The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

Species-specific prevalence of mermithid parasites in populations of six congeneric host caddisflies of Ecnomus McLachlan, 1864 (Trichoptera: Ecnomidae)

Mermithid nematodes are entomophagous parasites and, despite being present in diverse aquatic insects, studies of caddisflies acting as definitive hosts are few and the ecological impacts on host populations are largely unknown. During a four-year study in a stream in southeastern Australia, parasitic mermithid worms were commonly found inside adult caddisflies, but only species of the genus Ecnomus McLachlan, 1864 (Ecnomidae). Ecnomus were the definitive host and parasite prevalence ranged from <1% to nearly 50% across six species. Species-specific prevalence varied little between years and was typically higher in males than in females. Parasite intensity ranged from 1 to 6 (median = 1), but did not vary between species or sexes. Infected hosts could fly, but were castrated and died when worms emerged. High prevalence and virulence (reproductive failure and death of the host) suggests that these parasites could potentially play a role in the population dynamics of some Ecnomus spp.     

Systemic infection with Alaria americana (Trematoda).

Alaria americana is a trematode, the adult of which is found in mammalian carnivores. The first case of disseminated human infection by the mesocercarial stage of this worm occurred in a 24-year-old man. The infection possibly was acquired by the eating of inadequately cooked frogs, which are intermediate hosts of the worm. The diagnosis was made during life by lung biopsy and confirmed at autopsy. The mesocercariae were present in the stomach wall, lymph nodes, liver, myocardium, pancreas and surrounding adipose tissue, spleen, kidney, lungs, brain and spinal cord. There was no host reaction to the parasites. Granulomas were present in the stomach wall, lymph nodes and liver, but the worms were not identified in them. Hypersensitivity vasculitis and a bleeding diathesis due to disseminated intravascular coagulation and a circulating anticoagulant caused his death 8 days after the onset of his illness.     

Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites?

Density-dependent effects on parasite fitness have been documented from adult helminths in their definitive hosts. There have, however, been no studies on the cost of sharing an intermediate host with other parasites in terms of reduced adult parasite fecundity. Even if larval parasites suffer a reduction in size, caused by crowding, virtually nothing is known about longer-lasting effects after transmission to the definitive host. This study is the first to use in vitro cultivation with feeding of adult trematodes to investigate how numbers of parasites in the intermediate host affect the size and fecundity of adult parasites. For this purpose, we examined two different infracommunities of parasites in crustacean hosts. Firstly, we used experimental infections of Maritrema novaezealandensis in the amphipod, Paracalliope novizealandiae, to investigate potential density-dependent effects in single-species infections. Secondly, we used the crab, Macrophthalmus hirtipes (Ocypodidae), naturally infected by the trematodes, M. novaezealandensis and Levinseniella sp., the acanthocephalan, Profilicollis spp., and an acuariid nematode. These four helminths all develop and grow in their crustacean host before transmission to their bird definitive host by predation. In experimental infections, we found an intensity-dependent establishment success, with a decrease in the success rate of cercariae developing into infective metacercariae with an increasing dose of cercariae applied to each amphipod. In natural infections, we found that M. novaezealandensis-metacercariae achieved a smaller volume, on average, when infrapopulations of this parasite were large. Small metacercariae produced small in vitro-adult worms, which in turn produced fewer eggs. Crowding effects in the intermediate host thus were expressed at the adult stage in spite of the worms being cultured in a nutrient-rich medium. Furthermore, excystment success and egg-production in M. novaezealandensis in naturally infected crabs were influenced by the number of co-occurring Profilicollis cystacanths, indicating interspecific interactions between the two species. Our results thus indicate that the infracommunity of larval helminths in their intermediate host is interactive and that any density-dependent effect in the intermediate host may have lasting effects on individual parasite fitness.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

Alternative reproductive strategies in the progenetic trematode Coitocaecum parvum: comparison of selfing and mating worms

The progenetic opecoelid trematode Coitocaecum parvum can reproduce either precociously by selfing in its second intermediate amphipod host or by mating in its normal definitive fish host. In this study, we describe and compare the infection parameters and some life history traits of both egg-producing worms and non-egg producing worms in both their second intermediate and definitive hosts. We showed that 58% of worms start to produce eggs while still in the amphipod. The relative abundance of progenetic worms increased with amphipod size, and egg-producing worms achieved greater size in amphipods than in fish. These 2 findings support the reproductive insurance hypothesis. No difference in size was revealed between eggs produced in the amphipods and those produced in the fish. Although more information is needed to thoroughly assess the respective costs and benefits of selfing and mating in this species, our conclusion is that adopting progenesis may have few, if any, long-term negative consequences for the parasite.     

