Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies

Intermediate host exploitation by parasites is presumably constrained by the need to maintain host viability until transmission occurs. The relationship between parasitism and host survival, though, likely varies as the energetic requirements of parasites change during ontogeny. An experimental infection of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) was conducted to investigate host survival and growth throughout the course of parasite development. Individual isopods were infected by exposure to fish feces containing parasite eggs. Isopods exposed to A. lucii had reduced survival, but only early in the infection. Mean infection intensity was high relative to natural levels, but host mortality was not intensity dependent. Similarly, a group of naturally infected isopods harboring multiple cystacanths did not have lower survival than singly infected isopods. Isopods that were not exposed to the parasite exhibited sexual differences in survival and molting, but these patterns were reversed or absent in exposed isopods, possibly as a consequence of castration. Further, exposed isopods seemed to have accelerated molting relative to unexposed controls. Infection had no apparent effect on isopod growth. The effects of A. lucii on isopod survival and growth undermine common assumptions concerning parasite-induced host mortality and the resource constraints experienced by developing parasites.     

Isopod (Asellus Aquaticus) size and acanthocephalan (Acanthocephalus lucii) infections

We examined the effect of isopod size and age on the success of an acanthocephalan infection and on the effects of that infection on the growth and survival of the isopods. Groups of isopods (Asellus aquaticus) belonging to 4 size classes (juveniles, maturing adults, young adults, and older adults) were exposed to infective acanthors of Acanthocephalus lucii. At the end of the experiment, survival of the isopods, lengths of male and female isopods, and numbers of different developmental stages of A. lucii larvae in infected isopods were assessed. Acanthocephalus lucii prevalence was significantly lower in juvenile isopods than in adults. Intensity of infection increased with the size of isopods at exposure, and cystacanth intensity correlated positively with isopod size at the end of the experiment. Exposed juveniles and maturing adults survived significantly better than unexposed individuals, but the opposite was true of the 2 largest size classes. At the end of experiment, exposed isopods, and, especially, cystacanth-infected isopods, were significantly larger than unexposed isopods in every size class. We suggest that isopod size not only affects the success of A. lucii infection but also affects the ability of A. lucii to affect the survival (and perhaps the growth) of the isopod hosts.     

Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala)

The growth and eventual size of larval helminths in their intermediate hosts presumably has a variety of fitness consequences. Therefore, elucidating the proximate factors affecting parasite development within intermediate hosts should provide insight into the evolution of parasite life histories. An experimental infection that resulted in heavy intensities of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) permitted the examination of parasite developmental responses to variable levels of resource availability and intraspecific competition. Isopods were infected by exposure to egg-containing fish feces, and larval infrapopulations were monitored throughout the course of A. lucii development. The relative rate of parasite growth slowed over time, and indications of resource constraints on developing parasites, e.g., crowding effects, were only observed in late infections. Consequently, the factors likely representative of resource availability to larval parasites (host size and molting rate) primarily affected parasite size in late infections. Moreover, at this stage of infection, competitive interactions, gauged by variation in worm size, seemed to be alleviated by greater resources, i.e., larger hosts that molted more frequently. The relatively rapid, unconstrained growth of young parasites may be worse for host viability than the slower, resource-limited growth of larger parasites.     

Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission?

Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing the hosts to increased predation. This is generally considered a parasite strategy evolved to enhance transmission to the next hosts. However, the adaptive value of host manipulation is not clear as it may be associated with costs, such as increased susceptibility to predators that are unsuitable next hosts for the parasites. We examined the ratio between the benefits and costs of host manipulation for transmission success of Acanthocephalus lucii (Acanthocephala), a parasite that alters the hiding behaviour and pigmentation of its isopod hosts. We experimentally compared the susceptibility of infected and uninfected isopods to predation by perch (Perca fluvialis; definitive host of the parasite) and dragonfly larvae (dead end). We found that the parasite predisposed the isopods to predation by both predators. However, the increased predation vulnerability of the infected isopods was higher towards perch. This suggests that, despite the costs due to non-host predation, host manipulation may still be advantageous for the parasite.     

