. Currently it is recognized as Leucocytozoon (Akiba) caulleryi in the subgenus Akiba (Valki unas, 2005), which was selected as the type species by Bennett et al. (1965). The taxonomic features of L. caulleryi are: (1) its vector is a species of Culicoides, oocysts are produced within the mid gut, and sporozoites are up to 11 m in length; and (2) the nature of its exoerythrocytic schizogony, where megaloschizonts have a lateral body instead of a central body. These characters sufce to warrant separating this single species into the Akiba subgenus (Valki unas, 2005), distinct from the other Leucocytozoidae parasites that undergo sporogony in Simulium ies and where the exoerythrocytic schizonts possess a central body. The vector of L. caulleryi in Japan was shown by Akiba (1960) to be Culicoides arakawae, later conrmed by Morii et al. (1965). This presumably explains the transmission of species of Leucocytozoidae in regions where the usual vector, Simulium is absent, such as in Kenya (Garnham, 1950). Morii
953 et al. (1965) also incriminated C. circumscriptus and C. schultzei (a species normally feeding on cattle) as alternative vectors in Japan. Akiba et al. (1958) gave a clear account of exoerythrocytic schizogony in Japanese chickens dying of the disease. The illness is often so rapid that death of apparently healthy birds occurs overnight. More detailed studies on L. caulleryi showed that temperature has a clear effect on sporogonic development in different Culicoides vectors (Morii & Kitaoka, 1968). Sporozoite production was observed at 1530 C, but at 30 C sporozoites were not viable; the highest sporozoite production was recorded at 25 C (Morii & Kitaoka, 1968). Interestingly, infectious bites of C. arakawae through the shell membranes of chicken eggs can successfully infect embryos with L. caulleryi, some of which subsequently hatch, but die within a few days of hatching (Takamatsu, Fujisaki & Kitaoka, 1978). It has been suggested that vector abundance parallels natural transmission of Haemoproteus parasites in birds, with seasonal peaks in colder areas of North America compared to the year-round transmission of sub-tropical Florida (Atkinson, 1991). However, detailed knowledge on the epizootiology (i.e. the sum of the factors controlling the occurrence of a disease or pathogen of animals) of Haemoproteus species is only available for a few species, such as H. mansoni (Atkinson et al., 1983; Atkinson, 1988) and H. danilewskii (Garvin & Greiner, 2003). An important protocol originating from these studies is vertical sampling of vectors within study sites because species abundance of Culicoides can change from the canopy to the understorey (Service, 1969; Atkinson, 1991; Garvin & Greiner, 2003). Vertical stratication could inuence the haemosporidian parasites that can infect a species, if that species has a preferred vertical stratum for nesting and roosting (Garvin & Greiner, 2003).
III. ADVANCES SINCE THE FIRST APPLICATION OF MOLECULAR METHODS (PCR) The rst attempts to identify the vertebrate host from the insect vectors blood meal applied immunological tests (Washino & Tempelis, 1983): during the early 20th Century researchers used precipitin tests (Bull & King, 1923), and during the 1970s a uorescent antibody method to stain erythrocytes and detect the host DNA in mosquitoes (McKinney, Spillane & Holden, 1972). Later, enzyme-linked immunosorbent assay methods were developed (Burkot, Goodman & De Foliant, 1981; Beier et al., 1988; Hunter & Bayly, 1991; Chow, Wirtz & Scott, 1993; Thapar et al., 1998). Although immunological tests to identify vertebrate hosts proved useful, the necessity for high-quality antiserum and high antibody specicity to avoid crossreactivity from closely related species precluded such tests from becoming a fast, accurate, or widely applicable methodology. At the end of the century PCR methods to identify vertebrate hosts began to be applied (e.g. Boakye et al., 1999), and later rened (Lee et al., 2002; Ngo & Kramer, 2003). These PCR methods used a sequence fragment of the mtDNA cytochrome b (cyt b), which subsequently
954 was compared with existing cyt b sequence records stored in databases (e.g. GenBankTM ) to identify the vertebrate host. Recently, a new blood meal analysis method was developed in which the amplied sequence fragment corresponds to the bar code gene (COI mtDNA; Alcaide et al., 2009). Sequences obtained using this new method can be compared to those stored in the BOLD systems database, which holds the largest collection of COI sequences from all groups of organisms (Ratnasingham & Hebert, 2007). PCR methods have helped in the identication of putative Diptera vectors in the transmission of Haemosporida parasites and the delimitation of vector feeding preferences (Tables 14). For example, Valki unas et al. (2010a) and Levin et al. (2011) used PCR methods to amplify a fragment of the parasite mtDNA cyt b from the thorax of Hippoboscidae ies in the Galapagos Islands. Because the Galapagos Islands are a relatively simple system, it is probable that the identied louse ies represent the natural vectors of H. multipigmentatus (Valki unas et al., 2010a) and H. iwa (Levin et al., 2011). Furthermore, the use of PCR techniques to identify putative vectors has uncovered surprising results: Ishtiaq et al. (2008) and Njabo et al. (2011) identied mosquitoes (Culicidae) infected with Haemoproteus lineages when this Diptera family was thought only to transmit Plasmodium parasites, while Martinez-de la Puente et al. (2011) and Santiago-Alarcon et al. (2012) identied Plasmodium lineages infecting Culicoides (Diptera: Ceratopogonidae) vectors when this Diptera family is supposed to transmit only Haemoproteus parasites. Laboratory experiments are needed in order to verify whether these atypical vectors are competent. PCR applied to the blood meal contained in a vectors mid gut have helped to dene their feeding preferences. Malmqvist et al. (2004) and Hellgren et al. (2008) identied the vertebrate hosts of several species of blackies (Diptera: Simuliidae) in Sweden using a fragment of the mtDNA cyt b. They suggested that Simuliidae vectors in Sweden have narrow avian host preferences, precluding parasites from switching hosts and producing strong coevolution (Hellgren et al., 2008). Recently, Santiago-Alarcon et al. (2012) amplied a fragment of the mtDNA COI gene from the blood meals of Culicoides vectors, and found that feeding preferences are rather exible, even for those species that are considered to be either ornithophilic or mammalophilic. For example, C. kibunensis a y considered ornithophilic was found to feed commonly on humans. Surprisingly, many Culicoides species carrying avian haemosporidian parasites (identied using PCR) fed readily on humans (Santiago-Alarcon et al., 2012), providing the potential for parasite jumps across vertebrate hosts. Bensch et al. (2000) provided the rst molecular phylogeny of avian haemosporidians. Molecular research on avian blood parasites was based on the screening of avian haemosporidian parasites from the blood of different vertebrate hosts using the mtDNA cyt b gene. This innovative method opened new possibilities for deeper analysis of phylogenetic relationships between different haemosporidian species as predicted by Atkinson (1991). Molecular studies have revealed remarkable genetic diversity of haemosporidian

