Acquired resistance of bluegill sunfish Lepomis macrochirus to glochidia larvae of the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) after multiple infections

The effects of multiple infections on the host-parasite relationship between bluegill sunfish (Lepomis macrochirus) and parasitic glochidial larvae of the freshwater mussel Utterbackia imbecillis were examined. Na?ve, young-of-the-year bluegills were infected with glochidia and placed in individual observation chambers. Each day, water was drained from each chamber and the numbers of dead glochidia, live glochidia, partially metamorphosed glochidia, and fully metamorphosed juvenile mussels were counted. The same fishes were infected a total of 4 times. After 2 infections, the fish began to exhibit evidence of acquired resistance to glochidia. During the third and fourth infections, this resistance was clearly evidenced by the marked increase in the percentage of dead and live glochidia shed during the first 5 days of the infection and by the significant decrease in the success of metamorphosis. The total number of glochidia that successfully attached to the fish decreased significantly during the fourth infection relative to the first. The number of larvae attached to the host fish was positively correlated with the size of the fish during the first infection but was negatively correlated during all subsequent infections. Variance to mean ratios indicated that larvae were aggregated among host fishes during the infections. This study has important implications in propagation and conservation efforts of this endangered group of organisms.     

Influence of cortisol on the attachment and metamorphosis of larval Utterbackia imbecillis on bluegill sunfish (Lepomis macrochirus)

The larvae of unionid freshwater mussels (i.e., glochidia) undergo a parasitic stage requiring their attachment to the external epithelia of fish hosts, where they metamorphose into free-living juveniles. We describe the physiological effects in bluegill sunfish (Lepomis macrochirus) of infection with glochidia from the paper pondshell (Utterbackia imbecillis). Glochidia accumulation on bluegill increased dramatically at concentrations of 2000 glochidia liter(-1) and above, reaching a maximum attachment density of about 30 glochidia g(-1) fish at 4000 glochidia liter(-1). Plasma cortisol was the most sensitive indicator of biological effect to glochidial exposure, increasing significantly in hosts exposed to 2000 glochidia liter(-1) or greater. Glochidia were 31% more likely to undergo successful juvenile metamorphosis when attached to bluegill with elevated plasma cortisol, largely due to the enhanced survivorship of these larvae during the first 48 h after infection. We tested the hypothesis that glochidial attachment and juvenile metamorphosis were stimulated directly by plasma cortisol in fish hosts. Bluegill were given an intraperitoneal injection of cortisol, then infected with 1000 glochidia liter(-1) at 48 h after hormone supplementation. Cortisol-injected fish had a 42% increase in the number of attached glochidia g(-1) fish and a 28% increase in larval metamorphosis compared to sham-injected and control fish. We provide evidence that cortisol enhances glochidial metamorphosis on hosts by improving the retention of attached glochidia. This study gives insights into the influence of host physiology on glochidial attachment and juvenile mussel transformation.     

Survival of glochidial larvae of the freshwater pearl mussel, Margaritifera laevis (Bivalvia: Unionoida), at different temperatures: a comparison between two populations with and without recruitment

The viability of free-living glochidia of the freshwater pearl mussel (Margaritifera laevis) was studied in the laboratory at water temperatures of 10 degrees C, 15 degrees C and 20 degrees C. To obtain glochidia, gravid female mussels were collected from the Chitose River, inhabited by adult and juvenile mussels, and from the Abira River, where only adult mussels were found. Daily survival rates of glochidia from each population at various water temperatures were significantly different, and survival time was longest at the lowest temperature in each population. Maintenance of some field mussel populations might become difficult at higher water temperatures due to the short survival time of glochidia and expected low density of host fish. Daily survival rates of glochidia were compared between the Abira population at 15 degrees C and the Chitose population at 20 degrees C, since these temperatures were close to the mean water temperature during the period of glochidial release in the respective rivers. Daily mean survival rates were significantly different between the Abira population at 15 degrees C and the Chitose population at 20 degrees C. Mean glochidial survival rate for the Chitose population changed from 85.3% to 66.2% from 9 to 13 h, whereas that for the Abira population dropped suddenly from 80.4% to 34.2% from 10 to 14 h after the initiation of experiment. Absence of juveniles in the Abira River might have been caused by the low glochidial viability. Survival times of free-living glochidia in Margaritiferidae tend to be shorter than in other families in Unionoida. A trade-off is suggested between high fertility and low glochidial survival rate in Margaritiferidae.     

