Intensity-dependent alteration of minnow (Pimephales promelas) behavior by a brain-encysting trematode

We examined the relationship between the numbers of brain-encysting trematodes (Ornithodiplostomum ptychocheilus) and the magnitude of altered behaviors in fathead minnows (Pimephales promelas). Because cysts develop within a brain region that integrates visual stimuli with motor response. we evaluated the standard optomotor response (OMR). Monitoring this task involved recording the time minnows spent following a spinning drum, on which alternating black and white stripes had been painted. Minnows were exposed to 0, 5, 20, 120, and 300 cercariae and then their OMR was evaluated at 2-wk postinfection. Surprisingly, only minnows that had high numbers of parasites (155 +/- 31 worms/fish) or low numbers of parasites (3 +/- 3 worms/ fish) differed significantly in their optomotor performance compared with controls. Reduced OMR of heavily infected minnows was positively correlated with reduction in minnow activity. In contrast, reduced OMR in lightly infected minnows was independent of host activity and was likely associated with the rapid development of parasite larvae within the optic tecta. The nonlinear relationship between parasite intensity and effect on host behavior was consistent with an earlier study, but the underlying mechanisms producing this pattern are unknown.     

Changes in minnow, Pimephales promelas Rafinesque, schooling behaviour associated with infections of brainencysted larvae of the fluke, Ornithodiplostomum ptychocheilus

The schooling behaviour of unparasitized fathead minnows, Pimephales promelus Rafinesque, was compared to that of minnows infected with brain-dwelling metacercariae of the fluke, Ornithodiplostomum ptychocheilus (Faust). Laboratory results showed that schools of infected fish divided more frequently, were less compact, and occupied positions closer to the water surface than control schools. These results are discussed with reference to the possibility that this larval parasite manipulates minnow behaviour to increase host vulnerability to predation.     

Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas)

Intensity-dependent development of Ornithodiplostomum ptychocheilus metacercariae was studied in fathead minnows (Pimephales promelas) exposed to 0, 20, or 120 cercariae. Subsamples of hosts were necropsied at 2-wk intervals to monitor parasite recruitment, growth, and time to encystment. The complex development of metacercariae within the cranium of minnows involved growth, encystment, and consolidation phases, each of which were affected by intensity. At the end of the growth phase, metacercariae from low-dose fish were 20% longer than those from high-dose fish and the latter took 2-4 wk longer to encyst. At the end of the postencystment consolidation phase (6-8 wk postinfection), the size of metacercariae decreased by approximately 50%. The rate of consolidation was slower in high-dose fish. Our results show that time, intensity, and temperature affect development of O. ptychocheilus. Because metacercariae development and differentiation are linked to infectivity, events occurring in intermediate hosts can potentially impact the structure and size of trematode suprapopulations.     

Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows

Metacercariae of the trematode Ornithodiplostomum ptychocheilus cause a conspicuous enlargement of the cranium of juvenile fathead minnows (Pimephales promelas). Minnows sampled from 2 naturally infected ponds in northern Alberta, Canada, had 12% higher and 7% wider craniums compared to fish from an adjacent, uninfected pond. We tested the prediction that cranial distortion was caused by encystment of metacercariae on the brains of slow-growing minnows in a factorial experiment. Juvenile fish were either exposed once to 120 cercariae or 3 times to 40 cercariae; they were then fed either a low- or high-quantity diet for 8 wk. Results showed that after controlling for host size, cranial heights were affected by infection regime and host diet but not by the infection x diet interaction. Cranial distortion was most prominent in minnows exposed once to cercariae, showing that the rapid, simultaneous growth of metacercariae interfered with the normal development of the cranium. Thus, the expression of the parasite-induced phenotype was context dependent, the result of factors associated with the dynamics of cercariae transmission and host growth rate.     