parasites and have helped determine the phylogenetic relationships of this parasite group (Perkins & Schall, 2002; Ricklefs & Fallon, 2002; Martinsen et al., 2008; Perkins, 2008; Santiago-Alarcon et al., 2010; Outlaw & Ricklefs, 2011). Using this tool, more than 1000 genetic lineages of haemosporidian parasites have been deposited in GeneBank and MalAvi databases (Bensch et al., 2009). We now know that many morphologically determined species possess a high level of genetic diversity (e.g. Valki unas et al., 2010a), which may corroborate early experimental ndings of morphologically identical morphospecies differing in physiological characteristics (Huff, 1927, 1929, 1932a, 1938). DNA analyses have allowed conrmation or rejection of some species, genus, or higher taxonomic units. High sensitivity of molecular methods is valuable in ecological studies, where naturally infected birds may carry low parasite levels. However, Valki unas et al. (2006, 2008a, 2009b) demonstrated that different PCR protocols can underestimate mixed infections of Haemoproteus and/or Plasmodium parasites. The authors noted that in some cases sensitivity of PCR was not related to the intensity of parasitemia, showing that PCR might be selective for certain parasite strains. They stressed that a combination of microscopy and molecular approaches is advisable in studies of avian haemosporidian parasites (Valki unas et al., 2008a). Hellgren et al. (2007) suggested for haemoproteids that a more than 5% genetic difference between mitochondrial cyt b genetic lineages represented different morphological species. These assumptions were supported by further studies (Palinauskas et al., 2007; Valki unas et al., 2007a, b, 2010a, b; Iezhova et al., 2010; Kri zanauskien e et al., 2010). However, Haemoproteus pallidus and H. minutus represent an exception to this rule. These parasites are readily distinguished by morphological features, but their genetic distance based on cyt b sequence fragments is only 0.2%. Cytochrome b sequences have been recently used in the description of new haemosporidian parasites [e.g. H. parabelopolskyi (Valki unas et al., 2007a), Leucocytozoon toddi group (Valki unas et al., 2010b), H. pallidulus (Kri zanauskien e et al., 2010)] and in the identication of their putative vectors [e.g. Microlynchia galapagoensis as vector of H. multipigmentatus (Valki unas et al., 2010a)]. It has become common taxonomic practice to attach cyt b sequences to morphologically determined parasites. This is an advance in haemosporidian taxonomy because we can use cyt b fragments to determine species identity when blood smears are not available. Currently, many genetic lineages remain to be attached to morphological species. Table 5 lists all taxonomic studies that have used molecular methods to aid in the description of new species of haemosporidians or in the determination of genetic lineages of known species. Valki unas et al. (2007a) found that mitochondrial cyt b lineages of what was recognized at that time as Haemoproteus belopolskyi clustered in two different clades. Haplotypes of one clade were found in Acrocephalus and Hippolais warblers, and haplotypes from the other clade were obtained from Sylvia warblers. The genetic distance between the two clades

