Ecological parasitology of polymorphic Arctic charr, Salvelinus alpinus (L.), in Thingvallavatn, Iceland

The helminth endoparasite fauna in four Arctic charr morphs, Salvelinus alpinus (L.), small benthivorous (SB), large benthivorous (LB), planktivorous (PL) and piscivorous (PI) charr, from Thingvallavatn, Iceland consisted of: Crepidostomum farionis (Trematoda: Allocreadiidae); Diplosttomum sp. (Trematoda: Diplostomatidae); Eubothrium salvelini; Diphyllobothrium dendriticum; D. ditremum (Cestoda: Pseudophyllidae); Proteocephalus longicollis (Cestoda: Proteocepha-lidae): and Philonema oncorhynchi (Nematoda: Filariidae). The morphs exhibited distinctive patterns in prevalences and parasite burdens (mean intensity and mean relative density of parasites). SB charr had high prevalence and parasite burden of the eye fluke Diplostomum sp. and none to very light infections of the other parasite species. LB charr had relatively high prevalence and parasite burden of the intestinal fluke C. farionis , whereas infections of the remaining parasite species were light to moderate. PL and PI charr had high prevalences and worm burdens of Diphyllobothrium spp. and P. longicollis . PL charr differed from PI charr in higher worm burden off P. longicollis and lighter burden of £. salvelini . Prevalences of P. oncorhynchi were high in PL and PI charr. Association of parasite intensities and age and length offish were investigated. The different infection patterns among the morphs agree well with their partitioning in food and habitat utilization, and confirm that there is a high degree of ecological segregation between the morphs. The results demonstrate the importance of ecological factors influencing transmission efficiency of parasites to the fish host.     

Proteolytic Activity of Microflora Associated with the Digestive-Transport Surfaces of Intestine of the Burbot Lota lota and of Eubothrium rugosum Parasitized in It

The presence of symbiotic microflora associated with the digestive-transport surfaces of the burbot intestine and of Eubothrium rugosum (Cestoda, Pseudophyllidea) parasitizing in it has been shown. The bacteria absorb amino acids from the cultivation medium or release proteolytic enzymes into the medium, depending on its composition. The studied microorganisms act either as competitors of the parasite and host for nutritive substrates or as suppliers of proteolytic enzymes that can be subsequently used by the parasite and host in the digestive processes. The amino acid absorption and release of proteolytic enzymes by the bacteria do not depend on the medium pH. The microorganisms that are more closely associated with the studied surfaces seem to make a greater contribution to digestive processes both of the parasite and of the host, as bacteria present in the intestinal contents are removed faster from the digestive tract.     

Parasite Infections in Danish Trout Farms

Samples from 5 Danish freshwater trout farms rearing rainbow trout (Oncorhynchus my kiss) were examined for parasite infections from October 1993 until November 1994 and recorded parasites are listed. In addition, results from an examination of a mariculture net cage system are presented as well. A total of 10 metazoan and 10 protozoan parasites were recorded. The metazoans included Gyrodactylus derjavini, Gyrodactylus salaris, Eubothrium crassum, Triaenophorus nodulosus, Proteocephalus sp., Diplostomum spathaceum, Tylodelphus clavata and Argulus foliaceus from the freshwater farms. The protozoans Hexamita salmonis, Ichthyobodo necator, Ichthyophthirius multifiliis, Apiosoma sp., Epistylis sp., Trichodina nigra, T. mutabilis, T. fultoni, Trichodinella epizootica, and an Ichthyophonus like intestinal parasite were also detected in the freshwater trout farms. Based on lectin binding studies, few fish were found positive for the myxosporean parasite PKX although no clinical cases were reported. In the mariculture system, Lepeophtheirus salmonis and Caligus elongatus were found.     

The association between parasite infection and growth rates in Arctic charr: do fast growing fish have more parasites?

