Pathogenicity of trypanosomatids on insects

Parasitology Today, vol.

IO, no. I2, I994

463

Pathogenic@ of Trypanosomatids on Insects G.A. Schau b More and more effects of typanosomatids on insects have been recognized in the pastJ%-wyears. Here, Giinter A. Schaub reviews such eflects, class$jng theJagel2ates according to the intensity of the eficts on the insect host into pathogenic, subpathogenic and apathogenic typanosomatids. He emphasizes that subpathogenic typanosomatids which cause only minor eficts under qptimal conditions might act synergistically with natural styesso~s, thereby being an important regulate y factor in insect populations. More than 700 species of trypanosomatids have been described’. Nearly all heteroxenous trypanosomatids, which belong to the genera Leishmania, Typanosoma, Endotypanum and Phytomonas, are transmitted by insects. In contrast to the strong effects on the vertebrate hosts or plants, in most cases the heteroxenous trypanosomatids do not affect their vector@. Very strong effects are known only for T. rangeli in Rhodnius prolixus (see Ref. 6 for review). Homoxenous (entomophilic) trypanosomatids also colonize the intestinal tract of the insects, very often in high densities, and some species of both groups also invade the haemocoele (Table 1). Homoxenous trypanosomatids are species of the genera Herpetomonas, Crithidia, Rhynchoidomorras, Blastocrithidia and Leptomenus, and are characterized by their development only in one group of hosts or one host species, mainly arthropods. Although most homoxenous trypanosomatids are classified alsparasites, there is little evidence of pathogenic@ (see Box 1). Effects have been reported for some specie@5,7-9. Only the pathogenicity of B. triatomae on Triutoma infestans has been investigated in detai15. Since the publication of my recent reviews, which was concerned solely with pathological effects of trypanosomatids on insects, some trypanosomatid / insect vector systems have been investigated in more detail. The effects will be discussed here under five headings: (1) behavioural alterations; (2) disturbances of organ systems; (3) effects on pre-adult development; (4) effects on adults; and (5) synergistic effects of trypanosomatids and other stressors. Alterations of host behaviour In many systems, the hosts are either weakened by the infection or the transmission rate is increased by parasite-induced alterations of behaviour, ie. infected bloodsucking insects attack the hosts more often (see Ref. 5 for review). The consequences of reduced fitness have been investigated only in bumblebees naturally infected with C. bomb94 and in water striders naturally infected with B. gerridis and/or C. jIexonema1*J2. In both insects, the infections reduce the collection

Giinter A. Schaub is at the Department and Parasitology, Ruhr-University-Bochum, Germany. 0

1994, Elsevier Science Ltd

of Special Zoology D-44780 Bochum,

and predation of food, respectively. Heavy infections also drastically reduce the fitness and thereby mating success of infected male water stridersu. A preference of females for males with low parasite loads (which has been reported especially in mammals and birdsis) has not been investigated in trypanosomatid infections of insects. Modifications of feeding behaviour are induced by many heteroxenous trypanosomatids. In some systems, trypanosomatids and insect hosts seem to compete for metabolites in the ingested blood, making the insects hungry earlier (see Ref. 5 for review). However, the causative agents of leishmaniasis, Chagas disease and Nagana interfere with the ingestion process of sandflies, triatomines and tsetse, respectively. Multiple small cutaneous lesions may be caused by interrupted feeds of a single infected sandfly (see Ref. 14 for review), and one of the T. rangeli-infected bugs ingested no blood at all even after 28 probe@. Infected bugs and tsetse probe significantly more times than do uninfected flieGJ6 but, in the latter system, discrepancies using different Salivaria species or stocks occur (see Ref. 14 for review). If blood ingestion of the infected insects is delayed, or if it is interrupted by the host’s repulsive actions, or if no or only small bloodmeals are taken, the vectors may quickly move on to another host. Different mechanisms seem to be responsible for the enhancement of transmission in the different trypanosomatid/vector systems (see Ref. 14 for review). The pharynx of the sandfly can be blocked in its entire length with a plug of parasites, and the lumen of the foregut is significantly narrowed by the parasites. In cases of partial blockage, the parasites should impair flow by exceeding the capacity of the cibarial pump.

