Choanotaenia - an overview | ScienceDirect Topics

Tapeworms
Despite a diet of predominately seeds, zebra finches can be infested with tapeworms, which generally require an insect or annelid host to complete their life cycle. At the authors’ facility, several birds died or were euthanized because of ill health within 2 weeks of arrival from a vendor. At necropsy, one zebra finch was found to have its intestines impacted with worms; eggs containing hexacanth embryos were noted on fecal flotation exams (Fig. 23.18). The cestodes were identified as Choanotaenia sp. (courtesy of Dr. Mike Kinsella; Fig. 23.19); exact speciation was not possible because some taxonomic features, e.g., a complete ring of rostellar hooks, were lost during processing. Interestingly, there is a report of estrildid finches experiencing an infestation of Choanotaenia spp. in Australia about 30 years ago (McOrist et al., 1984); the affected adult birds were depressed and had diarrhea prior to death. The two Choanotaenia spp. involved could not be determined, but one was similar to C. infundibulum, a tapeworm common in chickens and other birds (Morishita and Schaul, 2007), occasionally in insectivores and rodents, and at least once in a rhesus macaque (Jones et al., 1980). Another U.S. research institution had zebra finches with tapeworms that were identified as Raillietina sp. (Dr. Larry Carbone, personal communication). Oral praziquantel (10 mg/kg in water by oral gavage weekly for 3 weeks) is effective in eliminating adult tapeworms. Most animal facilities would lack the intermediate hosts for their continued propagation.
Intermediate Hosts of Parasites
Tapeworms (cestodes), flukes (trematodes), roundworms (nematodes), and thorny-headed worms (acanthocephalans) of many species that infest domestic and wild animals use beetles as intermediate hosts. Animals become infested by ingesting parasitized beetles that contaminate feed or bedding (tenebrionids, carabids) or that are attracted to animal dung (scarabaeids) or by ingesting water in which infective beetles have disintegrated.
Two tapeworms that infest the small intestines of poultry are the broad-headed tapeworm (Raillietina cesticillus) and Choanotaenia infundibulum (Fig. 9.11). Both parasites cause enteritis and hemorrhaging in chickens, turkeys, pheasants, and guinea fowl. A few tenebrionids and scarabaeids and more than 35 species of carabid beetles, notably in the genera Amara and Pterostichus, are intermediate hosts for R. cesticillus (Cheng, 1973). Some tenebrionid and dermestid species, including the lesser mealworm beetle, are intermediate hosts for C. infundibulum. Proglottids or tapeworm eggs ingested by beetle larvae or adults develop into cystercerci (encysted larvae) that can then infest birds that eat the beetles. Chicks are most susceptible to serious infestations and often die from worm burdens.
The beef tapeworm (Taenia saginata) can use dung beetles and carabids as intermediate hosts, although they are not essential for transmission. Beetles associated with infective dung or debris can ingest proglottids or eggs as in the case of poultry worms. Cattle and humans infested with the tapeworm may exhibit mild symptoms such as weight loss, abdominal pain, and increased appetite.
The dwarf tapeworms (Hymenolepis nana and H. diminuta) that usually infest rodents, especially rats and mice, can infest humans when the intermediate host beetles are accidentally ingested. Tenebrio molitor may act as an intermediate host for H. nana, although this worm is readily transmitted directly from one vertebrate host to another. Several species of tenebrionids (Tenebrio spp. and Tribolium spp.) are required intermediate hosts for H. diminuta. Larval and adult beetles infesting grain and cereals ingest worm eggs that develop into cysticercoid stages that infest rodents or humans, usually children, who ingest the beetles. Dwarf tapeworms produce minimal symptoms in rodents and people, although heavy infestations in children may cause abdominal pain, diarrhea, convulsions, and dizziness.
Beetles are known to be intermediate hosts for only a few trematodes. These are parasites of frogs that become infested by ingesting parasitized dytiscid beetles and pose no problem for other vertebrate animals.
