Host fecundity reduction: a strategy for damage limitation? - Cell Press

Opinion

TRENDS in Parasitology Vol.17 No.8 August 2001

Host fecundity reduction: a strategy for damage limitation? Hilary Hurd Host fecundity reduction is a life-history trait that is commonly exhibited in parasitic associations. It is particularly prevalent in female invertebrate hosts that invest heavily in egg production during a relatively short life span. Here, Hilary Hurd uses examples of parasitized insects and trematode infections of snails to consider the evolutionary significance of this response to infection. Studies of host egg production and reports of the physiological mechanisms underlying reduction of host reproductive success are used to evaluate the hypotheses that fecundity reduction might be a by-product of infection, or an adaptive strategy on the part of parasite or host.

Hilary Hurd Centre for Applied Entomology and Parasitology, School of Life Sciences, Huxley Building, Keele University, Keele, Staffordshire, UK ST5 5BG. e-mail: [email protected]

At the heart of any parasitic relationship is a conflict of interest, but the battle for host resources is usually resolved in favour of the parasite1. In spite of this pressure on the host, selection for antiparasite measures does not always occur, because the maintenance of surveillance and defence systems can also require resources2–4. Thus, the cost of infection can be less than that of resistance and the host might tolerate some degree of harm without dying. From the viewpoint of the parasite, the costs and benefits resulting from harm done to the host might depend, among other things, on the mode of parasite transmission5. The success of many transmission routes is dependent upon mobile, long-lived hosts, and the good health of the host might be a component of parasite fitness6,7. Utilization of host resources could be expected to diminish host longevity. However, this outcome will neither be beneficial for parasites with long prepatent periods that must mature before their host dies, nor for parasites for which opportunities for transmission exist only as long as their host is alive. How can these parasites remove host resources without adversely affecting host life span? All organisms exhibit tradeoffs between the allocation of resources to reproduction and to maintenance and growth. Evolutionary theory suggests that depressed or delayed reproduction results in an increased life span8, and there is much evidence to support this9,10. Curtailing host reproduction might be the only way in which host resources can be utilized without decreasing host survival11–13. Host fecundity reduction is certainly a very common outcome of parasitic infection. It could be simply a debilitating by-product of infection that is of no adaptive significance. Alternatively, it might be a damagelimitation strategy that results in a host with more nutrients available for its own survival. Such hosts could http://parasites.trends.com

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provide a richer environment for the parasite, and might have a greater life span than a host that maintained the same reproductive effort as an uninfected individual. If this is the case, fecundity reduction could be an adaptive strategy that has evolved in response to parasitism, or it could reflect the manipulation of the host by the parasite. These alternative hypotheses predict that host fecundity reduction should increase either the fitness of the host, or the fitness of the parasite. Theories that address the evolutionary history of parasitic relationships, such as those outlined in this review, are difficult to test. To assess the adaptive significance of host fecundity reduction, it is necessary to understand both the immediate molecular and physiological mechanisms that underlie this trait, and the outcome for the parasite and host in the natural environment in which transmission occurs. Evolutionary models that predict the probable outcome of parasite–host interactions are of limited value if we do not know whether there is sufficient plasticity in the physiology of the host to respond to infection in this manner, or whether the parasite can produce manipulator molecules that control host reproduction. Just as pathology should be viewed in an evolutionary context, it will help evolutionary parasitologists to understand the physiological basis of their observations. Unfortunately, unified studies of parasite-induced fecundity reduction are non-existent, and there is a marked lack of data on both lifetime reproductive success of infected hosts and on the mechanisms that underlie reduced reproductive output. Parasite-induced changes in vertebrate sexual behaviour have attracted considerable attention12,14. However, fecundity reduction is particularly associated with infections of invertebrates that are acting as intermediate hosts or vectors. Although the literature is full of examples of fecundity reduction of parasitized invertebrates15, few have been studied in sufficient depth to enable us to bring experimental evidence to bear upon its adaptive basis. Notable exceptions are some snail–trematode associations16,17, and protozoan, nematode and cestode infections of insects18. Fecundity reduction as a by-product of infection