Table I. Natural invasion of the Trypanosomatidae” Trypanoromatid Leishmonia tropica Tryponosoma sp. T. range/i Trypanozoon sp. Phytomonas nordicus Blastocrithidia caliroa Herpetomonas sp. H. bombycis H. muscarum H. swainei Leptomonas chattoni I_ emphyti I_ fimiliaris saxatilis L mercieri L naucoridis L pyrrhocoris

haemocoele

of insects by

Host insect (order) fhlebotomus sergenti (Diptera) Glossina palpalis (Diptera) Rhodnius prolixus (Hemiptera) Glossina pallidipes (Diptet-a) Troilus luridus (Hemiptera) Caliroa cerasi (Hymenoptera) Mythimna separata (Lepidoptera) Bombyx mori (Lepidoptera) Musca domestica (Diptera) Hippolaces pusio (Diptera) Neodiprion swainei (Hymenoptera) Agrotis pronubana (Lepidoptera) Emphytus cinctus (Hymenoptet-a) Lygaeus saxatilis (Hemiptera) Simulium reptans (Diptera) Naucoris maculatus (Hemiptera) Pyrrhocorisapterus (Hemiptera)

“Data from Ref. 34, and see Refs I, 52 and 53 for reviews.

Parasitology Today, vol.

464

IO,

no.

12,

I994

Box 1. Pathogenicity In a classification according to the intensity of the effects on the insect host, the majority of trypanosomatids must be classified to be apathogenic *, ie. they will not affect survival of the host even under adverse conditions. Recently, we separated from this group the ‘subpathogenic’ trypanosomatids, which will not affect the life span of the host under optimum conditions, but which do harm the insect under adverse conditions, ie. they might act synergistically with other biotic or abiotic stressors. So far, only a few pathogenic trypanosomatids are known that kill the insect under optimum conditions (see Table). A classification of trypanosomatids into the three groups can easily be Table. Classification of pathogenicity of trypanosomatids for insects obtained for hemimetabolous insect Host insect Pathogenicity class hosts. Late instar larvae should be colSubpathogenic lected in the field from populations with a known high infection rate and mainSandfly Leishmonia oethiopica

tained in the laboratory under standard-

ized optimum conditions. After moult to the

final instar or adult stage, the re-

spective parameters (eg. developmental times, life expectancy or reproduction rate) can be determined and the parasite burden after death. In holometabolous insects, ageing may complicate the

classification and therefore, the physiological age of the adult insects has to be determined. If effects are observed which can be correlated with the para-

site burden, then the trypanosomatid is a pathogenic one. If no effects occur, a second stressor should be included (eg. food deprivation). If the assessed parameter is reduced in infected insects and this reduction correlates with the parasite burden, the species can be

L amazonensis

Sandfly

I._braziliensis T@anosoma spp (of toads, lizards) T. b. brucei T. congolense

Sandfly Sandfly

Tsetse Tsetse

T. cruzi

Triatomine

Blastocrithidiagerridislcrithidiafrexonema

Water

Subpathogeniclpathogenic Leishmania donovani

strider

intermediate Sandfly

L major

Sandfly

Crithidia bombi

Bumblebee

Pathogenic Trypanosoma lewisi

T. rangeli

Rat flea Triatomine Bed bug Hymenoptera

Blastocrithidiacaliroa 6. triatomae

Triatomine

classified into the subpathogenic group

Herpetomonas muscarum

Diptera

of trypanosomatids. If no effects occur at all, it is apathogenic.

H. swainei Leptomonas

*I prefer the terms ‘apathogenic’ and ‘subpathogenic’, since the temx

Hymenoptera pyrrhocoris ‘avirulent’ and ‘subvirulent’ focus more on the developmental

Red soldier bug capacity of a parasite

and not on Its pathogenicity.

However, Schlein et ~1.17emphasize that the cardiac valve is damaged by Leishmania (affecting gorging) and that, during contraction of the food pumps, the parasites in the midgut are regurgitated into host skin. A further mode of action might be due to the firm attachment of Salivaria to mechanoreceptive sensilla which act as fluid flow meters, thereby disturbing the correct function. There are also direct pathological effects of these trypanosomatids on the salivary glands’s, presumably reducing the cholinesterase activity in the secretion of the salivary glands of infected tsetselg. In T. rungeli-infected bugs, the parasites invade the haemocoele and the salivary glandGo (M. Schwarzenbach, PhD thesis, University of Basle, 1987) and decrease salivary antihaemostatic componentszl.

