David M. Spratt

Neuro-angiostrongyliasis: unresolved issues.

Angiostrongylus cantonensis, the rat lungworm, probably evolved with its hosts, members of the genus Rattus and closely related species, in south-east Asia. Since its first discovery in rats in China and in a case of human infection in Taiwan, the parasite has been found to infect humans and other mammals across a wide and ever-increasing territory, which now encompasses much of south-east Asia, Melanesia, Polynesia and eastern Australia. It has also established a foothold in Africa, India, the Caribbean and south-eastern USA. This dispersal has been a direct result of human activity, and in some cases has been linked with the spread of the African giant land snail, Achatina fulica. However, this snail is not critical to the extension of the parasites range, as numerous other indigenous molluscan species serve as adequate intermediate hosts; the importance of Achatina to the life cycle may have been over-emphasized. In Australia, the parasite is established along parts of the east coast, and the presence of an indigenous close relative, Angiostrongylus mackerrasae, suggests a long association of the parasite with its local rat hosts, a situation analogous to that of Angiostrongylus malaysiensis in south-east Asia. These three Angiostrongylus species share virtually the same life cycle, but only A. cantonensis has been confirmed to be a human pathogen.

The origins and evolutionary expansion of the Strongylida (Nematoda)

The Strongylida are thought to have arisen from free-living rhabditoid nematodes, but the relationships between the major groupings within the Strongylida, the Strongylina, the Metastrongylina, Trichostrongylina and the Ancylostomatina are far from clear in spite of the abundance of morphological data now available for analysis. Evolutionary mechanisms including co-evolution, host switching, host dispersal, use of intermediate hosts, various sites of localisation within the definitive host and modifications of life-cycle strategies appear to have been utilised in the expansion of the Strongylida, with different mechanisms predominating in different families or superfamilies. Co-evolution appears to have been a major mode of evolution in the Strongylina, in contrast to the Trichostrongylina, which have used host dispersal and host-switching to great advantage. The phylogeny of the Ancylostomatina shows little association with host evolution, but does match the feeding preferences of the hosts. The Metastrongylina have utilised intermediate hosts and life cycle modifications including a shift to extra-intestinal sites as major means of diversification, in contrast to the other sub-orders. The review, while indicating much progress in our understanding of the phylogeny of the Strongylida, also reveals that enormous gaps still exist, and emphasises the tentative nature of many of the phylogenetic hypotheses tendered to date.

Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: A review

Highlights • Twenty-one species of Angiostrongylus are recognised from wildlife around the world.• Details of hosts, life cycles, pathogenesis, geographical range are known for nine.• Six species are spreading into new regions locally or globally.• Two species, A. cantonensis and A. costaricensis, are zoonotic.• A. mackerrasae, A. malaysiensis and A. siamensis are potentially zoonotic.• Debilitating disease occurs in avian and mammalian wildlife and humans in Australia.

Mitochondrial DNA polymorphism within and among species of Capillaria sensu lato from Australian marsupials and rodents

The nucleotide variation in a mitochondrial DNA (mtDNA) fragment within and among species of Capillaria sensu lato from Australian marsupials and rodents was analyzed using a mutation scanning/sequencing approach. The fragment of the cytochrome c oxidase subunit I (COI) was amplified by PCR from parasite DNA, and analysed by single-strand conformation polymorphism (SSCP) and sequencing. There was no significant variation in SSCP profiles within a morphospecies from a particular host species, but significant variation existed among morphospecies originating from different host species. The same morphospecies was found to occur in 1-3 tissue habitats within one host individual or within different individuals of a particular species of host from the same or different geographical areas, and morphospecies appeared to be relatively host specific at the generic level. The results indicated that the species of Capillaria sensu lato examined, although highly variable in their host and tissue specificity, may exhibit the greatest degree of specificity at the level of host genus.

The role of helminths in the biological control of mammals.