Ultrastructural alterations in branchial chloride cells of Atlantic salmon, Salmo salar, during parr-smolt transformation and early development in sea water

The ultrastructure of the gill primary lamellae of juvenile Atlantic salmon was examined during the parr-smolt transformation and for 42 days after smolts were exposed to sea water. Scanning electron microscopy indicated that primary lamellae were characterized by rough convoluted surfaces that became rougher throughout the experimental period and that crypts did begin to form in freshwater fish. Crypt formation increased in sea water.
Transmission electron microscopy indicated that parr preadapt for life in sea water in part by changes in chloride cells. Chloride cells show an elaboration of rough endoplasmic reticulum in fresh water and a decline of rough endoplasmic reticulum after 42 days of sea water exposure. The tubular membrane system becomes well developed in fresh water, and apical vesicles become abundant only after seawater exposure. Mitochondria are both spherical and elongate through the period and contain well developed cristae. No evidence of mitochondrial rupture was observed. The junctions between chloride cells and adjacent cells were characterized in fresh water by long tight junctions with desmosomes. This type of junction continued in sea water and was the norm between chloride cells and accessory cells after 42 days of seawater exposure. While leaky junctions appeared to be forming, no evidence was found of membrane interdigitation between accessory cells and chloride cells after 42 days of seawater exposure. It also appeared that seawater exposure influenced the number of chloride cells exposed to the external milieu.
Pavement cells showed an elaboration in fresh water of free ribosomes and rough endoplasmic reticulum and these elements became less prominent after seawater exposure.     

Mucous cell types in the branchial epithelium of the euryhaline fish Poecilia vivipara

On transfer to sea water for 45 days, the return of appetite was later and growth rates tended to be lower for triploid Atlantic salmon, Salmo salar , reared together with diploid Atlantic salmon. All mortalities comprised of triploid salmon (29%) and were attributable to failed smolt syndrome. No correlation was found between the growth of diploid or triploid fish in fresh water and their subsequent growth on transfer to sea water.     

Site selection and attachment duration of Anodonta woodiana (Bivalvia: Unionacea) glochidia on fish hosts

The relationship between parasitic glochidia of Anodonia woodiana (Unionidae: Anodonti-nae) and potential fish hosts was investigated in the laboratory. Intensity of parasitism was highest on the exotic fish Gambusia affinis , lower on the native species Puntius semijascio-latus and Metzia takakii , and least on Rhodeus sinensis . Glochidia generally attached at fin margins, particularly the pectorals and caudal. In Gambusia affinis , the incidence of glochidia on the pectorals was higher than would be expected on the basis of ratios between fin margin lengths. Apparently, the role of the pectoral fins in locomotion makes them more liable to glochidial contact, thereby increasing their susceptibility to attachment.
The duration of glochidial attachment was shortened as temperatures increased. Mean values ranged from 14-4 days at 15°C to 6 days at 27°C. At 33°C glochidia rapidly detached and metamorphosis was unsuccessful. Significantly, water temperatures in A. woodiana habitats in Hong Kong rarely exceed 30°C.     