Disturbances in organ systems

Gut. Although trypanosomatids colonize the intestinal tract in high numbers, disturbances of digestion have been only rarely observed (see Ref. 5 for review). The mechanisms of pathogenicity vary according to the different lineage of the different regions of the intestine: foregut and hindgut are covered by a cuticle whereas the midgut wall cells are protected by the thin peritrophic membranes or homologous structures. In the foregut, the cuticle and underlying epithelial cells can be damaged in Leishmuniu-infected sandflies by secreted enzymes (a chitinase and a N-acetylglucosaminidase)z, affecting gorging and enabling parasite

transmission (see above). Since haemoglobin inhibits the chitinase secretion in vitro, lysis of chitinous components of the peritrophic membranes coincides with the digestion of haemoglobin=. In this system, there is a direct effect on digestive enzymes of the midgut by a secretion of glycoconjugatesz4. In our system (B. friatomue and different species of Triatominae), ingested blood is not well digested in infected bugs. Electron microscopy shows that the extracellular membrane layers (acting like the peritrophic membranes in other insects), the microvilli and the epithelial cells are sequentially damaged ~6 (Fig. 1). These subunits of the midgut are also affected by other trypanosomatids, but no pronounced effects on digestion occur (see Ref. 5 for review). Destroyed midgut cells have been observed in B. gerridis-infected water striders (A.O. Frolov and M.N. Malysheva, pers. commun.) and Phytomonus nordicus-infected bugs (A.O. Frolov, S.A. Podlipaev and S.O. Skarlato, pers. commun.). In the hindgut, the cuticle can be covered by a carpet of parasites (Fig. 2); the absorption of metabolites by specialized structures (the rectal glands) may be impaired, but there is as yet no proof for this. The rarely observed direct effects on the cuticle might be explained by the same enzymatic mechanisms as in the foregut (see Ref. 5 for review). Mdpighiun tubules. The function of the Malpighian tubules - the secretion of urine - is strongly affected in bugs infected with either B. friutomue or T. rungeli (see Ref. 5). After ingestion of blood (6-12 times their

Parasitology Today, vol. IO, no. 12, I 994

465

Fig. 1. (/eft) Transmission eleztron micrograph of the midgut of a Blastocrithidia triatomae-infected Triatoma infestann Pathologicaleffects are indicated by the lacking extracellular membrane /ayes the reduced microvilfar border (arrow) and the vacuolization of epithelial cells. Arrowhead, basal /amino; h, haemocoele; I, lumen ofmidguc n, nucleusofa cell ofthe intestinal wall; v, wcuole. Scale bar = 2 pm. fig. 2. (right) Scanning electron micrograph of a carpet of Blastocrithidia triatomae in the rectum of the bug Triatoma infestans. In estab lished infections, the small free area ofthe rectal cuticle will also be covered by about five layers of flagellates. Scale bar = 5 pm.

body weight), rapid excretion of water is essential for a normal movement, and bugs can reduce their body weight by 40% within 214h of blood ingestion. In infected bugs, the abdomen can remain swollen even after several days. Tissue darnage by T. rungeli, the lack of diuretic hormone or the presence of a chemical inhibitor in the haemolymph decreases the secretion of Malpighian tubules 27. Pathological effects on the ultrastructure of the cells of the Malpighian tubules are also evident in B. triutozrzue-infected T. in&stuns (eg. a reduction in the number of basal cell interdigitations, mitochondria and microvilli), but secretion rates of isolated tubules from infected and uninfected bugs are nearly identical. Also, the storage and release of diuretic hormone in infected bugs is unaffecteds. Our hypothesis that the reduced tracheal system is responsible for the discrepancy between in vitro and in viva measurements seems to be supported by most recent results showing that the tracheal supply of the Malpighian tubules is reduced in B. triutomue-infected T. infesfuns (and also in aposymbiotic bugs) (G.A. Schaub and S. Eichler, unpublished). Huemocoele. The immune system in the haemocoele is responsible for the success or failure of the establishment of haemocoele-invading trypanosomatids. Whereas bacterial infections induce the production of antibacterial proteins, invasion of the haemocoele by flagellates presumably does not induce an antiflagellate response. However, in the haemolymph of tsetse and bugs, an antitrypanosomal factor acts against specific species (see Ref. 5 for review). In bugs, T. rungefi suppresses the humoral response, in that the prophenoloxidase system is not activated28. A cellular immune response is induced by T.. rungeh; the number of phagocytic cells increases strongly in T. infestuns and R. proiixus29. However, T. rungeli multiplies inside the phagocytic haemocytes of R. prolixus and destroys them,

