Consistency of host responses to parasitic infection in the three‐spined stickleback fish infected by the diphyllobothriidean cestode Schistocephalus solidus

Among populations of the three‐spined stickleback fish in Alaska, females appear to show two forms of sterility tolerance to infection by the diphyllobothriidean cestode Schistocephalus solidus. In contrast to sticklebacks in other regions of the northern hemisphere, female fish are capable of producing clutches of eggs despite supporting large parasite burdens. Nonetheless, nutrient loss to the parasite, coupled with the energetic demands of host reproduction, eventually curtails spawning among infected females. Host females in Walby Lake experience ‘fecundity reduction’ resulting from nutrient theft as a side effect of infection. In Scout Lake, infected females show ‘fecundity compensation’, an adaptive, inducible response allowing them to increase current fecundity to compensate for reduction or loss of future reproduction. This multi‐year study of sticklebacks from each lake addresses two empirical questions for a better understanding of the dynamic interplay between host and parasite. First, is there is any annual variation within the two responses to parasitism in each host population; and, if so, is it related to parasite burden? Second, do the two host responses show consistent differences between the populations of sticklebacks despite any yearly variation in them? We found annual, intra‐population variation within the response shown by each population of stickleback which appears to have been influenced by the parasite : host mass ratio and possibly by unknown environmental conditions affecting the reproductive physiology of stickleback females. Moreover, the data support the hypothesis that ovum mass is more sensitive to parasitism (parasite burden) than clutch size in females from Walby Lake which exhibit fecundity reduction. Notwithstanding the intra‐population variation within each host response, the responses to infection occurred consistently within each respective stickleback population and appear to reflect stable, fundamental characteristics of the populations. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 958–968.     

Abundance and distribution of Diphyllobothrium ditremum Creplin (Cestoda: Pseudophyllidea) plerocercoids in benthic whitefish, in northern Finnish Lapland

The prevalence of Diphyllobothrium ditremum plerocercoids in whitefish Coregonus lavaretus ranged between 70 and 100% in Lake Kilpisjärvi and in three other lakes in Northern Lapland, Finland. The mean abundance in Lake Kilpisjärvi (age groups 1+-10+ years), ranged between 103·5± 71·3 in 1992–1993 to 110·9± 80·0 plerocercoids per fish in 1997. The asymptotic value of the infection levelled at 113 plerocercoids per host after age 3. No significant difference in abundance was detected between study years ( P >0·10). Abundances in other lakes ranged between 4·8±9·7 and 91·1±115·1. Two seasonal peaks of plerocercoid recruitment were observed in Lake Kilpisjärvi; between March and April ( P <0·002) and between September and October ( P =0·042). In autumn the numbers of larvae increased particularly in female fish. The invasion rate of the parasite was lower in other lakes studied, and the infection rate in whitefish was closely related to the copepod food eaten.     

Infection patterns of Tylodelphys barilochensis and T. crubensis (Trematoda: Diplostomatidae) metacercariae in Galaxias maculatus (Osmeriformes: Galaxiidae) from two Patagonian lakes and observations on their geographical distribution in the southern Andean region,Argentina

In the Patagonian Andean region, 2 species of diplostomatids parasitize the brains of Galaxias maculatus.The purpose of this study was to evaluate seasonal variation, spatial variation, and association with host age in the transmission of Tylodelphys barilochensis and T. crubensis in several oligotrophic lakes in Argentinian Patagonia. Fishes were captured monthly in Lake Gutiérrez and bimonthly in Lake Escondido. One summer or autumn sample was also taken in several other Patagonian lakes. Infection parameters were calculated and compared using nonparametric tests. The 2 species co-occurred in most of the sampled lakes, with high values of prevalence and mean intensity. In Lake Gutiérrez and Lake Escondido, the intensity of both diplostomatid species did not show significant differences between sexes and co-varied with host length. All age classes were infected; maximum prevalence values were reached before maximum mean intensity values in the 1-yr age class. A seasonal pattern of prevalence and mean intensity of the 2 parasite species with autumn mean intensity values differing significantly from those of the other seasons was evident only in Lake Gutiérrez.     

