International Journal for Parasitology 31 (2001) 648652

www.parasitology-online.com

Invited Review

The more insect trypanosomatids under study-the more diverse

Trypanosomatidae appears
Sergei Podlipaev*
Zoological Institute Russian Academy of Sciences, 199034, St. Petersburg, Russia
Received 16 October 2000; received in revised form 2 January 2001; accepted 2 January 2001

Abstract
From 10 trypanosomatids genera six comprise monogenetic parasites of insects and for the rest of four genera insects may serve as vectors.
The invertebrate host is an essential element of trypanosomatids life cycle, but from more than 900 recognised vertebrate hosts only about
500 species of insects have been discovered to be the hosts of homoxenous trypanosomatids. Nothing or very little is known about insect
trypanosomatids in many extensive areas such as South East Asia, Australia, Japan and some others. Each new region explored brings many
new ndings. Recently agellates were found in new insect species and families. The border of parasites distribution was expanded till
Central Asia, Far East and North over the Polar Circle. As paleogeographical events are now under contemplating in trypanosomatids
phylogeny researches so northern insect trypanosomatids may attract some attention as the elements of postglacial fauna which is denitely
young. Very broad host specicity of insect trypanosomatids and high probability to isolate non-specic parasite show causes that only the
investigation of a culture may solve the question `what parasite was really isolated?'. Examination of cell morphotypes in the host has clearly
demonstrated that they are not sufcient for classication and may lead us to be mistaken. The number of insect trypanosomatid cultures is
inadequate for characterisation of the diversity of insects trypanosomatids. Trypanosoma is actually the only trypanosomatid genus which is
out of questions. Insect trypanosomatids comprise the most diversied part of trypanosomatids evolutionary tree. Recent ssrRNA phylogenetic analysis and morphological data show that three insect isolates represent new lineages on trypanosomatid evolutionary tree, as well as
dendrograms derived from PCR data demonstrated some new groups of isolates. Therefore, the more insect trypanosomatids are involved in
laboratory investigations - the more new clusters or/and new lineages are appearing on the tree. q 2001 Australian Society for Parasitology
Inc. Published by Elsevier Science Ltd. All rights reserved.
Keywords: Diversity; Fauna; Insects; Phylogeny; Taxonomy; Trypanosomatidae

The medical and economical importance of causative

agents of dangerous diseases resulted in preferential investigation of trypanosomatids of vertebrates (and for the same
reasons of parasites of plants) while trypanosomatids from
insects were forgotten for a long time. Recently it is brightening more and more that insect trypanosomatids play very
important role as objects of researches and are probably
close to be the key point to establish more or less believable
trypanosomatid phylogeny.
From 10 trypanosomatids genera six comprise monoxenous parasites of insects and for the rest of four genera
insects may serve as vectors. Trypanosoma and Leishmania
- Endotrypanum are described from more than 900 vertebrates species. Trypanosoma amounted to about 600 species
whereas the largest monoxenous genus - Leptomonas - a

* Tel.: 17-812-114-6651; fax: 17-812-114-0444.

E-mail address: sergei@weed.zin.ras.spb.ru (S. Podlipaev).

little bit more than 100 descriptions (Wallace, 1966; Podlipaev, 1990).
Only 350 species of insects (and almost 100 plants
species) have been discovered to be the hosts of monoxenous trypanosomatids for the rst century of trypanosomatids investigation (Wallace et al., 1983; Podlipaev, 1990).
Over the next 20 years about 200 insects host species from
limited number of locations were added. Nothing or very
little is known about insect trypanosomatids in many extensive areas such as South East Asia, Australia, Japan and
some others. Probably up to date Brazil (mostly due to
efforts of Erney Camargo team) and Former Soviet Union
(Russia and New Independent Central Asian States) represent the best explored territories: it means only that these
areas are investigated more or less better than others.
Approximately from more than 1000,000 known species
of insects no more than 20002500 species have been investigated by parasitologists. The vast majority of insect trypanosomatids are still to be described.

