Relative distribution of glutathione transferase, glyoxalase I and glyoxalase II in helminths

Glutathione transferase, glyoxalase I and glyoxalase II activities were not evenly distributed among the major helminth groups. Intestinal cestodes and digeneans had higher glutathione transferase activity than parasitic nematodes. High glyoxalase II activity was found in cestodes and digeneans but no glyoxalase I was detectable. Glyoxalase I and II were both detected in nematodes. These results are discussed in relation to the enzymes' suggested role in protection against secondary lipid peroxidation products.     

Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea.

An important component of the parasite fauna of seabirds in arctic regions are the flukes (Digena). Different species of digeneans have life cycles which may consist of 1 intermediate host and no free-living larval stages, 2 intermediate hosts and 1 free-living stage, or 2 intermediate hosts and 2 free-living larval stages. This study examined the distribution of such parasites in the intertidal zones of the southern coast of the Barents Sea (northwestern Russia and northern Norway) by investigating 2 species of periwinkles (Littorina saxatilis and L. obtusata) which are intermediate hosts of many species of digeneans. A total of 26,020 snails from 134 sampling stations were collected. The study area was divided into 5 regions, and the number of species, frequency of occurrence and prevalence of different digenean species and groups of species (depending on life cycle complexity) were compared among these regions, statistically controlling for environmental exposure. We found 14 species of digeneans, of which 13 have marine birds as final hosts. The number of species per sampling station increased westwards, and was higher on the Norwegian coast than on the Russian coast. The frequency of occurrence of digeneans with more than 1 intermediate host increased westwards, making up a larger proportion of the digeneans among infected snails. This was significant in L. saxatilis. The prevalence of different species showed the same pattern, and significantly more snails of both species were infected with digeneans with complicated life cycles in the western regions. In L. saxatilis, environmental exposure had a statistically significant effect on the distribution of the most common digenean species. This was less obvious in L. obtusata. The causes of changing species composition between regions are probably (1) the harsh climate in the eastern part of the study area reducing the probability of successful transmission of digeneans with complicated life cycles, and (2) the distribution of different final hosts.     

Helminth parasites of British rodents and insectivores

Field and laboratory studies on the helminths of rodents have mainly involved direct life-cycle nematodes (of the super families Rhabditoidea, Oxyuroidea, Trichuroidea and Trichostrongyloidea) and, to a lesser extent, indirect life-cycle cyclophyllidean cestodes (of the families Catenotaeniidae and Hymenolepididae). In insectivores on the other hand, because of their different feeding habits, the composition of the helminth fauna largely comprises hymenolepid and dilepidid cestodes together with brachylaemid and dicrocoeliid digeneans, the life cycles of which are little known. The value of further studies on the biogeography of helminths of rodents and insectivores in the British Isles is emphasized. The role of rodent nematodes as laboratory models for chemotherapy is also discussed.     

Variation and evolution of the complex life cycle in Adelgidae (Hemiptera)

The family Adelgidae is a small group of insects within Aphidoidea (Hemiptera). Adelgids are typically holocyclic with host‐alternation between the primary and secondary hosts, but some anholocyclic species persist either on the primary or secondary host. Like Aphididae, complexities and variation of adelgid life cycles are good models for understanding the evolution of complex life cycles. In this review, we outline the complex life cycles of adelgids, and current status and recent advances in adelgid life cycle studies. We also discuss the evolution of adelgid life cycles by comparing them to closely related aphid life cycles. A switch from holocycly to anholocycly on the primary host needs evolutionary innovations in gallicola behavior and reproduction. This radical evolution can be explained by mutations in a regulatory system that controls the sequence of gene sets producing phenotypes of one morph. In contrast, anholocycly on the secondary host consists of a series of exulis generations already existing in the holocycle. Thus, it may evolve by loss of primary‐host generations through extinction of the primary host, expansion beyond the geographical range of the primary host, or loss of male‐producing sexuparae that return to the primary host. Although the holocycle and its anholocyclic derivatives have been regarded as different species, morphological, ecological and genetic differences are too subtle to separate them into different species. The holocycle and its anholocyclic derivatives should not be split into different species without clearly identifiable morphological differences.     