Do environmental differences between lakes in northwestern Argentinean Patagonia affect the infection of Philureter trigoniopsis (monogenea) in Galaxias maculatus (osmeriformes)?

Philureter trigoniopsis is the only parasite found in the ureters and urinary bladder of Galaxias maculatus in Patagonian Andean lakes. The dynamics of this endoparasitic monogenean were studied in Lake Gutiérrez, a body of water with scarce shoreline vegetation, where the host has an annual cycle of migration to the deep pelagic zone of the lake. To compare variations of the infection related to differences between lakes, G. maculatus specimens were sampled monthly with baited traps from September 1998 to November 1999 in Lake Moreno, which is an oligotrophic body of water with emergent shoreline vegetation and where the fish do not migrate to the deep pelagic areas of the lake. In addition, data for summer infections of P. trigoniopsis from 10 Andean Patagonian lakes that differ in aquatic vegetation, depth, and area were compared. In Lake Moreno prevalence of P. trigoniopsis showed a seasonal pattern, with 1-yr-old fish exhibiting the highest values of prevalence and mean intensity. Negative correlations between water temperature and prevalence and between age of fish and abundance were found. Our results suggest that age of fish may be the main factor structuring the distribution of P. trigoniosis in populations of G. maculatus. At the regional level the relationship between the infection and the characteristics of the lakes was also observed, with prevalence and mean intensity of P. trigoniopsis in G. maculatus higher in large deep lakes without macrophytes.     

青海湖裸鲤寄生舌状绦虫的空间格局研究

舌状绦虫裂头蚴只寄生在体长小于２２０ｍｍ的青海湖裸鲤中,其种群在宿主种群中呈聚集分布。其聚集分布的强度随寄生虫种群平均密度的增加而降低。由于舌状绦虫在宿主体腔生长,产生明显的空间拥挤效应,可能导致宿主死亡或被食鱼鸟类捕食而转移到终末宿主中。在体长小于１２０ｍｍ的宿主中,密度依赖的死亡过程可能是使聚集强度降低的原因;而体长１４０－２００ｍｍ的鱼中,则是非密度依赖的全死过程使聚集强度增加．     

Properties of crowding indices and statistical tools to analyze parasite crowding data

Crowding, i.e., the size of the infrapopulation inhabiting an individual host, is a major component of parasites' environment, which often influences both morphological and life-history characters (the so-called density-dependent characters) in different parasite taxa. Although crowding equals intensity in case of a single parasite individual, mean intensity of the host population does not define mean crowding of the parasite population. Crowding indices are notoriously hard to handle statistically because of the inherently large number of nonindependent values in data. In this study, we aim to investigate the apparently paradox features of crowding indices and to make some proposals and also to introduce statistical methods to calculate confidence intervals and 1-sample and 2-sample tests for mean crowding. All methods described in this study are supported by the freely distributed statistical software Quantitative Parasitology.     

Body condition and reproductive capacity of three‐spined stickleback infected with the cestode Schistocephalus solidus

The relationship between reproductive ability and the residual index of body condition in three‐spined stickleback Gasterosteus aculeatus from a population infected with the cestode macroparasite Schistocephalus solidus in Walby Lake, Alaska, was examined. In general, reproductive activities resulted in significantly lower levels of body condition in three‐spined stickleback during the latter part of the breeding season, and relatively high levels of S. solidus infection intensified the energetic drain. Although female body condition did not differ significantly due just to the presence of S. solidus , increased parasite index did have a significant negative effect on female body condition. Males showed significantly lower levels of body condition in response to S. solidus infection alone and in association with a greater parasite index. Males had greater mean parasite indices than females. Females had significantly lower body condition than males, which may be due to discrepancies in energy expenditure between the sexes during reproduction. Females with greater body condition were significantly more likely to produce a clutch of eggs than those with lower condition, suggesting a threshold effect of body condition on reproductive capacity.     