A delayed effect of the aquatic parasite <Emphasis Type="Italic">Margaritifera laevis</Emphasis> on the growth of the salmonid host fish <Emphasis Type="Italic">Oncorhynchus masou masou</Emphasis>

Parasitic species often have detrimental effects on host growth and survival. The larvae of the genus Margaritifera (Bivalvia), called glochidia, are specialist parasites of salmonid fishes. Previous studies have reported negligible influences of the parasite on their salmonid hosts at natural infection levels. However, those studies focused mainly on their instantaneous effects (i.e., during the parasitic period). Given the time lag between physiological and somatic responses to pathogen infections, the effect of glochidial infection may become clearer during the post-parasitic period. Here, we examined whether the effect of glochidial infections of Margaritifera laevis on its salmonid host Oncorhynchus masou masou would emerge during the post-parasitic period. We performed a controlled aquarium experiment and monitored fish growth at two time intervals (i.e., parasitic and post-parasitic periods) to test this hypothesis. Consistent with previous observations, the effects of glochidial infection were unclear in the middle of the experiment (day 50; parasitic period). However, even with a natural glochidial load (48 glochidia per fish), we found a significant reduction in growth rates of infected fish in the extended period of the experiment (day 70; post-parasitic period). Our results suggest that examining only instantaneous effects may provide misleading conclusions about mussel–host relationships.     

Return migration of Atlantic salmon in the River Tana: the role of environmental factors

Multi-sea-winter Atlantic salmon (75–115 cm fork length L _F, 2–4-winter fish) were radio-tagged in the Tanafjord (700 N), Norway, in 1992–1993, and 130 fish entered the large subarctic River Tana (Teno). They entered the fresh water at any time of the tidal cycle but more so during the high and ebbing tides. No diel rhythm was detected in river entry under polar day conditions. There were no differences in the change of flow between days when salmon moved and when they did not, but during active migration increasing discharge was associated with increased swimming activity of salmon, especially later in the summer. Increasing air temperature was also associated with enhanced migration activity. Low river flow was associated with increasing delay in salmon passing the first riffle area of the river, 35 km from the sea.     

The effects of hypophysectomy, prolactin therapy and environmental calcium on freshwater survival and salinity tolerance in the brown trout Salmo trutta L.

Hypophysectomy resulted in a loss of ability of the euryhaline salmonid, Salmo trutta to survive in fresh water. The mean survival time was 4–5 days. Maintenance in a medium containing 5 mM calcium increased the mean survival time to 8 days while 10 mM decreased it. Injection of 0–21.U./gm prolactin enabled hypophysectomized fish to survive the 2-week duration of the experiment.
High environmental calcium, or pre-adaptation to a medium of high calcium, increased salinity tolerance of the brown trout probably by promoting a quick return of plasma electrolyte concentration to normal after transfer to sea water.     

Early life stages of exotic gobiids as new hosts for unionid glochidia

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Glochidium metamorphosis in the endangered freshwater mussel Margaritifera auricularia (Spengler, 1793): a histological and scanning electron microscopy study

The metamorphosis of the glochidium of the critically endangered Margaritifera auricularia in the gills of a host is studied here for the first time. Siberian sturgeon, Acipenser baeri, were infected with glochidia and regularly inspected using scanning and optical microscopy. The mature glochidia immediately attach to the epithelium of the sturgeon gill filaments, piercing the secondary lamellae and the connective tissues, blood cells, and vessels within the lamellae. Once the epithelium is pierced, overlapping host lamellae cover the glochidium and form a cyst. Metamorphosis takes place inside the cyst. Sixteen days after infection the glochidium becomes spherical in shape and the larval muscle is reabsorbed. The two adductor muscles of the juvenile are observed 34 days after infection at 16-20 degrees C. Metamorphosis is complete in approximately 51 days at 18-22 degrees C and in 65 days at 16-17 degrees C. Released juveniles have a spherical shell with a thin rim of new shell material and a finely ciliated foot. Juvenile mean measurements are: length = 190 microm, width = 193 microm, and height = 210 microm.     

Ontogenesis of osmotic regulation in the striped mullet, Mugil cephalus L.