Hatching strategies in monogenean (platyhelminth) parasites that facilitate host infection

In parasites, environmental cues may influence hatching of eggs and enhance the success of infections. The two major endoparasitic groups of parasitic platyhelminths, cestodes (tapeworms) and digeneans (flukes), typically have high fecundity, infect more than one host species, and transmit trophically. Monogeneans are parasitic flatworms that are among the most host specific of all parasites. Most are ectoparasites with relatively low fecundity and direct life cycles tied to water. They infect a single host species, usually a fish, although some are endoparasites of amphibians and aquatic chelonian reptiles. Monogenean eggs have strong shells and mostly release ciliated larvae, which, against all odds, must find, identify, and infect a suitable specific host. Some monogeneans increase their chances of finding a host by greatly extending the hatching period (possible bet-hedging). Others respond to cues for hatching such as shadows, chemicals, mechanical disturbance, and osmotic changes, most of which may be generated by the host. Hatching may be rhythmical, larvae emerging at times when the host is more vulnerable to invasion, and this may be combined with responses to other environmental cues. Different monogenean species that infect the same host species may adopt different strategies of hatching, indicating that tactics may be more complex than first thought. Control of egg assembly and egg-laying, possibly by host hormones, has permitted colonization of frogs and toads by polystomatid monogeneans. Some monogeneans further improve the chances of infection by attaching eggs to the host or by retaining eggs on, or in, the body of the parasite. The latter adaptation has led ultimately to viviparity in gyrodactylid monogeneans.     

On the Procercoid Protonephridial Systems of Three Diphyllobothrium Species (Cestoda, Pseudophyllidea) and Janicki's Cercomer Theory

Because the types of hooks are so similar in the oncosphacra/procercoid ef cestodes and in several groups of monogenclic trcmatodes and because the exterior of a procercoid with the hooks in a cercomer is so suggestive of a monogenetic nematode, the development of the procercoids of three Diphyllobothrium species was studied. The intention was to determine whether or not the procercoid protonephridial system would have a developmental stage when its type is similar to, or identical with that type which characterizes the monogeneans. Such a conformity would greatly support the theory of a common origin of monogeneans and ceslodes. However, it has emerged that no similar developmental stage exists. The ontogeny revealed a thorough metamorphosis from a very simple primary protonephridial system (identical with that of the miracidium larva in digeneans) to a secondary system, which develops into the system of the adult tapeworm. This fact may be interpreted as an argument against the supposed inter-relalionships between monogeneans and cestodes. However, the type of hooks and the procercoid cercomer still indicate common ancestors. An analysis of the miracidium, the oncosphaera and the oncomiracidium (the monogenean larva) with reference to their different developmental stages when hatching, gave rise to my interpretation of the fundamental structure of both the miracidium and the oncosphaera as primitively simple and not reduced, Especially the identical type of protonephridial system indicates. in my view, that digeneans and ceslodes originally had a common larva type. If the ceslodes and the monogeneans have common ancestors, then the procercoid may be interpreted as the ontogenetic recapitulation of a common hook-armed ancestor, here named hexucanthoid. This rhabdocoelan creature with six hooks in the cercomer and adapted to an ectocommensalic/ectoparasitic mode of life, is thought to have given rise to the monogeneans, the gyrocotylideans, the amphilinideans and the cestodes. The monogeneans were found to have two fundamentally different types of marginal hooks, and on this basis ihe existence of two different lines of evolution in Monogenea is indicated.     

A study of the internal parasites of small rodents from woodland areas in Surrey

The occurrence of helminth parasites and leptospires from the Long-tailed field mouse, Apodemus sylvaticus , the Bank vole, Clethrionomys giareolus and the Short-tailed vole, Microtus agrestis has been studied from four woodland areas in Surrey. The composition of the helminth fauna of these rodents, particularly A. sylvaticus and C. giareolus , differs from that of previous studies carried out in the British Isles in consisting largely of cestodes and fewer species of digeneans and nematodes. On the other hand the degree of infection of the rodents with nematodes as in the case of A. sylvaticus infected with the trichostrongylid Nematospiroides dubius and theoxyurid Syphacia stroma and of C. giareolus with thecap-illarid Capillaria muris sylvatici is greater than the cestode and digenean infections and is probably linked with the monoxenous nature of the nematode life cycles.
Differences in the number, incidence and degree of infection of mice and voles with species of helminths is undoubtedly linked with differences in the feeding habits of the respective hosts but the present study has also confirmed that infection levels in both leptospires and helminths are influenced by the age/sex relationships of the host together with season and habitat. The relationship between the distribution of rodents infected with leptospires and some helminths suggests similarities in the mode of their transmission.     

Cestode lysosomes

By differential centrifugation method a lysosomal fraction was obtained from five species of cestodes, which possesses the highest specific activity of acidic phosphatases as compared to other subcellular fractions. By isopyknic centrifugation in the density gradient of saccharose the lysosomal fraction is divided into primary and secondary lysosomes. Lysosomes of cestodes are similar to those of vertebrate animals in the character of fractional distribution of acidic phosphatase, sedimentation abilities and sensitivity of membranes to triton X-100.     