Effects of water quality and trophic status on helminth infections in the cyprinid fish, Schizothorax niger Heckel, 1838 from three lakes in the Kashmir Himalayas

Water quality greatly influences the population density of aquatic biota, including parasites. In order to evaluate the relationship between fish parasites and water quality in Kashmir Himalayas, we assessed helminth parasite densities in Schizothorax niger Heckel, 1838 (an endemic cyprinid fish of Kashmir) from three lakes, namely Anchar, Manasbal and Dal, which reflected the varied stages of eutrophication. The overall prevalence of helminth infections was higher in the hypertrophic Anchar Lake (prevalence = 18.6%) compared to Manasbal Lake, which was the least eutrophied (prevalence = 6.4%). Furthermore, mean prevalence of monoxenous and heteroxenous parasites was higher in lakes containing higher levels of water degradation (Anchar and Dal). The mean number of helminth species per fish host was the highest in the hypertrophic lake (1.3 ± 0.3) in comparison to the least eutrophic lake (0.2 ± 1.5). Variability of calculated infection indices (prevalence, mean intensity and mean abundance) revealed that helminth parasite composition in the fish was affected by the lakes' environmental stress (degraded water quality). Therefore, data on the density of helminth parasites in fish can provide supplementary information on the pollution status of a water body.     

Do heavy burdens of Schistocephalus solidus in juvenile threespine stickleback result in disaster for the parasite?

The diphyllobothriidean cestode Schistocephalus solidus typically infects threespine sticklebacks that are too small to allow the parasite to reach a mature size. As a result, the parasite must allow further growth of its host to reach the size at which it becomes competent to infect and reproduce in the definitive host. At times, however, intensity of infection can be high, leading to crowding among parasites and to heavy burdens causing mortality among hosts. Our data show that, during a previously observed epizootic, large percentages of plerocercoids (average 75% per host, 82% among all parasites pooled) did not grow to become massive enough in 1-yr-old threespine sticklebacks to be capable of establishment and maturation in the definitive host. Massive deaths of 1-yr-old sticklebacks due to infection during the epizootic resulted in the great misfortune of a disaster for a large number of parasites, resulting in dramatically reduced transmission of S. solidus.     

Shape variation of cysticercoids of Hymenolepis diminuta (Cyclophyllidea) from fed, partially fed, and fasted Tribolium confusum (Coleoptera)

Quantitative studies of a crowding effect on cysticercoids of Hymenolepis diminuta in the intermediate host are few and limited in scope. In this study, we developed a technique to rapidly collect morphological information on large numbers of parasites, and verified the utility of geometric models for simple and accurate estimation of cysticercoid size for quantitative studies. These models were tested using measurements from 4,899 H. diminuta obtained from 666 Tribolium confusum exposed 1-4 wk previously. Length, width, and depth of the body and cercomer (when present) can be used in conjunction with these models to provide the most accurate estimation of parasite size. However, parasite body length alone can be used, with adjustment for effects of host diet and infection intensity, to predict the remaining measurements in incomplete specimens. Parasites that developed in higher intensity infections, or in hosts with reduced food intake, were narrower and had a proportionately shorter cercomer. Host age, sex, and mating status, and parasite age also had statistically significant, but small-magnitude, effects on parasite shape.     

Some (worms) like it hot: fish parasites grow faster in warmer water,and alter host thermal preferences