0020-7519/01/$20.00 q 2001 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved.
PII: S00 20-7519(01)0013 9-4

S. Podlipaev / International Journal for Parasitology 31 (2001) 648652

Current faunistic data shows apparently random or unorder distribution of trypanosomatids among insect taxa: in
two orders - Hemiptera and Diptera - about 300 described
species and undetermined trypanosomatids are allocated. A
few, sporadic or unreliable ndings (about 20 in total) were
done in seven other orders (see Podlipaev, 1990). Such
disproportion may be determined by the evolution of trypanosomatids (see Vickerman, 1994). From another hand the
scantiness of our knowledge about insect trypanosomatids
fauna led us to be very cautious. Especially, insects from
ancient and small orders have to be involved in faunistic
work as well as insects from interesting biogeograhical
regions.
The isolation of laboratory culture is a crucial condition
for the correct description of new species of trypanosomatids, but if it is impossible to obtain the culture the description based on natural infection of the host may also be
justied (Wallace et al., 1983; Podlipaev et al., 1991; Podlipaev, 1999). If we wait for the acquisition of the laboratory
culture in each new case of infection the fauna of trypanosomatids in large regions may remain unknown. For example, the rst reports on trypanosomatids from insects and
plants in Central Asia (Podlipaev, 1986; Podlipaev,
1988a,b) were done without culture isolation and it is doubtful not only to obtain cultures but even visit some of those
remote and dangerous areas in the nearest future.
Investigation of new hosts and territories has illustrated
enormous quantities of as yet ungathered materials.
Recently more than 200 insect species belonging to 123
genera from 30 families as well as 47 plant species from
Russian Far East till Baltic Sea and from the Polar Circle till
former Soviet Union Central Asian border were investigated
for the rst time. This enormous area was a real tabula rasa:
there were no reports about monoxenous trypanosomatids,
no cultures were isolated. Totally about 26 monoxenous
trypanosomatids and `Phytomonas' in milkweed were
found, including 14 new species of insect trypanosomatids
and one new genus (Wallaceina, former Proteomonas).
Northern border of insect trypanosomatid distribution is
expanded over the Polar Circle, parasites are found in
deserts and high mountains (an altitude of 3500 m). Two
new families of bugs (Hemiptera: Nabidae and Saldidae)
and one new dipterous family (Dixidae) were found to be
the hosts of trypanosomatids (Podlipaev, 1985; Podlipaev,
1986; Frolov and Malysheva, 1989; Podlipaev et al., 1990;
Podlipaev et al., 1991; Podlipaev, unpublished etc.). Several
dozen of cultures were isolated, including some unusual
ones, for example: the rst culture from Mecoptera
(Panorpa communis), the culture from the bug Nabis brevis
(Nabidae) during winter adult diapause (Frolov and Malysheva, 1989) and the culture from Salda littoralis (Saldidae)
which lives under washed ashore material in the upper intertidal zone of the White Sea in high salinity conditions
(Podlipaev et al., 1991).
As paleogeographical events are now under contemplating in trypanosomatids phylogeny researches thus northern