Table 5. Taxonomic studies using molecular methods (mtDNA cyt b gene) to aid morphological descriptions of haemosporidian parasites
Haemosporidian parasite Haemoproteus iwa H. multipigmentatus H. cyanomitrae Leucocytozoon mathisi, L . buteonis, and L . toddi H. pallidulus Plasmodium minuoviride, P. koreafense, P. megalotrypa, and P. gemini P. lacertiliae P. lucens, P. multivacuolaris and P. parahexamerium P. megaglobularis, P . globularis, and H . vacuolatus P. elongatum P. relictum and P. circumexum H. parabelopolskyi H. balmorali, H. belopolskyi, H. lanai, H.minutus, H. pallidus, H. payevskyi P. ashfordi H. majoris

955 haemoproteid. Authors specied that the 5% molecular criterion for species determination should be applied only in one direction. That is, genetic lineages of more than 5% genetic divergence are likely to be morphologically distinguishable, but a difference of less than 5% does not mean that there would be no morphological differences between two lineages. Perhaps morphological variation is also linked to host specicity, where generalists, by virtue of their adaptability to different host physiologies, could have a more variable morphology compared to specialists, in particular when hosts are not closely related. Using molecular tools and analyses of two genes (mitochondrial cyt b and COI), Martinsen et al. (2006) questioned the status of the subgenera Novyella and Giovannolaia which had previously been doubted by Corradetti, Garnham & Laird (1963a), Corradetti, Verolini & Neri (1963b), Seed & Manwell (1977), and Laird (1998). Martinsen et al. (2006) found that Novyella and Giovannolaia do not form monophyletic clades and that morphological features were not phylogenetically informative. They presented evidence for three other subgenera (Haemamoeba, Hufa, and Bennettinia) conrming that they were clearly dened and phylogenetically robust. Martinsen et al. (2006) suggested the reevaluation of some features, such as elongated gametocytes, hitherto important for the identication of parasites. While we agree that PCR is a powerful tool in molecular and evolutionary studies it also has certain shortcomings, and further development is needed (e.g. P erez-Tris & Bensch, 2005; Valkiunas et al., 2006; Sz oll osi, Hellgren & Hasselquist, 2008). Such taxonomic problems will only be resolved by using additional genes in phylogenetic studies, conducting experimental infections in both vectors and vertebrate hosts to examine parasite morphology across all developmental stages, and by increased sampling effort in tropical areas, where undescribed species might allow clarication of phylogenetic problems. The analysis of parasite stages in vectors should have priority in haemosporidian taxonomic, ecological, and evolutionary studies.
References Levin et al. (2011) Valki unas et al. (2010a) Iezhova et al. (2010) Valki unas et al. (2010b) Kri zanauskien e et al. (2010) Perkins & Austin (2009) Perkins & Austin (2009) Valki unas et al. (2009b) Valki unas et al. (2008b) Valki unas et al. (2008c) Palinauskas et al. (2007) and Valki unas et al. (2007b) Valki unas et al. (2007a) Hellgren et al. (2007) Valki unas et al. (2007b) Kri zanauskien e et al. (2006)
Redescription of morphological species with the help of mtDNA cyt b, erythrocytic parasite stages, and distributional information. For these Leucocytozoon parasites, molecular methods were used to dene cryptic species that, based on morphology alone, were considered synonyms (Valki unas, 2005). Authors highlight the importance of the morphology of the cytoplasmic processes of host cells as a taxonomic character (Valki unas et al., 2010b). New Plasmodium species from New Guinea lizards. Studies attaching a segment of the mtDNA cyt b gene to previously described morphological species.
(>5%) led the authors to suggest that these should be two different species. By conducting precise morphological analysis of Haemoproteus spp. parasites of three lineages from two clades, a new species was described from Sylvia birds based largely on the size of the macrogametocytes nucleus. Clarication of the Leucocytozoon toddi group involved studies combining both PCR and microscopy for taxonomic purposes. Greiner & Kocan (1977) noted that L. toddi based on the morphology of the blood stages may comprise a species complex. Later, Sehgal et al. (2006) revealed that L. toddi likely represents a group of cryptic species, because the divergence between some lineages was over 10%. Valki unas et al. (2010b) then compared the morphology of two L. toddi parasites whose haplotypes grouped in separate clades. Precise morphological analysis revealed that Leucocytozoon parasites from Accipiter and Buteo are morphologically distinguishable. Moreover, the authors suggested for the rst time that cytoplasmic processes of the host cell could be of taxonomic importance during description of Leucocytozoon spp. A recent study by Kri zanauskien e et al. (2010) employed both microscopy and PCR to describe a new species of