Many nematodes infest livestock and wildlife, but only a few use beetles as intermediate hosts. Spirurid nematodes of various species infest livestock and, rarely, humans. Physocephalus sexalatus and Ascarops strongylina eggs develop in many species of scarabaeid dung beetles (Geotrupes spp., Onthophagus spp., and Scarabaeus spp.) that then may be ingested by pigs. Both wild and domestic swine can be infested with these stomach worms that cause digestive problems in heavily infested young animals. Gongylonema pulchrum is a parasite of the upper digestive tract of sheep, cattle, goats, and other ruminants as well as horses, dogs, and humans. The worms burrow in the mucosa and submucosa of the oral cavity and esophagus and may cause bleeding, irritation, numbness, and pain in the mouth and chest. Scarabaeid and tenebrionid beetles serve as intermediate hosts for the larvae. Scarabaeid dung beetles are also the intermediate hosts for Spirocerca lupi, the esophageal worm of dogs and wild canids. Physaloptera caucasica, another spirurid, often parasitizes monkeys in tropical Africa, where humans are also commonly infested. This nematode causes digestive distress by infesting the alimentary tract from the esophagus to the terminal ileum. Scarabaeid dung beetles are its intermediate hosts.
The acanthocephalans, aptly named for their thorny heads, include species found worldwide infesting swine, rodents, and carnivores such as dogs. Macracanthorhynchus hirudinaceus, which attaches to the small intestines of swine, causes enteritis and produces intestinal nodules that lower the value of these tissues when they are sold to make sausage casings. Eggs of this parasite are ingested by scarab beetle larvae of species belonging to various genera (Phyllophaga, Melolontha, Lachnosterna, Cetonia, Scarabaeus, and Xyloryctes), including May and June beetles, leaf chafers, dung beetles, and rhinoceros beetles. Infested beetle larvae, as well as the pupae and adults that develop from them, are infective to both pigs and humans. Humans and pigs often show no symptoms. However, in cases of heavy infestations, both human and porcine hosts may experience digestive problems, such as abdominal pain, loss of appetite, and diarrhea that can lead to emaciation.
Two other acanthocephalan worms that parasitize the small intestines of their hosts use scarab beetles or tenebrionids as intermediate hosts. They are Macracanthorhynchus ingens, which infests raccoons and occasionally dogs and humans, and Moniliformis moniliformis, a parasite of rodents and dogs.
Niclosamide (4): It is a safe and highly effective drug for treating tapeworm infections in cats, dogs, sheep, cattle, horses and poultry. A dose of 100-125 mg/kg of the drug has been found to provide excellent activity against Taenia ovis, T. hydatigena, T. taeniformis, T. pisifơrmis and M. multiceps in cats and dogs. Niclosamide also possesses 100% activity against E. granulosus in dogs at a dose of 50 mg/kg [69a]. The drug shows high activity against the intestinal tapeworms, Moniezia expansa, M. benedeni, Thysaniezia giardi and Aviŧellina spp. in sheep at an oral dose of 50-75 mg/kg; however, its activity against the bile-duct dwelling tapeworms is not satisfactory [9,67].
In horses, higher doses (200-300 mg/kg) of niclosamide may be needed to eliminate the mature and immature stages of Anophlocephala spp. However, the drug exhibits excellent efficacy against Choanotaenia infundibulum, Hymenolepis spp., and Dicranotaenia spp. etc. in chicken and ducks at an oral dose of 50-80 mg/kg [67–69]. A combination of niclosamide and tetramisole, called niclomisol-O, has been found to be highly effective against the intestinal nematodes, Haemonchus, Oesophagostomum, Bunostomum and Trichostrongylus spp. in sheep [63b].
Niclosamide shows weak activity against Fasciola spp., but is nearly 100% effective against immature paramphistomes in sheep at a dose of 50-90 mg/kg. The drug, therefore, may be used to control paramphistome outbreak in sheep flocks [68,69].