649

insect trypanosomatids may attract some attention as the

elements of postglacial fauna, which is denitely young.
Anyway isolates investigated till now from Russian North
had demonstrated the tendency to occupy the tree crown on
ssrRNA phylogeny as well as on PCR based dendrogram
(Bulat et al., 1999; Merzlyak et al., 2001).
When natural infected insect is investigated it is almost
impossible to recognise the mixed infection. For example
pond skaters (Gerridae) demonstrates very well how multivarious are trypanosomatids in natural infected hosts.
Usually several classical morphotypes may be noted in
each insect, including so unusual as trypomastigote-like
cells in Gerris. There are also many cells with undetermined
morphotypes. By the rules of Zoological Nomenclature the
slide from the insect serves as a type material but no one can
be sure what cells (or parasites) represented in the insect
(and on the type slide) and isolated from infected insects
will establish the culture.
For instance Blastocrithidia gerricola was described on
the base of the presence of about 98% epimastigotes in the
host but, according to the morphology of the cells in culture
and from the presence of rare promastigotes in the host, it
was supposed, that there was a mixed infection in the insect
and that an organism other than Blastocrithidia might have
been isolated (Podlipaev, 1985). In the case of B. gerricola
the minor component was isolated instead of main parasite.
Molecular markers have shown that the B. gerricola culture
is very close to Wallaceina (Bulat et al., 1999; Merzklak et
al., 2001).
Strictly speaking from our collection, we can be more or
less sure that only two isolates represent a specic infection.
First, Leptomonas rigidus from the bug S. littoralis because
the host inhabits very specic biotope under washed ashore
material in upper intertidal of the White Sea and is ecologically isolated from all other Hemiptera in the place (Podlipaev et al. 1991). Second case is Wallaceina brevicula,
which was isolated from a host during host winter adult
diapause under snow (Frolov and Malysheva, 1989).
A special point of interest is monoxenous trypanosomatids in the same insect vectors, which harbor Trypanosoma
and Leishmania. In strict words interesting fact is the lack of
such parasites. Leishmania vectors have been found free
from their own monoxenous parasites except one obscure
case of Crithidia sp. nding in Phlebotomus; experimental
infection of Phlebotomus by Crithidia fasciculata; and
recent reports about Leptomonas sp. isolated from Lutzomia
(Sousa et al., 1998) then two doubtful monoxenous parasites
were noted in Glossina morsitans in the thirties; nally only
Triatoma infestans have genuine monoxenous Blastocrithidia triatoma, which was isolated in the culture (see Podlipaev, 1990). Obviously the lack of monoxenous
trypanosomatids in sandies and Glossina needs to be
checked. It seems that monoxenous parasites might be
expected in vectors. Even if we totally accept the `vertebrate
rst' scenario of trypanosomatids evolution, from all molecular phylogenies published it have to be concluded that

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S. Podlipaev / International Journal for Parasitology 31 (2001) 648652

Leishmania have roots in the crown of trypanosomatids

evolutionary tree among insect trypanosomatids. From
phylogenetic point of view Leishmania together with Phytomonas are the insect trypanosomatids lineages which had
successfully colonised several groups of vertebrates and
plants (Podlipaev, 2000).
The revealed position of B. triatoma the only investigated monoxenous trypanosomatid from vector near the
root of the tree (Merzlyak et al., 2001) is very intriguing
because a monogenetic blastocrithidia-like organism was
supposed to be the ancestral trypanosomatid form (Baker,
1963; Hoare, 1972) and have to attract attention to possibility of parallel parasite populations in vectors. Analysis of
obtained phylogenetic trees demonstrated that the rRNA
data corresponds to various scenarios of the early divergence of B. triatoma within the Trypanosomatidae, including a possibility of the origin of trypanosomatids from a
monogenetic epimastigote (Maslov et al., 2001; Merzlyak
et al., 2001).
Very broad host specicity of insect trypanosomatids and
high probability to isolate non-specic parasite (Podlipaev
and Bulat, 1998; Bulat et al., 1999) show causes that only
the investigation of a culture may solve the question `what
parasite was really isolated?'. Examination of cells morphotypes in the hosts have clearly demonstrated that they are
not sufcient for classication and may lead us to be mistaken (Podlipaev, 2000; Merzlyak et al., 2001).
As cultures investigation is the basic element of modern
researches we have to remember that the procedure of trypanosomatids isolation from host to culture and the cultivation
itself might perform a selective choice of some certain genotypes in parasite population. When clonal colonies on solid
media were investigated several distinctive phenotypes
were determined as heritable ones: for example hemispherical or amoeba-like colonies were found to be such characters for Leptomonas peterhof (Podlipaev, 1985); they
remained stable during at least 5 years of cultivation. One
of the evidences of such selection is the decreasing number
of amoeba-like colonies in culture of L. peterhof. They
amounted 1520% of the total colonies number just after
culture isolation and presented single colonies per Petri dish
in 5 years of laboratory cultivation (Podlipaev and Naumov,
2000).
Besides the discrete character of the form, trypanosomatids colonies may differ by their size. The comparison of
colony diameter distribution in ve species of trypanosomatids shows that in L. rigidus and Crithidia guilhermei the
mode at the area of 0.10.3 mm can be noticed, whereas in
Crithidia acantocephali and Leptomonas seymouri it may
be found at 0.40.6 mm area. Herpetomonas muscarum has
bimodal distribution of this size parameter, modes lying at
the same areas (Podlipaev and Naumov, 2000). The
described distribution of colony size remains stable for at
least 2 years of cultivation. Thus we can conrm that in the
species studied there are two heritable phenotypes differing
by sizes of colonies. In H. muscarum colonies of both types

