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Susceptibility of different insect species to infection by Hymenolepis diminuta and Moniliformis moniliformis

Holt, Rohan H.F. (1989) Susceptibility of different insect species to infection by Hymenolepis diminuta and Moniliformis moniliformis. PhD thesis, University of Glasgow.

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Abstract

Chapter 2 Natural concurrent infections of rats with H. diminuta and M. moniliformis may increase the chances of individual insects being infected by both parasites simultaneously. Although previous work has shown H. diminuta and M. moniliformis can co-exist in the small intestine of the rat, it was considered important to determine the length of time the two species would be simultaneously patent. This time period would occur during maximum rate of egg production by both parasite species, determined from numbers of eggs found the rat's faeces. It was concluded that although eggs of both species were found in the faeces for proximity 11 weeks post-infection, the chances of an insect acquiring an infection would be highest at the time of peak egg production. This was approximately 6 weeks in the mid-patent period of M. moniliformis. Chapter 3 The initial process leading to an infection of the intermediate host by H. diminuta and M. moniliformis were examined; i.e. egg ingestion, hatching, passage along the insect gut and penetration of the midgut wall. Adaptations by the larvae of both species of parasite to infect the intermediate host were shown to influence host-specificity. H. diminuta and M. moniliformis hatched in the guts of a wide variety of insect species, but only M. moniliformis acanthors penetrated the gut wall of P. americana. H. diminuta oncospheres only penetrated the gut walls of the locusts, Schistocerca gregaria and their natural hosts, the flour beetles Tribolium confusum and Tenebrio molitor. Transit time for food material passing along the gut was found to be important in the synchronisation of parasite hatching with arrival at the site of gut penetration. P. americana holds food items and parasites in the foregut (crop) until partially digested before allowing them into the midgut. Thus any H. diminuta oncospheres stimulated to hatch by the insect's mouthparts only progressed as far as the crop until initial digestion was completed; the time taken for crop contents to be passed in to the midgut tended to exceed the time larvae remained active and capable of gut penetration. In contrast, M. moniliformis acanthors hatch over a longer time period and therefore enter the midgut in a state capable of gut penetration. The abilities of the two species of parasite to tunnel through the midguts of different insect species was compared in vitro using a qualitative assay technique. H. diminuta oncospheres were unable to penetrate the tissues of P. americana midgut. Chapter 4 Eggs from both species of parasite were fed simultaneously to insects. It was initially proposed that oral infections of cockroaches with M.moniliformis might facilitate penetration of the cockroach gut by H. diminuta oncospheres, if the gut tissues were sufficiently disrupted by the former parasite. However, only locusts could be simultaneously infected with both species orally, infected, and viable H. diminuta oncospheres fed to cockroaches were found to adversely affect the success of a simultaneously offered dose of M. moniliformis eggs (acanthors). A hypothesis was put forward to explain this result; that H. diminuta oncospheres perturbed the midgut tissues in their unsuccessful attempt to burrow through the gut wall, thus initiating a wound-healing response by the hosts immune system. This resulted in gut-penetrant M. moniliformis larvae being killed by a melanotic encapsulation reaction. Unfortunately, light and electron microscopy has revealed little evidence of such a wounding in the gut which might have initiated such an immune response. Chapter 5 H. diminuta oncospheres were injected directly into the cockroach haemocoele, as it has been previously shown that a small number of parasites survive. By repeatedly passaging the few surviving cysticercoids from each infection through the rat/cockroach system it was hoped to raise a cockroach-infective strain of H. diminuta. However, their infectivity to cockroaches did not increase in successive generations; several explanations for the possible failure of this selection programme have been put forward. Intrahaemocoelic injections of pre-hatched H. diminuta oncospheres or M. moniliformis acanthellae into the host made it possible to by-pass the gut and thus investigate concurrent haemocoelic infections of cockroaches with both species of parasite. When H. diminuta was injected into M. moniliformis-infected cockroaches, prevalence and intensity of the former were significantly elevated compared to naive controls, indicating that a putative immunosuppressive action from M. moniliformis facilitated H. diminuta development. In some instances, H. diminuta was found to have burrowed through the envelope surrounding M. moniliformis and continued normal development within, unmolested by the host's haemocytes. This was considered as further evidence for the protective nature of the acanthocephalan envelope. Chapter 6 In Chapter 6, assays for aspects of haemocyte behaviour was performed on insects (in particular, P. americana) experimentally infected with either M. moniliformis or H. diminuta. It was found that the phenomenon seen in Chapter 4, whereby H. diminuta adversely affected the success of M. moniliformis when fed simultaneously to cockroaches, appears to be a direct consequence of the stimulatory effect of H. diminuta on the immune system. Conversely, the developing larvae of M. moniliformis were shown to depress haemocytic activity; possibly explaining why elevated numbers of injected H. diminuta survive in M. moniliformis-infected cockroaches. To investigate the affects of immune stimulation on the survival of parasites, locusts were injected with Zymosan, a derivative of yeast cell walls containing 1,3-glucans. H. diminuta oncospheres, injected into Zymosan-stimulated locusts appeared to be partially encapsulated, resulting in a temporary arrest in their development when compared to controls. An assay was devised to observe the encapsulation of materials in vitro by the haemocytes of P. americana. This method was used to show differences in the haemocytic encapsulation reaction to the different larval stages of M. moniliformis and H. diminuta. Both the gut-penetrant stages of each parasite (i.e. oncospheres and acanthors) were encapsulated, whereas the haemocoelic stages (i.e. cysticercoids and acanthellae to cystacanths) remained free of haemocytes. Chapter 7 Finally, in Chapter 7, a model for the alternative pathways leading to success or failure of parasitism by H. diminuta and M. moniliformis in the insect host has been discussed. The results presented here contribute to the fuller understanding of how immune stimulation and immunosuppression affect the survival of helminth parasites, particularly in the cockroach host. These two phenomena have also been shown to be effected by the parasites themselves.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Additional Information: Faculty of Science.
Subjects: Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences
Supervisor's Name: Lackie, Dr. Ann
Date of Award: 1989
Depositing User: Elaine Ballantyne
Unique ID: glathesis:1989-2439
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 21 Mar 2011
Last Modified: 05 Feb 2014 15:39
URI: http://theses.gla.ac.uk/id/eprint/2439

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