IV. FUTURE DIRECTIONS IN UNDERSTANDING THE ECOLOGY AND EVOLUTION OF HAEMOSPORIDIAN PARASITES (1) A current limitation Two factors suggest that the ecology and evolution of haemosporidian parasites is more exible than hitherto thought. First, specicity by vectors is known only in a few cases (e.g. Culex nr. piliferus feeding on ducks; Fallis & Bennett, 1961a). Second, modern molecular and phylogenetic methods have shown that host switching of parasites, sometimes across large phylogenetic distances, is rather common (Ricklefs & Fallon, 2002; Ricklefs, Fallon & Bermingham, 2004). Thus, in combination with the fact that detailed data on parasites are only available for a few haemosporidian systems and restricted to specic populations (e.g. Knowles et al., 2011), the conclusion emerges that many published results pertain only to the
956 specic populations studied and are not easily generalized to other parasite or vector species or even to the same species in a different temporal or spatial context. We agree with Huff (1938) that many contradictions originate from false generalizations based upon work with one species of mosquito or vertebrate host. For example, at the beginning of the 20th Century it was assumed that all Anopheles mosquitoes could transmit human malaria, and now we know this is not true. Nowadays, generalizations are frequently made by evolutionary biologists and ecologists without proper evidence. Garnham (1966) and Valki unas (2005) warned that such generalizations could mislead researchers. (2) The dynamic nature of haemosporidian transmission Since the interactions between parasites and vectors and between vectors and vertebrate hosts are not species-specic, a necessary consequence is that the interactions among parasites, vectors, and vertebrate hosts can vary markedly across space and time, thereby likely forming a coevolutionary mosaic (see Thompson, 2005). Spatial and temporal variation is caused by different environmental conditions and varying abundances of parasites, hosts, and vectors. This variation suggests that new interactions are likely to be established if parasites and/or vectors are moved or spread naturally into new areas (e.g. LaPointe et al., 2005; Marzal et al., 2011). What are the evolutionary and ecological consequences of the dynamic nature of haemosporidian transmission? Current research shows that evolutionary dynamics can happen rapidly, within the same time scale of ecological dynamics (Schoener, 2011). The introduction of avian malaria to the Hawaiian Islands provides an example of this. The appearance of avian malaria produced dramatic changes in lowland bird community structure, restricting the range of endemic birds to highland areas free of malaria and driving some species to extinction (van Riper et al., 1986). Subsequently, some endemic birds evolved immunity against malaria, and slowly are returning to the islands lowlands (Woodworth et al., 2005). This is an example both of rapid adaptation and of newly established interactions between parasites, their vectors and vertebrate hosts. Organisms dispersing (either by natural events or by human introductions) into new areas can alter the ecology of the local community, and hence the direction of evolution (Schoener, 2011). We emphasise that data are currently lacking to understand the evolutionary dynamics of haemosporidian parasites, their vectors, and their vertebrate hosts. In this context a recent study was the rst to establish: (i ) tness costs of acute Plasmodium infections in blue tits (Cyanistes caeruleus) that likely coevolved with two species of Plasmodium parasites, (ii ) smallscale spatial variance in those tness costs between areas of high and low parasite prevalence, and (iii ) differences in virulence between Plasmodium circumexum and P. relictum (Lachish et al., 2011). This study illustrated that generalisations on the effects of parasites are not warranted and that tness effects can be spatially variable (see also Wood et al., 2007).