Parasite effects on isopod feeding rates can alter the host's functional role in a natural stream ecosystem

Changes to host behaviour as a consequence of infection are common in many parasite-host associations, but their effects on the functional role hosts play within ecosystems are rarely quantified. This study reports that helminth parasites significantly decrease consumption of detritus by their isopod hosts in laboratory experiments. Natural host and parasite densities across eight contiguous seasons were used to estimate effects on the amount of stream detritus-energy processed. Extrapolations using mass-specific processing rates from laboratory results to field patterns suggest that the effects of the parasites occur year round but the greatest impact on the amount of detritus processed by isopods occurs in the autumn when the bulk of leaf detritus enters the stream, and when parasite prevalence in the isopod population is high. Parasites have a lesser impact on the amount of detritus processed in spring and summer when isopods are most abundant, when parasite prevalence is not high, and when fish predation on isopods is high. These results support the idea that parasites can affect the availability of resources critical to other species by altering behaviours related to the functional role hosts play in ecosystems, and suggest that seasonality may be an important factor to consider in the dynamics of these parasite-host interactions.     

The bionomics of the free-living larvae and the transmission of Dictyocaulus filaria between lambs in North-East England.

The bionomics of the free-living larvae of Dictyocaulus filaria on pasture, and the transmission of infection between lambs, were studied during different seasons of the year in North-East England. The rate of development of first-stage larvae to the third stage took 4-9 days in late spring and summer, 1 1/2-4 weeks in autumn and 5 1/2-7 weeks in winter. The proportion of first-stage larvae developing to the third stage ranged from 10-28% in autumn and winter, and 2-25% in spring and summer. The rate of mortality of the third-stage larvae was approximately logarithmic in nature, although the survival time was shorter in spring and summer than in autumn and winter. Third stage larvae were able to survive from autumn until the spring of the following year in sufficient numbers to perpetuate transmission but not to cause clinical disease. In a transmission study, the survival of the infective larvae on the experimental plot was poor in summer, but the larval population increased in the autumn and then declined slowly throughout the winter. Infection in the susceptible lambs was related to the level of infection on the herbage increasing in severity from early summer to late autumn. However, those lambs infected in the summer were resistant to the heavy autumn challenge of larvae on pasture.     

Inhibition patterns and seasonal availability of nematodes for beef cattle grazing on argentina''s western pampas

The seasonal population trends of cattle nematodes in tracer calves are described from 1981 to 1987. Successive worm-free calves were grazed with growing beef cattle for 20–30 days at 6 week intervals and then slaughtered for nematode counts 2 weeks after their removal from pasture. Ostertagia, Cooperia, Trichostrongylus and Haemonchus were the main genera recovered. O.ostertagi was the most often found and acquisition of inhibition-prone larvae began in late winter and reached a peak in spring, while maximum larval availability was in autumn. The seasonal inhibition and larval availability pattern for T. axei was similar to that of Ostertagia. Cooperia showed greatest inhibition during winter with maximum larval availability in autumn and spring. Haemonchus was more prevalent during summer to early autumn and no inhibition was observed. It was concluded that infective larval availability for tracer calves was highest during autumn, and most reduced in summer. All predominant species were able to survive over summer on pasture,     

Seasonal dynamics of the acanthocephalan Pomphorhynchm laevis (Müller, 1776) in its intermediate and preferred definitive hosts

No seasonal cycle was found in either the prevalence or the intensity of natural Pomphorhynchus laevis infections in Leuciscus cephalus . There was a slight seasonal change in female maturity distribution but only irregular fluctuations in the size structure of the adult parasite population throughout the year. Cystacanths were available in all seasons. Rates of parasite growth, maturation and mortality, but not establishment, increased with water temperature (or factors indirectly associated with elevated water temperature) in laboratory-infected Salmo gairdneri . Increased rates of parasite growth and maturation mask any marked shifts in the size and maturity structure of the adult parasite population which might otherwise be due to the higher turnover of adult parasites in the summer months.     