Trophically transmitted parasites are known to impair fish growth in experimental studies, but this is not well documented in natural populations. For Arctic charr [Salvelinus alpinus (L.)], individual growth is positively correlated with food consumption. However, increased food consumption will increase the exposure to trophically transmitted parasites. Using a correlative approach, we explore the association between parasite abundance and the individual growth of Arctic charr from five lakes within the same watercourse. The studied parasite species differ in their life cycles and cost to the host. We predicted a positive association between parasite abundance and fish growth for parasites of low pathogenicity reflecting high consumption rates, and a negative association at higher parasite abundances for more costly parasites. We found no direct negative associations between parasite abundance and fish growth. The relationship between parasite abundance and growth was linearly positive for the low costly Crepidostomum sp. and concave for the more costly Eubothrium salvelini. In natural fish populations, the negative effects of parasites on fish growth might be outweighed by the energy assimilated from feeding on the intermediate host. However, experimental studies with varying food consumption regimes are needed to determine the mechanisms underlying our observations.

     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

Trophic interactions in the system host (eelpout Lota lota)—Parasite (Eubothrium rugosum)—Symbiotic microflora at hydrolysis of carbohydrate food components

It is established that bacteria with the ability to produce enzymes hydrolyzing carbohydrates of different complexity degrees are associated with the intestine digestive-transport surfaces of the eelpout Lota lota (L.) and of cestoids Eubothrium rugosum parasitizing in it. The release by bacteria of enzymes hydrolyzing not only complex carbohydrates, but also disaccharides, decreases the energy expenditures of the host and parasite for synthesis of their own hydrolases and increases the glucose concentration near the transport surfaces, which allows all members of this formed community to use glucose. The total amylolytic activity (TAA) of enzymes and the α-amylase activity of the studied bacteria are realized in a wide range of pH values. The levels of the enzyme general amylolytic activity and of bacterial α-amylase activity under the experiment conditions are comparable with similar characteristics of enzymes desorbed from the studied surfaces and participating in the membrane digestion processes in the host and parasite, which can suggest a significant contribution of the symbiotic microflora enzymes to digestion of the host and parasite.     

Helminths in an intensively stocked population of lake trout, Salvelinus namaycush, from Lake Huron

Eighty stocked lake trout Salvelinus namaycush (Salmonidae), collected from 2 locations in Lake Huron in May 1995, were examined for parasites. The parasite fauna of this top predator in Lake Huron was characterized by only 6 helminth species. Echinorhynchus salmonis infected all lake trout with a mean intensity of 163.9. The intensity of this acanthocephalan species significantly increased with host length and weight. Eubothrium salvelini infected 78 lake trout with a maximum number of 81 scoleces counted. Diplostomum sp., Cyathocephalus truncatus, Capillaria salvelini, and Neoechinorhynchus sp. infrequently infected lake trout. The low parasite species richness in these lake trout is believed to be due to their large size at stocking and to the loss of historical enzootic host-parasite relationships that followed the absence of this fish species in Lake Huron for 26 yr.     

Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi--cat model.

A striking feature of lymphatic filariasis is the considerable heterogeneity in infection burden observed between hosts, which greatly complicates the analysis of the population dynamics of the disease. Here, we describe the first application of the moment closure equation approach to model the sources and the impact of this heterogeneity for macrofilarial population dynamics. The analysis is based on the closest laboratory equivalent of the life cycle and immunology of infection in humans--cats chronically infected with the filarial nematode Brugia pahangi. Two sets of long-term experiments are analysed: hosts given either single primary infections or given repeat infections. We begin by quantifying changes in the mean and aggregation of adult parasites (inversely measured by the negative binomial parameter, kappa in cohorts of hosts using generalized linear models. We then apply simple stochastic models to interpret observed patterns. The models and empirical data indicate that parasite aggregation tracks the decline in the mean burden with host age in primary infections. Conversely, in repeat infections, aggregation increases as the worm burden declines with experience of infection. The results show that the primary infection variability is consistent with heterogeneities in parasite survival between hosts. By contrast, the models indicate that the reduction in parasite variability with time in repeat infections is most likely due to the ''filtering'' effect of a strong, acquired immune response, which gradually acts to remove the initial variability generated by heterogeneities in larval mortality. We discuss this result in terms of the homogenizing effect of host immunity-driven density-dependence on macrofilarial burden in older hosts.     