Reduction in, or cessation of, egg production could be a direct consequence of parasite-induced pathology and might be of no adaptive significance. Unequivocal examples of this occur when parasites feed on gonadal tissue19. This has been termed ‘mechanical castration’20,21 and is quite rare16. Examples among invertebrates are chiefly confined to trematode infections of molluscs, and include the castration caused by rediae of Fasciola hepatica, which consume the ovotestis of Lymnaea truncatula22. In many invertebrates, egg production is related to nutritional status. Thus, if a parasitic infection affects food acquisition, or parasites compete directly for a large proportion of host nutrients, fecundity might decline as a direct consequence.

1471-4922/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(01)01927-4

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Impaired feeding

It is possible that infected insects produce fewer eggs because their food intake is reduced. This has been suggested as an explanation for the reduced reproductive capacity observed in the mosquito, Aedes aegypti, when it feeds on chickens that are infected with Plasmodium gallinaceum23. However, although feeding on infected mice does not reduce the haemoglobin and plasma protein content of the bloodmeal, malaria does reduce the reproduction of anopheline mosquitoes24. The presence of oocysts on the midgut, or sporozoites in the salivary glands, also causes fecundity reduction in mosquitoes feeding to repletion, without a decrease in bloodmeal size, on uninfected mice25. In addition, enzyme activity and protein digestion in mosquitoes are unaffected by malaria infection26. Thus, the amino acids acquired for yolk protein synthesis are the same in infected, as in uninfected, insects. Similarly, reduced protein intake cannot explain fecundity reduction in blackflies, Simulium ornatum, infected with the filarial nematode, Onchocerca lienalis27. In these experiments, egg production was reduced when females took a normal bloodmeal from an uninfected source and microfilariae were subsequently inoculated into the blackflies27. If reproductive curtailment cannot be linked to reduced food intake by infected insects, is it a direct consequence of the depletion of host nutrients by the parasite? Direct nutrient competition

Nutrient competition has been evoked to explain insect fecundity reduction in several species. For example, both longevity and fecundity of the fruit fly, Drosophila nigrospiracula, infested with a macrochelid mite, Macrocheles subbadius declined as mite load increased, probably because of haemolymph extraction by the mites28. In this case, however, fecundity reduction does not appear to confer an advantage to the parasite or host and is probably a by-product of infection. Parasite nutrient requirements are related to parasite biomass, with microparasites expected to require fewer metabolic resources than do macroparasites. The parasite:host biomass ratio and metabolically demanding processes, such as parasite growth and reproduction will be major factors determining the damage that nutrient removal causes. Thus, if direct nutrient competition caused fecundity reduction, a positive relationship between the reduction in host reproductive success and parasite biomass is predicted. This has been observed when Ae. aegypti is infected with the filarial nematodes, Brugia pahangi and Dirofilaria repens29, and when bark beetles, such as Polygraphus rufipennis or Dendroctonus simplex are infected with allantonematid nematodes, such as Sulphuretylenchus pseudoundulatus or Contortylenchus reversus, respectively30. However, host fecundity reduction can occur when parasite biomass is very small, relative to the host26,27,31, or when parasites first invade a host and do not exert a pathological drain on nutrients that would affect egg production25. In the case of rat tapeworm, Hymenolepis http://parasites.trends.com

diminuta, infections of the mealworm beetle, Tenebrio molitor, for example, nutrient competition is unlikely to cause host fecundity reduction because only the early stages of metacestode development, with small biomass, produce factors(s) that downregulate vitellogenin synthesis by the beetle. In addition, only haemolymph from donor beetles that are infected with these early stages causes a reduction in the ovarian protein content of recipient uninfected females. Similarly, when worm burden was increased from one to 20 O. lienalis microfilariae, there was no significant increase in the reduction in protein content of ovaries from the blackfly, Simulium ornatum, over that caused by one worm27. Fecundity reduction caused by Plasmodium yoelii nigeriensis infection of the Anopheles gambiae mosquito is more pronounced when ookinetes are invading the midgut and have not yet started to grow, than it is during later stages of infection (H. Hurd, unpublished). None of these latter examples supports the premise that nutrient robbery is the direct cause of fecundity reduction in insects. Indirect nutrient competition