Comparative life histories of two diplostomid trematodes, Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum

A lack of comparative studies limits our understanding of interspecific variation in parasite life histories, especially for species that incorporate asexual and resting stages into their life cycles. Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum are sympatric diplostomid trematodes that share the same first (pond snail, Physa gyrina) and second (fathead minnow, Pimephales promelas) intermediate hosts within lakes in Alberta, Canada. Interspecific differences in the body sizes of adults, cercariae, and metacercariae were evaluated from parasites recovered from laboratory-raised chickens, snails, and minnows, respectively. Differences in adult worm fecundity and cercariae production were estimated from chickens and snails exposed to known numbers of parasite larvae. Posthodiplostomum minimum adults, metacercariae, and eggs were 97, 86, and 5% larger than those of 0. ptychocheilus, respectively. The average numbers of eggs produced per day by P. minimum was 3 times higher than for O. ptychocheilus, and P. minimum produced approximately twice as many cercariae per day. Although the larger of the 2 species had higher egg and cercariae production, conclusions regarding covariation between adult worm size and the reproductive rates of other life cycle stages require further studies on related species.     

Population dynamics of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas) from four northern-Alberta lakes

Annual, seasonal, and interlake variation in prevalence and intensity of Ornithodiplostomum ptychocheilus (Faust) metacercariae was assessed in populations of fathead minnows (Pimephales promelas) collected from 4 lakes in north-central Alberta. Mean metacercariae intensity in young-of-the-year minnows varied extensively (5-123 metacercariae/host) among year, month, and lakes. In 2 of the lakes, prevalence always reached 100%, and mean intensity always peaked in September or October. The high spatial and annual variation in metacercarial recruitment was partly attributable to variation in host size. but variation in water depth, temperature, snail densities, and bird visitation likely also played a role. A laboratory experiment demonstrated that host and metacercariae survival was intensity-independent during a period of simulated winter. Thus, metacercariae recruited in the fall survive until the following spring.     

Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda)

Because resistance to parasites usually has a cost for host species, it is theoretically expected that, in case of multi-infection, host immune responses should vary according to the levels of parasite pathogenicity. The crustacean gammarid Gammarus aequicauda is the second intermediate host of 4 trematode species. Three of these parasites always encyst in the abdomen of gammarids and have no particular effect on the host. However, 1 of these species is sometimes able to encyst in the cerebroid ganglia of the gammarid and strongly alter its behavior in a way that increases its predation risk by aquatic birds, the definitive hosts. In accordance with the hypothesis that the level of parasite pathogenicity influences the likelihood and the degree of host reaction, cases of melanization in our gammarid collection almost exclusively concern the cerebral metacercariae. Our results also indicate that this melanization is able to cancel the behavioral alterations induced by the parasite, suggesting that the cause of the manipulation is not the physical presence of metacercariae in the brain.     

Biology of the minnow Phoxinus phoxinus and its interactions with brown trout Salmo trutta in Øvre Heimdalsvatn, Norway

Minnows have recently been introduced into the mountain lakes of southern Norway. In Øvre Heimdalsvatn, an intensively studied lake, the minnow population has increased rapidly during the last decade. Studies were performed on feeding habits, habitat preferences, age, growth, energy content, densities, parasites, predation and spawning activities. Several aspects were found to be different from other studies, e.g. higher age of sexual maturation, lower growth rate, no feeding on plants, and low infection of parasites. The interaction with the only other fish, the brown trout, is discussed in relation to the minnow population. In 1978 the minnows constituted little more than 10% of production and food consumption of the trout population, and only limited food competition and predation was documented. Increasing competition is likely with a greater minnow population.     

Infectivity of Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum (Trematoda: Diplostomidae) cercariae following exposure to cadmium

The effect of cadmium (Cd) exposure on infectivity of cercariae of 2 trematode species (Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum) to their second intermediate fish host was evaluated. Individual fathead minnows (Pimephales promelas) were exposed to cercariae that had been treated with Cd solutions at concentrations of 0, 2, 20, or 200 microg/L for 2 hr. Two weeks later, the numbers of encysted metacercariae in the brain (O. ptychocheilus) and body cavity (P. minimum) of the fish were evaluated. ANOVA analyses indicated a strong negative effect of Cd concentration on cercaria infectivity. The species x Cd concentration interaction was not significant, indicating that the magnitude of Cd-induced reduction in infectivity was similar between O. ptychocheilus and P. minimum. The results show that short-term exposure to Cd, even at low concentrations, interferes with transmission processes that affect the recognition and penetration of cercariae, the migration and survival of metacercariae within the second intermediate host, or both.     

