Effects of the eye fluke Diplostomum spathaceum on the energetics and feeding of Arctic charr Salvelinus alpinus

In the present study, effects of the trematode eye fluke Diplostomum spathaceum infection and parasite‐induced cataract on energetic costs and feeding of hatchery‐bred one‐summer‐old Lake Saimaa Arctic charr Salvelinus alpinus were examined. The energetic effects (measured as oxygen uptake) of acute eye fluke infection on S. alpinus were negligible, but in the chronic infections mean oxygen consumption of infected fish was significantly higher than that of controls. Feeding capability of S. alpinus was studied in aquarium experiments, and uninfected healthy‐eyed fish reacted to zooplankton more rapidly and caught zooplankton with better success compared to individuals with cataracts in the same school. The results suggested that to compensate energetic costs and impaired feeding capability caused by eye fluke, cataract‐bearing fish spend more time foraging, which may result in increased predation risk.     

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.     

Polymorphism and speciation in Arctic charr

The Arctic charr Salvelinus alpinus exhibits 1–4 sympatric morphs in postglacial lakes, of which one or two are epibenthic zoobenthos feeders, one is a limnetic planktivore and one is a piscivorous form. In addition, northern rivers support partly migratory populations with anadromous and freshwater resident fish. The morphs vary in their coloration, morphology, life history, behaviour and genetic characteristics. The morphs usually differentiate according to their ontogenetic stage at maturity, which parallels paedomorphism in amphibians. The young usually start as epibenthic zoobenthivores, but may become pelagic at a certain size according to the predation risk experienced at that time. From a length of > 20–25 cm, charr start to become piscivorous. The proportion of piscivorous fish increases with increasing body size. In partly anadromous populations, fish that mature before smolting become freshwater resident, the others anadromous. In some rivers, the morphs occupy separate niches (epibenthic and limnetic), from emergence onwards. The morphs exhibit different degrees of reproductive isolation that vary from a high degree of interbreeding to complete isolation. Usually, they spawn within morph (assortative mating), but alternative male mating behaviour (sneaking, fighting) may occur in stream‐spawning populations and at great depths in lakes. Morphologically specialized morphs appear to feed more effectively than intermediate forms, and selection according to feeding mode, site fidelity and associated assortative mating are prerequisites for the evolution of the different morphs. Charr morphs develop into stable feeding niches under conditions of intense intraspecific competition when there is little competition with other species. Sympatric morphs exhibit different degrees of speciation, but similar morphs in different systems are not individual species because of (1) their polyphyletic origin, (2) the supporting systems are often young, transient environments making the future situation for the populations uncertain, and (3) the genetic differentiation among morphs is low. Sympatric morphs may interbreed and produce fertile hybrids. Nevertheless, sympatric charr morphs should be managed as separate species. Changes in the natural conditions or human impacts to which the morphs are adapted will have a strong influence on the persistence and survival of each different morph.     

Piscivory and cannibalism in Arctic charr

Piscivory and cannibalism in Arctic charr, Salvelinus alpinus , were studied in three lakes in northern Norway: Guolasjavri, which contains only charr, Takvatn, where Arctic charr coexist with three-spined sticklebacks, Gasterosteus aculeatus and brown trout, Salmo trutta , and Stuorajavri, where whitefish, Coregonus lavarelun dominate a fish community containing six species. The prevalence of piscivory in the Arctic charr populations generally increased with increasing predator size. In all three lakes, many charr larger than 20 cm were piscivorous, but the extent of piscivory and cannibalism varied. The greatest prevalence of cannibalism was found in Guolasjavri, where 27% of charr greater than 20 cm in length had fed upon smaller conspeciflcs. In Takvatn, 5% of charr larger than 20 cm were cannibalistic, and an additional 9% had eaten three-spined sticklebacks. In Stuorajavri, up to 74% of the charr greater than 20 cm had eaten whitefish but cannibalism was not recorded. The possible role of cannibalism in population regulation within Arctic charr populations is considered.     