Parasitic infections create additional drains on host reserves that are not directly related to the nutrient needs of the host. One such cost is associated with mounting a defence response33. Finite resources such as L-Tyr, which is required both for melanin formation in an insect immune response and for the tanning of the egg chorion, might limit egg production, as it does in Armigeres subalbatus infected with Brugia malayi2. Many insect parasites invade their host via the gut, causing mechanical damage34,35 and, in some cases, initiate an immune response36. It is probable that these events divert resources into tissue repair or synthesis of antimicrobial peptides, respectively. We have been unable to demonstrate that wounding induces a reduction in egg production27, but artificial stimulation of the humoral immune response of A. gambiae affects ovarian protein content and egg production (H. Hurd, unpublished). The links between invertebrate defence systems, parasitic infection and reproductive success clearly warrant further investigation. Is the parasite in control? Parasite regulator molecules

If fecundity reduction cannot be attributed to nutrient competition, it could be an adaptive response on behalf of one of either host or parasite. Is it, therefore, an example of host manipulation by the parasite, implicating the existence of genes for reducing host reproductive output (virulence genes)37? The H. diminuta–T. molitor association supports this hypothesis, because metacestodes in early stages of development produce a manipulation factor that directly inhibits vitellogenin synthesis in the beetle fat body. Inhibition will occur in vitro if fat body from uninfected beetles is incubated with an acid extract of metacestodes. The parasite factor is being characterized. It has peptidelike properties but a molecular mass of 10–50 kDa

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Fig. 1. The effect of the metacestode, Hymenolepis diminuta, infection on the longevity of the mealworm beetle, Tenebrio molitor. Sixteen populations of 13 male (a) and 13 female (b) beetles were set up and mortality monitored every two days. All beetles were starved for the first three days post-emergence and then eight populations were exposed to H. diminuta eggs for 24 h. Infected and control populations were then maintained in identical conditions. Ten days after emergence, three female and three males were removed from each population and tested for the presence of nemastacodes. All beetles exposed to eggs were infected. There was a highly significant increase in the survival of infected beetles (P = 0.001), with a hazard ratio (a measure of relative risk) of 2.35 (i.e. control:experimental ratio). Median survival time to 50% mortality was increased by eight days for infected females and to four days for infected males (Cox’s proportional hazard regression). Broken line, uninfected control; unbroken line, infected experimental. Scale bar = 100 µm. Adapted, with permission, from Ref. 38.


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10 15 20 25 Survival (days)

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35 Hymenolepis diminuta

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(Ref. 32). However, this example of a parasite product that directly controls invertebrate–host reproductive fitness appears, at the present time, to be the only one to have been described. It is hoped that its discovery will stimulate the search for further examples.

many associations where trophic transmission via the food chain occurs, adaptive manipulation of the host by the parasite could occur, making the host more vulnerable to predation. A complex interplay of interactions between parasite and host could be resolved in different ways, depending upon the species involved.

