The role of chewing lice (Phthiraptera: Philopteridae) as intermediate hosts in the transmission of Hymenolepis microps (Cestoda: Cyclophyllidea) from the willow ptarmigan Lagopus lagopus (Aves: Tetraonidae).

The cestode Hymenolepis microps is an intestinal parasite of tetraonid birds, including the willow ptarmigan (Lagopus lagopus). This parasite is able to maintain a high prevalence and intensity throughout the year, even in a subarctic environment in bird populations with relatively low host densities, indicating effective transmission routes. Willow ptarmigan consume mainly vegetal material and active consumption of invertebrates is confined to the first two or three weeks of life. Ptarmigan are infected by different species of ectoparasites, of which two species of feather lice, Lagopoecus affinis and Goniodes lagopi, are the most abundant. In this study, we explored the hypothesis that feather lice may be suitable intermediate hosts for H. microps. We applied histological techniques and light microscopy to investigate lice for the presence of larval cestode stages (cysticercoids). We found 12 cysticercoid-like structures inside chewing lice collected on L. lagopus hosts harbouring H. microps. In addition, a polymerase chain reaction (PCR) screening of Ischnocera lice DNA, targeting the 18S rRNA gene of the cestode, showed positive results for two different short fragments of the 18S rRNA gene of H. microps which were sequenced from lice collected on birds. Both independent lines of evidence support the hypothesis that Ischnocera lice might be suitable intermediate hosts in the life cycle of H. microps in L. lagopus.

Insights on the host associations and geographic distribution of Hymenolepis folkertsi (Cestoda: Hymenolepididae) among rodents across temperate latitudes of North America.

Synoptic data and an understanding of helminth parasite diversity among diverse rodent assemblages across temperate latitudes of North America remain remarkably incomplete. Renewed attention to comprehensive survey and inventory to establish the structure of biodiverse faunas is essential in providing indicators and proxies for identifying the outcomes of accelerating change linked to climate warming and anthropogenic forcing. Subsequent to the description of Hymenolepis folkertsi in the oldfield mouse, Peromyscus polionotus, additional specimens of hymenolepidids were collected or discovered in archived museum repositories from multiple species of deer mice (Peromyscus maniculatus, Peromyscus leucopus), the golden mouse (Ochrotomys nuttalli), chipmunks (Tamias striatus, Tamias amoenus), the 13-lined ground squirrel (Ictidomys tridecemlineatus), and tree squirrels (Sciurus carolinensis, Sciurus niger) from disjunct localities in the USA spanning southern Georgia, Virginia, Pennsylvania, Connecticut, the Upper Peninsula of Michigan, Wisconsin, and central Idaho. Specimens were largely consistent morphologically with the original description of H. folkertsi. Initial DNA sequence data, from a portion of the mitochondrial NADH dehydrogenase subunit 1, demonstrated intraspecific variation among three apparently geographically isolated populations attributed to H. folkertsi (uncorrected genetic distances of 2.7 % (Idaho and Michigan), 2.4 % (Virginia + Pennsylvania and Michigan), and 1.89 % (VA + PA and ID). Geography rather than host association explains the distribution and occurrence of H. folkertsi, and host colonization among deer mice, chipmunks, and other sciurids within regional sites is indicated. Genetic divergence revealed across localities for H. folkertsi suggests historically isolated populations, consistent with extended evolutionary and biogeographic trajectories among hymenolepidids and species of Peromyscus and Tamias in North America. Field inventory, that revealed these parasite populations, substantially alters our understanding of the distribution of diversity and provides insights about the nature of the complex relationships that serve to determine cestode faunas in rodents.

Description of two new species of Hymenolepis Weinland, 1858 (Cestoda: Hymenolepididae) from rodents on Luzon Island, Philippines.