Histopathological and ultrastructural observations of metacercarial infections of Diplostomum phoxini (Digenea) in the brain of minnows Phoxinus phoxinus

The spatial distribution and histopathological changes induced by metacercariae of the digenean trematode Diplostomum phoxini (Faust, 1918) in the brains of European minnows Phoxinus phoxinus (L.) from the River Endrick, Scotland, were studied by light and electron microscopy. Post-mortem examination of a sample of 34 minnows revealed that 50% (n = 17) of the population was infected with 13.7 +/- 2.6 (mean +/- SE; range 1 to 38) metacercariae per infected host. Serial histological sections of the infected minnow brains revealed that the metacercariae were unevenly distributed throughout the brain, with aggregations occurring in the cerebellum, the medulla oblongata and the optic lobes. In fish with highest intensities of infection, over 40% of the cerebellar area and about 30% of the medulla oblongata area were occupied by larvae. Metacercariae disrupt the integrity of brain tissue, with individuals being found in small pockets surrounded by cellular debris. Metacercariae were rarely encountered on the surface of the brain. Electron microscopic examination of infection sites revealed that the granular layer surrounding metacercariae was necrotic, exhibited nuclear degradation and was marked by vacuolation of the cytoplasm. Rodlet cells, the only inflammatory cell types recorded in this study, were found only in parasitized brains and in close proximity to the teguments of metacercariae. It is hypothesised that secretions released from the teguments of metacercariae are a counter response to protect the metacercariae from the fish brain's cellular defence mechanisms.     

Cellular aspects of early development of Ornithodiplostomum ptychocheilus metacercariae in the brain of fathead minnows, Pimephales promelas

Trematode metacercariae typically are regarded as nonfeeding and metabolically inactive. However, the metacercariae of many trematode species undergo complex and prolonged periods of development within their intermediate hosts. In the present study, we used electron microscopy to document chronological changes in development of the tegument of Ornithodiplostomum ptychocheilus metacercariae recovered from the brains of experimentally infected fathead minnows (Pimephales promelas). Commencing at 4 days postinfection (PI), the smooth, thin, syncytial tegument transforms into a complex microlamellar and microvillar system that encircles the entire body surface. The microvilli are oriented in parallel in an extended pattern, reaching directly away from the parasite and toward the receding host tissue. The microvilli disappear at approximately 28 days PI, followed by deposition of the cyst wall and further transformation of the tegument into the spinose, a glandular structure typical of an immature adult. To our knowledge, the progressive disaggregation of host cells at the leading edge of elongating parasite microvilli has not been demonstrated previously for any trematode. These results provide morphological evidence that the metacercariae of some trematode species undergo complex developmental changes associated with feeding in their intermediate host.     

Ecological clustering within a diverse minnow assemblage according to morphological,dietary and isotopic data

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Phenology of recruitment and infection patterns of Ascocotyle pachycystis, a digenean parasite in the sheepshead minnow, Cyprinodon variegatus

In northwest Florida, Cyprinodon variegatus are parasitized by Ascocotyle pachycystis, a digenean parasite that forms metacercarial cysts in the lumen of the bulbus arteriosus. Field experiments revealed that fish accumulated parasites at an uneven rate within the highly seasonal trematode recruitment period. Older (= larger) fish had higher rates of parasite recruitment and higher parasite prevalences and densities (numbers of metacercariae per individual fish) than did younger (= smaller) fish. Nearly all adults were parasitized (prevalence range 70-100%), and parasite densities ranged from zero to 6800 per fish. Parasite distributions were clumped (= aggregated) in fish of all age classes but were less heterogeneous in early juveniles and adults than they were in late juveniles. Parasites affected the population dynamics of sheepshead minnows by causing reduced winter survivorship, as evidenced by an increase in the average size of fish and a decrease in the average infection intensity over the winter. This revised version was published online in July 2006 with corrections to the Cover Date.     