Advantages gained by the parasite

Parasites will gain from manipulating host resources away from reproduction if more nutrients become available to the parasite, or the host is longer lived. Measurement of host resources at different stages of infection should be possible, but it is difficult to conduct and interpret studies on the longevity of parasitized insects for two reasons: first, it is hard to simulate conditions found in the wild, in which additional stresses associated with feeding and locomotion are imposed. Thus, advantages that accrue from manipulating host fecundity might not be apparent in the laboratory; second, a control group of infected insects that do not exhibit fecundity reduction is required for valid comparisons to be made, and this is unlikely to exist. Comparisons must, therefore, be made between infected hosts exhibiting fecundity reduction and uninfected hosts. However, if there is no measurable difference between infected- and uninfected-host longevity, a decrease in reproductive success could protect against increased, or early mortality in the infected insects3. There are few data that allow us to link fecundity reduction and host longevity, but the H. diminuta– T. molitor model again provides an example. In a laboratory experiment that monitored eight populations of infected beetles and eight populations of uninfected beetles, infected females had a 40% increase, and males a 25% increase, in the time taken for 50% of the population to die. Overall, a highly significant difference in survival time (P < 0.001) between infected and control populations of beetles was observed, with a control:hazard ratio of 2.35 (Ref. 38) (Fig. 1). In this example, it appears that the parasites would gain from manipulating host fecundity. No host death occurred until after the period of metacestode maturation and increased host longevity would provide more opportunity for the host to be predated and, therefore, the parasite to be transmitted. However, in http://parasites.trends.com

Is the host in control?

Alternatively, curtailment of reproduction could be a host response to infection. Forbes39 used the theory of life-history tradeoffs to predict that parasitized hosts will make changes in the degree and timing of reproductive effort. He proposed that host decisions would be based upon the tradeoff between current, versus future, reproduction, and would be influenced by the pattern of development of the parasite in that host. He defined three types of parasite (Table 1) and proposed that a reduction in host reproductive effort occurs in infections with type I and type III parasites, at least during the early stages of infection. The type II parasite effect has been termed ‘fecundity compensation’40 and results in enhanced host reproduction early in infection and can be followed by early host death41. Examples of type II infections are, however, rare and the concept has only been explored in the context of trematode-infected snails. According to Forbes’ classification, larval trematodes correspond to type II parasites, and complete cessation of molluscan reproduction usually coincides with cercarial release. This has given rise to the term ‘parasitic castration’, but, in most cases, destruction of gonads does not appear to be the cause of sterility and there are reports that the response is reversible42. Schistosoma mansoni infections of Biomphalaria glabrata increase egg production during the initial stages of infection, although egg production eventually stops43,44. However, other investigations have not detected fecundity compensation in this parasite–host association45,46, nor in the well-studied trematode–snail model, Trichobilharzia ocellata– Lymnaea stagnalis16,17. Infection might also bring forward the age of maturity and, thus, allow the host some reproductive success, as occurs in female Culex pipiens mosquitoes infected with the microsporidian, Vavraia culicis47.

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Table 1. Reproductive decisions made by parasitized hosts. Host response will depend on the life history pattern of the parasite within the host. Parasites are classified as type I, II or III according to these patterns of growth and development39,a Classification

Effect on host

Host response

Examples

Type I parasite Rapid growth or multiplication Reduces resources followed by a phase available for current requiring fewer resources reproductive effort

Fecundity reduction occurs early in infection

Malaria–mosquito 25,26 Metacestode–beetle 32,49 Filarial nematode–blackfly 27

Type II parasite Slow but sustained growth or multiplication leading to growing resource requirements with time

Reduces resources available for future reproductive effort

Fecundity reduction or complete cessation of reproduction occurs later in infection and might include fecundity compensation

Trematode–snails Mite–fruit fly

22,43–46 28

Reduces resources for both current and future reproductive effort

Fecundity reduction or complete cessation of reproduction occurs early in infection and is sustained

Nematode–bark beetles

50

Type III parasite Rapid and sustained growth or multiplication aIn

Refs

all of these examples, the effect of the parasite is measured in terms of egg production, rather than total effort devoted to reproduction.

