Parasitism and Shoal Size in Juvenile Sticklebacks: Conflicting Selection Pressures from Different Ectoparasites?

In gregarious animals, group size correlates negatively with infection levels by some kinds of parasites and positively with infection by others. Conflicting selection pressures can be exerted simultaneously on a host species by different parasite species. Among stationary, mixed-species shoals of juvenile threespine sticklebacks, Gasterosteus aculeatus , and blackspotted sticklebacks, Gasterosteus wheatlandi , shoal size correlated differently with levels of infection by two species of ectoparasites. Stickleback shoal size correlated positively with infection levels by the copepod Thersitina gasterostei , which is transmitted among fish by short-lived planktonic larvae. In contrast, infection levels by the highly mobile crustacean parasite Argulus funduli did not decrease as shoal size increased, as predicted from an earlier laboratory experiment. The species composition of the different stickleback shoals also had an influence on some aspects of infection by these two parasite species. The contrasting mode of transmission of the two parasites results in one parasite species having a higher transmission rate among fish within large shoals, whereas the success of the other parasite species is independent of fish shoal size. The two ectoparasites may thus exert different selection pressures on stickleback shoal sizes.     

Quantitative effects of three species of parasites on a population of Three-spined sticklebacks, Gasterosteus aculeatus

The effects of Schistocephalus solidus, Diplostomum gasterostei and Echinorhynchus clavula on a population of Three-spined sticklebacks from a pond in Somerset were studied. Schistocephalus was present at the highest level of infection and had the greatest effects on the sticklebacks. It caused the fish to weigh less than uninfected ones of the same length, as shown by the lower condition factor, and to grow more slowly; and it delayed the sexual maturation of fish of both sexes and prevented many from breeding. Diplostomum also had a significant effect on the condition of the sticklebacks and all three parasite species probably caused death or predation of heavily infected fish. The quantitative effects of the parasites on the condition, length and weight of the fish were calculated; seasonal changes in the condition factor could then be seen, and the growth rates for both length and weight calculated.     

Metazoan parasites of sticklebacks on Sable Island, Northwest Atlantic Ocean: biogeographic considerations

Three species of sticklebacks ( Apeltes quadracus, Gasterosteus aculeatus , and Pungitius pungitius ( n = 236) were collected from five ponds on Sable Island. The nematodes Pseudoterranova decipiens, Contracaecum sp., Paracuaria adunca , and Cosmucephalus obvelatus , and the cestode Diphyllobothrium ditremum parasitized three-spined sticklebacks ( G. aculeatus ) and four-spined sticklebacks ( A. quadracus ) inhabiting four brackish water ponds. All the parasites except P. decipiens infected nine-spined sticklebacks ( P. pungitius ) from a freshwater pond. In addition, the cestode Schistocephalus pungitii , the copepod Thersitina gasterostei , and the monogenean Gyrodactylus canadensis occurred in nine-spined sticklebacks from the freshwater pond. The two cestodes, the copepod, and the sealworm, P. decipiens , were the most common parasites encountered. The remaining helminths were relatively rare. Most of the parasite species were larval forms which use gulls or seals as definitive hosts. These parasites probably colonized Sable Island with their definitive hosts, whereas only two species ( T. gasterostei and G. canadensis ) successfully colonized the island ponds with their fish hosts. The low parasite species richness encountered is attributed to the impoverished nature of the host fauna of Sable island, and the difficulty of colonization as a result of the island's isolation with respect to the mainland.     

Interactions among co-infecting parasite species: a mechanism maintaining genetic variation in parasites?

Individuals of free-living organisms are often infected simultaneously by a community of parasites. If the co-infecting parasites interact, then this can add significantly to the diversity of host genotypexparasite genotype interactions. However, interactions between parasite species are usually not examined considering potential variation in interactions between different strain combinations of co-infecting parasites. Here, we examined the importance of interactions between strains of fish eye flukes Diplostomum spathaceum and Diplostomum gasterostei on their infectivity in naive fish hosts. We assessed the infection success of strains of both species in single-strain exposures and in co-exposures with a random strain of the other species. Parasite infection success did not consistently increase or decrease in the co-exposure treatment, but depended on the combinations of co-infecting parasite strains. This disrupted the relative infectivity of D. spathaceum strains observed in single-strain exposures. The infection success of D. gasterostei strains was independent of exposure type. These results suggest that interactions among parasite species may be strain specific and potentially promote maintenance of genetic polymorphism in parasite populations.     