The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria

Plasmodium falciparum, the most virulent species of human malaria parasite, causes 1-3 million deaths per year. Because this parasite is susceptible to naturally acquired host immunity the main burden of diseases falls on young children. The mechanism of this immunity is still unclear. However, the parasite makes a considerable investment in the insertion of highly polymorphic antigens (parasite-infected-erythrocyte surface antigens, PIESA) on the infected erythrocyte surface, and these antigens are potentially important immune targets.     

The occurrence and life history of Asymphylodora kubanicum (Platyhelminthes: Digenea: Monorchidae) in the Worcester-Birmingham canal, with special reference to the feeding habits of the definitive host, Rutilus rutilus

Two hundred roach and over 400 molluscs were examined over a one year period to investigate the occurrence and life history of Asymphylodora kubanicum in the Worcester-Birmingham canal. Larval stages, infective to the fish definitive host, were present in molluscs throughout the year but did not show a seasonal fluctuation in numbers. Parasites in the intestine of the roach showed a marked annual cycle of occurrence and maturation: low winter infection levels preceded a dramatic increase in infection during the spring and summer. Maturation of the parasite population was rapid during the spring and summer and in late summer and early autumn the parasites laid their eggs and subsequently died. The death of parasites after egg-laying resulted in the low winter infection level during which time little recruitment occurred.
Roach became infected mainly in their third year when molluscs become a dominant component of their diet. Thereafter the older fishes (<2+) are all equally susceptible to infection, but the larger (older) fishes become more heavily infected because of the greater consumption of molluscs per fish. The sex of the fish made no difference to infection with the parasite.     

Inshore–offshore comparison of parasite infestation in Mytilus edulis: implications for open ocean aquaculture

Offshore production offers a new perspective for mussel aquaculture in the German Bight (North Sea) as no expansion is possible in the intertidal and subtidal zone of the Wadden Sea because of restrictions on the number of licenses. The development of offshore wind farms offers a unique opportunity because of the associated infrastructure. Service platforms, as well as the pylons themselves, offer perfect structures for mooring longlines and other culture units. One of the advantages of offshore culture may be a lower parasite load in offshore mussels compared with mussels produced under traditional inshore bottom culture. By sampling mussel spat from offshore suspended buoys or collectors, we simulated an offshore culture situation and compared parasite infestation rates with those in mussel spat obtained from suspended inshore buoys or collectors, in mussels from inshore benthic subtidal beds and from inshore benthic intertidal mussel beds. Mussels from offshore sites were free of trematodes and shell‐boring polychaetes. Parasitic copepods only occurred at a single offshore site, on a 20‐year‐old research platform, but not on buoys or collectors exposed for shorter time periods. All three monitored parasite taxa were present at all other sites. The highest prevalence was found for trematodes in inshore benthic intertidal mussels (78.7 ± 6.4%) and locally reached 100%. Through a variety of detrimental effects, trematodes, parasitic copepods and shell‐boring polychaetes are known to affect growth performance and product quality. We therefore propose that offshore mussel production could be a promising culture procedure because it seems to result in lower parasite burden than at traditional culture sites. Whether offshore production also results in better survival and growth, compared with inshore mussel culture on a commercial scale, needs to be investigated further.     

Metazoan parasite community structure of sea trout on the west coast of Ireland

A total of 129 sea trout smolts from 10 locations on the west coast of Ireland were examined for metazoan parasites. Of 11 species identified only four had a prevalence >20%. Two species Hysterothylacium aduncum and Hemiuris communis have a confirmed marine origin; Eubothrium crassum has been shown to exist in both the sea and fresh water. The remaining species were fresh water. Overall the parasite community was dominated by autogenic species with only Diphyllobothrium dendriticum having allogenic transmission. Infracommunity values for mean species richness, and Brillouins index of diversity were low, indicating the presence of an impoverished helminth community with little potential for interspecific interaction. The relationship between marine helminths and sea lice was also examined.     