Life history and population biology of adult Acanthocephalus lucii (Acanthocephala: Echinorhynchidae)

The life history and population biology of adult A. lucii in perch, Perca fluviatilis L., from the Forth and Clyde canal, Scotland, was investigated during May 1979-September 1981. There was an annual cycle in the size of the parasite population; prevalence and abundance (+/- SE) were highest during late spring and summer (70-90% and 14 +/- 4.3 to 16 +/- 5.6 worms/fish, respectively) but declined during late autumn and reached a minimum during winter (50-60% and 2.1 +/- 0.9 to 3.2 +/- 0.6 worms/fish). Parasite maturation was associated with higher water temperatures during spring and summer and most shelled acanthors were probably produced during summer and fall. There was only 1 generation of A. lucii per year, although generations tended to overlap and individuals within each generation did not develop synchronously. The sex ratio of adults was initially near unity but favoured females in the later stages of the infection. The distribution of A. lucii among perch was highly aggregated and stomach content analysis suggested that this was partly due to heterogeneity in perch feeding behaviour. The negative binomial and Poisson lognormal models fitted the data on worm distribution. Seasonal changes in the degree of parasite aggregation were detected, but no conclusive evidence of density-dependent controls on parasite population growth was obtained.     

Seasonal population dynamics of the nematode Cystidicoloides tenuissima (Zeder) from the River Swincombe, England

The seasonal population dynamics of adult and larval Cystidicoloides tenuissima were studied in its definitive hosts brown trout, Salmo trutta and juvenile Atlantic salmon, S. salar , and mayfly intermediate host, Leptophlebia marginata , from the River Swincombe, Dartmoor National Park, Devon, U.K. Infective larvae were present in each mayfly generation for almost its entire duration in the steam benthos. The infection parameters (prevalence and mean intensity) and maturation in the fish indicated C. tenuissima was an annual parasite exhibiting a seasonal periodicity and also systematic variation with the host age. Maturation was correlated to river water temperature. Infection parameters increased from September to May, then declined in June and July and remained relatively constant for the rest of the summer. Variation in the fish infection parameters over time, site, and host species appeared to be controlled by transmission related events; the availability of infective larvae, host feeding behaviour and water temperature. The availability of infective larvae and host diet controlled the rate at which parasites were added to the parasite population, but the pattern of gains and losses was determined by a temperature dependent rejection response.     

Asynchronous male and female life cycles in the sexually dimorphic, harem-forming isopod Paragnathia formica (Crustacea: Isopoda)

The complex life history of the sexually dimorphic, harem-forming isopod Paragnathia formica Hesse is described, combining published information with new observations. The results of a two-and-a-half year field study, carried out within the animal's saltmarsh habitat, are presented, revealing significant differences in the life cycles of males and females. Settlement to the breeding habitat of final stage male and female larvae, derived from the same annual generation, was recorded at very different times of the year. The total lifespan of males was shown to be twice that of females.
The larvae, temporary ectoparasites of estuarine fish, and the non-feeding, burrow-living adults are described and categorized into several developmental phases, whose numbers were recorded during the course of the study.
The annual production of larvae during a limited period in the autumn, and the subsequent settlement of final stage larval females and males the following year, were monitored. Larval females entered the burrows of adult males in the spring to breed, and died after releasing viviparous broods in the autumn. Larval males settled later in the summer, reaching adulthood in the autumn and overwintering before breeding some 18 months after their birth and dying at the end of the breeding season. Adult males thus bred with females from the next generation. The differences in male and female life cycles led to great seasonal variations in adult sex ratios, a huge winter bias towards males contrasting with a brief excess of females in the summer.     

Neuroendocrine regulation of seasonal morph development in a bivoltine race (Daizo) of the silkmoth, Bombyx mori L

We investigated the neuroendocrine regulation of the development of seasonal morphs in a bivoltine race (Daizo) of the silkmoth, Bombyx mori, by decerebration, the transplantation of brain-suboesophageal ganglion (Br-SG) complexes and the injection of active neuropeptides. When brains were removed from fresh pupae destined to develop into summer morphs (SD pupae) by embryonic and larval exposures to short days at low temperature, the pupae developed into autumn or intermediate morphs. However, in pupae destined to develop into autumn morphs (LD pupae), the operation did not show an effect on seasonal morph development. Br-SG complexes were excised from fifth-instar LD and fifth-instar SD larvae 2 days after larval ecdysis and were transplanted into the abdomen of SD larvae of the same age. The Br-SG complexes of LD larvae, but not the Br-SG complexes of SD larvae, shifted the host's seasonal morph development toward the autumn morph. Furthermore, when treated with crude pupal SGs extract and diapause hormone (DH), fresh SD pupae developed into autumn or intermediate morphs, respectively. Possibly the development of seasonal morphs in the silkmoth, B. mori, is regulated by a novel function of DH. Alternatively, DH may act on the imaginal wing disks at an earlier stage than on the ovaries.     