Terenol (resorantel, 5b): At a dose of 65 mg/kg, terenol shows high activity against Moniezia spp. in ruminants [69]. The above dose of the drug was also effective in removing 80-100% of the paramphistomes (P. cervi) from sheep, goats and cattle [68,69]. Terenol is effective against Gastrodiscus aegypticus infection in horses [69].
Oxyclozanide (7): This is an effective drug for treating Fasciola hepatica infection in sheep and cattle. The usual therapeutic dose of oxyclozanide is 13-15 mg/kg for mature flukes; however, repeated doses (15 mg/kg for 3) may be needed to eliminate immature flukes. Thus the drug may be used to control acute fascioliasis in ruminants [68–70].
Brotianide (8): The drug is currently used to treat fascioliasis in sheep. A dose of 7 mg/kg of brotianide shows 91-99% activity against 7-14 weeks old flukes; however, its activity against 6 weeks old flukes is weak (50-90%). It also possesses 85-90% activity against paramphistomes in sheep and cattle [68,69]. The maximum tolerated dose of brotianide is 27 mg/kg in sheep.
Hilomid (9a,b): At a dose of 60 mg/kg, this mixture of bromosalicylanilides (bromsalans) removes 12 week old F. hepatica from sheep. For eliminating flukes above 12 weeks of age, a lower dose of 30 mg/kg is sufficient [72–75]. The maximum tolerated dose of hilomid in sheep is only 60 mg/kg [69].
Rafoxaniđe (12): Rafoxanide is an effective drug for treating F. hepatica infection in sheep and cattle. An oral dose of 10-15 mg/kg of this anthelmintic eliminates 91-99% of the mature flukes and 50-90% of the younger flukes in ruminants. However, the above dose level of rafoxanide has been found to be almost 100% effective against immature and mature F. magna in cattle. About 92% of the immature paramphistomes may also be removed from sheep and goats at an oral dose of 15 mg/kg of rafoxanide [68,69]. It is effective against the roundworms, Haemonchus contortus and Oestrus ovis in sheep. The maximum tolerated dose in sheep is 45 mg/kg [68,69].
Clioxanide (13): The drug has been evaluated against mature and immature liver flukes in grazing sheep causing 98-100% reduction of adult worms of F. hepatica at a single oral dose of 25 mg/kg. Even a dose range of 10-25 mg/ kg of clioxanide was effective in eliminating adult liver flukes. However, a higher dose of 40 mg/kg was necessary for removing the young flukes. The drug was found to be well tolerated as only 0.03% of the animals died when 25,000 sheep were treated. The maximum tolerated dose of clioxanide in sheep is 100 mg/kg [69,76–78]. Clioxanide, therefore, may be used to cure fascioliasis in sheep and cattle with very low toxicity [79].
Closantel (14): It is a highly effective salicylanilide for eliminating liver flukes, F. hepatica, F. gigantica and blood-sucking nematodes, Haemonchus contortus in sheep, horses and cattle at an oral dose of 7.5-10 mg/kg [80,80a]. However, its activity against adult flukes is more pronounced than the younger ones. Closantel is also effective against Bunostomum spp. in ruminants [70] and against Fascioloides magna in sheep [81]. The drug has been shown to be highly active against H. contortus resistant to either benzimidazoles or levamisole [71]. The usual recommended dose of clioxanide in sheep is 7.5-10 mg/kg. In cattle it is given at a dose of 2.5 mg/kg as injectable solution [69].
5.1.1 Antechinus stuartii (Table 5)
This species is of particular parasitological interest because it has a diverse array of parasitic helminths (45 known species) given its small size, occupying an exceptional spectrum of host tissues (Beveridge and Barker, 1976; Spratt, 1986). A. stuartii belongs to the family which is morphologically closer to the South American microbiotheriids than most other Australian families and has an unusual life history, with a short (3–4 week) synchronous mating period followed by the death of all males (Lee and Cockburn, 1985). The gastrointestinal tract of Antechinus spp. is simple, with the short intestine and colon merging almost imperceptibly into one another (Hume et al., 1989) (Figure 5A).