Reef Fishes Have Higher Parasite Richness at Unfished Palmyra Atoll Compared to Fished Kiritimati Island

We compared parasite communities at two coral atolls in the Line Islands chain of the central Pacific (Kiritimati Island and Palmyra Atoll). Palmyra Atoll is relatively pristine while Kiritimati Island is heavily fished. At each island, we sampled five fish species for helminth and arthropod endoparasites: Chromis margaritifer, Plectroglyphidodon dickii, Paracirrhites arcatus, Acanthurus nigricans, and Lutjanus bohar. The surveys found monogeneans, digeneans, cestodes, nematodes, acanthocephalans, and copepods. Parasite richness was higher at Palmyra compared to Kiritimati for all five fish species. Fishes from Palmyra also tended to have more parasites species per host, higher parasite prevalence, and higher parasite abundance than did fishes from Kiritimati. The lower parasitism at Kiritimati may result from a simplified food web due to over fishing. Low biodiversity could impair parasite transmission by reducing the availability of hosts required by parasites with complex life cycles. Most notably, the lower abundances of larval shark tapeworms at Kiritimati presumably reflect the fact that fishing has greatly depleted sharks there in comparison to Palmyra.     

The terminology of larval cestodes or metacestodes

The terminology associated with the nomenclature of larval or metacestodes is reviewed as well as the various morphological and developmental characters used to define different types of larval cestodes. Based on a review of the literature, the key characters differentiating the types of larval cestodes are the presence of a primary lacuna and the invagination/retraction of the scolex. The presence of a cercomer and of a bladder-like enlargement of the larval cestode were considered to be useful secondary characteristics. Using these characters, six basic types of larval cestodes were identified: the procercoid, an alacunate form which cannot develop further until ingested by a second intermediate host; the plerocercus, an alacunate form with a retracted scolex; the plerocercoid, an alacunate form with an everted scolex; the merocercoid, an alacunate form with an invaginated scolex; the cysticercoid, a lacunate form with a retracted scolex; and the cysticercus, a lacunate form with an invaginated scolex. The diversity of larval types within the broad classifications of cysticercoid and cysticercus can be differentiated by the use of appropriate prefixes. Deficiencies in knowledge of specific types of larval cestodes are identified and further avenues of research are indicated.Pseudonym for the contributors of a workshop on metacestode terminology, chaired by I. Beveridge, which took place during the Third International Workshop for Tapeworm Systematics,Sofia, Bulgaria, 20-24 July, 1999 (Organiser: B.B. Georgiev).     

Diversity and biogeographical relationships of the Australian cestode fauna

The Australian cestode fauna remains poorly documented with a total of 342 species recorded to date. The best-studied host groups are the elasmobranchs and the marsupials, but even in these groups, only 32 and 25% of known host species, respectively, have been examined for parasites. Overall, cestodes have been reported from only 5% of the known vertebrate species. Representatives of virtually all cestode orders and most of the cyclophyllidean families have been recorded from Australia. In spite of these deficiencies, some biogeographical patterns are discernible. In the elasmobranchs, a significant proportion of the known cestodes is endemic while other associations exist with eastern Pacific and Indo-west Pacific faunas. Also identifiable is a group of cosmopolitan species. The nematotaeniids of amphibians suggest Gondwanan affiliations, while the known proteocephalideans, parasitic in reptiles and amphibians, may represent an Asian invasion. Associations of the avian cestodes represent an unexplored but potentially rewarding avenue of biogeographical study. The cestodes of mammals include families with a Gondwanan distribution (Linstowiidae, Hymenolepididae) as well as those (Anoplocephalidae) with an apparent origin in southeast Asia. In addition, a number of genera of cyclophyllidean cestodes (Anoplotaenia, Dasyurotaenia) occurring in marsupials represent biogeographical challenges, not being accommodated within any of the known cestode families. The Australian cestode fauna therefore provides potentially outstanding opportunities for studies of the biogeographical relationships of a number of cestode groups.     