Perrin and Christe48 challenged Forbes’ model39 by suggesting a distinction between total lifetime investment in reproduction or reproductive effort (RE) and current reproductive success (CRS). They argued that the effect of the parasite on the shape of the relationship between RE and CRS will determine whether current reproductive effort is increased or decreased. In practice, it is difficult to measure all aspects of reproductive effort, and most studies of parasitized invertebrates have only determined egg production. However, even using egg production as a measure of current reproductive success is problematical because ‘current’ needs to be defined. For how long should egg production be measured? During the initial infection phase, while the parasite is growing or reproducing, or throughout the infection period? In addition, some organisms produce eggs continuously, while others are batch producers. There is an urgent need for studies that define the period of study, relative to the life history of the parasite, more clearly, and for studies that monitor host RE. These would provide the empirical evidence with which to assess the adaptive nature of reproductive decisions made by parasitized hosts. As with the hypothesis concerning parasite manipulation, it is essential to demonstrate that the physiological mechanisms that underlie the allocation of resources to reproduction are altered by infection. If the host is in control of resource allocation, it should be possible to identify the specific molecules involved and trace their origin to the host. Insects do possess mechanisms to control reproductive effort in response to environmental and physiological conditions such as food supply and mating status. Reproduction regulators, such as antigonadotropins, neuropeptides, ecdysteroides and juvenile hormone, control different aspects of insect vitellogenesis and oogenesis. Thus, there is sufficient plasticity in reproductive versus somatic investment to adjust to infection. Few studies have been made of the effect of infection on these regulators. However, we have demonstrated that female, and not male, T. molitor http://parasites.trends.com

recently infected with H. diminuta metacestodes, produce a circulating antigonadotrophin that reduces ovarian protein content in recipient beetles in which no nutrient deprivation exists32. This strongly suggests that the female host is regulating reproduction in response to infection. Evidence that regulation is initiated by the host also comes from the T. ocellata–L. stagnalis model. Once cercariae are present in the daughter sporocysts, a host-derived factor, schistosomin, is released from cells of the internal defence system. This molecule appears to have cytokine-like properties and performs multiple functions in infected snails, including the inhibition of aspects of female and male reproduction and the alteration of growth rate17. Advantages gained by the host

Tenebrio molitor responds to infection by the type I parasite H. diminuta (Table 1) by immediately reducing fecundity15. This model provides evidence that a longevity advantage is associated with infection38 (Fig. 1). But does this increased longevity represent a fitness advantage to the host? Egg production does not cease in infected females, so an extension in life span could provide the opportunity to lay more eggs than an infected beetle that did not reduce CRS upon infection. To test this hypothesis, we need to measure RE and to demonstrate a physiological link between fecundity reduction and longevity. Again, studies of this sort across a wide range of host–parasite systems are needed. It is noteworthy that life span is only marginally increased in infected male T. molitor (Fig. 1). This sexspecific effect could indicate that fitness advantages gained from resource manipulation might differ in males and females. Infected males invest less effort in mating behaviour as they produce less sex pheromone and respond less well to female pheromone than do uninfected males32. However, the reduction in pheromone production probably does not save as much energy as does a reduction in egg production by females.

Opinion


If curtailment of reproductive effort is a strategy used by many parasitized hosts, we should also question whether this is a general response to all infections, which is modulated by the defense system. Clearly, the parasite must produce a signal that is recognized by the host, and that initiates the change in resource allocation. Evidence from T. ocellatainfected snails suggests that cells of the defence system are involved in downregulating reproduction17, but further studies are needed to investigate this idea. Is this a win–win situation?

Acknowledgements I am grateful to Andrew Read, Chris Arme and four anonymous referees for constructive comments on the article. I thank Tony Polwart for help with graphics.