Our helminthological examination of murid rodents on Luzon Island, Philippines, revealed a remarkable diversity of Hymenolepis Weinland, 1858. Here we describe two new species based on specimens from murid rodents Rattus everetti (Günther) and Apomys datae (Meyer) collected from Luzon Island. Hymenolepis alterna n. sp. differs from all known species of Hymenolepis in having irregularly alternating genital pores. This feature has not been reported from any previously known member of Hymenolepis. Additionally, Hymenolepis alterna n. sp. also differs from other Hymenolepis spp. in the relative position of both poral and antiporal dorsal osmoregulatory canals which are shifted towards the middle of the proglottis in relation to the ventral canals on both sides of the proglottides, and in having curved or twisted external seminal vesicle, covered externally by a dense layer of intensely stained cells. Hymenolepis bilaterala n. sp. differs from all known species of Hymenolepis in the relative position of both poral and antiporal dorsal osmoregulatory canals, which are shifted bilaterally towards the margins of proglottides in relation to the ventral canals, and in possession of testes situated in a triangle and eggs with very thin outer coat. A total of seven species of Hymenolepis are known from the Philippine archipelago. This total includes the cosmopolitan species Hymenolepis diminuta (Rudolphi, 1819), which was likely introduced to the island with invasive rats. Strikingly, all seven known species occur on the island of Luzon alone. By comparison, only six Hymenolepis spp. are known from the whole Palaearctic and seven from the Nearctic despite a much better level of knowledge of rodent helminths in these zoogeographical regions, as well as vast territories, diverse landscapes and very rich rodent fauna. This suggests that Hymenolepis spp. may have undergone an unusually active radiation in the Philippines. Possible explanations of this phenomenon are discussed.

The anthelmintic efficacy of natural plant cysteine proteinases against Hymenolepis microstoma in vivo.

Little is known about the efficacy of cysteine proteinases (CP) as anthelmintics for cestode infections in vivo. Hymenolepis microstoma is a natural parasite of house mice, and provides a convenient model system for the assessment of novel drugs for anthelmintic activity against cestodes. The experiments described in this paper indicate that treatment of H. microstoma infections in mice with the supernatant of papaya latex (PLS), containing active cysteine proteinases, is only minimally efficacious. The statistically significant effects seen on worm burden and biomass showed little evidence of dose dependency, were temporary and the role of cysteine proteinases as the active principles in PLS was not confirmed by specific inhibition with E-64. Worm fecundity was not affected by treatment at the doses used. We conclude also that this in vivo host-parasite system is not sensitive enough to be used reliably for the detection of cestocidal activity of compounds being screened as potential, novel anthelmintics.

Basic and applied problems in developmental biology and immunobiology of cestode infections: Hymenolepis, Taenia and Echinococcus.

Differentiation and development of parasites, including longevity in host animals, are thought to be governed by host-parasite interactions. In this review, several topics on the developmental biology of cestode infections are discussed from immunobiological perspective with a focus on Hymenolepis, Taenia and Echinococcus infections. The basic premise of this review is that 'differentiation and development of cestodes' are somehow affected by host immune responses with an evolutionary history.

Sequential and concurrent exposure of flour beetles ( Tribolium confusum ) to tapeworms ( Hymenolepis diminuta ) and pesticide (diatomaceous earth).

The response of Tribolium confusum to sublethal levels of 2 environmental stressors was studied, i.e., parasitic infection represented by the cestode Hymenolepis diminuta , and a physical stressor represented by the natural pesticide diatomaceous earth (DE). These were applied sequentially (DE, then infection) to detect indirect or carryover effects of DE, and concurrently (DE applied immediately after exposure to parasites and DE presence maintained throughout the infection) to detect direct effects of DE. DE alone, but not parasitism alone, produced significant host mortality, and concurrent treatment with DE and parasitism did not increase mortality over DE alone. Parasite abundance was significantly higher following sequential, but not concurrent, DE exposure. Parasite abundance in mated hosts was significantly higher than in virgin hosts. Parasitic infection resulted in significantly fewer eggs retained in the oviduct of beetles, but there was no difference in the number of eggs that accumulated in the culture medium and no difference in the surface-seeking behavior of beetles. Mating status of beetles in all treatments, and DE exposure in concurrent treatments significantly increased their surface-seeking behavior. Concurrent exposure to DE also resulted in a 4- to 6-fold increase in host egg numbers that accumulated in the culture medium. Although DE exposure increased parasite numbers in the beetles, these 2 stressors otherwise appeared to act independently.

Morphological features of Cloacotaenia megalops (Nitzsch in Creplin, 1829) (Cestoda, Hymenolepididae) from different hosts.