Cestode transmission patterns

The paradox of high prevalence but low probability of having an egg develop to an adult has been resolved by the evolution of 3 major and basic strategies involving transmission: evolution of life cycles interpolated into host biology; presentation of infective stages that increase probability of contact between host and parasite; and increase in reproductive potential. The rarity of direct cycles confirms that cycles in themselves, with at least 2 hosts, are a key element of cestode success because they provide a vehicle for dispersal and transmission of infective stages. Transmission is primarily by passive stages that become incorporated through intermediate hosts or accidentally in the food chain. High host specificity results from efficient transmission pathways but may represent a fragile system for the evolution of the species. Probability of transmission is increased through diversity of intermediate hosts, making eggs more susceptible to ingestion and by behavioral manipulation of hosts by parasite stages. Spatial and temporal aspects of transmission may be increased through paratenesis. Asexual proliferation of immature stages is uncommon and is favored where there is selective predation; such proliferation may be part of a transmission strategy of colonial cestodes that require high infrapopulations in order to survive. Hyperapolysis may be part of a transmission strategy used by the Tetraphyllidea, Trypanorhyncha, and Lecanicephalidea to increase proglottid production. The dynamics of transmission for cestodes of humans and domestic animals require a different perspective than those of wild hosts. All strategies are reviewed within the framework of certain cestode morphological and ecological constraints. A total of 11 figures and 48 references complements the text.     

Microsporidian life cycles and diversity: the relationship between virulence and transmission

The microsporidia are obligate intracellular parasites which have diverse life cycles involving both horizontal and vertical transmission and parasitise a wide range of vertebrate and invertebrate hosts. In this paper we consider the life cycles and diversity of the microsporidia. We focus in particular on the relationship between parasite transmission and virulence and its implications for host-parasite coevolution. The use of horizontal and vertical routes of transmission varies between species and there is a strong link between transmission and virulence. Horizontal transmission is characterised by a high parasite burden and associated pathogenicity. In contrast, vertical transmission is characterised by low virulence, which has led to under-reporting of this important transmission route. Vertically transmitted microsporidia may also cause male killing or feminisation of their host, with implications for host population sex ratio and stability. Phylogenetic analysis shows that vertical transmission occurs in diverse branches of the Microspora. We find that there is evidence for vertical transmission in both vertebrate and invertebrate hosts and conclude that it is a common or possibly even ubiquitous transmission route within this phylum.     

Interaction of the uterus and developing eggs in cyclophyllidean cestodes with different fecundity

The interaction of morphological changes of the uterus and fecundity of the strobilae of cestodes has been investigated. It is shown that cestodes with maximal fecundity have different and highly effective ways of supplying eggs with nutrients. It is noted that differences in fecundity of cestodes depend not only on their strategy of reproduction, ecology, and complexity of life cycles but also on the complexity of interactions between the uterus and the developing eggs.     

Optimal growth strategies of larval helminths in their intermediate hosts

We consider optimal growth of larval stages in complex parasite life cycles where there is no constraint because of host immune responses. Our model predicts an individual's asymptotic size in its intermediate host, with and without competition from conspecific larvae. We match observed variations in larval growth patterns in pseudophyllid cestodes with theoretical predictions of our model. If survival of the host is vital for transmission, larvae should reduce asymptotic size as intensity increases, to avoid killing the host. The life history strategy (LHS) model predicts a size reduction <1/intensity, thus increasing the parasite burden on the host. We discuss whether body size of competing parasites is an evolved LHS or simply reflects resource constraints (RC) on growth fixed by the host, leading to a constant total burden with intensity. Growth under competition appears comparable with "the tragedy of the commons", much analysed in social sciences. Our LHS prediction suggests that evolution generates a solution that seems cooperative but is actually selfish.     

Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics

The Adelgidae form a small group of insects in the Aphidoidea. They are cyclically parthenogenetic with host alternating, multiple-generation complex life cycles and are restricted to certain host genera in the Pinaceae. Species that host alternate always have Picea as the primary host where sexual reproduction and gall formation occur, and another genus in the Pinaceae as the secondary host where a series of parthenogenetic generations are produced. Other species that do not host alternate complete their entire life cycle on one host and only reproduce parthenogenetically. We studied relationships within Adelgidae using DNA sequences from the mitochondrial COI, COII, and cytb genes, and the nuclear EF1alpha gene. Analysis of the combined data resulted in a well-resolved phylogeny in which the major adelgid clades correspond neatly to their association with secondary host genera. Specialization on each secondary host genus occurred only once and was followed by diversification on the host genus. Molecular dating of divergence times in the Adelgidae suggest that diversification among host genera occurred in the Late Cretaceous and Early Tertiary when the Pinaceae genera were diverging. It is not clear, however, whether the Adelgidae and Pinaceae co-diversified because the relationships among the Pinaceae genera are not fully resolved. We discuss implications for adelgid taxonomy, life cycle evolution, and evolution of the interaction between adelgids and their host plants.     