Epigenetic regulation of trophic morphology through feeding behaviour in Arctic charr, Salvelinus alpinus

Several models of speciation suggest that in species that are phenotypically plastic, selection can act on phenotypic variation that is environmentally induced in the earliest stages of divergence. One trait that could be subject to this process is foraging behaviour, where discrete foraging strategies are common. One species which is highly plastic in the expression of phenotype, the Arctic charr, Salvelinus alpinus (L.), is characterized by discrete variation in the anatomy of the head and mouthparts. These traits have been shown to have a functional significance, but the expression of which is thought to be at least partly phenotypically plastic. Here we test the hypothesis that foraging behaviour may regulate the anatomy of the head and mouthparts in Arctic charr. In a dyad experiment, size‐matched pairs of fish from a mixed family group were fed a diet of either Mysis (a hard‐bodied shrimp) or Chironomid larvae. Nine morphometric measures of head dimensions that describe wild trophic morphs were measured at the start of the experiment and 24 weeks later. Principal component scores of size‐corrected morphometric measures showed highly significant differences between fish exposed to the two diets. Univariate ANOVA analysis of the head morphometric variables showed that fish fed on Chironomids developed longer, wider jaws, longer heads and a larger eye for a given body length than did those fish fed upon Mysis. We conclude that foraging anatomy in Arctic charr is phenotypically plastic and that variation in foraging behaviour that results in feeding specialization in the wild could induce variation in head anatomy. This in turn could reinforce foraging specialization. Very rapid epigenetic divergence into distinct feeding morphs (as demonstrated here) would allow selection to act at more than one mode and thus could promote rapid evolutionary divergence, initially prior to genetic segregation, in species which are highly plastic. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 43–49.     

Phenotypic variation in infectivity of Diplostomum spathaceum cercariae within a population

The present study examined phenotypic variation in infectivity of Diplostomum spathaceum (Trematoda) cercariae within a natural population. Twelve infected Lymnaea stagnalis were collected from the field, and the infectivity of cercariae from individual snails was assessed under constant laboratory conditions. At a water temperature of 16.3 C, the mean infectivity of cercariae from the snails varied between 55.5% and 87.5%. Depending on the source of variation, this may have important ecological and evolutionary implications for both natural parasite populations and those occurring in aquaculture.     

Adaptibility of Diplostomum cercariae in carp and the effect of a prior infestation

Experiments on the infection of carp fry with cercariae of Diplostomum have shown that cercariae of Diplostomum spathaceum can penetrate crystalline lens of larvae of these fishes in three days after their hatching and that the adaptability of cercariae of D. paracaudum to carp is much higher than that of cercariae of D. spathaceum. After the first infection with cercariae a relative postinfectious immunity against infection with cercariae of this or close species of this genus arises in carp fry.     

A protein with lectin activity in penetration glands of Diplostomum pseudospathaceum cercariae

Homogenates of Diplostomum pseudospathaceum cercariae agglutinated mouse erythrocytes. The haemagglutination could be inhibited by certain glycoconjugates containing beta-1,3- and beta-1,4-glycan chains and also by some simple saccharides. The most potent inhibitors were heparin and some other glycosaminoglycans, bacterial lipopolysaccharides, laminarin (a beta-1,3-glucan) and lactulose. After electrophoresis of cercarial proteins, a dominant double band appeared in the 22-24 kDa region of gels. On blots, this protein bound labelled laminarin and it was also one of the few proteins recognised by mouse antibodies raised against cercarial haemagglutinins. In addition, mouse polyclonal antibodies against the beta-1,3-glucan-binding protein bound exclusively to the 22-24 kDa region on Western blots. Histochemistry revealed strong binding of labelled laminarin to cercarial penetration glands; this reaction was fully blocked by unlabelled laminarin. Other labelled glycoconjugates such as heparin, hyaluronic acid and a bacterial lipopolysaccharide also bound to the glands. Immunohistochemistry confirmed the localisation of the beta-1,3-glucan-binding protein in penetration glands. Reaction of the cercarial protein with immunoglobulins from non-immunised mice was observed on both nitrocellulose membranes and histological sections; this could be blocked by laminarin in incubation buffers. We consider the cercarial haemagglutinin to be a lectin which is identical with the 22-24 kDa beta-1,3-glucan-binding protein. According to the binding specificity and localisation we speculate on a role of this lectin in cercarial penetration into the host, probably as a tissue recognition or antibody rendering factor.     