We are far from understanding the causes of spatial and temporal variability in haemosporidian transmission. One explanation for this is that although many studies have described the seasonal dynamics of haemosporidian parasite infections in different bird species (e.g. Klei & DeGiusti, 1975, and references therein; Bensch et al., 2007; Hasselquist et al., 2007; Santiago-Alarcon et al., 2011), almost none have analyzed the seasonal dynamics of both the parasite and its insect vector (but see Klei & DeGiusti, 1975; Atkinson, 1988, 1991). Studies on haemosporidian parasites usually address the phenology of the parasites and their putative vectors separately. Better knowledge on the identity and phenology of vector species will allow us to determine their inuence on the seasonal and spatial variability in parasite prevalence among populations (Forrest & Miller-Rushing, 2010). Future research must integrate the temporal (within and across years) dimension of parasites, insect vectors and vertebrate hosts, to allow better predictions on the effects that habitat alteration and climate change can have on these host-parasite systems (e.g. Mller, 2010). We propose that the use of network analysis will allow us to tackle the dynamics of these complex parasite systems once the critical players (i.e. vectors, parasites, vertebrates) and the interaction strengths among them are known. Network analyses are used increasingly for addressing ecological processes among multiple species, but are still rare in the analysis of host-parasite interactions (Poulin, 2010). The few studies applying network analysis to host-parasite interactions have shown that interactions among the species involved are highly asymmetric. A nested network structure was observed, where species with few interactions (specialists) tend to associate with species with many interactions (generalists), leading to a core of generalists interacting frequently and presumably strongly among themselves and many specialists interacting asymmetrically with generalists (V azquez et al., 2005). A possible explanation for this pattern is the abundance of the different host and parasite species in the community, where abundant species tend to have more interacting partners than rare species. Hence, abundant species asymmetrically affect their rare partners, whereas pairs of interacting abundant species tend to show more symmetric, reciprocally strong effects (V azquez et al., 2007). A corollary of the asymmetric nature of host-parasite networks is that specialists will have limited opportunity for coevolution because they are asymmetrically inuenced or selected by their abundant, generalized interaction partners (V azquez et al., 2005, 2007). It is the interactions among abundant generalists that have the greatest potential for strong reciprocal effects and, hence, coevolution (V azquez et al., 2007). Geographic variation in the relative abundance of species can lead to a geographic mosaic of coevolution (Thompson, 2005)with pairs of species coevolving in sites where they are both abundant and not coevolving in sites where one or both are rare. Based on parasite infection data in vectors and hosts, network analysis can be used, for example, to identify (i ) vectors that are crucial for maintaining parasite reservoirs