thereby reducing the number in old and heavy infections (see Ref. 5 for review). Cuticle. In Hemiptera, infection with either T. rungeli or B. triutomue results in a pale cuticlem-3, and the mucous coating of Hymenoptera larvae desiccates and peels off in B. culirou infection@. In the first system, this seems to be caused by the parasite’s multiplication in the epidermal cell.+, whereas the second species does not invade the haemocoele, but affects especially concentrations of those amino acids that are specifically used for development of the new cuticle (eg. the concentration of tyrosine in the haemolymph is statistically significantly reduced in infected bugs). An increase in the concentration of /3-alanine and an accumulation of its precursor, aspartate, indicate the importance of this mode of pathogenicity33. In Pyrrhocoris upterus, we are uncertain whether or not the pale cuticle (reported by Lipa35) is due mainly to the L. pyrrhocoris infections (M. Kagel and G.A. Schaub, unpublished). Investigating naturally infected bugs, we often find uninfected pale or infected normally coloured bugs. In a wild population of another bug, Gruphosomu line&urn, which is also coloured black and red and in which the paler specimens occur more regularly in autumn, dark red and pink specimens from Mallorca, Spain showed no infections of any flagellate (G.A. Schaub, unpublished). Other organs. Many organs (eg. salivary glands, fat body and nervous system in T. range&infected bugsz7) are destroyed if the parasites invade the haemocoele and multiply intracellularly. The fat body is reduced in Herpetomonus swuinei-infected sawfly larvae and B. triutomue-infected bugssJ6. Effects on pre-adult development and mortality Whereas T. cruzi has no adverse effects on the preadult stages of triatomines under optimum maintenance

466

conditions37, T. rungeli and B. triatomae are highly pathogenic. Typanosoma rangeli only affects species of the genus Rho&us, while B. triutomae is pathogenic to all other triatomines except those of the genus Rhodniuss6. Groups of T. range&infected R. prolixus need lo-40% more time to reach the adult stage than do the uninfected group+. The total pre-adult mortality rate for T. range&infected Rhodnius species is 20-60% higher than in the respective uninfected groups and even higher for Cimex5. Since the T. rungeli strains show a strong attenuation during culture in vitro, systems in which parasite and vector originate from the same village should be used to investigate contrary results with respect to sensitivity of the different larval instars and sex-related sensitivitys, since salivary gland infections arise in more male hosts than female@. Using a natural mode of infection with B. triatomae, ie. infecting the bugs solely by maintaining uninfected and infected animals together, the mean developmental time of T. infestans up to the imaginal moult is increased by 40% (Ref. 40). In such groups, a direct transmission of B. triatomae between bugs occurs, normally by coprophagy, but cannibalism is not excluded41. Increasing the likelihood of infection by addition of more infected bugs increases the infection rate of the T. infes tans-population and (clearly correlated therewith) the mortality rate, the final larval instar showing the highest mortality rate+. Investigating mainly T. infestans, the correlation of infection and mortality rate is also evident in in vitro infections by feeding a mixture of blood and the infeccysts, tious stage of B. triatomae, the drought-resistant through artificial membranes”. Pathological effects are observed after a time lag of about two months, ie. after infection of first, second or third instar larvae, effects occur in the third, fourth or fifth instar, respectively (G.A. Schaub and S. Wolf, unpublished). Increasing the developmental times by lowering the maintenance temperatures, but not by long-term starvation, increases the effects&. Starvation increases the developmental times of R. prolixus, but the bugs remain unaffected and this species is therefore classified to be tolerant to B. triatomae infections. Investigating different species of triatomines, Panstrongylus megistus and Dipetuloguster maxima and the Triatoma species T. infestans, T. braziliensis, T. sordida, T. pallidipennis and T. spinolai are susceptible and sensitive (Ref. 5; G.A. Schaub, unpublished) and, therefore, B. triutomae is a good candidate for the biological control of vectors of Chagas d&as&. The sensitive bug species are much more seriously affected by B. triatomae than are those affected by T. rangeli, the mortality rate being increased by 20-80%; in some groups of D. maxima, all larvae died. apterus system, an infection In our L. pyrrhocoris/P. due to the offer of Lepptomonas-infected food to thirdand fourth-instar larvae only slightly increases the developmental time of the final instar but does cause high mortality rates. Infections of final&star larvae do not affect either the pre-adult developmental period or the mortality rate (M. Kagel and G.A. Schaub, unpublished). Such a restriction or increase of effects to/after infections of young larvae is also evident in H. swuinei infections of the jack pine sawfly (Hymenoptera) and in Herpetomonas muscarum-infected eye gnats (Diptera). Up to 20% more sawfly larvae die in

Parasitology Today, vol.