Nonhost species reduce parasite infection in a focal host species within experimental fish communities

The dilution effect describes the negative association between host biodiversity and the risk of infectious disease. Tests designed to understand the relative roles of host species richness, host species identity, and rates of exposure within experimental host communities would help resolve ongoing contention regarding the importance and generality of dilution effects. We exposed fathead minnows to infective larvae of the trematode, Ornithodiplostomum ptychocheilus in minnow‐only containers and in mixed containers that held 1–3 other species of fish. Parasite infection was estimated as the number of encysted worms (i.e., brainworms) present in minnows following exposure. The results of exposure trials showed that nonminnow fish species were incompatible with O. ptychocheilus larvae. There was no reduction in mean brainworm counts in minnows in mixed containers with brook sticklebacks or longnose dace. In contrast, brainworm counts in minnows declined by 51% and 27% in mesocosms and aquaria, respectively, when they co‐occurred with emerald shiners. Dilution within minnow + shiner containers may arise from shiner‐induced alterations in minnow or parasite behaviors that reduced encounter rates between minnows and parasite larvae. Alternatively, shiners may act as parasite sinks for parasite larvae. These results highlight the role of host species identity in the dilution effect. Our results also emphasize the complex and idiosyncratic effects of host community composition on rates of parasite infection within contemporary host communities that contain combinations of introduced and native species.     

Experimental differences in mortality patterns between European minnows, Phoxinus phoxinus, infected with sympatric or allopatric trematodes, Diplostomum phoxini

A factorial experiment was conducted to examine if the digenetic trematode parasite Diplostomum phoxini influences minnow growth and survival negatively and if different parasite populations differ in their effects on hosts. Juvenile full-sibling minnows from a lake located at the northern edge of the Swiss Alps were infected experimentally with D. phoxini from either their own or another lake. When exposed to sympatric parasites, the minnows survived a low and a high infection dose more or less equally, but with allopatric parasites mortality increased with infection dose. Parasites did not reduce host growth and minnows exposed to a low infection dose grew quicker than either non-infected ones or ones exposed to a high infection dose. Thus, the results show different patterns of pathogenicity between two parasite populations and suggest that (1) the observed differences are at least partially genetic and that (2) the co-evolved, sympatric host-parasite association has reached a degree of low pathogenicity. Differences between the findings presented here and those of a previously published study are discussed.     

Clonorchis sinensis metacercarial infection in the pond smelt Hypomesus olidus and the minnow Zacco platypus collected from the Soyang and Daechung Lakes

The pond smelt Hypomesus olidus and minnow Zacco platypus were collected from the Soyang and Daechung Lakes in January 2003, and their metacercarial infections was examined by the muscle compression and artificial digestion techniques. In the Soyang Lake, 161 metacercariae of Clonorchis sinensis (0.35 per fish) were harvested from 459 pond smelts examined. Also, 13 metacercariae of C. sinensis (0.43 per fish), 1 of Metagonimus sp., 4 of Echinostoma sp., 148 of Centrocestus armatus and 44 unidentified species were collected from 30 minnows. In the Daechung Lake, 369 metacercariae of C. sinensis (3.69 per fish) and 51 unidentified species were recovered from 100 pond smelts. The metacercariae of C. sinensis were fed to experimental rats, in which the adult flukes were identified. The pond smelts and minnows collected from the Soyang and Daechung Lakes were verified to be the second intermediate hosts and the sources of human C. sinensis infection.     

Tests of ecological equivalence of two species of terrestrial gastropods as second intermediate hosts of Panopistus pricei (Trematoda: Brachylaimidae)