Shedding of gravid proglottids and destrobilation in experimental infections of foxes with Mesocestoides leptothylacus Loos-Frank, 1980 (Cestoda)

The implications of the confused taxonomy of the genus Mesocestoides and the misuse of the name M. lineatus are described. In Southwest Germany rodents are intermediate hosts and red foxes are definitive hosts of M. leptothylacus. The shedding patterns of experimentally infected foxes showed that destrobilation occurs frequently and that there are long periods during which no gravid proglottids are shed at all. Lengths of worms can be taken as a measure of a possible crowding effect only when worms with gravid segments are present, i.e. at the end of the prepatent period (11 to 13 days) or at the beginning of a shedding period.     

Parasites may exit immunocompromised northern pig-tailed macaques(Macaca leonina) infected with SIVmac239

Parasites can increase infection rates and pathogenicity in immunocompromised human immunodeficiency virus(HIV) patients. However, in vitro studies and epidemiological investigations also suggest that parasites might escape immunocompromised hosts during HIV infection.Due to the lack of direct evidence from animal experiments, the effects of parasitic infections on immunocompromised hosts remain unclear. Here,we detected 14 different parasites in six northern pig-tailed macaques(NPMs) before or at the 50 th week of simian immunodeficiency virus(SIV) infection by ELISA. The NPMs all carried parasites before viral injection. At the 50 th week after viral injection, the individuals with negative results in parasitic detection(i.e., 08247 and 08287) were characterized as the Parasites Exit(PE) group, with the other individuals(i.e., 09203, 09211, 10205, and 10225) characterized as the Parasites Remain(PR) group. Compared with the PR group, the NPMs in the PE group showed higher viral loads, lower CD4~+T cells counts, and lower CD4/CD8 rates. Additionally, the PE group had higher immune activation and immune exhaustion of both CD4~+and CD8~+T cells. Pathological observation showed greater injury to the liver, cecum, colon,spleen, and mesenteric lymph nodes in the PE group.This study showed more seriously compromised immunity in the PE group, strongly indicating that parasites might exit an immunocompromised host.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

Exploitation of asymmetric predator–prey interactions by trophically transmitted parasites

The directionality of asymmetric interactions between predators (definitive hosts) and prey (intermediate hosts) should impact trophic transmission in parasites. This study tests the prediction that trophically transmitted parasites are funneled towards asymmetric predator–prey interactions where intermediate hosts have few predators and definitive hosts feed upon many prey (‘downward asymmetry’). The distribution of trophically transmitted parasites was examined in four published food webs in relation to mismatch asymmetry of predator–prey interactions. We found that trophically transmitted parasites exploit downwardly asymmetric interactions in a nonrandom manner, and particular predator–prey pairs contain more trophically transmitted parasites than would be expected by random chance alone. These findings suggest that food web topology has great bearing on the ecology of trophically transmitted parasites, and that consideration of parasite life cycles in the context of food web organization can provide insights into the forces affecting the evolution of trophic transmission.     

Hybridisation between the digeneans Schistosoma haematobium and S. mattheei : viability of hybrids and their development in sheep

The F1 and F2 hybrids of Schistosoma haematobium male × S. mattheei female were studied with regard to infectivity to intermediate and definitive hosts, isoenzymes (phosphoglucomutase) of individual male worms, randomly amplified polymorphic DNAs of individual adult worms and scanning electron micrographs of the tubercles of male worms. The infection rate of the F1 hybrid miracidia in Bulinus globosus (41.7%) was greater than that achieved in B. wrighti (16.3%); the infection rate of the F2 in B. wrighti was 15.4%. In the definitive hosts: in sheep only male F1 hybrids (i.e. no females and no F2 worms)were recovered; but in hamsters both paired F1 worms and unpaired F1 males were recovered, as were one pair of worms and unpaired males of the F2 generation. The S. mattheei and S. haematobium male worms showed very distinctive PGM patterns, and the F1 hybrids showed additive patterns and a polymorphism with two distinct types of band patterns which are the result of polymorphism in the S. haematobium. The RAPD profiles of the F1 hybrids were also composite of the two parental species. Scanning electron micrographs of the tubercles of male S. haematobium showed them to be heavily spined, whereas those of S. mattheei males were devoid of spines. The F1 hybrids did show variation ranging from non-spined, some with partial spination, to those with heavily spined tubercles. Male worms of the F2 generation possessed tubercles either with or without spines. The potential significance of hybridisation in areas of sympatry between S. haematobium and S. mattheei is discussed.     