within areas over time, (ii ) vectors, hosts and parasites that are responsible for maintaining the integrity of the vectorparasite-vertebrate community (i.e. network persistence), (iii ) coevolutionary hot- and coldspots among populations of the same interacting species, and (iv) species (e.g. parasites) that are likely to go extinct within a community [for methods in different contexts, see Rezende et al. (2007) and Saavedra et al. (2011)]. Network analyses further can help to understand which vertebrate hosts and which vector species are most likely to share parasites and thus could be a tool to predict parasite host switches. Moreover, network analyses should help focus our attention on specic parts of the antagonistic community where more detailed analyses (e.g. experiments and conrmatory studies) are needed. Finally, if detailed spatial and temporal data are available (e.g. Wood et al., 2007), network analyses could allow us to identify how anthropogenic factors (e.g. fragmentation and climate change) will affect network attributes and structure (i.e. the stability of the host-parasite community), predicting parasite range expansion/contraction and probable emergent diseases (e.g. Johnson & Carpenter, 2008). Risk of new emergent and reemergent diseases increases as humans encroach and alter the environment. Thus, in order to maintain a balance in many host-parasite interactions that not only affect humans but also animals and plants, it is necessary to develop a program that underscores the ecological services of pristine and/or healthy ecosystems in combination with habitat restoration and a social development-conservation education plan, in particular for developing nations (see Barbier et al., 2011). (3) Taxonomy and systematics In Section II.2 we noted the problematic taxonomic status of the Haemoproteus genus and its division into two subgenera: Haemoproteus and Parahaemoproteus (Valki unas, 2005). Parasites belonging to these two subgenera are sometimes presented as monophyletic (Valki unas et al., 2010a; Outlaw & Ricklefs, 2011) and sometimes as paraphyletic (Martinsen et al., 2008; Santiago-Alarcon et al., 2010), and are transmitted by different Diptera families (Valki unas, 2005). Moreover, research to date indicates that parasites of the subgenus Haemoproteus infect only non-passerine birds (SantiagoAlarcon et al., 2010; Levin et al., 2011). Despite identifying their taxonomy as problematic, Fallis & Bennett (1961b) decided to keep the subgenera within the same genus because of their morphological similarities. We believe this issue deserves more thorough attention in order to determine whether the two Haemoproteus subgenera should be split into two new genera. Currently, phylogenetic approaches to estimate the ages of the different haemosporidian groups (Ricklefs & Outlaw, 2010) are based on rather debatable methods (e.g. using the molecular clock of birds to calibrate a molecular clock for haemosporidians) and on controversial assumptions (e.g. using a strict clock rate of molecular evolution across the entire Haemosporida phylogeny when the rate is known to
957 vary, particularly between mammal and bird parasite lineages, see Outlaw & Ricklefs, 2010). Molecular phylogenies for insect vectors should be constructed and calibrated based on amber fossils (Poinar & Poinar, 2007). This will allow the reconstruction of phylogenies of the three players, which can be used to improve our current haemosporidian age estimates using molecular clocks under a framework similar to that proposed by Ricklefs & Outlaw (2010). These data, together with a phylogeographic approach, should help us understand how this group of parasites diversies. We now know that haemosporidians present a high rate of vertebrate host switching, but do haemosporidian parasites present a cospeciation pattern in reference to the insect host? What is the most likely speciation mechanism (allopatric, parapatric, or sympatric) of haemosporidians? From a biodiversity perspective, avian haemosporidians are relatively well studied. However, most of this knowledge is restricted to temperate regions (see Valki unas, 2005) and a similar level of sampling in tropical regions is clearly needed. In addition, we call for more widespread taxonomic sampling of other vertebrate groups, and more detailed investigations of Diptera vectors in order to determine complete haemosporidian life cycles.
V. CONCLUSIONS (1) Knowledge on haemosporidian dipteran vectors is most complete for parasites of the genus Plasmodium, in particular for those that infect human populations. Despite this, we are still far from having a complete knowledge of the vectors transmitting haemosporidian parasites, in particular for genera other than Plasmodium. (2) PCR applied to blood meals can be used to determine a preliminary set of vectors on which subsequent detailed experimental infections can be conducted in order to determine viability and to study the full life cycle of these parasites. (3) The same morphological haemosporidian species can be composed of several genetic lineages, which can have different tness effects on the same host species, and these effects can vary within and across host populations, suggesting a coevolutionary geographic mosaic. Similarly, the same parasite lineage/species can have widely different effects on different hosts. Moreover, the same vector species can also have different susceptibilities and viability to the same parasite species/lineage, depending on the population of origin of the vector. Thus, generalizations about vector and vertebrate host specicity and tness effects by different haemosporidian parasites are yet not possible. (4) Blood-sucking dipterans can have plastic feeding preferences, and such plasticity can extend across different vertebrate groups. They may be susceptible to parasite genera for which they were not previously thought to be vectors (e.g. Culicoides spp. infected by Plasmodium spp.), but experimental studies are needed to conrm their vectorial capacity. These ndings question the validity of the so-called vector
958 family-avian haemosporidian genera specity (e.g. Culicidae vectors were believed only to transmit Plasmodium parasites). (5) Vectors suffer tness consequences (i.e. lower ight capacity, mortality) from haemsoporidian infections. Insects have many barriers to prevent infection, such as haemolymph factors, peritrophic membrane and a mid-gut microbial ora that directly interacts with invasive parasites and mediates insect immune reactions. Hence, vectors are not just vessels transmitting parasites to their nal destination as previously believed. (6) Molecular phylogenies have helped to solve some taxonomic problems, but are currently limited due mainly to the use of a few genes and the lack of samples from vertebrate groups other than birds and mammals; in particular, mammals other than primates and rodents are not well represented. Furtheremore, sampling is mostly restricted to temperate regions. Further sampling is clearly needed in tropical regions. The inclusion of dipteran vector phylogenies should help to improve our haemosporidian age estimates from molecular phylogenies. (7) Attaching cyt b genetic lineages to clearly dened morphological species will aid faster parasite identication by PCR in large-scale screening projects, which is particularly important when blood smears are not available or their quality is low. Thus, it should be common practice among researchers to determine the genetic diversity of each morphological species. The inclusion of morphological traits of sporogonic developmental stages can provide additional features to separate species; however, based on current knowledge, it should be noted that the morphology of oocysts and soporozoites presents little variation across species, which makes PCR an essential tool for identifying parasite species infecting vectors. VI. ACKNOWLEDGEMENTS We thank G. Valki unas and two anonymous reviewers for thorough comments that signicantly improved the quality ez-Bernal commented, reviewed, and of the paper. S. Ib an corrected synonyms in the scientic names of the different Diptera families. A. Cooper, assistant editor, for making our paper more readable. This work was supported by the Deutsche Forschungsgemeinschaft (H.M.S., grant number 1008/6-1) and the Alexander von Humboldt Foundation (D.S.-A., post-doctoral grant).