Metacercariae of Panopistus pricei (Brachylaimidae) are common parasites of 2 species of terrestrial gastropods (Neohelix albolabris; Webbhelix multilineata) in southeastern Nebraska. Field data were collected to determine if individuals of N. albolabris and W. multilineata function as ecologically equivalent second intermediate hosts of P. pricei along a transect on the western edge of the Missouri River. Metacercariae were recovered and measured from samples of 30 snails of each species collected at each of 6 sites; whole kidneys from snails of both species were examined to quantify microhabitat use. Microhabitat use of P. pricei did not differ between host species; in both N. albolabris and W. multilineata, metacercariae were concentrated in the primary ureter and occurred throughout the kidney proper. Prevalences and mean abundances did not differ between host species at any site, nor did the relationship between parasite abundance and host size. Prevalences and mean abundances across sites were positively correlated between host species. At 2 sites, demographics of metacercariae differed between host species, suggesting short-term differences in the history of encounters with cercariae in the environment and differences in transmission to shrew definitive hosts. Overall, N. albolabris and W. multilineata appear to be equivalent and required second intermediate hosts of P. pricei in the area studied.     

Comparison of compensatory growth responses of juvenile three-spined stickleback and minnow following similar food deprivation protocols

The compensatory growth responses of individual juveniles of two co- existing species were compared after identical periods of starvation to determine inter-specific similarities and differences. The carnivorous stickleback Gasterosteus aculeatus was compared with the omnivorous minnow Phoxinus phoxinus. Both species experienced 1 or 2 weeks of starvation before being re-fed ad libitum. The two species differed in their response to the starvation periods, with minnows showing a lower weight-specific loss. Both species showed compensatory responses in appetite, growth and to a lesser extent, growth efficiency. Minnows wholly compensated for 1 and 2 weeks of starvation. At the end of the experiment, sticklebacks starved for 2 weeks were still showing a compensatory response and had not achieved full compensation. The compensatory responses of the sticklebacks showed a lag of a week before developing in the re-feeding phase, whereas the response of the minnows was immediate. Analysis of lipid and dry matter concentrations suggested that the compensatory response restored reserve lipids while also bringing the fish back to the growth trajectory of continuously fed fish.     

Fathead Minnows, Pimephales promelas, Learn to Recognize Chemical Alarm Cues of Introduced Brook Stickleback, Culaea inconstans

In four experiments conducted over a 6-year period, we investigated whether fathead minnows, Pimephales promelas, could acquire the ability to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. A laboratory experiment documented that stickleback-naïve minnows did not exhibit an anti-predator response when exposed to the chemical alarm cues of stickleback. In a laboratory experiment conducted 5 years after the introduction of stickleback to the pond, minnows exhibited an antipredator response to stickleback cues. Moreover, in a field experiment the minnows exhibited avoidance of areas labelled with stickleback alarm cues. Minnows raised from eggs taken from the test pond did not exhibit an anti-predator response to stickleback cues while minnows from the test pond that had experience with stickleback cues did respond to stickleback cues. Our results provide clear evidence that cross-species responses to chemical alarm cues of fishes can be learned. Learned recognition of alarm cues has important implications for predator/prey interactions.     

Timing of Spawning and Host-nest Choice for Brood Parasitism by the Japanese Minnow,Pungtungia herzi,on the Japanese Aucha Perch,Siniperca kawamebari

A field study of the breeding ecology of the Japanese aucha perch, Siniperca kawamebari, and brood parasitism by the Japanese minnow, Pungtungia herzi, on nests of the perch was carried out from 1989 to 1991. Observations of perch nests under natural conditions in 1990 showed that brood parasitism by the minnow was concentrated on host nests in which nest owners had just begun their nesting cycle. When spawned in a perch nest with recently spawned perch eggs, parasite eggs always hatched earlier than host eggs. An experiment with imitation perch eggs in 1991 confirmed that changing colour of host eggs was the cue for the parasites to distinguish between different developmental stages of host eggs. Parasite eggs rapidly disappeared without guarding by a host male (Baba et al. 1990). This loss was caused by predation by fishes. Parasite fry left the nest immediately after hatching, so parasite eggs spawned in a host nest in an early stage should be well guarded until they hatch. In the field, minnows deposited their eggs in perch nests which had larger numbers of newly spawned perch eggs. Since the perch males always deserted their nests when their own eggs disappeared, the parasite's choice of host nests with larger numbers of host eggs may ensure survival of the parasite eggs. The timing of egg deposition and choice of host nest by the minnow appear to be adaptive in terms of brood parasitism on nests of the perch.