Although there are associations in which host fecundity reduction is a non-adaptive side effect of infection, many studies of parasite–host interactions provide data that support the hypothesis that repartitioning of resources occurs independently of mechanical damage or nutrient competition and might be an adaptive strategy. Host fecundity reduction has been viewed as both a parasite strategy and a host strategy. If reproduction is associated with a cost to host longevity, it is more intuitive that reducing host RE will help parasite transmission, but the benefits to the host of downregulating CRS and increasing longevity have also been presented in this review. However, the association between metacestodes of the rat tapeworm and a beetle intermediate host (H. diminuta–T. molitor ) clearly demonstrates that these hypotheses are not mutually exclusive, because both parasite and host downregulate reproduction but operate via different points of control of egg production. This association also illustrates that both

References 1 Price, P.W. (1980) Evolutionary Biology of Parasites, Princeton University Press 2 Ferdig, M.T. et al. (1993) Reproductive costs associated with resistance in a mosquito–filarial worm system. Am. J. Trop. Med. Hyg. 49, 756–762 3 Yan, G. et al. (1996) Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 51, 441–450 4 Kraaijeveld, A.R. and Godfrey, H.C.J. (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278–280 5 Ebert, D. (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086 6 Ewald, P.W. (1995) The evolution of virulence: a unifying link between parasitology and ecology. J. Parasitol. 81, 659–669 7 Combes, C. (1997) Fitness of parasites: pathology and selection. Int. J. Parasitol. 27, 1–10 8 Price, P.W. (1984) Insect Ecology, John Wiley & Sons 9 Stearns, S.C. (1992) The Evolution of Life Histories, Oxford University Press 10 Carlson, K.A. and Harshman, L.G. (1999) Extended longevity lines of Drosophila melanogaster: abundance of yolk protein gene mRNA in fat body and ovary. Exp. Gerontol. 34, 173–184

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partners can gain from this strategy. The host has a slower rate of egg production, but its longer life span might provide enough time for lifetime fecundity to equal or exceed that of an uninfected female. There is also more time in which the host of such parasites can be predated, thus increasing the probability of transmission. Regardless of evolutionary history, this parasite-induced resource diversion might increase the epidemiological stability of the host–parasite complex by affording the host some protection from mortality. Even if each partner in a parasitic symbiosis does gain some benefit, they will still conflict over the extent of host fecundity reduction. Whether the parasite or host or both is controlling resource allocation, we are probably observing a tradeoff position where fecundity reduction provides maximum damage limitation with respect to the costs that this strategy imposes upon the instigator. Parasite–host associations will produce many scenarios, played out to different endpoints, and careful examination of more examples must be made before we can draw any firm conclusions. Although these investigations are difficult, we need to understand how parasites influence host egg production throughout the period of infection, and to assess the fitness consequences for both parties, before we can begin to understand the evolutionary framework of fecundity reduction. Investigations into physiological mechanisms should go hand in hand with the production of theoretical models and the assessment of fitness benefits, so that we can obtain a complete picture of the role of fecundity reduction in the life histories of parasites and hosts.

11 Obrebski, S. (1975) Parasite reproductive strategy and evolution of castration of hosts by parasites. Science 188, 1314–1316 12 Read, A.F. (1990) Parasites and the evolution of host sexual behaviour. In Parasites and Host Behaviour (Barnard, C.J. and Behnke, J.M., eds), pp. 117–158, Taylor Francis 13 Hurd, H. and Webb, T.J. (1997) The role of endocrinologically active substances in mediating changes in insect hosts and insect vectors. In Parasites: Effects on Host Hormones and Behaviour (Beckage, N.E., ed.), pp. 179–201, Chapman & Hall 14 Hillgarth, N. and Wingfield, J.C. (1997) Testosterone and immunosupression in vertebrates: implications for parasite-mediated sexual selection. In Parasites: Effects on Host Hormones and Behaviour. (Beckage, N.E., ed.), pp. 143–156, Chapman & Hall 15 Hurd, H. (1990) Parasite induced modulation of insect reproduction. Adv. Invertebr. Reprod. 5, 163–169 16 Hurd, H. (1990) Physiological and behavioural interactions between parasites and invertebrate hosts. Adv. Parasitol. 29, 271–318 17 De Jong-Brink, M. (1995) How schistosomes profit from the stress responses they elicit in their hosts. Adv. Parasitol. 35, 177–256