The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch

Incidence, intensity and frequency distributions of infections in perch, Perca fluviatilis , with the eyeflukes Tylodelphys clavata and Diplostomum gasterostei were studied in a lake at monthly intervals over a period of two years. T. clavata had appeared in the lake immediately prior to the study, and its levels of infection continued to rise throughout the period of investigation whereas those of D. gasterostei remained relatively steady. The main period of infection of fish by both species of parasites was late summer, but a second and minor infection took place in spring. In the first year after its introduction T. clavata exhibited a seasonal cycle in incidence and intensity of infection and disappeared from fish in summer, but in the second year this cycle was masked by increased variation in development times and lack of synchrony throughout the parasite population. It is concluded that T. clavata has a life span of one year or less and that the parasites die within the fish, mainly in summer. D. gasterostei in contrast has a life span of at least one year, and disappearance of the parasite from the population is probably due to death of some heavily infected fish, although it was not possible to determine if this was due directly to the presence of the parasite.     

Infectivity of two nematode parasites, Camallanus lacustris and Anguillicola crassus, in a paratenic host, the three-spined stickleback Gasterosteus aculeatus

Three-spined sticklebacks Gasterosteus aculeatus are frequent paratenic hosts of the nematode parasites Anguillicola crassus and Camallanus lacustris. As paratenic hosts, sticklebacks could spread infection by carrying high numbers of infective stages. In contrast, low infective ability of either parasite for the paratenic host could hinder the spread of infection. In the present study, G. aculeatus was, for the first time, infected under controlled laboratory conditions with defined doses of the parasites. Sticklebacks were exposed to 6, 12, 18 and 24 parasite larvae to determine the infective ability of the 2 nematode species. There were significantly higher infection rates for C. lacustris (18 to 49%) than for A. crassus (4 to 14%) at each exposure dose. In C. lacustris-infected sticklebacks, infection rates tended to be highest after exposure to 12 C. lacustris larvae and lowest after exposure to 24 parasites. In A. crassus-infected sticklebacks, no effect of parasite exposure dose on infection rates was observed. Immunity parameters such as respiratory burst activity and lymphocyte proliferation of head kidney leukocytes recorded 18 wk post exposure were not significantly affected by either parasite or exposure dose. Granulocyte:lymphocyte ratios were elevated only within the stickleback group showing the highest infection intensity of C. lacustris, i.e. to those exposed 18 parasites.     

Reciprocal Interaction Matrix Reveals Complex Genetic and Dose-Dependent Specificity among Coinfecting Parasites

Abstract Understanding genetic specificity in factors determining the outcome of host-parasite interactions is especially important as it contributes to parasite epidemiology, virulence, and maintenance of genetic variation. Such specificity, however, is still generally poorly understood. We examined genetic specificity in interactions among coinfecting parasites. In natural populations, individual hosts are often simultaneously infected by multiple parasite species and genotypes that interact. Such interactions could maintain genetic variation in parasite populations if they are genetically specific so that the relative fitness of parasite genotypes varies across host individuals depending on (1) the presence/absence of coinfections and/or (2) the genetic composition of the coinfecting parasite community. We tested these predictions using clones of fish eye flukes Diplostomum pseudospathaceum and Diplostomum gasterostei. We found that interactions among parasites had a strong genetic basis and that this modified genetic variation in infection success of D. pseudospathaceum between single and multiple infections as well as across multiply infected host individuals depending on the genetic identity of the coinfecting D. gasterostei. The relative magnitude of these effects, however, depended on the exposure dose, suggesting that ecological factors can modify genetic interactions between parasites.     

Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation,host adaptation,or side effect?