Linking predator–prey interactions with exposure to a trophically transmitted parasite using PCR‐based analyses

Parasite transmission is determined by the rate of contact between a susceptible host and an infective stage and susceptibility to infection given an exposure event. Attempts to measure levels of variation in exposure in natural populations can be especially challenging. The level of exposure to a major class of parasites, trophically transmitted parasites, can be estimated by investigating the host's feeding behaviour. Since the parasites rely on the ingestion of infective intermediate hosts for transmission, the potential for exposure to infection is inherently linked to the definitive host's feeding ecology. Here, we combined epidemiological data and molecular analyses (polymerase chain reaction) of the diet of the definitive host, the white‐footed mouse (Peromyscus leucopus), to investigate temporal and individual heterogeneities in exposure to infection. Our results show that the consumption of cricket intermediate hosts accounted for much of the variation in infection; mice that had consumed crickets were four times more likely to become infected than animals that tested negative for cricket DNA. In particular, pregnant female hosts were three times more likely to consume crickets, which corresponded to a threefold increase in infection compared with nonpregnant females. Interestingly, males in breeding condition had a higher rate of infection even though breeding males were just as likely to test positive for cricket consumption as nonbreeding males. These results suggest that while heterogeneity in host diet served as a strong predictor of exposure risk, differential susceptibility to infection may also play a key role, particularly among male hosts. By combining PCR analyses with epidemiological data, we revealed temporal variation in exposure through prey consumption and identified potentially important individual heterogeneities in parasite transmission.     

Physiological specificity of the interaction between Traenophorus nodulosus (Cestoda) and its host--fishes

The influence of the T. nodulosus plerocercoid invasion on the liver of the intermediate fish hosts (perch) was studied. The water, protein, glycogen and glucose contents was examined in adult worms inhabiting the intestine of definitive hosts (pike), the rate of glucose accumulation along the strobile of parasite and an ability of adult worms to hydrolyze the main nutrients was also investigated. As a result of the plerocercoid infection, the glucose and glycogen contents in the liver of perch juveniles decreased, while the wet weight of liver increased. It was found, that the water and protein contents from the anterior to posterior section of strobile in T. nodulosus adults was not significantly different, while the glucose contents and the rate of its accumulation decreased. The data confirming the possibility to realize the final stages of protein and carbohydrate hydrolisis with the participation of membrane digestion on the surface of helminths and proving the ability of cestodes. The problems of relations of T. nodulosus with intermediate and definitive hosts at the level of the whole organisms are discussed.     

Maternal transmission by Alaria marcianae (Trematoda) and the concept of amphiparatenesis

The term amphiparatenic host was coined originally for hosts of Alaria marcianae that as adults are paratenic hosts, but as juveniles serve as definitive hosts. In this study the concept of amphiparatenesis is placed in a theoretical context, maternal transmission shown to be the basic mechanism, and the concept extended to include Toxocara canis, T. cati, T. pteropodis, Neoascaris vitulorum, Ancylostoma caninum, Uncinaria lucasi, various species of Strongyloides, Pharyngostomoides procyonis, and P. adenocephala. Alaria marcianae mesocercariae were used in a feline model to show that male and nonlactating female cats are definitive hosts, but lactating cats are primarily paratenic hosts. Inoculation of 1 female cat resulted in the infection of 21 of her offspring via the milk over the course of 5 litters and after a 3-yr period she still had viable larvae in her tissues. The ability of parasites to remain immature in amphiparatenic hosts is believed to be an adaptation on the part of the parasite to promote dissemination through maternal transmission and not the result of resistance, immunological or otherwise, on the part of the host. The amphiparatenic concept has important implications that include: the use of pregnant and lactating females as reservoirs of infection for the offspring; infection transmitted through a contagious transplacental or transmammary pathway; a parasite population structure in which adult worms are in greater abundance in neonate than adult hosts; and the effective control of parasites utilizing this strategy proving to be very difficult.     