The osmoregulatory capabilities of juvenile striped mullet, Mugil cephalus L ., of three size-groups (20–29, 30–39 and 40–9 mm s.l.) were compared in a series of six salinities ranging from fresh water to full sea water. The two smaller size-groups were able to tolerate instantaneous transfer from the brackish water in which captured, to all salinities but fresh water, while the 40–69 mm group were tolerant of instantaneous transfer to all experimental salinities. At high environmental salinities, the osmotic regulatory capabilities improved with growth in size to an apparently definitive condition in fish of 40–69 mm s.l. The smallest of these individuals were estimated to be about 7.5 months old. The osmotic regulatory capability in waters of low salinity had reached a definitive state with the development of tolerance to such salinities. The ontogenetic pattern for Mugil cephalus is virtually identical to that of the Atlantic salmon, Salmo salar .     

Evolutionary-physiological aspects of adaptation of the Pacific salmon fry of the Oncorhynchus genus to migration to the sea water

A complex of adaptive changes occurring in the Pacific salmon fry in the process of migration to the sea is described, including behavior, ion content in carcasses, and morphological changes in Stannius bodies, gill epithelium, and nephron tubular epithelium. Participating in experiments with transfer from fresh water into a two-layer aquarium (the lower layer - sea water, the upper layer - fresh water) were smolts of chum salmon and underyearlings of masu salmon as well as the trachurus and leiurus forms of the three-spined stickleback Casterosteus aculeatus. All fish, regardless of their salt preference, at once after placement into the two-layer aquarium, occupied the sea water zone, at the very bottom of the aquarium. After 1 h, there started brief excursions of masu salmon and chum salmon to the upper, fresh water layer; however, both forms of the three-spined stickleback did not participate in these excursions. After 12 h, the chum salmon settled down in the lower, sea water layer, while the masu salmon - in the upper, fresh water layer. Both forms of the three-spined stickleback never left the sea water layer and felt quite comfortably on the aquarium bottom. It seems that the high tolerance of the both stickleback forms to wide salinity limits allows them to choose the convenient position regardless of the water salt composition. By analyzing the material obtained for three years (2001-2003) on structure and functions of the gill epithelium chloride cells (CC), we have come to the conclusion that the fresh water fry of two salmon species, chum and masu salmons, caught at the same time and practically in the same water reservoirs can be divided into three groups. The underyearlings of the masu salmon as a rule are characterized by the thickened epithelium of secondary gill lamellae, but by a very small number of CC. In smolts of chum salmon, on the contrary, the epithelium is sufficiently thin, but enriched in the CC that demonstrate an active structure in the very beginning of migration to sea. However, with approaching the sea (and with an increase of terms of migration) the CC activity drops, but their amount does not change. And only after migration to the sea the CC activity rises again, although their amount seems to remain unchanged. The described peculiarities of behavior and of the ion composition regulation in the migrating salmon fry confirm the hypothesis that the salmons evolutionized in fresh water, that the Oncorhynchus genus appeared in large spaces of saltish waters, such as the Japan Sea at the period of the early Pleistocene, and that learning of fry of the Oncorhynchus genus (for instance, of O. gorbuscha and O. keta) is the most specialized in the salmons migrating to the sea, whereas the fresh water species of chars (Salvelinus) and of trouts (Salmo) are more primitive.     

Divergence in juvenile growth and life history in two recently colonized and partially isolated chinook salmon populations

In 47 families of New Zealand chinook salmon, Oncorhynchus tshawytscha derived from two populations, differing in mean spawning date by 11–17 days and in juvenile life history, neither mean ovum weight nor mean time to hatch differed between the two populations, but substantial differences in mean family weight were apparent from 6 months after fertilization. Differences in growth rates from 12 to 24 months were relatively small, suggesting that most of the divergence in size and growth occurred during the first 6 months of life. There were differences in mean weight for families spawned 11–17 days apart, the approximate interval by which peak spawning date differs between the two populations, but these did not persist beyond 7 months. Differences between the two populations are consistent with their natural life history. The slower growing population experiences cooler temperatures during stream residence and is dominated by fish which spend a year in fresh water before seaward migration, whereas the faster growing population normally experiences warmer temperatures and migrates to sea in the first year of life. These results provide further evidence of life history evolution in partially isolated chinook salmon populations within 90 years ( c. 30 generations) of becoming established.     