Biological control of invertebrates has been successful while that of vertebrates has been, with the exception of myxomatosis in rabbits, unsuccessful; reasons for this are discussed. Demographic studies of small mammals suggest that population regulation occurs by several different mechanisms, more than one of which may be acting at the same time. Coevolution is an important phenomenon in host-parasite associations, nevertheless parasites may limit host population abundance. The basis of the regulatory effect on the host population is that parasite-induced host mortality or reduction in fecundity is density-dependent. Increasing evidence of the density-dependent effects of helminths on host survival and reproduction is forthcoming from laboratory studies but has not been confirmed in the field. The theory that a helminth parasite may regulate mammal population abundance has been verified recently in the laboratory. A multidisciplinary research programme aimed at understanding the mechanisms responsible for formation of house mouse (Mus domesticus) plagues and seeking strategies to reduce mouse numbers is discussed. One aspect of the work involves investigation of the potential of the nematode, Capillaria hepatica, as a biological agent in the control of wild mice in the cereal-growing regions of Australia. Biological control of mammals is viewed within the context of integrated pest management. A helminth species which reduces host survival or fecundity at an increasing rate as host abundance increases has a role in host population regulation. There is potential to capitalize on that role and apply the helminth as a biological agent in the control of mammals which have attained pest status.

The geographic distribution and host range of Capillaria hepatica (Bancroft) (Nematoda) in Australia

The geographic distribution, host range and prevalence of Capillaria hepatica were recorded in 4629 house mice, Mus domesticus, 263 black rats, Rattus rattus, and 58 Norway rats, R. norvegicus. The parasite was found at five localities, all in or near large towns along the coast. The two Rattus species appeared to be the primary hosts of C. hepatica in Australia. Published and unpublished data on helminth infections of Australian native mammals from 1162 murids (26 species), 3018 marsupials (67 species) and 99 monotremes (two species) were compiled. Only seven animals from three murid species were infected with C. hepatica; all were from the same rainforest in northern Queensland. C. hepatica was distributed widely, occurring in the house mouse, black rat and Norway rat on a 10,850 ha farm but there was no infection in cattle, sheep or goats (abattoir records). Also, 52 rabbits, four cats and one fox (shot samples) and 27 marsupial mice, Sminthopsis crassicaudata (museum specimens), had no sign of C. hepatica infection. Overall, the results indicate that transmission of C. hepatica to native, domestic and feral mammals is rare, presumably because of ecological constraints on egg embryonation and survival. In the light of these findings, the potential use of C. hepatica as a biological agent to control mouse plagues in Australia is discussed.

The occurrence of species flocks in the nematode genus Cloacina (Strongyloidea : Cloacininae), parasitic in the stomachs of kangaroos and wallabies

The occurrence of species flocks within the nematode genus Cloacina was examined using the criteria of host specificity, co-occurrence and monophyly. Species of Cloacina generally exhibited a high degree of host specificity, with most species occurring either in a single host species or in two closely related host species. The frequency distribution of numbers of component species of Cloacina per host species indicated that most host species harboured 2–4 species of nematodes, with an approximately exponential decline in the number of species of parasites to a maximum of 20 species of nematode per host species. Host species harbouring eight or more species of Cloacina were found within a single recent macropodid clade, but there was no correlation between evolutionary age of the host and the number of parasite species harboured. Sampling effort was significantly correlated with the number of nematode species found and, in partial regression analysis, subsumed the effects of host body size and geographic range, which were found to be significant correlates with the number of nematode species present in preliminary analyses. Analysis of co-occurrences of nematode species indicated significant variation between host species, with some hosts (e.g. Macropus agilis) most commonly harbouring a single species of Cloacina, while closely related host species (e.g. M. dorsalis) most commonly harboured numerous species. Parsimony analysis of species of Cloacina based on morphological data suggested that while small series of related nematode species could be identified within a single host species, the species flock in each host species is polyphyletic in origin. Species flocks contributed significantly to community richness in some host species.