Parasitic infections may cause alterations in host life history, including changes in reproductive investment (absolute amount of energy allocated to reproduction) and reproductive effort (proportion of available energy allocated to reproduction). Such changes in host life history may reflect: 1) a parasite tactic: the parasite adaptively manipulates energy flow within the host so that the host is induced to make a reduction in reproductive effort and reproductive investment, making more energy available to the parasite; 2) no tactic: there is no change in host reproductive effort and reproductive investment simply decreases as a side effect of the parasite depleting host energy stores; 3) a host tactic: the host adaptively increases reproductive effort in the face of infection and loss of body condition, reproductive investment possibly being reduced despite the increased reproductive effort. Females in Alaskan lake populations of threespine sticklebacks ( Gasterosteus aculeatus ) are capable of clutch production when parasitized by the cestode Schistocephalus solidus despite large relative parasite masses. We analyzed the somatic energy reserves, maturation stage and ovarian mass of female sticklebacks collected from an Alaska lake during a single reproductive season. We found that parasitized females were less likely to carry fully-matured gametes, had smaller ovarian masses, and had lower somatic energy stores than unparasitized females. The relationship between reproductive investment and energy storage did not differ between parasitized and unparasitized females. Thus, reproductive effort did not change in response to parasitic infection. We conclude there was no indication of either a parasite tactic or a host tactic. Simple nutrient theft is involved in the parasite's influence on host reproduction, consistent with an earlier hypothesis that reproductive curtailment in threespine sticklebacks is a side effect.     

Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host

The cestode Schistocephalus solidus is a frequent parasite of three-spined sticklebacks and has a large impact on its host's fitness. Selection pressure should therefore be high on stickleback defence mechanisms, like an efficient immune system, and also on parasite strategies to overcome these. Even though there are indications for manipulation of the immune system of its specific second intermediate host by the cestode, nothing is yet known about the chronology of specific interactions of S. solidus with the stickleback immune system. We here expected sticklebacks to first mount an innate immune response directly post-exposure to the parasite to clear the infection at an early stage and after an initial lag phase to upregulate adaptive immunity. Most interestingly, we did not find any upregulation of the specific lymphocyte-mediated immune response. Also, the pattern of activation of the innate immune system did not match our expectations: the proliferation of monocytes followed fluctuating kinetics suggesting that the parasite repeatedly installs a new surface coat not immunogenic to the host. Furthermore, the respiratory burst activity, which has the potential to clear an early S. solidus infection, was upregulated very late during infection, when the parasite was too big to be cleared but ready for transmission to its final host. We here suggest that the late activation of the innate immune system interferes with the neuroendocrine system, which mediates reduced predation avoidance behaviour and so facilitates the transmission to the final host.     

Parasitism, oddity and the mechanism of shoal choice

When choosing between shoals differing in Schistocephalus solidus infection status, uninfected test sticklebacks Gasterosteus aculeatus showed a preference for joining uninfected conspecifics when shoal sizes were equal, but reversed this preference when the relative size of the infected shoal was increased by a factor of 3. When given a choice between a shoal composed of size-matched minnows Phoxinus phoxinus and a shoal composed of the same number of all uninfected or all S. solidus -infected sticklebacks, test fish always preferred the sticklebacks, regardless of their infection status, over the minnow shoal. These observations suggest that species, parasite status and shoal size are all of importance when fish decide which shoal to join.     

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.     

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.     

Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes

Freshwater populations of three-spined sticklebacks (Gasterosteus aculeatus) in northern Germany are found as distinct lake and river ecotypes. Adaptation to habitat-specific parasites might influence immune capabilities of stickleback ecotypes. Here, naive laboratory-bred sticklebacks from lake and river populations were exposed reciprocally to parasite environments in a lake and a river habitat. Sticklebacks exposed to lake conditions were infected with higher numbers of parasite species when compared with the river. River sticklebacks in the lake had higher parasite loads than lake sticklebacks in the same habitat. Respiratory burst, granulocyte counts and lymphocyte proliferation of head kidney leucocytes were increased in river sticklebacks exposed to lake when compared with river conditions. Although river sticklebacks exposed to lake conditions showed elevated activation of their immune system, parasites could not be diminished as effectively as by lake sticklebacks in their native habitat. River sticklebacks seem to have reduced their immune-competence potential due to lower parasite diversity in rivers.     