18 Hurd, H. (1993) Reproductive disturbances induced by parasites and pathogens of insects. In Parasites and Pathogens of Insects (Beckage, N.E. et al., eds), pp. 87–105, Academic Press 19 Sparks, A.K. (1985) Synopsis of Invertebrate Pathology, Elsevier Science 20 Cheng, T.C. et al. (1973) Parasitic castration of the marine prosobranch gastropod Nassarius obsoletus by the sporocysts of Zoogonus rubellus (Trematoda): histopathology. J. Invertebr. Pathol. 21, 183–190 21 Baudoin, M. (1975) Host castration as a parasitic strategy. Evolution 29, 335–352 22 Wilson, R.A. and Denison, J. (1980) The parasitic castration and gigantism of Lymnaea truncatula infected with the larval stages of Fasciola hepatica. Z. Parasitenkd. 61, 109–119 23 Freier, J.E. and Friedman, S. (1976) Effect on host infection with Plasmodium gallinaceum on the reproductive capacity of Aedes aegypti. J. Invertebr. Pathol. 28, 161–166 24 Taylor, P. and Hurd, H. (2001) The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implications for enhanced malaria transmission. Parasitology 122, 491–496 25 Hogg, J.C. and Hurd, H. (1995) Plasmodium yoelii nigeriensis: the effects of high and low incidence of infection upon the egg production and blood-meal size of Anopheles stephensi during three gonotrophic cycles. Parasitology, 111, 555–562

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26 Jahan, N and Hurd, H. (1998) The effect of Plasmodium yoelii nigeriensis (Haemosporidia: Plasmodidae) on Anopheles stephensi (Diptera: Culicidae) vitellogenesis. J. Med. Entomol. 35, 956–961 27 Renshaw, M. and Hurd, H. (1994) The effect of Onchocerca infection on the reproductive physiology of the British blackfly, Simulium ornatum. Parasitology 109, 337–345 28 Polak, M. (1996) Ectoparasitic effects on host survival and reproduction: the Drosophila– Macrocheles association. Ecology 77, 1379–1389 29 Javadian, E. and MacDonald, W.W. (1974) The effect of infection with Brugia pahangi and Dirofilaria repens on the egg-production of Aedes aegypti. Ann. Trop. Med. Hyg. 68, 477–481 30 Tomalak, M. et al. (1990) Pathogenicity of Allantonematidae (Nematoda) infecting bark beetles (Coleoptera: Scolytidae) in Manitoba. Can. J. Zool. 68, 89–100 31 Hacker, C.S. and Kilama, W.L. (1974) the relationship between Plasmodium gallinaceum density and the fecundity of Aedes aegypti. J. Invertebr. Pathol. 23, 101–105 32 Webb, T.J. and Hurd, H. (1999) Direct manipulation of insect reproduction by agents of parasite origin. Proc. R. Soc. London Biol. Sci. 266, 1537–1541 33 Moret, Y. and Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168


34 Lethbridge, R.C. (1971) The hatching of Hymenolepis diminuta eggs and penetration of the hexanths in Tenebrio molitor beetles. Parasitology 64, 389–400 35 Han, Y.S. et al. (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J. 19, 6030–3040 36 Richman, A.M. et al. (1997) Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO J. 16, 6114–6119 37 Poulin, R. and Combes, C. (1999) The concept of virulence: interpretations and implications. Parasitol. Today 15, 474–475 38 Hurd, H. et al. A parasite that increases host lifespan. Proc. R. Soc. London Biol. Sci. (in press) 39 Forbes, M.R.L. (1993) Parasitism and host reproductive effort. Oikos 67, 444–450 40 Minchella, D.J. (1985) Host life-history variation in response to parasitism. Parasitology 90, 205–216 41 Polak, M. and Starmer, W.T. (1998) Parasiteinduced risk of mortality elevates reproductive effort in male Drosophila. Proc. R. Soc. London Biol. Sci. 265, 2197–2201 42 Etges, F.J. and Gresso,W. (1965) Effect of Schistosoma mansoni infection upon fecundity in Australorbis glabratus. J. Parasitol. 51, 757–760 43 Minchella, D.J. and Loverde, P.T. (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. Am. Nat. 118, 876–81

Entomopathogenic nematodes for the biocontrol of ticks Michael Samish and Itamar Glazer Entomopathogenic steinernematid and heterorhabditid nematodes are increasingly used to control insect pests of economically important crops. Laboratory and field simulation trials show that ticks are also susceptible to these nematodes. The authors review the potential of entomogenous nematodes for the control of ticks.