Using Combined Morphological, Allometric and Molecular Approaches to Identify Species of the Genus Raillietiella (Pentastomida)

Taxonomic studies of parasites can be severely compromised if the host species affects parasite morphology; an uncritical analysis might recognize multiple taxa simply because of phenotypically plastic responses of parasite morphology to host physiology. Pentastomids of the genus Raillietiella are endoparasitic crustaceans primarily infecting the respiratory system of carnivorous reptiles, but also recorded from bufonid anurans. The delineation of pentastomids at the generic level is clear, but the taxonomic status of many species is not. We collected raillietiellids from lungs of the invasive cane toad (Rhinella marina), the invasive Asian house gecko (Hemidactylus frenatus), and a native tree frog (Litoria caerulea) in tropical Australia, and employed a combination of genetic analyses, and traditional and novel morphological methods to clarify their identity. Conventional analyses of parasite morphology (which focus on raw values of morphological traits) revealed two discrete clusters in terms of pentastome hook size, implying two different species of pentastomes: one from toads and a tree frog (Raillietiella indica) and another from lizards (Raillietiella frenatus). However, these clusters disappeared in allometric analyses that took pentastome body size into account, suggesting that only a single pentastome taxon may be involved. Our molecular data revealed no genetic differences between parasites in toads versus lizards, confirming that there was only one species: R. frenatus. This pentastome (previously known only from lizards) clearly is also capable of maturing in anurans. Our analyses show that the morphological features used in pentastomid taxonomy change as the parasite transitions through developmental stages in the definitive host. To facilitate valid descriptions of new species of pentastomes, future taxonomic work should include both morphological measurements (incorporating quantitative measures of body size and hook bluntness) and molecular data.

Angiostrongylus cantonensis as a Cause of Cerebrospinal Disease in a Yellow-tailed Black Cockatoo (Calyptorhynchus funereus) and Two Tawny Frogmouths (Podargus strigoides)

Abstract A captive yellow-tailed black cockatoo (Calyptorhynchus funereus) and 2 free-living tawny frogmouths (Podargus strigoides), both native Australian species, were presented with neurologic signs including depression and pelvic limb paresis and paralysis. Despite supportive treatment, all 3 birds died or were euthanatized. On histologic examination, sections of metastrongyloid nematode larvae were found in the central nervous system of all 3 birds, whereas intact larvae, identified as Angiostrongylus cantonensis, were recovered from the brain and spinal cord of 2 birds. Angiostrongylus cantonensis, the rat lungworm, has an obligatory migratory phase through the hosts central nervous system, which can cause severe pathologic lesions. Natural infections in accidental hosts have been documented only in mammals, and to our knowledge, angiostrongyliasis in avian hosts has not been previously reported.

Aspects of the life history of Cercopithifilaria johnstoni (Nematoda:Filarioidea).

Abstract Spratt D.M. and Haycock P. 1988. Aspects of the life history of Cercopithifilaria johnstoni (Nematoda:Filarioidea). International Journal for Parasitology 18 : 1087–1092. Cercopithifilaria johnstoni (Nematoda:Filarioidea) occurs in the subcutaneous connective tissues of a spectrum of native murid and marsupial hosts in Eastern Australia. Life cycle studies revealed that: (i) microfilaria occur in lymphatic capillaries and extravascular connective tissue of the dermis (= ‘skin-inhabiting’), (ii) ixodid ticks, particularly Ixodes trichosuri , are intermediate hosts in nature, (iii) development from microfilariae to infective third-stage larva occurs only while the tick is off the host, that is, during ecdysis from larva to nymph or from nymph to adult. Transmission of C. johnstoni in a wild population of bush rats ( Rattus fuscipes ) occurred in summer and winter, and was associated with peaks in the number of larval and/or nymphal stages of ticks on rats. C. johnstoni was transmitted experimentally to bandicoots ( Isoodon macrourus, Perameles nasuta ), bush rats and laboratory rats ( R. norvegicus ), indirectly by subcutaneous inoculation of third-stage larvae and directly by tick feeding. The prepatent period was approximately 3 months and the longest duration of microfilariae in the ‘ skin’ was more than 25 months. Dermal and ocular lesions were observed in R. fuscipes . The host-parasite relationship has the potential for development as an inexpensive and practical model for human onchocerciasis.