Elevated environmental temperatures associated with anthropogenic warming have the potential to impact host‐parasite interactions, with consequences for population health and ecosystem functioning. One way that elevated temperatures might influence parasite prevalence and intensity is by increasing life cycle completion rates. Here, we investigate how elevated temperatures impact a critical phase of the life cycle of the bird tapeworm Schistocephalus solidus – the growth of plerocercoid larvae in host fish (three‐spined sticklebacks Gasterosteus aculeatus). By 8 weeks post‐infection, plerocercoids recovered from experimentally infected sticklebacks held at 20 °C weighed on average 104.9 mg, with all exceeding 50 mg, the mass considered consistently infective to definitive hosts. In contrast, plerocercoids from sticklebacks held at 15 °C weighed on average 26.5 mg, with none exceeding 50 mg. As small increases in plerocercoid mass affect adult fecundity disproportionately in this species, enhanced plerocercoid growth at higher temperatures predicts dramatically increased output of infective parasite stages. Subsequent screening of thermal preferences of sticklebacks from a population with endemic S. solidus infection demonstrated that fish harbouring infective plerocercoids show significant preferences for warmer temperatures. Our results therefore indicate that parasite transmission might be affected in at least two ways under anthropogenic warming; by enhancing rates of parasite growth and development, and by increasing the likelihood of hosts being able to seek out proliferating warmer microhabitats. Furthermore, our results suggest the potential for positive feedback between parasite growth and host thermal preferences, which could dramatically increase the effects of even small temperature increases. We discuss the possible mechanisms underpinning our results, their likely ecological consequences and highlight key areas for further research.     

Evolutionary significance of fecundity reduction in threespine stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus

Parasites may cause fecundity reduction in their hosts via life‐history strategies involving simple nutrient theft or manipulation of host energy allocation. Simple theft of nutrients incidentally reduces host energy allocation to reproduction, whereas manipulation is a parasite‐driven diversion of energy away from host reproduction. We aimed to determine whether the diphyllobothriidean cestode parasite Schistocephalus solidus causes loss of fecundity in the threespine stickleback fish (Gasterosteus aculeatus) through simple nutrient theft or the manipulation of host energy allocation. In one stickleback population (Walby Lake, Matanuska‐Susitna Valley, Alaska), there was no difference in the sizes and ages of infected and uninfected reproducing females. Lightly‐ and heavily‐infected females produced clutches of eggs, but increasingly smaller percentages of infected females produced clutches as the parasite‐to‐host biomass ratio (PI) increased. Infected, clutch‐bearing sticklebacks showed reductions in clutch size, egg mass, and clutch mass, which were related to increases in PI and reflected a reduction in reproductive parameters as growth in parasite mass occurs. The findings obtained for this population are consistent with the hypothesis of simple nutrient theft; however, populations of S. solidus in other regions may manipulate host energy allocation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 835–846.     

Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in transmission

Eighteen species of fishes were collected during the open water (1985-1987) and winter seasons (1985-1986) from Dauphin Lake, Manitoba, Canada (51 degrees 17'N, 99 degrees 48'W) and examined for plerocercoids of Ligula intestinalis (L.). Plerocercoids were most prevalent (5.3%) in spottail shiners (Notropis hudsonius), the major fish host for Ligula in Dauphin Lake. Detailed analysis of the spottail shiner-Ligula host-parasite system revealed that the number of plerocercoids differed between years and among habitats but there was no statistically significant seasonal pattern; recruitment of new worms was highest in young fish and decreased with age, and infected spottails had reduced gonad development. Analysis of host and parasite growth revealed that the soma of male spottails infected with Ligula weighed more but had a reduced growth rate. Growth rate of females was unaffected by Ligula but somatic weight was slightly increased. This appears to be related to the greater metabolic stress on infected males. Based on increased mean somatic weight and skewness of the weight distribution for infected fish, we propose that infected spottails are subjected to size-selective mortality. Some of the contradictions in the literature may be attributed to underestimated prevalence due to increased numbers of spawning fish in the spring, mixed age-classes of Ligula in separate age-classes of fish, and differential effects on growth due to infection in male versus female hosts.     