The helminth fauna of A. stuartii is dominated numerically by the Trichostrongyloidea (12 species), particularly by the family Herpetostrongylidae, with representatives of eight other nematode superfamilies, three species of cestodes and three species of trematodes. The superfamilies or families of helminths represented are frequently those expected in carnivores or insectivores, with many of the species presumably requiring arthropods as intermediate hosts. In the case of the cestodes, the species of Potorolepis, P. aklei and P. bradleyi, belong to a distinctive Australian genus, but the affinities of this genus are unclear (Vaucher et al., 1984; Vaucher, 1992). Choanotaenia ratticola represents an acquisition from Rattus fuscipes, a native rodent which is commonly parasitized by this cestode (Obendorf, 1979) and which is abundant in habitats frequented by A. stuartii. Both cestode genera utilize insects as intermediate hosts.
The relationships of the diverse trichostrongyloid nematodes have been investigated by a number of authors, and they apparently have multiple phylogenetic origins. The six genera of trichostrongyloid nematodes present in A. stuartii belong to three families, Herpetostrongylidae, Mackerrastrongylidae and Dromaeostrongylidae.
The Herpetostrongylidae, containing the genera Woolleya, Dessetostrongylus, Patricialina and Nasistrongylus, is closely related to the family Viannaiidae since some members of both families possess three ventral body ridges. The Viannaiidae occurs in South American marsupials and rodents. This host and geographical association has lead to the hypothesis (Humphery-Smith, 1983) that the herpetostrongylid nematodes were part of the parasite fauna introduced by the dispersing microbiotheriids and that they have radiated subsequently within the Australian marsupials.
Two additional trichostrongyloid genera, Sprattellus and Tetrabothriostrongylus, belong to the family Mackerrastrongylidae which was considered by Durette-Desset and Chabaud (1981) to have diversified in monotremes and invaded marsupials secondarily. Whether this transition occurred in Australia or prior to the dispersion of the marsupials to Australia is not known.
The third family, Dromaeostrongylidae, represented by the genus Peramelistrongylus, is closely related to the Trichostrongylidae, of which the best known representatives parasitize domestic ruminants. The genera of the Trichostrongylidae appear to be derived from an ancestor similar to the genus Libyostrongylus, a parasite of ostriches, which is closely related to Dromaeostrongylus in another ratite bird, the emu (Durette-Desset and Chabaud, 1981). The remaining genera of the Dromaeostrongylidae, of which Peramelistrongylus is one, are apparently derived from a colonization of marsupials by this family. Peramelistrongylus occurs in the stomachs of dasyurid marsupials, bandicoots and the musky rat kangaroo, Hypsiprymnodon moschatus (see Spratt et al., 1991).
Thus the eight genera of trichostrongyloid nematodes in A. stuartii belong to three different phylogenetic lineages within the Trichostrongyloidea, one linked to similar parasites in South American marsupials, another apparently derived from monotremes and a third apparently derived from ratite birds endemic to the Australian region. None of their life cycles has been elucidated.
The metastrongyloid genus Marsupostrongylus contains numerous species parasitic in various families of Australian marsupials (Spratt, 1979, 1984) but no hypotheses have been advanced to explain their phylogenetic relationships. The Angiostrongylidae, to which the genus belongs (Anderson, 1978), contains genera in insectivores, carnivores and rodents as well as in Australian and South American marsupials. A hypothesis similar to that advanced for the Herpetostrongylidae by Humphery-Smith (1983) would account for its introduction to Australian marsupials with dispersal via microbiotheriids and subsequent radiation within Australian marsupials. Species of Marsupostrongylus studied to date utilize gastropod intermediate hosts (Mackerras, 1955; Spratt, 1979).