Infection risk dictates immunological divergence among populations in a Mediterranean lizard

The ability of vertebrates to evolve different defence strategies in response to varying parasitism regimes remains poorly understood. Hosts may adopt two different strategies to defend themselves against parasites: tolerance (hosts alleviate the negative fitness consequences of parasite infection) and resistance (hosts strengthen their immune response as parasite burden increases). Both strategies are effective, but fitness has been reported to decline faster in less‐tolerant individuals. Here, we assessed the number of splenocytes and the cell‐mediated response (proxies for resistance) and body condition (a proxy for tolerance) in four populations of a Greek endemic lizard (Podarcis gaigeae), each exposed to different infection risks (defined as the cumulative effect of parasite burden and duration of exposure). We anticipated that populations with heavy parasite burden would enhance the efficacy of their immune response (resistance) compared to lizards deriving from parasite‐poor habitats. We also predicted that populations with longer exposure to parasites would be adopted and be more tolerant. Each factor (duration of exposure and parasite burden) had a distinct effect on the immune response, and thus, our results were rather complicated. Lizards with heavy parasite burden and aperiodic exposure demonstrated resistance, whereas lizards with heavy parasite burden and chronic exposure were more tolerant. Populations with low parasite burden and minimal exposure were more resistant. Our results suggest that the development of some immunological strategies may be differentiated under different infection risks, even within the same species.     

Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of the coastal Atlantic Forest,Brazil

Parasites are considered to play an important role in the regulation of wild animal populations. We investigated parasite burden of gastrointestinal nematodes and body condition in specialist and generalist small mammal species in secondary forest fragments in the highly endangered coastal Atlantic Forest. We hypothesized that body condition decreases with increasing parasite load and that parasite burden increases with increasing fragmentation in specialist species but not in generalist species as a consequence of differing responses to fragmentation effects. Investigated species were Akodon montensis, Oligoryzomys nigripes, and Delomys sublineatus (rodents) and the marsupials Marmosops incanus and Gracilinanus microtarsus. Prevalence of parasites was high in all species except for the arboreal G. microtarsus, presumably because of decreased infection probability. No correlation was found between body condition and parasite load in any of the species. Contrary to our expectations, body condition of the specialists D. sublineatus and M. incanus increased in both species with increasing fragmentation. In D. sublineatus, parasite burden increased and body condition decreased in fragments with relatively high density probably due to increased contact rates and facilitation of infection with nematodes. In all generalist species, low or no correlation between parasite burden and fragmentation was detected, suggesting little effect of fragmentation on population health.     

A preliminary study of parasite diversity in the anadromous Kamchatkan mikizha Parasalmo mykiss mykiss (Osteichthyes: Salmoniformes: Salmonidae)

The study of parasites associated with the anadromous mikizha from several rivers of the Western Kamchatka has revealed 44 parasite species. The majority of parasites (59%) belong to marine and estuarine-marine species. Lecithophyllum bothryophorum, Echinorhynchus leidyi and plerocercoids of the family Litobothriidae were found for the first time in anadromous fish entering into Asian continental watersheds. It has been revealed that only a few specimens of the anadromous mikizha feed in fresh waters. Most of feeding fish consume a minor amount of food, and this feeding is occasional. Young forms of intestinal parasites of the freshwater and estuarine-freshwater groups (Neoechinorhynchus spp., Crepidostomum spp., Cucullanus truttae, Eubothrium salvelinf) come into anadromous fishes mainly before their entering in fresh waters.     