Michael Samish* Kimron Veterinary Institute, PO Box 12, Bet Dagan 50250, Israel. *e-mail: msami_vs@ netvision.net.il Itamar Glazer Dept of Nematology, Plant Protection Institute, PO Box 6, Bet Dagan 50250, Israel.

Biological agents such as oxpeckers, fungi and parasitic wasps are known to control ticks efficiently1,2 but no such agents are used commercially to control ticks. Practical biological control of insect plant pests is well established, and alternatives to chemical pesticides are desirable for several reasons, such as an increased awareness of the potentially harmful effects of chemical residues in food and in the environment, the growing demand for ‘organic’ food, the increasing resistance of pests to pesticides, and the high cost of developing new compounds. One strategy is to develop entomopathogenic nematodes as agents to control arthropod pests. http://parasites.trends.com

44 Thornhill, J.A. et al. (1986) Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni. Parasitology 93, 443–450 45 Meier, M. and Meier-Brook, C. (1981) Schistosoma mansoni: effect of growth, fertility and development of distal male organs in Biomphalaria glabrata exposed to miracidia at different ages. Z. Parasitenkd. 66, 112–131 46 Crews, A.E. and Yoshino, T.P. (1989) Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Exp. Parasitol. 68, 326–334 47 Agnew, P. et al. (1999) Age and size at maturity in the mosquito Culex pipiens infected by the microsporidian parasite Vavraia culicis. Proc. R. Soc. London Biol. Sci. 266, 947–952 48 Perrin, N. and Christe, P. (1996) On host life-history response to parasitism. Oikos 75, 317–320 49 Hurd, H. (1998) Parasite manipulation of insect reproduction: who benefits? Parasitology 116, S13–S21 50 Thong, C.H.S. and Webster, J.M. (1975) Effects of Contortylenchus reversus (Nematoda; Sphaerulariidae) on haemolymph composition and oocyte development in the beetle Dendroctonus pseudotsugae (Coleoptera: Scolytidae). J. Invertebr. Pathol. 26, 91–98

Commercial production of entomopathogenic nematodes from the families Steinernematidae and Heterorhabditidae (Rhabditida) goes on in four continents – mainly as a cottage industry, but also in large fermenters of up to 100 000 l – for the control of insect pests of forest, agricultural and horticultural importance3. More than 25 species of Heterorhabditis and Steinernema nematodes are known to be pathogenic to ~3000 insect species4. About 10 million US$ worth of nematodes were sold in 1998 for the control of insect pests, being added to irrigation systems or sprayed on crops from the ground or air. The infective juvenile stage (IJs) of nematodes is generally used in pest control. When the juveniles encounter a susceptible host, they penetrate the hemocoel by using enzymes and mechanical force. Once inside the host, the nematodes release symbiotic bacteria (eg. Xenorhabdus spp. or Photorhabdus spp.) that colonize and kill the host. Nematode virulence to ticks

Studies during the past decade have shown that entomopathogenic nematodes are also pathogenic to ticks5 (Fig. 1b). Of 16 ixodid tick species from six genera and three argasid species from two genera tested, only one species was not susceptible to nematodes (Table 1). However, in Petri-dish trials engorged female ticks from several species showed large differences in susceptibility to nematodes (Fig. 2a,c; Table 1). Studies in soil-filled cups showed that engorged ixodid (Hyalomma dromedarii) females were more susceptible to nematodes than were argasid ticks6,7. Fully engorged argasid and ixodid

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