Accumulation of plerocercoids of Triaenophorus crassus in the second intermediate host Coregonus lavaretus and their effect on growth of the host

Patterns of accumulation of Triaenophorus crassus in its second intermediate host whitefish Coregonus lavaretus s.l. were studied between 1991 and 1996 from two host populations in two separate areas of Lake Saimaa, Finland. Whitefish were infected commonly with several T. crassus plerocercoids and the parasites were aggregated into the oldest hosts. In one host population the annual parasite accumulation was 0·9 parasites in all host age groups between 3 and 8 years. In the other host population the annual accumulation was 1·6 parasites in 3–5-year-old fish, but increased up to 3 to 4 parasites per year in fish over 5 years old. The increase did not coincide with the period of maturation or any increase in whitefish growth, both of which could alter the food intake of the fish. The sharp increase in the annual accumulation suggests a threshold intensity above which the probability of acquiring further parasites increases. In spite of a heavy aggregation of parasites there was no evidence of parasite-induced host mortality. The annual increase in mean abundance was not correlated with the mean annual weight increase in 2–4-year-old fish within cohorts. However, evidence of a negative effect of parasites on whitefish growth was revealed by back-calculation of lengths of uninfected and infected whitefish and correlations between length or weight of fish and intensity of infection with fish age. Both analyses suggested that larger young fish harboured more parasites than the smaller ones while in older fish the reverse was true, a pattern that has not been shown earlier for parasitized fish.     

The abundance and distribution of Diphyllobothrium dendriticum (Nitzsch) and D. ditremum (Creplin) in the char Salvelinus alpinus (L.) in Sweden

A total of 654 char, Salvelinus alpinus (L.) and 33 brown trout, Salmo trutta L., were examined for the plerocercoids of Diphyllobothrium dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1825). Only char were found to be infected. Both parasitic species were abundant. The incidence and mean intensity of infection for D. dendriticum were 83.2% and 8.8, respectively; for D. ditremum 93.7% and 45.0. There was no variation in the intensity of infection between different parts of the lake. The incidence and intensity of infection increased with the age of the fish to age 8+ for both species. From this age the intensity of infection leveled off or decreased. No differences in intensity of infection between the sexes were found. The frequency distribution of parasite counts were overdispersed and fitted the negative binomial distribution even within single age-groups. The two parasite species showed a high positive correlation in intensity of infection, D. ditremum was concentrated in the stomach and pyloric caeca. D. dendriticum was more widely distributed within the host and was supposed to kill heavily infected fish.     

Habitat quality and endoparasitism in the Pacific sanddab Citharichthys sordidus from Santa Monica Bay, southern California

Prevalence, mean abundance and mean intensity of the most common endohelminths infecting Pacific sanddab Citharichthys sordidus were compared among six trawl stations in the Santa Monica Bay. These trawl stations varied in their distance from the 8 km effluent of the Hyperion treatment plant which is situated adjacent to Santa Monica Bay. Juvenile stages of Anisakis sp., Corynosoma sp., Lacistorhynchus dollfusi and Tetraphyllidean plerocercoids were found infecting Pacific sanddabs. Significantly higher prevalence and mean intensity of L . dollfusi and Anisakis sp. were seen at the non-outfall stations compared to outfall stations either immediately surrounding or in the vicinity of the outfall. These differences appeared to be related to changes in invertebrate population densities in response to the presence of contaminants. Canonical analysis of discriminance using parasite abundance data discriminated non-outfall from outfall stations. The cestode L . dollfusi explained most of the variability in discriminant scores generated from the analysis and appears to warrant further investigation as a potential bioindicator of pollution exposure in its fish host.     

Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum

We studied the 'crowding effect' in Tribolium confusum infected with Hymenolepis diminuta. Manipulations included age and number of parasites, and diet, sex, age and number of exposures of hosts. Volume per parasite was unaffected until an intensity of at least 5-10 parasites per host, then declined approximately inversely as intensities increased. Parasite size was affected by host sex but not age or reproductive status. Host diet affected parasite size and the impact of crowding. Daily gain in parasite volume peaked partway through the developmental period and preceded the first evidence of a crowding effect. Parasites that established during a second exposure had a transient developmental delay but eventually grew as large or larger than parasites from a single exposure with the same total intensity. Parasites responded to crowding by differential allocation of resources. Cercomer volume decreased even with slight crowding, the capsule surrounding the scolex was not reduced until crowding became more severe, and scolex width was reduced only in the most extreme conditions. The data support the hypothesis that the crowding effect in this system is driven primarily by nutrient, rather than space limitations.     

Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population

Sampling of the fish community was carried out for 20 years in the Mirgenbach reservoir, in North-Eastern France. The prevalence and the mean intensity of Ligula intestinalis (Cestoda) were analysed in roach (Rutilus rutilus) and silver bream (Blicca bjoerkna) populations, the main two infected species. The aim of this study was to investigate the host switch from roach to silver bream and the consequences of L. intestinalis infestation in silver bream, which is an unusual host for this parasite as Ligula parasitism in silver bream appears to be rare. We analysed in detail the relationships between parasitism index (PI), gonadosomatic index (GSI), perivisceral fat abundance (PFA) and condition index (CI) in the silver bream population. In 1998, prevalence of L. intestinalis highlighted a clear host switch from roach to silver bream. In the silver bream population, young fish were the most severely infected and the impact of plerocercoids appeared to be different depending on the host sex. In male silver bream, plerocercoids drew energy from fat reserves even if GSI was also slightly impacted. On the contrary, in females energy was diverted from gonad maturation rather than from perivisceral fat reserves. No significant difference was observed in terms of CI in either sex.     

金钱鱼体内惠州长宫吸虫种群动态分析

金钱鱼肠道内的惠州长宫吸虫,随着宿主体长的生长,其感染强度、平均丰盛度、平均拥挤度和宿主体长小于30mm的感染率呈逐渐增加的趋势,而宿主在不同体长组中,除了体长小于30mm以外,其感染率变化相对较稳定;在不同的月份中,吸虫在宿主体内的感染率从2月起呈逐渐下降趋势,感染强度则有逐渐增大倾向;平均丰盛度除从4～7月份有1个明显先上升后下降的变化外,其它月份变化差异不大。从吸虫在宿主体内的频率分布变化中,表明多数宿主不感染或只感染少量的吸虫,而少数宿主感染吸虫数量较大;吸虫种群在不同宿主体长组和不同月份的分布格局类型均为聚集分布,在不同宿主体长组中聚集分布强度随着种群密度增加而增强。       

The relationship between individual seed quality and maternal plant body size in crowded herbaceous vegetation

Aims In most natural plant populations, there is a strong right-skewed distribution of body sizes for reproductive plants—i.e. the vast majority are relatively small, suppressed weaklings that manage not just to survive effects of crowding/competition and other hazards but also to produce offspring. Recent research has shown that because of their relatively large numbers, these relatively small resident plants collectively contribute most of the seed offspring production available for the population in the next generation. However, the success of these offspring will depend in part on their quality, e.g. reflected by seed size and resource content. Accordingly, in the present study, we used material from natural populations of herbaceous species to test the null hypothesis that there is no significant relationship between body size variation in resident plants—resulting from between-site variation in the intensity of crowding/competition—and variation in the mass or N content of their individual seeds.Methods Using populations of 56 herbaceous species common in eastern Ontario, total above-ground dry plant mass, mean mass per seed and mean nitrogen (N) content per seed were recorded for a sample of the largest resident plants and also for the smallest reproductive plants growing in local neighbourhoods with the most severe crowding/competition from near neighbours.Important findings Mass per seed was numerically smaller from the smallest resident plants for most study species, but with few exceptions, this was not significantly different (P> 0.05) from mass per seed from the largest resident plants. The results therefore showed no general effect of maternal plant body size on individual seed mass, or N content. This suggests that the reproductive output of the smaller half of the resident plant size distribution within these populations is likely to contribute not just most of the seed production available for the next generation but also seed offspring that are just as likely—on a per individual basis—to achieve seedling/juvenile recruitment success as the seed offspring produced by the largest resident plants. This conflicts with the traditional 'size-advantage' hypothesis for predicting plant fitness under severe competition, and instead supports the recent 'reproductive-economy-advantage' hypothesis, where competitive fitness is promoted by capacity to produce offspring that—despite severe body size suppression imposed by neighbour effects—in turn have capacity to produce grand-offspring.