Size-scaling of zooplankton foraging in Arctic charr

Prey capture rate (number of prey s⁻¹) and the mode of feeding of Arctic charr Salvelinus alpinus were studied by performing foraging experiments with two sizes (1·1 and 1·8 mm) of Daphnia longispina prey. Arctic charr were particulate feeders at all densities tested. Adjusted for the effect of prey density, the capture rate showed a hump-shaped relationship with Arctic charr size for both sizes of D. longispina . Estimated attack rates ( a ) also tended to show a hump-shaped relationship with fish size. The estimated size-scaling exponent of the attack rate function, however, was relatively small, implying small changes in attack rate over fish sizes. Simultaneous estimations of a and handling time were used in combination with published data on fish metabolism and dry mass rations of prey to estimate maintenance resource density of prey as a function of Arctic charr mass. Maintenance resource densities increased monotonically with Arctic charr size, and rapidly as optimum fish size relative to attack rate on prey was passed.     

Changes in survival characteristics of Diplostomum spathaceum cercariae emerged from cadmium-exposed Lymnaea stagnalis

The effect of exposing Lymnaea stagnalis (Gastropoda: Pulmonata), infected with Diplostomum spathaceum (Trematoda: Diplostomatidae), to 100 microg l(-1) cadmium for 7 days on survival characteristics (survival, tail loss, decaudized cercarial life-span) of emerged cercariae was investigated. Exposure of L. stagnalis to cadmium resulted in significantly increased D. spathaceum cercarial survival and an inhibited tail loss compared to controls. The normal parallel relationship which exists over time between decreasing cercarial survival and increasing tail loss in controls was changed in cercariae from cadmium-exposed hosts with an increased proportion of cercarial deaths occurring without tail loss. The decaudized cercarial life-span over the survival period of the cercarial population did not significantly change. However comparisons between individuals decaudized during the initial 24 h time period with those which were decaudized during the final period of cercarial survival showed a significantly altered life span which did not occur in the control population. As a potential indicator of penetration 'fitness' comparisons were also undertaken between control and exposed cercariae decaudized during the initial 24 h time period, which revealed that the decaudized cercarial life-span from the exposed hosts was significantly different from controls. This may have important implications for the ability of cercariae to migrate through the tissues of their target host. The importance and relevance of these results to parasite transmission are discussed.     

Arctic charr in sympatry with burbot: ecological and evolutionary consequences

The trophic niche and parasite infection of Arctic charr (Salvelinus alpinus) were explored in two lakes with sympatric burbot (Lota lota) and two lakes without burbot in subarctic Norway. The CPUE of burbot and charr were similar in one lake, but burbot had a low population density in the other. Burbot were benthivorous in both lakes. Other co-occurring species like brown trout (Salmo trutta), Atlantic salmon parr (Salmo salar), grayling (Thymallus thymallus) and minnow (Phoxinus phoxinus) were also benthivores. At high densities, benthivorous burbot forced the whole Arctic charr population to utilise mainly the limnetic trophic niche. In contrast, at low burbot density or without burbot present, Arctic charr were primarily benthivorous in the littoral zone. Thus, a clear interactive segregation in diet was observed between Arctic charr and burbot at high burbot densities. There was also a high predation pressure from burbot on young Arctic charr along the benthic zones. The extensive use of zooplankton as prey caused a high parasite infection pressure of copepod transmitted Diphyllobothrium spp. larvae, with the potential for high negative impact on the Arctic charr population. As the benthivore trophic niche was occupied by burbot, the ecological opportunities for polymorphism with benthivorous ecotypes or morphs of Arctic charr were probably prevented. Therefore, the sympatry with burbot seems to have large ecological and evolutionary consequences for this Arctic charr population compared with neighbouring lakes where burbot is absent.     