IO, no. 12, I994

the late larval instars. This effect may be increased during the winter, in which 80% of the infected pupae die (compared to 30% of uninfected pupaeas). In H. muscarum-infected eye gnats, 41% fewer adults emerge compared to uninfected populations%. No detailed laboratory studies have been performed with the haemocoele-invading B. culirou, which seems to be responsible for the collapse of outbreaks of a fruit-tree pest, the Hymenoptera Caliroa cerasiM. Effects on adult life span and reproductive rate Investigations of effects of heteroxenous trypanosomatids on adults are contradictorys. In future investigations on Leishmania, salivarian trypanosomes and T. cruzi, the vector should also originate from the same locality as the flagellate and should be reared under optimal conditions. Maudlin and co-workers have shown that, 60 days after an infective feed, T. brucei rhodesiense infections significantly reduce the longevity of Glossina morsituns morsituns of both sexes (I. Maudlin and P.J.M. Milligan, pers. commun.). Presumably because more infections mature in males than in females47, this reduction is seen more markedly in males. Trypnosoma congolense, which does not infect the salivary glands, does not affect longevity. Reductions in life span that are due to the invasion of midgut cells are evident after infections of fleas with the rat trypanosome T. Iewisi. After infection with T. avium the number of eggs produced by the experimental vector Aedes aegypti were reduceds. Whereas the life span of T. rangeli-infected R. prolixus adults may be only slightly reducedBp39, egg production is reduced by about two-thirds compared to controls; in the infected bugs the percentage of unviable eggs increases by 22% (Ref. 31). Considering homoxenous trypanosomatids, the adult life span is reduced by 9-25% in H. muscarum-infected eye gnats&. The B. triutomae infection reduces the mean life span of females or males of T. infeshzns after moult to the adult stage by 74% (females) or 60% (males)s. The life span of P. apterus is reduced in bugs having high L. pyrrhocoris loads in comparison to uninfected (longer-living) animals (G.A. Schaub, unpublished). In investigations of the reproduction rate, results with H. swainei are contradictory, but B. pessoai (syn. L. pessoai) affects the ovaries of Anopheles. Infections with B. triatomae reduce the number of laid eggs per day, egg weight, hatching rate and weight of the first instar larvae of T. infestuns, compared to uninfected controls (see Ref. 5 for review). Spring queens infected with C. bombi have less-developed ovaries than do uninfected specimenslo, and after founding a nest the initial oviposition rate of infected queens is reducedu. Synergistic effects of trypanosomatids and other stressors Natural populations of insects are often subjected to adverse biotic and abiotic stressors that are absent in the laboratory. Only some of the abiotic stressors have been investigated in detail with trypanosomatidinfected insects, but these do not include temperature and relative humidity. The reduced emergence rate of H. muscurum-infected eye gnats (see above) indicates the importance of such stressors. A synergistic effect of infection and capture and transport to the laboratory may cause a high mortality rate. The action of

ParasitologyToday, vol. IO, no. 12, I 994

insecticides is increased in T. b. brucei- and T. congolense-infected tsetse, males reacting more sensitively than females, but in T. i;nfestuns,infections with 2’. cruzi or B. friafumae do not a.ct synergistically with insecticides (see Ref. 5 for review). The normal social interactions of the investigated insect species must be remembered, since maintenance in isolation or in overcrowded conditions can be a stress factor. Under either of these stress conditions, infections of T. infestunswith B. friufomue increase preadult developmental periods, but only overcrowding (not isolation) increases the mean total mortality rates by 25% (Ref. 49). The non-optimal maintenance conditions may act by weakening the insect host. In that case, the intensity of the effects may be caused, in part, by secondary infections. Since the effects of B. friufomue vary in groups infected with the same dose and maintained under identical conditions, there might be an increase either in the sensitivity to B. friufomue infections or in the susceptibility to other pathogens which cannot develop in uninfected bugs, or which only do so to a harmless level. The determination of the starvation resistance offers a good opportunity to recognize subpathogenic trypanosomatids (Box 1). Infections of male water striders with B. gerridis and /or C. flexonemu, which do not affect survival time of regularly fed bugs reared under optimum conditions, reduce the starvation resistancell. Comparing laboratory populations of uninfected and T. cruziinfected T. infesfuns, the mean starvation resistance period is decreased by ;3% in third-instar larvae, 14% in fourth-instar larvae and 17% in fifth&star larvaeso. The respective data for the B. friufomue-infected bugs, 51%, 55% and 32%, show the difference between the subpathogenic