The tapeworm species Cloacotaenia megalops (Nitzsch in Creplin, 1829) is characterized by a very specific morphology. A particularly distinct feature is a large almost square scolex in which four fleshy suction cups are embedded and a rudimentary rostellum. During standard studies of wild duck cestode fauna in northwestern Poland, some morphological differences were observed among specimens, mainly in the shape of scolices and hermaphroditic proglottids of C. megalops isolated from different bird species. This paper attempts to demonstrate the impact of the host species on morphology of the parasite. The study material consisted of 39 individuals of C. megalops (19 from Aythya fuligula, 10 from Anas platyrhynchos, 4 from Bucephala clangula, 4 from Aythya marila and 2 from A. ferina). The isolated parasites were fixed and stored in 70% ethanol and solid preparations were made. Selected external and internal structures of the parasite were measured and photographed using a Zeiss microscope, a microscope camera Opta Tech 2.1 and Opta View 6.0.2.2. It was stated that the sizes of the most important elements of the parasite morphology are generally consistent with those presented in the available literature, nevertheless some differences were observed in both morphology and sizes of some anatomical structures, especially in the form of scolices and hermaphroditic proglottids between specimens isolated from hosts representing three different eco-tribes (Aythyini, Anatini and Mergini).

Cloacotaenia megalops (Nitzsch in Creplin, 1829) (Cestoda, Hymenolepididae) in wild ducks in Western Pomerania, Poland.

Cloacotaenia megalops (Nitzsch in Creplin, 1892) is a polyxenic and cosmopolitan tapeworm from the family Hymenolepididae. Its generic name derives from their typical location (cloaca), and the typical final hosts which are birds typically associated with water and marsh environments: Anseriformes, Galliformes and Gruiformes. In Poland, the presence of C. megalops has been observed so far in 16 species of ducks from the Baltic coast, the Mazurian Lake District, Wielkopolsko-Kujawska Lowland, Mazovian Lowland, and Podlasie Lowland. In Western Pomerania, quantitative structure analyses were only carried out on Anas platyrhynchos, and therefore the aim of this study was the detailed analysis of environmental populations of C. megalops in wild ducks. The examined tapeworms were isolated from the digestive tract of 1005 wild ducks representing 17 species belonging to three different eco-tribes: Anatini (n=225), Aythyini (n=413) and Mergini (n=367), from northwestern Poland. During the Study 187 C. megalops were found in 89 birds (8.8% of examined ducks) belonging to 7 species: Anas crecca (common teal), A. querquedula (garganey), A. platyrhynchos (mallard) (Anatini); Aythyaferina (pochard), A. fuligula (tufted duck), A. marila (greater scaup) (Aythyini) and Bucephala clangula (goldeneye) (Mergini). The results show the differences in the quantitative structure of C. megalops among the examined species of ducks. The highest prevalence was found in mallard (18.6%) and the lowest in greater scaup (3.2%). The highest mean intensity was observed in greater scaup (4.0), and the lowest in garganey and common teal (1.0). Relative density was at a similar level in the tested birds. Based on the ratio of dominance, it was found that C. megalops is a rare species in the cestodofauna in the examined birds.

[The effect of helminth invasion on lipid metabolism in amphipoda of the White Sea].

Comparative study of lipid metabolism parameters in amphipods (Gammaridae) of the White Sea infested by helminthes Podocotyle atomon (Trematoda), Levinseniella propinqua (Trematoda) and Hymenolepis microsoma (Cestoda) during different seasons was performed. It is shown that increase in the parameters of infestation induced amplification of the defense reaction of host organism, which exhibited itself by the shift in the contents of the basic membranous lipids and by the increased activity of membrane-bound enzymes, such as cytochrome P-450, at the level of the biochemical parameters examined. Since autumn increased content of phosphatidylcholine and ratio phosphatidylcholine/phosphatidylethanolamine in crustacean lipid composition was recorded. The role of phosphatidylcholine in the change of liquid-crystal state of membranes and its role as an effector of peroxidase activity of cytochrome P-450 in the amphipods infested by helminthes are discussed.

[The evolution of forms of hermaphroditism in Cyclophyllidea (Cestoda). 1. Morpho-functional causes of the formation of tapeworms with the protandrous type of genital apparatus development].

Morpho-fuctional causes of the formation of protandrous Cyclophyllidea (tapeworms) have been studied. Two forms of protandry are described. The protandry type I is typical for polymeric (polysegmental) Hymenolepididae. It appears independently in different taxa of this family (Aploparaksis, Echinatrium, Wardium, Diorchis and others) while the narrow-strobila forms with a low prolificacy of proglottids are formed. The development of this living form of hymenolepidids is ecologically caused by the high density of their aggregation in intestines of hosts. The primordium results in the development of genitals in the juvenile strobila proglottids with the limited internal space. Due to this process, parallel morphogenesis of male and female gonads is proved to be impossible. A selection leading to the overtaking development of testicles and copulative apparatus regarding morphogenesis of ovary and vitellarium is based an earlier maturation of testicles and group copulation of proglottids with and underdeveloped ovary that is typical in original euandrogyne forms. The group insemination of proglottids from a polysegmented strobila reduces the number of copulation and improves an efficiency of cross-copulation of tapeworms and. As a result, morpho-functional zones of male proglottids characterized by an immature ovary and those of fertile female segments losing their testicles are differentiated in the strobila. The protandry type II is typical of mesomeric tapeworms (Dilepididae, Schistotaeniidae, Anoplocephalidae). It is also resulted from a limited space of proglottids for developing the hermaphroditic genital apparatus. This is caused by the shift of genital morphogenesis process into juvenile proglottids and also by the enlargement of gonad sizes as the result of a selection for a higher prolificacy of proglottids. The dissociation of the development of male and female gonads takes place because of the retardation of ovary morphogenesis.