Evolutionary-physiological aspects of adaptation of the Pacific salmon fry of the oncorhynchus genus to migration to the sea water

A complex of adaptive changes occurring in the Pacific salmon fry in the process of migration to the sea is described, including behavior, ion content in carcasses, and morphological changes in Stannius bodies, gill epithelium, and nephron tubular epithelium. Participating in experiments with transfer from fresh water into a two-layer aquarium (the lower layer—sea water, the upper layer—fresh water) were smolts of chum salmon and underyearlings of cherry salmon as well as the trachurus and leiurus forms of the three-spined stickleback Casterosteus aculeatus. All fish, regardless of their salt preference, at once after placement into the two-layer aquarium, occupied the sea water zone, at the very bottom of the aquarium. After 1 h, there started brief excursions of cherry salmon and chum salmon to the upper, fresh water layer; however, both forms of the three-spined stickleback did not participate in these excursions. After 12 h, the chum salmon settled down in the lower, sea water layer, while the cherry salmon—in the upper, fresh water layer. Both forms of the three-spined stickleback never left the sea water layer and felt quite comfortably on the aquarium bottom. It seems that the high tolerance of the both stickleback forms to wide salinity limits allows them to choose the convenient position regardless of the water salt composition. By analyzing the material obtained for three years (2001–2003) on structure and functions of the gill epithelium chloride cells (CC), we have come to the conclusion that the fresh water fry of two salmon species, chum and cherry salmons, caught at the same time and practically in the same water reservoirs can be divided into three groups. The underyearlings of the cherry salmon as a rule are characterized by the thickened epithelium of secondary gill lamellae, but by a very small number of CC. In smolts of chum salmon, on the contrary, the epithelium is sufficiently thin, but enriched in the CC that demonstrate an active structure in the very beginning of migration to sea. However, with approaching the sea (and with an increase of terms of migration) the CC activity drops, but their amount does not change. And only after migration to the sea the CC activity rises again, although their amount seems to remain unchanged. The described peculiarities of behavior and of the ion composition regulation in the migrating salmon fry confirm the hypothesis that the salmons evolutionized in fresh water, that the Oncorhynchus genus appeared in large spaces of saltish waters, such as the Japan sea at the period of the early Pleistocene, and that learning of fry of the Oncorhynchus genus (for instance, of O. gorbuscha and O. keta) is the most specialized in the salmons migration to the sea, whereas the fresh water species of chars (Salvelinus) and of trouts (Salmo) are more primitive.     

Direct and circulatory paths of Permethrin (NRDC-143) causing histopathological changes in the gills of rainbow trout, Salmo gairdneri Richardson

Rainbow trout were exposed to sublethal concentrations of Permethrin in water (0.09, 0.18 and 0.35 μg l⁻¹) and in food (85, 180 and 350 μg kg⁻¹ dry diet) in 20–0 day experiments. Histological changes in the gills included epithelial separation or necrosis, mucus cell hyperplasia, clubbing of epithelial cells or hyperplasia and fusion of adjacent secondary lamellae. These changes were noted in all fish, suggesting that the pesticide or its metabolites reached the gills not only directly through the water, but also indirectly via the circulation.     