The functional significance of inherited differences in feeding morphology in a sympatric polymorphic population of Arctic charr

Artificially fertilised eggs from wild-caught Arctic charr parents of two sympatric morphs (benthivorous and planktivorous) from Loch Rannoch, Scotland were reared in the laboratory under identical conditions. During the subsequent 2 years, aspects of their trophic anatomy and feeding behaviour were compared. As previously described for wild-caught fish, charr derived from the benthivorous morph had an increasingly wider mouth gape for a given body length than those derived from the planktivorous morph. The functional significance of these differences in gape was tested by comparing the maximum size of prey that could be handled by each of the two morphs. In both forms, a larger gape enabled larger food particles to be eaten, but the elevation of the regression of maximum prey size on gape was higher in the benthivorous form, indicating the existence of additional morphological and/or behavioural differences influencing the size of prey consumed. When offered a choice between a typical benthic prey item and a typical pelagic food item, charr of benthivorous origin were more likely to feed on the former, whereas those of planktivorous origin were more likely to feed on the latter. Thus inherited differences in gape place constraints on foraging ability and are associated with inherited differences in dietary preference. We conclude that the functional significance of the foraging specialisations indicate a strong selection pressure for the evolution of the divergence and propose that heterochronic growth is the mechanism resulting in the divergence of tropic anatomy.     

Growth, maturation and reproductive investment in Arctic charr

Size and rates of growth in a cohort of 1 + Arctic charr housed in standard conditions were tracked over 12 months (December to December) and mature and immature males and females compared retrospectively. In both sexes, maturing fish were larger than non-maturing ones. In males, this size differential was the result of differences in growth in winter and early spring, but not in the remainder of the study period. In females, size differentials resulted mainly from growth rate differences immediately prior to breeding. In females but not in males, gonadosomatic index was predicted by growth rates in the months leading up to maturation, and among the females that matured, faster growing fish produced more eggs. Lipid reserves in July were correlated negatively with growth during the previous 7 months and, in females only, lipid reserves were significantly lower in maturing fish than in non-maturing fish, indicating that mobilization of lipid energy reserves in maturing fish had commenced by this time. Variation in investment in gonadal tissue, measured as gonadosomatic index, was not explained by variation in July lipid reserves for either males or females. However, July lipid reserves were negatively correlated with egg number, so females investing more in ova exhibited greater depletion of lipid reserves. These results are discussed in the context of the relationship between body condition and the onset of maturation in salmonids, relative investment in reproduction and sexual differences in the cost of reproduction.     

Allometric trajectories of body and head morphology in three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs

A study of body and head development in three sympatric reproductively isolated Arctic charr (Salvelinus alpinus (L.)) morphs from a subarctic lake (Skogsfjordvatn, northern Norway) revealed allometric trajectories that resulted in morphological differences. The three morphs were ecologically assigned to a littoral omnivore, a profundal benthivore and a profundal piscivore, and this was confirmed by genetic analyses (microsatellites). Principal component analysis was used to identify the variables responsible for most of the morphological variation of the body and head shape. The littoral omnivore and the profundal piscivore morph had convergent allometric trajectories for the most important head shape variables, developing bigger mouths and relatively smaller eyes with increasing head size. The two profundal morphs shared common trajectories for the variables explaining most of the body and head shape variation, namely head size relative to body size, placement of the dorsal and pelvic fins, eye size and mouth size. In contrast, the littoral omnivore and the profundal benthivore morphs were not on common allometric trajectories for any of the examined variables. The findings suggest that different selective pressures could have been working on traits related to their trophic niche such as habitat and diet utilization of the three morphs, with the two profundal morphs experiencing almost identical environmental conditions.     

Exposure to a common environment erodes inherited between‐population trophic morphology differences in Arctic charr

Arctic charr Salvelinus alpinus juveniles reared from eggs collected from four Scottish populations showed inherited variation in their expression of trophic morphology, measured as a suite of eight characteristics of the head and mouth, before their first exogenous feeding. This demonstrated a genetic component to trophic morphology expression. During a period of 5 months following first feeding, typified by rapid growth, the differential between groups exposed to a common rearing and feeding environment was reduced significantly. It was concluded that this was the result of common environmental exposure acting on phenotypic plasticity in trophic morphology.     