Exploitation of the same trophic link favors convergence of larval life-history strategies in complex life cycle helminths

Switching from one host to the next is a critical life-history transition in parasites with complex life cycles. Growth and mortality rates are thought to influence the optimal time and size at transmission, but these rates are difficult to measure in parasites. The parasite life cycle, in particular the trophic link along which transmission occurs, may be a reasonable proxy for these rates, leading to the hypothesis that life cycle should shape life-history strategy. We compiled data on the size and age at infectivity for trophically transmitted helminths (i.e., acanthocephalans, cestodes, and nematodes), and then categorized species into trophic links (e.g., planktonic crustaceans to fish, insects to terrestrial vertebrates, etc.). Comparative analyses that explicitly included stabilizing selection within trophic links fit the data significantly better than random walk models, indicating that parasites with different life cycles have different optimal times/sizes for host switching. The major helminth groups have often independently evolved similar life cycles, and we show that this has frequently led to convergent and/or parallel evolution of size and age at infectivity. This suggests that for particular life cycles there are universal optimal transmission strategies, applicable to widely divergent taxa, although the cases of parallelism might indicate that lineage-specific constraints sometimes prevent evolution to a single adaptive peak.     

The nature and evolution of the association among digeneans, molluscs and fishes

Patterns of association of digenean families and their mollusc and vertebrate hosts are assessed by way of a new database containing information on over 1000 species of digeneans for life-cycles and over 5000 species from fishes. Analysis of the distribution of digenean families in molluscs suggests that the group was associated primitively with gastropods and that infection of polychaetes, bivalves and scaphopods are all the results of host-switching. For the vertebrates, infections of agnathans and chondrichthyans are apparently the result of host-switching from teleosts. For digenean families the ratio of orders of fishes infected to superfamilies of molluscs infected ranges from 0.5 (Mesometridae) to 16 (Bivesiculidae) and has a mean of 5.6. Individual patterns of host association of 13 digenean families and superfamilies are reviewed. Two, Bucephalidae and Sanguinicolidae, are exceptional in infecting a range of first intermediate hosts qualitatively as broad as their range of definitive hosts. No well-studied taxon shows narrower association with vertebrate than with mollusc clades. The range of definitive hosts of digeneans is characteristically defined by eco-physiological similarity rather than phylogenetic relationship. The range of associations of digenean families with mollusc taxa is generally much narrower. These data are considered in the light of ideas about the significance of different forms of host association. If Manter's Second Rule (the longer the association with a host group, the more pronounced the specificity exhibited by the parasite group) is invoked, then the data may suggest that the Digenea first parasitised molluscs before adopting vertebrate hosts. This interpretation is consistent with most previous ideas about the evolution of the Digenea but contrary to current interpretations based on the monophyly of the Neodermata. The basis of Manter's Second Rule is, however, considered too flimsy for this interpretation to be robust. Problems of the inference of the evolution of patterns of parasitism in the Neodermata are discussed and considered so intractable that the truth may be presently unknowable.     

Progenesis and facultative life cycle abbreviation in trematode parasites: Are there more constraints than costs?

Complex life cycles provide advantages to parasites (longer life span, higher fecundity, etc.), but also represent a series of unlikely events for which many adaptations have evolved (asexual multiplication, host finding mechanisms, etc.). Some parasites use a radical strategy where the definitive host is dropped; life cycle abbreviation is most often achieved through progenesis (i.e. early maturation) and reproduction in the second intermediate host. In many progenetic species, both the typical and abbreviated life cycles are maintained. However, conditions that trigger the adoption of one or the other strategy, and the pros and cons of each parasite life history strategy, are often complex and poorly understood. We used experimental infections with the trematode Coitocaecum parvum in its fish definitive host to test for potential costs of progenesis in terms of lifespan and fecundity. We show that individuals that adopt progenesis in the intermediate host are still able to establish in the definitive host and achieve higher survival and fecundity than conspecifics adopting the typical three-host life cycle. Our results and that of previous studies show that there seems to be few short-term costs associated with progenesis in C. parvum. Potential costs of self-fertilization and inbreeding are often suggested to select for the maintenance of both life-history strategies in species capable of facultative progenesis. We suggest that, at least for our focal species, there are more constraints than costs limiting its adoption. Progenesis and the abbreviated cycle may become the typical life-history strategy while reproduction in the vertebrate definitive host is now a secondary alternative when progenesis is impossible (e.g. limited host resources, etc.). Whether this pattern can be generalized to other progenetic trematodes is unknown and would require further studies.