Diel vertical movements,and effects of infection by the cestode <Emphasis Type="Italic">Schistocephalus solidus</Emphasis> on daytime proximity of three-spined sticklebacks <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis> to the surface of a large Alaskan lake

We conducted a field study in Iliamna Lake, Alaska, to test the hypothesis that proximity of three-spined sticklebacks Gasterosteus aculeatus to the lake’s surface during the daytime varies with macroparasitic cestode parasite Schistocephalus solidus infection in a manner consistent with enhanced vulnerability to avian predators. Extensive sampling in the lake and likelihood-based modeling revealed that sticklebacks displayed a diel vertical migration, being closer to the surface at night than during the evening and early morning. Additional sampling, also coupled with a likelihood-based modeling approach, showed that fish caught at the surface of the lake during the day were more often parasitized (76 vs. 65%), more heavily parasitized (26.8 vs. 22.7% of their body mass), and had larger individual parasites (0.24 vs. 0.20 g) than those caught at night. Parasite infection was related, non-linearly, to fish size, which also differed between day and night sampling at the surface. We performed statistical competitions among nested hierarchies of models that accounted for this effect of length. The most likely models indicated that fish captured during the day had greater parasite prevalence, higher parasite burdens, and larger parasites than did fish captured at night. Proximity to the surface during the day in this very clear lake would likely increase the vulnerability of sticklebacks to predation from birds, enabling completion of the parasite’s lifecycle.     

Dispersion patterns of parasites in 0+ year three-spined sticklebacks: a cross population comparison

Two ciliates and 16 metazoan parasites were identified in 434 0+ year three-spined sticklebacks Gasterosteus aculeatus collected from two small rivers and four lakes located in Schleswig-Holstein, Germany. By repeated sampling and analysis of dispersion patterns of six frequently occurring parasites no consistent evidence was found for mortality induced by a single parasite species. Linear log-variance to log-mean abundance ratios with slopes of c. 2 indicated negative binomial distributions for five of the six parasites. The numbers of these six parasites were combined as multiples of S.D. of each parasite species over all samples to form an 'individual parasitation index' ( I _PI), which showed that only in one locality a slight decrease in parasite burden occurred between September and April. In two of the lake populations, however, there was a distinct decline in the degree of dispersion in spring samples. This indicates that a combination of different species might cause parasite-induced host mortality, undetectable by patterns obtained from single species. There were differences in parasite diversity and intensity of infection among river compared to lake populations suggesting a role for parasites as selective agents in the ecological divergence of three-spined sticklebacks.     

A non-invasive morphometric technique for estimating cestode plerocercoid burden in small freshwater fish

A non-invasive morphometric technique is presented which can be used to predict the infection status and the proportion of infected fish weight contributed by parasite tissue in three-spined sticklebacks Gasterosteus aculeatus infected with plerocercoids of Schistocephalus solidus (Cestoda: Pseudophyllidea)     

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.     

MHC genes and oxidative stress in sticklebacks: an immuno-ecological approach

Individual variation in the susceptibility to infection may result from the varying ability of hosts to specifically recognize different parasite strains. Alternatively, there could be individual host differences in fitness costs of immune defence. Although, these two explanations are not mutually exclusive, they have so far been treated in separate experimental approaches. To analyse potential relationships, we studied body condition and oxidative stress, which may reflect costs of immunity, in three-spined sticklebacks that had been experimentally exposed to three species of naturally occurring parasite. These sticklebacks differed in a trait, which is crucial to specific parasite defence, i.e. individual genetic diversity at major histocompatibility complex (MHC) class IIB loci. Oxidative stress was quantified as tissue acrolein, a technique that has been applied to questions of immuno-ecology for the first time. We measured gene expression at the MHC and other estimates of immune activation. We found that fish with high levels of MHC expression had poor condition and elevated oxidative stress. These results indicate that MHC-based specific immunity is connected with oxidative stress. They could, thus, also be relevant in the broader context of the evolution of sexually selected signals that are based on carotenoids and are, thus supposed to reflect oxidative stress resistance.     

A comparison of the behavioural responses of parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia

Eighty sticklebacks (32 parasitized, 48 uninfected) were subjected to a serial reduction in dissolved oxygen (DO) concentration until they showed continuous aquatic surface respiration for longer than 10s (> 10s ASR). An analysis of results showed that (1) parasitized adult male and female sticklebacks reacted to low DO significantly earlier than non-parasitized controls; (2) severity of parasite infection was significantly correlated with DO at which > 10s ASR occurred; (3) gravid, non-parasitized females show ASR at a relatively high DO, with a threshold response similar to that of parasitized fish.
It is suggested that the metabolic respiratory demand of the parasitic tapeworm larvae causes the stickleback to modify its behaviour at lowered DO. This behavioural modification causes the fish to surface, where they are likely to be at risk from predatory birds. Field data on DO levels at the study site show that environmental conditions in the shallow lake margins approach the range required to affect the behaviour of heavily parasitized sticklebacks.