Host specificity and geographical distribution of Eubothrium in European salmonid fish

The host specificity and distribution of Eubothrium crassum (Bloch, 1779) and Eubothrium salvelini (Schrank, 1790), morphologically fairly similar pseudophyllidean tapeworms parasitizing salmonid fish, were critically assessed on the basis of morphological and genetic evaluation of extensive material collected from different definitive hosts and geographical regions in Europe. Eubothrium crassum occurs in fish of the genera Salmo, i.e. salmon (S. salar - both freshwater and marine), sea trout (S. trutta trutta), brown trout (S. trutta fario), and lake trout (S. trutta lacustris), and also in Danubian salmon (Hucho hucho) and vendace (Coregonus albula). Eubothrium salvelini parasitizes Arctic char (Salvelinus alpinus) and brook trout (Salvelinus fontinalis) in Europe, and also whitefish (Coregonus wartmanni). Rainbow trout (Oncorhynchus mykiss), which is not a native European fish species, was found to be a suitable definitive host for both Eubothrium species, which may occur simultaneously in the same fish. Previous records of E. crassum in Arctic char and brook trout, and those of E. salvelini in fish of the genus Salmo were most probably misidentifications. Most studies of Eubothrium have involved salmonids from the northern part of Europe, with few records from southern and south-eastern Europe. This study also confirmed the reliability of the morphology of the apical disc for the discrimination of E. crassum and E. salvelini.     

Decomposing health: tolerance and resistance to parasites in animals

Plant biologists have long recognized that host defence against parasites and pathogens can be divided into two conceptually different components: the ability to limit parasite burden (resistance) and the ability to limit the harm caused by a given burden (tolerance). Together these two components determine how well a host is protected against the effects of parasitism. This distinction is useful because it recognizes that hosts that are best at controlling parasite burdens are not necessarily the healthiest. Moreover, resistance and tolerance can be expected to have different effects on the epidemiology of infectious diseases and host-parasite coevolution. However, studies of defence in animals have to date focused on resistance, whereas the possibility of tolerance and its implications have been largely overlooked. The aim of our review is to (i) describe the statistical framework for analysis of tolerance developed in plant science and how this can be applied to animals, (ii) review evidence of genetic and environmental variation for tolerance in animals, and studies indicating which mechanisms could contribute to this variation, and (iii) outline avenues for future research on this topic.     

Age‐related parasite load and longevity patterns in the sedge warbler Acrocephalus schoenobaenus

We report the results from a nine‐year study on parasite infection in males of a small migrant passerine, the sedge warbler Acrocephalus schoenobaenus. Every year, for each male caught during territory establishment we estimated infection intensity of two lineages of Haemoproteus belopolskyi (SW1 and SW3), using molecular methods. We found a significant relationship between infection intensity and males’ longevity in both studied lineages. There was severe mortality of second‐year sedge warblers after their first breeding season, with lower parasite load in survivors. The lower infection intensity in older age classes was related to between‐individual change in both lineages, but was also a result of differences in infection intensity during the lifetime of individual males in the SW3. The relation between parasite load and longevity suggests that parasite load may be an age‐dependent factor influencing individual survival.     

The occurrence of the trematode Plagiorchis muris in the wood mouse Apodemus sylvaticus in North Yorkshire, UK

Wood mice Apodemus sylvaticus were trapped each September over a 13-year period, from 1993 to 2005, in a wooded area adjacent to Malham Tarn, Yorkshire, UK. Plagiorchis muris was found to be the dominant intestinal trematode and occurred in every year of sampling, with an overall prevalence of 16.9%. This appears to be the first record of P. muris in A. sylvaticus within the UK. The mean worm burden was 2.03 and the distribution of the parasite within mice was typically overdispersed. No difference in prevalence relative to host sex was evident although there was a higher prevalence of 21.9% in larger older mice compared with 9.1% in juveniles, which probably relates to a greater foraging activity in older mice. Annual prevalence values of P. muris infections varied significantly over the study period with higher prevalences being associated with years with a high spring/summer rainfall. The second intermediate hosts for P. muris include a variety of aquatic insect larvae and it is likely that the higher rainfall may result in the occurrence of temporary water bodies suitable for the development of insect larvae.     

Natural Selection on Individual Variation in Tolerance of Gastrointestinal Nematode Infection

Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host–parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.