[Activity of the anthelmintic agent trichlorophen on the models of human helminthiasis]. / Aktivnost' otechestvennogo antigel'mintika trikhlofena na modeliakh gel'mintozov cheloveka.

Trials of trichlorophen have shown its high efficacy on models of cestode infections: hymenolepiasis (at the adult and cysticercoid stages of development on three types of animals: outbred albino mice, albino rats and golden hamsters), preimaginal echinococciasis alveolaris, larval alveolar echinococciasis (at the early stage of development of the parasite in experiments on cotton rats). The high nematodical activity of trichlorophen was first found on models of trichocephaliasis in DBA/2y mice, nippostrongyloidiasis (in in vitro experiments), and aspiculuriasis in outbred mice. The agent proved to be ineffective at the tissue developmental stage of Hymenolepsis nana (H. nana), the dwarf tapeworm, in albino mice, during experimental opisthorchiasis in golden hamsters. It showed a low efficacy in treating trichinosis in outbred albino mice. Unlike carbamatebenzimidazoles, trichlorophen was inactive at the tissue stage of H. nana; it exerted no effects on the eggs of a dwarf tapeworm in trichinosis. Trichlorophen was also inactive in treating experimental opisthorchiasis in golden hamsters.

Hymenolepis microstoma: direct life cycle in immunodeficient mice.

The mouse bile duct tapeworm Hymenolepis microstoma requires beetles as the obligatory intermediate host. However, when congenitally athymic NMRI-nu mice were infected with the mature tapeworm and allowed to eat their own faeces with tapeworm eggs, the oncospheres penetrated the intestinal tissue and developed to cysticercoids. After excysting, growth to adult worms occurs in the lumen of the small intestine and bile duct. Furthermore, the same happened when NMRI-nu mice, non-obese diabetic severe combined immunodeficiency (NOD/Shi-scid) mice and NOD/Shi-scid, IL-2 Rgamma(null) (NOG) mice were orally inoculated with shell-free eggs of this parasite. Differences between the cysticercoids of H. microstoma and H. nana developed in the mouse intestinal tissues were: (i) the time course for the development of fully matured cysticercoids of H. microstoma in mice was about 11 days but only 4 days for H. nana; and (ii) cysticercoids of H. microstoma developed in mice had a tail while those of H. nana had none.

Infection increases the value of nuptial gifts, and hence male reproductive success, in the Hymenolepis diminuta-Tenebrio molitor association.

During copulation, male insects pass accessory gland components to the female with the spermatophore. These gifts can affect female reproductive behaviour, ovulation and oviposition. Here, we show that female mealworm beetles, Tenebrio molitor, mated with males infected with metacestodes of the rat tapeworm, Hymenolepis diminuta, produced significantly more offspring than those mated with uninfected males. There is a significant positive relationship between parasite intensity in the male and reproductive output in the female. Infection results in a significant increase in bean-shaped accessory gland (BAG) size. We suggest that infected males pass superior nuptial gifts to females and discuss the confounding effects of infection in male and female beetles upon overall fitness costs of infection for the host and the likelihood that the parasite is manipulating host investment in reproduction.

Quantitative trait loci for susceptibility to tapeworm infection in the red flour beetle.