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Biol. Rev. (2012), 87, pp. 928964. doi: 10.1111/j.1469-185X.2012.00234.

Avian haemosporidian vectors and taxonomy

D. Santiago-Alarcon and others

Avian haemosporidian vectors and taxonomy

D. Santiago-Alarcon and others

Proven natural vector

Avian haemosporidian vectors and taxonomy

Proven natural vector

An. albimanus Cx. salinarius Cx. territans Cx. pipiens

D. Santiago-Alarcon and others

Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite Sporozoite

Avian haemosporidian vectors and taxonomy

Proven experimentally Region

Proven natural vector

Most advanced developmental stage observed in vector References

PCR on PCR on whole vector blood unengorged meal vectors

PCR on thoracic parts of vectors

Proven experimentally Region References

Proven natural vector

Most advanced developmental stage observed in vector

PCR on PCR on whole vector blood unengorged meal vectors

PCR on thoracic parts of vectors

P. subpraecox P. giovannolai P. fallax

Cx. tarsalis Cx. pipiens Cx. pipiens Ae. albopictus

Ae. atropalpus An. quadrimaculatus

Cs. melanura Cs. longiareolata Cs. morsitans

D. Santiago-Alarcon and others

Cq. crassipes Cq. perturbans Ae. sollicitans

Proven experimentally Region

Proven natural vector References

Most advanced developmental stage observed in vector

PCR on PCR on whole vector blood unengorged meal vectors

PCR on thoracic parts of vectors

P. vaughani Sporozoite Sporozoite Sporozoite Sporozoite

Cx. pipiens Cs. morsitans Cq. perturbans Cx. pipiens

Avian haemosporidian vectors and taxonomy

P. elongatum + Oocyst Sporozoite USA USA NA

Cx. restuans Cx. tarsalis

USA USA Malaysia Brazil Japan Malaysia Malaysia

Fallisia neotropicalis Plasmodium lineage LIN1p

Cx. tritaeniorhynchus Cx. annulus Aedeomyia squamipennis Cx. sitiens

Plasmodium lineage LIN2

Malaysia Malaysia Venezuela New Caledonia New Caledonia Vanuatu

Parasite species + NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA Cameroon Cameroon Cameroon + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +

Proven experimentally Region

Proven natural vector

PCR on whole unengorged vectors

PCR on thoracic parts of vectors

Plasmodium lineage LIN3p

P. juxtanucleare lineage LIN4p Haemoproteus lineage LIN5h

An. farauti Cx. quinquefasciatus

Haemoproteus lineage LIN6h

An. farauti Ae. hebrideus Ae. alternans

Verrallina lineata Ae. aegypti

Plasmodium lineage PlasCoq1 Plasmodium lineage PlasCoq2

Cq. aurites Cq. spp. Cq. aurites

D. Santiago-Alarcon and others

Plasmodium lineage PlasCoq3

Cq. spp. Cq. metallica Cx. spp.

Parasite species Region

Proven natural vector

Plasmodium lineage PlasCoq4

Plasmodium lineage PlasCoq5