are phenotypically expressed, while in other species under

discussion - only one of them. It may be considered, therefore, that in cultures, where the single size class predominates some selective factors eliminate cells, which could
form colonies of certain diameter. Such factor may be
connected with a procedure of isolation or with cultivating
conditions. Colony size distribution in C. guilhermei and L.
rigidus possesses a positive asymmetry; therefore these
cultures have enough cells, which can form rather big colonies. It may be suggested that in the case of selection the
number of such cells may increase and the second mode of
size distribution could be obtained (Podlipaev and Naumov,
2000). Therefore, laboratory cultures generally do not
precisely correspond to natural infection and may reect
the structure of the real parasite population rather incorrectly.
The latter especially refers to classical cultures (like
Crithidia oncopelti and Crithidia fasciculata) isolated
many years ago. Since several Crithidia escape from the
genus Crithidia to the monophyletic clade of symbiont bearing trypanosomatids (Du et al., 1994; Hollar et al., 1998),
only C. fasciculata represents the whole genus Crithidia on
the rRNA tree. However in the illustrations from the original
description of C. fasciculata, Leger (1902) depicted epimastigotes among other cells; this fact raises some doubts and it
also allows to presume the possibility of a mixed infection
(Podlipaev, 1990). In different laboratories there are several
cultures designated as C. oncopelti. Two independent cell
populations that differ from each other by many features
were discovered in one of such cultures (Krylov et al.,
1985). Later it has been found that there are two isolates
both named C. oncopelti differing from each other in the
sequence of their RNA genes (Du and Chang, 1994; Clark,
1997; Hollar et al., 1998) therefore it may be supposed that
different organisms were named C. oncopelti.
Currently there are more than 300 descriptions of insect
trypanosomatids in the literature (Podlipaev, 1990) with
many synonyms or descriptions of organisms of dubious
origin among them. At the same time, only a limited number
of isolates have been investigated in culture. Fifteen years
ago, 1015 isolates had been studied in different laboratories (Wallace et al., 1983). Today this number is no
more than 3040 isolates obtained from a limited range of
hosts and locations. This is obviously inadequate to characterise the diversity of insect trypanosomatids, nor does it
allow carrying out the full investigation of the phylogenetic
relationships within the family. Many cultures are questionable by their history and identity, therefore new cultures are
desirable for modern investigations. Insects serve as harbors
for many very different trypanosomatids. Cultures under
study represent only a minority of parasites.
The universally-primed PCR/cross-hybridisation (Bulat
et al., 1999) analyses of recently isolated cultures demonstrated very high level of insect trypanosomatids diversity.
The results of cross dot blot hybridisation of UP-PCR
products showed that 16 isolates represent 12 well-separated