heteroxenous

and the pathogenic hom-

oxenous flagellate. Investigating natural populations of P. upferus, the starvaltion resistance of bugs is reduced in bugs having high L. pyrrhocoris loads in comparison to uninfected (longer-surviving) animals (G.A. Schaub, unpublished). Mechanisms of pathogenicity Whereas the pathogenic@ of Leishmuniu seems to be due to the excretion of chitinases and glycoconjugates,

other trypanosomatids directly affect organs (eg. by a penetration of cells, an intracellular multiplication or an attachment to mechanoreceptors). In only some systems in which flagellates invade the haemocoele (Table 1) has pathogenicity been (observed (Box 1). However, a rapid multiplication of parasites in the haemocoele should result in deleterious effects. In the two systems in which many effects have been investigated in detail (‘r. range&infected R. prolixus and B. friufomue-infected T, irzfesfuns), the similar complex sickness syndrome may be due to the same mechanism. Similar effects occur in aposymbiontic bugs and Watkins31 emphasizes that the number of symbionts is reduced in T. rungeli-infected R. prolixus. A reduction of the number of symbionts near the flagellates was also evident in electron microscopy of B. ruubeiinfected Coreus murginufus (H.G. Kallenbom and M.

Thiirnmes, pers. commun.). (Pathogenic@ studies have not been performed for &is system.) Since supplementation of blood with B-group vitamins supports the initial development of B. triutomue in the small intestine

467

of young T. infesfuns and strongly reduces the pathogenic@, a competition of the bug and the flagellates for the vitaminslmetabolites or other effects on the symbionts may be the mechanism of the pathogenic@ of trypanosomatids in Hemipterasl (C. Jensen, PhD thesis, University of Freiburg, 1987). Since T. infesfuns possesses other species of symbionts than do R. prolixus (G.A. Schaub, unpublished), the phenomenon that B. friutomue and T. rungeli affect differing species

of triatomines might be caused by differences in the sensitivity of the different species of symbionts. Most recently, we showed that the number of symbionts is reduced in B. friufomue-infected 7’. infestuns, but not in B. triutomue-infected R. prolixus (G.A. Schaub and S. Eichler, unpublished).

Conclusion Usually no pathological effects of infections with trypanosomatids can be observed in insects. However, the weakening of insects, eg. by agein or adverse weather conditions, may increase the pa a ogenicity of the flagellates. These subpathogenic trypanosomatids might be important in regulating insect populations but offer no chance for a biological control of insects. Such control campaigns can only be performed with highly pathogenic trypanosomatids. However, only 1% of the described species of trypanosomatids are pathogenic and of these seven species only B. triutomue is a good candidate for a control of vectors of Chagas disease. So far, only insecticides and, to a minor extent, improvements on housing standards are successfully used to control the triatornines4. Disadvantages for the use of B. friutomue are that the bugs have to take up the cysts orally during coprophagy and the slow action, effects mainly occurring in the late larval instars. However, advantages seem to be more important: the flagellate does not affect vertebrates, is highly pathogenic for many species of triatomines and suppresses development of T. cruzi in double infections (G.A. Schaub and M. Mehl, unpublished). In addition, some cysts remain virulent even after storage in dry faeces for 13 years (G.A. schaub and J.M. Lohse, unpublished). Preliminary field trials are needed to test whether or not B. triutomue can be included in an integrated control

programme.