Mast cell responses to Ergasilus (Copepoda), a gill ectoparasite of sea bream

Immunocytochemical, light microscopy and ultrastructural studies were conducted on gill of sea bream, Sparus aurata L., naturally parasitized with the important parasitic copepod Ergasilus sp. to assess pathology and cellular responses. Thirty-seven S. aurata were examined from a fish farm; 26 (70%) were parasitized, with infection intensity ranging from 3 to 55 parasites per fish. Hosts were divided into two groups, lightly infected fish (<15 parasites per fish) and heavily infected fish (>15 parasites per fish). In histological sections, the copepod encircled gill lamellae with its second antennae, compressed the epithelium, provoked hyperplasia and hemorrhage, occluded arteries and often caused lamellar disruption. Fusion of the secondary lamellae due to epithelial hyperplasia was common in all infected fish; heavily infected fish showed more intense branchial inflammation. In both healthy and infected fish, mast cells (MCs) were free within the connective tissue inside and outside the blood vessels of the primary lamellae and made close contact with vascular endothelial cells, mucous cells and rodlet cells (RCs). MCs were irregular in shape with a cytoplasm filled by numerous electron-dense, membrane-bound granules. Immunostaining of primary and secondary gill filaments with an antibody against the antimicrobial peptide (AMP) piscidin 3 (anti-piscidin 3 antibody, anti-HAGR) revealed a subpopulation of MCs that were positive. These MCs were more abundant in gills of heavily infected fish than in either lightly infected or uninfected fish (ANOVA, P<0.05). Our report documents the response of gill to ectoparasite infection and provides further evidence that mast cells and their AMPs may play a role in responding to branchial ectoparasite infections.     

Glochidiosis of salmonid fishes. II. Comparison of tissue response of coho and chinook salmon to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae)

Coho salmon (Oncorhynchus kisutch) are more resistant to experimental infection with the glochidia of the freshwater mussel (Margaritifera margaritifera) than are chinook salmon (Oncorhynchus tshawytscha). Histological sections made at intervals during the infection showed that coho salmon sloughed the parasites from their gills by 4.5 days postinfection, but the parasites remained encysted in the gills of chinook salmon for 12 weeks, when metamorphosis to juvenile mussels was complete. Coho salmon sloughed the parasites by a well-developed hyperplasia. No such pronounced hyperplastic reaction was seen in the gills of chinook salmon.     

Movements of adult Atlantic salmon through a reservoir above a hydroelectric dam: Loch Faskally

Movements of adult Atlantic salmon were determined as they migrated through Loch Faskally, a 4-km long hydroelectric reservoir in North-east Scotland. The horizontal and vertical movements of four salmon were monitored for periods of 4–7 days using depth-sensing acoustic transmitters in June–July 1995. Each fish began sustained directed upstream movements within 5·5 h after release at swimming speeds of 0·15–0·40 bl s⁻¹. Three fish reached the head of the loch after 7·25–17 h, but then returned downstream. The four fish remained in the upper half of the loch for 15–51 days, making localized movements. Mean depths of fish were 3·7–4·0 m (max 20·7 m). Two fish were recorded at significantly shallower depths at night than during the day. Departure from the loch coincided with periods of high water flow into the reservoir. In May–July 1996, 17 radio-tagged salmon entered Loch Faskally and reached the head of the loch in 3 h–5·8 days (mean 39 h). The durations of stay in the loch varied from 3 h 50 min to 67·4 days (mean 10·9 days). Only two radio-tagged salmon left the loch under conditions of high water flow into the loch.     

Glochidia of the freshwater mussel,Anodonta anatina, affecting the anadromous European smelt (Osmerus eperlanus) from the Eider estuary, Germany

During a 2-year survey on external disease conditions of fish between January 1988 and December 1989, 0.2% of 40011 smelt, Osmerus eperlanus , from 30 stations in the German Wadden Sea and estuaries of tributary rivers, were infected with glochidia of the freshwater mussel Anodonta anatina . Seasonality was marked, with glochidia only being observed in March and April 1989, when prevalences were 37% and 15% respectively, in fish 10–20cm long at the most heavily infected site. A marked increase in prevalence in fish 15cm in length and longer, suggested that only temporarily resident spawning fish (as opposed to resident juveniles) were infected. Infection was almost exclusively restricted to the Eider estuary, where prevalence decreased with increasing salinity. It is concluded that the glochidia carried by smelt returning from their freshwater spawning sites in the Eider River to the sea would have died, thus representing a loss to the 1989 cohort of A. anatina from the Eider. The potential importance of the smelt– A. anatina relationship as indicator for the detection of (a) spawning mussel populations and of (b) possible ecological effects of climate changes is noted.