Parasites have profound effects on host ecology and evolution, and the effects of parasites on host ecology are often influenced by the magnitude of host susceptibility to parasites. Many parasites have complex life cycles that require intermediate hosts for their transmission, but little is known about the genetic basis of the intermediate host's susceptibility to these parasites. This study examined the genetic basis of susceptibility to a tapeworm (Hymenolepis diminuta) in the red flour beetle (Tribolium castaneum) that serves as an intermediate host in its transmission. Quantitative trait loci (QTL) mapping experiments were conducted with two independent segregating populations using amplified fragment length polymorphism (AFLP) markers and randomly amplified polymorphic DNA (RAPD) markers. A total of five QTL that significantly affected beetle susceptibility were identified in the two reciprocal crosses. Two common QTL on linkage groups 3 and 6 were identified in both crosses with similar effects on the phenotype, and three QTL were unique to each cross. In one cross, the three main QTL accounted for 29% of the total phenotypic variance and digenic epistasis explained 39% of the variance. In the second cross, the four main QTL explained 62% of the variance and digenic epistasis accounted for only 5% of the variance. The actions of these QTL were either overdominance or underdominance. Our results suggest that the polygenic nature of beetle susceptibility to the parasites and epistasis are important genetic mechanisms for the maintenance of variation within or among beetle strains in susceptibility to tapeworm infection.

Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle, Tribolium castaneum.

Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male-male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14-22% even when male-male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.

Juvenile hormone titre and egg production in Tenebrio molitor infected by Hymenolepis diminuta: effect of male and/or female infection, male age and mating.

Infection of Tenebrio molitor with Hymenolepis diminuta induces curtailment of female fertility. We examined ovulation and oviposition, and associated titres of juvenile hormone (JH), in relation to parasitism and mating. Oviposition was significantly increased in infected mated and virgin beetles by days 6 and 9 post-emergence. Ovulation was not changed by infection; by the end of the 18-day experiment, the total number of laid eggs was not significantly altered. On day 6, JH levels were significantly higher in virgin infected insects, compared to non-infected controls (236+/-37.7 and 107+/-9.62 pg/g wet weight). Oviposition increased after mating, but total eggs ovulated remained the same. JH levels were higher in mated females on days 12 and 18 post-emergence, for infected and control insects. Previous studies suggested that male reproductive potential might rise following infection, because uninfected females lay more eggs when mated to infected males. We tested whether this caused an increase in female JH. Males were mated on days 5 or 12, when significant changes in their reproductive physiology begin to be observed, and are maximal, respectively. However, male age was of greater significance in promoting JH levels in females (p=0.001), than infection status of either partner (p=0.33).

The embryonic development of the bodywall and nervous system of the cestode flatworm Hymenolepis diminuta.

Cestodes (tapeworms) are a derived, parasitic clade of the phylum Platyhelminthes (flatworms). The cestode body wall represents an adaptation to its endoparasitic lifestyle. The epidermis forms a non-ciliated syncytium, and both muscular and nervous system are reduced. Morphological differences between cestodes and free-living flatworms become apparent already during early embryogenesis. Cestodes have a complex life cycle that begins with an infectious larva, called the oncosphere. In regard to cell number, cestode oncospheres are among the simplest multicellular organisms, containing in the order of 50-100 cells. As part of our continuing effort to analyze embryonic development in flatworms, we describe here the staining pattern obtained with acTub in embryos and larvae of the cestode Hymenolepis diminuta and, briefly, the monogenean Neoheterocotyle rhinobatidis. In addition, we labeled the embryonic musculature of Hymenolepis with phalloidin. In Hymenolepis embryos, two different cell types that we interpret as neurons and epidermal gland cells express acTub. There exist only two neurons that develop close to the midline at the anterior pole of the embryo. The axons of these two neurons project posteriorly into the center of the oncosphere, where they innervate the complex of muscles that is attached to the hooklets. In addition to neurons, acTub labels a small and invariant set of epidermal gland cells that develop at superficial positions, anteriorly adjacent to the neurons, in the dorsal midline, and around the posteriorly located hooklets. During late stages of embryogenesis they spread and form a complete covering of the embryo. We discuss these data in the broader context of platyhelminth embryology.

Guanosine 3',5'-cyclic monophosphate: a tapeworm-secreted signal molecule communicating with the rat host's small intestine.

Tapeworms alter the physiological environment of the host's small intestinal lumen by contracting the intestinal smooth muscle, thereby slowing the transit of intestinal contents. We hypothesize that parasite-to-host molecular signaling is responsible for the specific patterns of small intestinal smooth muscle contraction observed both during tapeworm infection and after the infusion of tapeworm-secreted molecules into the intestinal lumen of unanesthetized rats. Of the tapeworm-secreted compounds tested, only lumenal infusion of guanosine 3',5'-cyclic monophosphate (cGMP) induced contractile patterns that mimic those observed during tapeworm infection. The response to cGMP occurred in a concentration-dependent fashion. Our study clearly demonstrates that cGMP can serve as an extracellular signal molecule regulating small intestinal motility mechanisms in vivo.