Acknowledgements The authorthanks Alexander0. Frolov, Helmut G. Kallenbom, Marina N. Malyshewa, Ian Maudlin, Sergei A. Podlipaev, Sergei 0. Skariato and Yosef Schlein for providing unpublished results or papen in press for this review. I am deeply grateful for funding of my investigations from the UNDP/World Bank/WHO Special Progtamme for Research and Training in Tropical Diseases and the Deutsche Forschungsgemeinschaft

References 1 Podlipaev, S.A. (1990) Proc. Zool. Inst. Acad. Sci. St Petersburg 217,1-177 2 Brooks, W.M. (1974) in Insect Diseases (Vol. 1) (Cantwell, G.E., ed.), pp 237-300, Marcel Dekker 3 Molyneux, D.H. (1977) Adv. ParasitoZ. 15, l-82 4 Molyneux, D.H. (1983) in Current Topics in Vector Research (Vol. 1) (Harris, K.F., ed.), pp 117-148, Praeger 5 Schaub, G.A. (1992) Adv. Purasitol. 31,255-319 6 D’Alessandro, A. (1976) in Biology of the Kinetoplustida (Vol. 1) (Lumsden, W.H.R. and Evans, D.A., eds), pp 327-403, Academic Press 7 Steinhaus, E.A. (1963) Insect Pathology, Academic Press

Parasitology Jodoy, vol. IO, no. I23 I994

468 8 Wallace, F.G. (1979) in SioZogy of the Kinetoplustida (Vol. 2) (Lumsden, W.H.R. and Evans, D.A., eds), pp 213-240, Academic Press 9 Tanada, Y. and Kaya, H.K. (1993) Insect Pathology, Academic Press 10 Shvkoff, J.A. and S&mid-Hempel, I’. (1991) Behavioral Ecol. 2, 245-248 11 Arnqvist, G. and M&i, M. (1990) Oecologiu 84,194-198 12 Arnqvist, G. (1990) Evolution 46,914-929 13 Read, A.F. (1988) Trends Ecol. Evol. 3,97-102 14 KiIlick-Kendrick, R. and Molyneux, D.H. (1990) Parasitology Today 6,188-189 15 Axiez, N. and East, J.S. (1984) Acfa Trap. 41,93-95 16 Jenni, L. et al. (1980) Nature 283,383-385 17 SchIein, Y. et al. (1992) Proc. Nut1 Acud. Sci. USA 89,9944-9948 18 Kokwaro, E.D. et al. (1991) Insect Sci. Applic. 12,661-669 19 Golder, T.K. et al. (1987) Actu Trop. 44,325-331 20 Hecker, H. et al. (1990) Parusitol. Res. 76,311-318 21 Garcia, E.S. et al. (1994) Exp. Purusitol. 78,287-293 22 SchIein, Y. et UI. (1991) Proc. R. Sot. London: Ser. B 245,121-126 23 Schlein, Y. and Jacobson, R.L. (1994) Parasitology 109,23-28 24 Borovsky, D. and SchIein, Y. (1987) Med. Vet. Entomol. 1,235-242 25 Jensen, C. et al. (1990) Purusitology lOO, l-9 26 Schaub, G.A. et al. (1992) Eur. 1. Protistol. 28‘322-328 27 Watkins, R. (1971) J. Invertebr. Pathol. 17,67-71 28 Greg&o, E.A. and Ratcliffe, N.A. (1991) Parasite Immunol. 13, 551-564 29 Zeledbn, R. and de Monge, E. (1966) J. Invertebr. Puthol. 8, 420 -424 30 Grewal, M.S. (1957) Exp. Purusitol. 6,123-130

Standardized Nomenclature of Parasitic Diseases I read with interest, with some concern, and with a certain grudging admiration, the letter of Dick Ashford of the Liverpool School of Tropical Medicine’. My interest was generated by the topic of the letter, namely the Standardized Nomenclature of Parasitic Diseases (SNOPAD) which has been advocatedby the World Association for the Advancement of Veterinary Parasitology (WAAVP), by the World Federation of Parasitologists (WFP), and by the European Federation of Parasitologists (EFP). My concern stemmed from the implication that this matter had not been discussed at ICOPA VII in Paris. It had indeed been discussed and at some length, at both the old and the new WFP Council Meetings (ie. 1986-l 990 and 1990-l 994 Councils). In addition, a joint board meeting of the WFP, the EFP and the WAAVP was held in

Old Uncle Tom Cobbley et al. Recommendation E IO of the International Code of Zoological Nomenclature (I 985) states that a ‘zoologist who cites the name of a genus or taxon of lower rank should cite the name of the author and the date at least once in each publication’.Some editors of scientific journals now insist this is done. It is with some dismay, therefore, that we