Can helminth community patterns be amplified when transferred by predation from intermediate to definitive hosts?

Helminth communities in definitive hosts are formed by the acquisition of packets of larvae arriving each time an intermediate host is consumed. It is thus possible that associations between parasite species or other aspects of community structure get transferred from intermediate to definitive hosts. Earlier computer simulations showed that associations between 2 parasite species, in particular positive associations, could be transferred up the food chain. Here, we alter some of the assumptions of previous models and generate new simulations of several ways in which source infracommunities in intermediate hosts can be transferred to target infracommunities in definitive hosts. In particular, we introduced nonrandom selection of intermediate hosts by predatory definitive hosts, to mimic the phenomenon of host manipulation by parasites; this consisted in biasing predation toward intermediate hosts harboring a certain parasite species. Overall, our results show that positive covariances between 2 parasite species can not only be transferred but can also be amplified during transmission to definitive hosts; significant covariance between parasite species can even appear in the definitive hosts when none existed in the intermediate hosts. Negative covariance was not as readily transferred to definitive hosts and amplified, in part because of properties of the presence-absence covariance index. Amplification of covariance results from intermediate host manipulation as well as from other processes taking place during transmission. These results suggest that the patterns of association between helminth species in definitive hosts cannot be taken to reflect the processes acting inside those hosts: they may simply be inherited, with amplification, from intermediate hosts.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Patterns of intermediate host use and levels of association between two conflicting manipulative parasites.

For many parasites with complex life cycles, manipulation of intermediate host phenotypes is often regarded as an adaptation to increase the probability of successful transmission. This phenomenon creates opportunities for either synergistic or conflicting interests between different parasite species sharing the same intermediate host. When more than one manipulative parasite infect the same intermediate host, but differ in their definitive host, selection should favour the establishment of a negative association between these manipulators. Both Polymorphus minutus and Pomphorhynchus laevis exploit the amphipod Gammarus pulex as intermediate host but differ markedly in their final host, a fish for P. laevis and a bird for P. minutus. The pattern of host use by these two conflicting manipulative parasites was studied. Their incidence and intensity of infection and their distribution among G. pulex were first examined by analysing three large samples of gammarids collected from the river Tille, Eastern France. Both parasites had low prevalence in the host population. However, temporal fluctuation in the level of parasitic infection was observed. Overall, prevalence of both parasite species was higher in male than in female G. pulex. We then assessed the degree of association between the two parasites among their intermediate hosts, using two different methods: a host-centred measure and a parasite-centred measure. Both measures gave similar results; showing random association between the two acanthocephalan species in their intermediate hosts. We discuss our results in relation to the selective forces and ecological constraints that may determine the pattern of association between conflicting manipulative parasites.     

Development of Trichosomoides nasalis (Nematoda: Trichinelloidea) in the murid host: evidence for larval growth in striated muscle fibres

Trichosomoides nasalis (Trichinelloidea) is a parasite of Arvicanthis niloticus (Muridae) in Senegal. Female worms that harbour dwarf males in their uteri, occur in the epithelium of the nasal mucosa. Young laboratory-bred A. niloticus were either fed females containing larvated eggs or intraperitoneally injected with motile first-stage larvae recovered from female uteri. Both resulted in successful infection. Organs examined during rodent necropsy were blood and lymphatic circulatory systems (heart, large vessels, lymphnodes), lungs, liver, kidneys, thoracic and abdominal cavities, thoracic and abdominal muscular walls, diaphragm, tongue, and nasal mucosa. Development to adult nasal stages took three weeks. Recovery of newly hatched larvae from the peritoneal fluid at four-eight hours after oral infection suggests a direct passage from the stomach or intestinal wall to the musculature. However, dissemination through the blood, as observed with Trichinella spiralis, cannot be excluded even though newly hatched larvae of T. nasalis are twice as thick (15 μm). Developing larvae were found in histological sections of the striated muscle of the abdominal and thoracic walls, and larvae in fourth moult were dissected from these sites. Adult females were found in the deep nasal mucosa where mating occurred prior to worms settling in the nasal epithelium. The present study shows a remarkable similarity between T. nasalis and Trichinella species regarding muscle tropism, but the development of T. nasalis is not arrested at the late first-larval stage and does not induce transformation of infected fibres into nurse cells. T. nasalis seems a potential model to study molecular relations between trichinelloid larvae and infected muscle fibres.