Population biology of Camallanus oxycephalus Ward and Magath, 1916 (Nematoda: Camallanidae) in white bass in western Lake Erie.

The distribution and abundance of the nematode Camallanus oxycephalus infecting white bass, Morone chrysops, in western Lake Erie was studied for over 2 years. Infection was generally more frequent and of higher intensity in large fish. The frequency distributions of nematode abundance in all segments of the fish population followed the negative binomial distribution. The data show seasonal cycles in population structure, site selection, intensity of infection, maturation, and reproduction. Infection occurs during July and August with a resulting peak in population density; during late summer and autumn, mortality, probably density-dependent, reduces the population by 30 to 60%; surviving worms are eliminated at 1 year of age. Growth and development of female worms is arrested from November to April, then proceeds at a rapid rate until the worms release their larvae and die. This growth pattern is probably related to temperature but may also involve host hormone cycles. The dispersal period of the nematode coincides with the annual maximum density of the intermediate host, a cyclopoid copepod,and is interpreted as an adaptation which increases the probability of successful transmission. Because the number of larvae produced by each female worm is a function of body volume, natural selection has favored rapid spring growth and attainment of large body size relative to the male worm. Both seasonal timing in the life cycle and the number of larvae produced are important factors in determining the abundance of this and perhaps other parasites. Evidence is presented suggesting that fluctuations of environmental parameters may disrupt the timing of transmission and alter the distribution and abundance of the parasite. It is hypothesized that the magnitude of such changes in parasite abundance may be related to the complexity of the host-parasite system.     

Seasonal cycles in the output of first stage larvae of the nematode Elaphostrongylus rangiferi from reindeer,Rangifer tarandus tarandus

Summary The output of first stage larvae of the neurotrophic nematode Elaphostrongylus rangiferi was studied both in a herd of reindeer in the field and in reindeer held in captivity. There was a marked seasonal cycle in the output of larvae from infected reindeer. This seasonal cycle is dependent on host sex. After an initial phase of logarithmic increase from the onset of patency in late winter/spring, the larval output declines to a minimum in summer in both female and male reindeer. From then onwards a yearly cycle is repeated with a maximum density of larvae in autumn/early winter from male reindeer, and in late winter/spring from female reindeer. E. rangiferi has an adult longevity of several years in the reindeer, and it is probable that the seasonal cycle of parasite output is linked to seasonal changes in the degree of host stress.     

Seasonal transmission ofRaphidascaris acus (Nematoda), a parasite of freshwater fishes,in definitive and intermediate hosts

Synopsis The seasonal transmission ofRaphidascaris acus was studied in two small lakes on Manitoulin Island, Ontario. Dragonfly nymphs and caddisfly larvae, acting as paratenic hosts, contained second-stage larvae. Several fishes, including percids and cyprinids, were intermediate hosts with second, third, and fourth-stage larvae in the liver. Yellow perch,Perca flavescens, was the most important of these. Intensities were up to 928 and increased with length and age of the perch; prevalence was 100%. Abundance ofR. acus tended to be higher in females but was not related to condition of the perch. Second-stage larvae were acquired from invertebrates in summer and developed to the fourth stage by November. They became surrounded by fibrous capsules during the next summer but remained alive for at least another year. The longevity of larvae in the intermediate host may ensure survival of the parasite through periods of low host abundance after winterkill. Northern pike,Esox lucius, was the definitive host. Abundance ofR. acus tended to be greater in larger pike but was not related to sex or condition of the fish. The parasite was acquired in late fall. Prevalence was 100% and mean intensities were over 200 in winter and spring, declining to 64–100% and less than 15, respectively, in summer. Mature worms were present from early spring through summer. Seasonality of infection in the definitive host is not attributable to seasonal availability of larvae in perch. Instead it may be controlled by timing of predation on perch and rate of development and longevity of the parasite. Transmission to pike apparently continues in summer. Low intensity may result from low recruitment rate and rapid turnover of the parasite population.     