The spiruroid nematode, Spirura aurangabadensis, found in the oesophagus of A. stuartii and other dasyurid and peramelid marsupials, occurs in bats and primates in South-East Asia (Spratt, 1985). This nematode species may have reached Australia with bats, or could have been introduced by an arthropod intermediate host. The parasites of Australian bats are still very poorly known, and the nematode may be found in bats in the future.
Both the acuarioid parasites of A. stuartii, Antechiniella suffodiax and Synhimantus australiensis, have as their closest relatives genera in birds. Several species of Synhimantus occur in Australian birds (Mawson et al., 1986). Antechiniella is found in the endemic rodents, Rattus fuscipes, R. lutreolusand Hydromys chrysogaster, as well as in marsupials (Obendorf, 1979; Smales, 1991). Based on the ontogeny of its larval stages, Antechiniella is derived from the genera Streptocara or Rusguniella (see Quentin and Beveridge, 1986) which are common parasites of the oesophagus and proventriculus of waterfowl in Australia (Mawson et al., 1986).
A. stuartii also harbours plerocercoids, other metacestodes, larval ascaridoid and spirurid nematodes and larval acanthocephalans, indicating its importance in the diet of larger reptilian, mammalian and avian predators.
The helminth parasites of A. stuartii thus form a complex assemblage in terms of their phylogenetic origins. The Herpetostrongylidae and possibly the metastrongyloids may have been parasitic in the original dispersing marsupials which reached Australia, while the remaining helminths, or at least those for which suggestions can be advanced as to their origins, were apparently derived from monotremes, ratite birds, birds belonging to orders other than the ratites, and bats.
Although none of their life cycles has been elucidated, limited ecological observations have been made on the helminth parasites of A. stuartii. Seasonal changes in abundance occur, with abundance of several species or genera increasing in the winter months, June to August (Beveridge and Barker, 1976). There is a major increase in abundance in helminths in male A. stuartii during this period of the year, which coincides with the mating season, and is associated with increased concentrations of free corticosteroids in the plasma, and with a consequent involution of lymphoid tissue and increased susceptibility to infection by helminths (Barker et al., 1978; Lee and Cockburn, 1985). Although minor pathological changes due to the parasites are detectable, including interstitial pneumonia caused by the metastrongyloid Marsupostrongylus lanceolatus, gastric erosion and ulceration associated with Capillaria rickardi and chronic fibrotic lesions caused by the burrowing activity of Antechiniella suffodiax in the stomach, none of the helminth parasites appear to cause the total demise of the male antechinus population following mating. The mortality is due rather to gastric haemorrhage, babesiosis or listeriosis (Barker et al., 1978). Nonetheless, the period of mating, with the immunocompromised state of the male antechinuses, does lead to a substantial increase in numbers of helminths and presumably therefore to increased environmental contamination with eggs. The parasites involved presumably are able to take advantage of this situation and yet obviate the potentially devastating effect of the loss of half of the host population each spring following mating. The detailed ecological studies necessary for an understanding of this situation have not been undertaken.
Apart from the annual loss of all males, A. stuartii inhabits an environment which is prone to disturbance by fire. Bush fires reduce the number of hosts or remove hosts and parasites entirely from a given locality, which is then gradually recolonized as the vegetation regrows. Studies both before and after bush fires (Spratt, 1986) have shown that following fire, the numbers of A. stuartii remain low for several years then increase dramatically although the diversity of the helminth community of A. stuartii is not significantly lower in the period of recolonization.
A. stuartii supports a diverse helminth community of 32 species in southern New South Wales (Spratt, 1986). It shares many of its helminths with the related species, A. swainsonii, but the community is distinct from those found in other sympatric small marsupials and rodents (Spratt, 1986) (Figure 6). The parasite communities of the two species of Antechinus are most similar to that found in Sminthopsis leucopus, another small dasyurid.