S. Podlipaev / International Journal for Parasitology 31 (2001) 648652

genospecies (natural groups) featured by specic genome

structure. Two subclusters in the PCR-based dendrogram
were found to be supported by the results of cross dot blot
hybridisation of UP-PCR products. The rst subcluster
consists of four isolates from three different genera and
demonstrates once more that the descriptions based on
cell morphology in the host may be an erroneous assumption. The second reliable cluster including the Leptomonas
isolates from insects of different orders (Leptomonas sp. P
from Mecoptera and Leptomonas nabiculae from Hemiptera) very likely represents the same taxon. This grouping
raises the problem of host specicity of trypanosomatids. It
seems that the different insects, even from different orders,
may host very similar or even the same parasites. However,
the possibility of temporary survival of an alien parasite in a
foreign host cannot be fully excluded. Anyway PCR/cross
hybridisation analysis shows that new cultures compose
new groups of similar organisms (Bulat et al., 1999).
Recent ssrRNA phylogenetic analysis and morphological
data of 10 newly investigated isolates from insects which
have been described by morphology as Leptomonas, Blastocrithidia and Wallaceina show that three insect isolates
(L. seymouri, Leptomonas sp. Nfm and Leptomonas collosoma) represent new lineages on trypanosomatid evolutionary tree (Merzlyak et al., 2001). The tree shows that
Leptomonas sp. Nfm, L. collosoma, and B. triatoma apparently do not belong to any of four major clades of nontrypanosomes identied earlier (Hollar et al., 1998) as
`Phytomonas', `Herpetomonas', `Endosymbiontic' and
`Slowly-evolving'. It is obvious that the set of investigated
cultures falls short of adequately representing the diversity
of insect trypanosomatids. New isolates from new geographical loci have in part lled this gap. Insects trypanosomatids comprise the most diversied part of trypanosomatids
evolutionary tree. Therefore, the more insect trypanosomatids are involved in laboratory investigations - the more new
clusters or/and new lineages are appearing on the tree.
Of course the diversity of insect trypanosomatids have to
be reected in taxonomy. The most obvious disagreement
between phylogeny and taxonomy, reported earlier, was the
polyphyly of the Herpetomonas and Crithidia (Du and
Chang, 1994; Du et al., 1994; Hollar et al., 1998). Endosymbiont-bearing species formed a well-dened `endosymbiontic' clade, while endosymbiont-free members formed
separate clades. The recent tree shows that the genera Blastocrithidia and Leptomonas are also articial taxa
(Merzlyak et al., 2001). This situation can be expected,
since the promastigote morphotype is shared by a variety
of trypanosomatids. A high level of genetic heterogeneity
within the genus Leptomonas was also reported earlier
(Camargo et al., 1992).
As at least four genera of trypanosomatids are polyphyletic, the classication system needs a revision. Morphology
can be used as an supplementary character, but cannot serve
as the base for the future taxonomy (Podlipaev, 2000).
Several monophyletic groups: trypanosomes, leishmanias

651

and some phytomonads could represent the natural taxa.

The existence of a separate genus Endotrypanum is questionable (Cupolillo et al., 2000). A new genus might be
proposed for the clade of endosymbiont-containing trypanosomatids. Application of additional markers and analysis
of a broader range of isolates will be needed in order to
reveal the true diversity of insect trypanosomatids.
The main division on the trypanosomatid evolutionary tree
is the split between Trypanosoma (which has no visible association on the tree with insect parasites) and all the rest of
non-Trypanosoma parasites, near related to trypanosomatids
from insects. Trypanosoma is actually the only trypanosomatid genus, which is out of questions. If even Trypanosoma
is subdivide into several genera - anyway it would remain as
monophyletic group. Insects trypanosomatids together with
their possible offsprings Phytomonas and Leishmania comprise the most polymorphic group among trypanosomatids and their investigations seem to be very relevant.
Acknowledgements
I wish to thank my colleagues for the pleasure of joint
work and our discussions: St. Petersburg Zoological Institute team (Dr A. Frolov and Dr M. Malysheva), Moscow
State University team (Dr A. Kolesnikov, E. Merzlyak and
Dr V. Yurchenko), Dr S. Bulat and Dr D. Maslov. However,
all mistakes and wrong interpretations are entirely of my
own. Many thanks to Dr Alberto Davila and Dr Kevin
Tyler for the invitation to participate TICSTT, for help
with presentation and for their patience. The work was
supported by the grant 99-04-49572 from the Russian Foundation for Basic Research.
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