31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53

Watkins, R. (1971) 1. Invertebr. Puthol. 17,59-66 Schaub, G.A. (1988) J. Invertebr. Pathol. 51,23-31 Schaub, G.A. et UI. (1990) J. Insect Physiol. 36,843-853 Lipa, J.J. et al. (1977) Actu Protozool. 16,121-129 Lipa, J.J. (1963) in Insect Puthol. (Vol. 2) (Steinhaus, E.A., ed.), pp 335-361, Academic Press Smirnoff, W.A. and Lipa, J.J. (1970) J. Invertebr. Puthol. 16, 187-195 Schaub, G.A. (1989) Parasitology Today 5,185-188 Aiiez, N. et al. (1987) Mem. Inst. OszouldoCruz 82,1-6 Tobie, E.J. (1965) 1. Purusitol. 51,837-841 Schaub, G.A. and Jensen, C. (1990) 1. Invertebr. Puthol. 55,17-27 Schaub, G.A. et al. (1989) J. Protozool. 36,171-175 Schaub, G.A. (1990) Purasitol. Res. 76,306-310 Schaub, G.A. (1991) J. Invertebr. Puthol. 58,57-66 Schaub, G.A. et al. (1990) Parasitology Today 6,361-363 Smimoff, W.A. (1974) Phytoprotection 55,64-66 Bailey, C.H. and Brooks, W.M. (1972) 1. Invertebr. Pathol. 20, 31-36 Maudlin, I. et al. (1990) Actu Trap. 48,9-15 Shykoff, J.A. and S&mid-Hempel, I’. (1991) Apidologie 22, 117-125 Schaub, G.A. (1990) J. Invertebr. Puthol. 56,249-257 Schaub, G.A. and L&h, P. (1989) Ann. Trap. Med. Parasitol. 83. 215-223 Jensen, C. and Schaub, G.A. (1991) Eur. J. Protistol. 27,17-20 Wallace, F.G. (1966) Exp. Parusitol. 18,124-193 Molyneux, D.H. et al. (1986) in Immune Mechanisms in Invertebrate Vectors (Lackie, A.M., ed.), pp 117-144, Clarendon Press

The Hague in September 1992, at which time, again,there was unanimity regarding acceptanceof SNOPAD. (Full minutes availablefrom Dr F. von Knapen, National Institute of Public Health and Earth Protection, PO Box I, 3720 BA Bilthoven, The Netherlands.) I think it is important for your readers to know that the idea of SNOPAD has been discussed at great length by the Councils of all three organizations above, and has been fully endorsed by all three of them. I have used some terms such as leishmaniasis for more than three decades (and been exposed to them for some five decades!). It is, accordingly, not easy to switch to other terms, no matter how logical and sensible such a changeis. However, the changes are logical and sensible and hence my grudging admiration for Ashford’s courage in publicly opposing SNOPAD [which evolved from SNOAPAD (Standardized Nomenclature of Animal Parasitic Diseases) as clearly explained in a Comment article in the same issuez].

We recognize that there will undoubtedly be a cadre of parasitologists who, like me, are getting long in the tooth, and who may be too set in their ways to be able to accommodateto the suggested changes recommended by SNOPAD. However we must recognize that such changesshould be made and that our heads should prevail over our hearts. Let us adopt SNOPAD and eschew obfuscation.

find the authors of Leishmanio columbiensis have left us with the task of citing ten names’. Even Old Uncle Tom Cobbley (of the English folk song) had only six colleagues! If Recommendation E IO is not changedin future editions of the Code, and if we are obliged to follow it, we shall carry this burden for eternity - unless grounds are found to reject or synonymize the name. (This temptation could warp a taxonomist’s objectivity!) In decryingthe modem trend for multiple authorities for names of taxa, Crosskey

acknowledged that muitidisciplinaty solutions to biological questions result in joint authorship more frequently now than in the past. Another reason for numerous authors may be that it is difficult to dazzle grant-giving bodies with the number of times one’s name appean merely in the acknowledgements, and it is preferable to be among the authors, however many. Crosskey was upset by ‘excessive multiple authorship for new species’and gave examples of a blackfly and sandfly each with five authors, and a Leishmonia species with

References

I Ashford, R.W. ( 1994) ParasitologyToday IO, 143 2 Kassai,T. and Burt, M.D.B. Today IO, l27- I28

(I 994)

Parasitology

Mick Burt

(President of the WFP) Department of Biology University of New Brunswick Fredericton New Brunswick Canada E3B 6E I