Seasonal population dynamics of Paraquimpevia tenevvima (Linstow) (Nematoda) in the European eel Anguilla anguilla (Linnaeus) in three localities of southwest England

Seasonal population dynamics of Puraquzmperia tenerrima (Linstow) in the European eel Anguillu anguillu (Linnaeus) have been investigated in three localities in Devon, southwest England. The nematode is common and exhibits very similar seasonal patterns in changes of prevalence and abundance in the three localities. The population increases over winter through to late spring or early summer as the recruitment of the new generation occurs throughout this period. Reproduction of the nematode starts in spring. A sharp decrease of prevalence and abundance accompanies or follows reproduction, and infection levels are very low in autumn and early winter. The dispersion pattern of the nematode varies with the infection levels from over-dispersion in spring and early summer to almost random dispersion in autumn and winter. It is suggested that P. tenerrimu is a common specific parasite of eels, especially in small streams or rivers and that insect larvae or species of crustaceans might serve as intermediate hosts for the nematode.     

Epidemiology of sheep infection by Oestrus ovis in Algeria

313 sheep were examined in 1996 to assess the importance and seasonal evolution of Oestrus ovis infection in the Algerian region of El-Tarf. Prevalence was found to be 67.4%. The larval burden was 18 larvae by infected sheep. The prevalence was higher in older sheep than in lambs; intensity was similar. The different larval stages were found all along the year in sheep with prevalence ranging from 33.1 to 80.5% for L1, 9.7 to 43.9% for L2 and 8.4 to 23.0% for L3. The sheep were the least infected in winter (prevalence from 35.7 to 44% and intensity seven to ten larvae per sheep). The highest infection was found during the warm season (spring to autumn, prevalence from 62 to 90% and intensity ranging from 15 to 25). This larval evolution profile suggested the existence of one long cycle (November-April) and possibly two shorts cycles (May-October). This epidemiological pattern is similar to that in Morocco but was slightly different from the situation in Tunisia where the winter cycle was apparently of lesser importance.     

Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co‐existence with parasites may increase the cost‐effectiveness of defence mechanisms.     

Seasonal occurrence of Ixodes ricinus (Acari) in vegetation and on small mammals in southern Sweden

Seasonal activity of Ixodes ricinus L. was studied with two different sampling methods at three localities in southern Sweden: blanket dragging in vegetation and collection from small mammal hosts (mainly larvae in the latter case). The blanket method yielded all development stages. The seasonal pattern - bimodal, with one peak in spring and another in autumn – was clearer for larvae collected on small mammals. The nymphs had a similar seasonal activity pattern as the larvae, but nymphal activity usually started somewhat earlier in spring. Adults had three activity peaks – spring, summer and autumn – in the vegetation.
The autumn peak seems similar to that found in other European countries, but the timing of the spring peak differs. Weather, influencing development rates, seems to be the main agent behind these differences, since ambient weather (above a certain threshold) cannot explain the patterns. Abundance and activity of hosts (different hosts for different developmental stages) probably also plays a certain role.     

The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.)

The introduction, establishment and subsequent history of a population of Ligula intestinalis in roach, Rutilus rutilus , of a small lake was studied over a period of seven years. The introduction is believed to be a natural, chance colonization achieved by the return of Great Crested Grebes as permanent residents. Within two years the parasite had infected 33% of the roach between 60–120 mm in size. It exhibited a pronounced seasonal cycle in infection. Fish were often infected when only a few months old in autumn, and young fish and parasites over-wintered together. Parasite growth resumed in the following summer, when some further infections occurred. The majority of infected fish died in or before their second winter, possibly as a result of selective predation, but a small proportion survived into a third year. Dispersion of the parasite was close to random for most of the time. Multiple infections and slight over-dispersion occurred only in summer months. Infections were scarcer in large fish, due partly to selective mortality of infected fish and partly to a change in the host diet. The pattern of seasonal infection compared favourably with other localities, but prevalence and intensity of infection were consistently lower, parasite dispersion closer to random and multiple infections much scarcer than elsewhere. Infection levels and parasite growth rates varied from year to year, but these annual fluctuations were irregular and showed no consistent pattern. The Ligula population exhibited both regulatory and destabilizing features and there was no definite evidence that it was stable. It is suggested that Ligula is an opportunist species. It is endemic in some sites but in others, especially small lakes, the populations are unregulated and unstable and so persist for short periods only in a non-equilibrium state.