Pelagic marine feeding of Arctic charr and sea trout

In a fjord in northern Norway, both immature and maturing individuals (170–500 mm fork length) of anadromous Arctic charr Salvelinus alpinus and anadromous brown trout (sea trout) Salmo trutta were captured up to 5000 m offshore. Both species had a high feeding intensity and an almost exclusive piscivorous diet, with herring Clupea harengus as the dominant prey, an apparently opportunistic response to a high density of small‐sized herring in the pelagic zone.     

Thermal adaptation of Arctic charr: experimental studies of growth in eleven charr populations from Sweden, Norway and Britain

1. Experimental growth data for Arctic charr (Salvelinus alpinus L.), all fed on excess rations, from 11 European watercourses between 54 and 70°N were analysed and fitted to a new general growth model for fish. The model was validated by comparing its predictions with the growth rate of charr in the wild. 2. Growth performance varied among populations, mainly because of variation in the maximum growth potential, whereas the thermal response curves were similar. The estimated lower and upper temperatures for growth varied between ?1.7 to 5.3 and 20.8–23.2 °C, respectively, while maximum growth occurred between 14.4 and 17.2 °C. 3. There was no geographical or climatic trend in growth performance among populations and therefore no indication of thermal adaptation. The growth potential of charr from different populations correlated positively with fish body length at maturity and maximum weight in the wild. Charr from populations including large piscivorous fish had higher growth rates under standardised conditions than those from populations feeding on zoobenthos or zooplankton. Therefore, the adaptive variation in growth potential was related to life‐history characteristics and diet, rather than to thermal conditions.     

Arctic charr strain crosses: effects on growth and sexual maturity

Three Arctic charr strains and their crosses were evaluated with respect to growth and sexual maturation frequency. No significant heterosis was observed for growth. One out of five crosses was heavier, but not significantly so, than the best performing parental strain at ages 1 + and 2. The five other crosses did not perform better than the best performing parental strain at any age. Cross-breeding was not recommended as an effective method to improve growth performance in Arctic charr. Growth performance of reciprocal crosses differed significantly in all strain combinations: crosses resembled more the male parent strain than the female parent strain. ANOVA for male maturation frequency showed a highly significant effect of the male parent strain and a weakly significant effect of female parent strain. In the Ottsjö strain mature males were significantly larger than immature fish and females. Such size difference was also observed in the offspring when sires of the Ottsjö strain were crossed with dams of the faster growing Honavan strain or with dams of the Rensjö strain. When Ottsjö dams were crossed to sires of the other strains no significant size difference between mature males and other fish was found.     

Sex chromosome polymorphisms in Arctic charr and their evolutionary origins

Current data on the Y-specific sex-determining region of salmonid fishes from genera Salvelinus, Salmo, and Oncorhynchus indicate variable polymorphisms in the homologous chromosomal locations of the sex-specific determining region. In the majority of the Atlantic lineage Arctic charr, including populations from the Fraser River, in Labrador Canada, as well as Swedish and Norwegian strains, the sex-determining locus maps to linkage group AC-4. Previously, sex-linked polymorphisms (i.e., variation in the associated sex-linked markers on AC-4) have been described in Arctic charr. Here, we report further evidence for intraspecific sex linkage group polymorphisms in Arctic charr (i.e., the detection of the SEX locus on either the AC-1 or AC-21 linkage group) and a possible conservation of a sex linkage arrangement in Icelandic Arctic charr and Atlantic salmon, involving sex-linked markers on the AC-1/21 homeologs and the European AS-1/6 homeologous linkage groups in Atlantic salmon. The evolutionary origins for the multiple sex-determining regions within the salmonid family are discussed. We also relate the variable sex-determining regions in salmonids to their ancestral proto-teleost karyotypic origins and compare these findings with what has been observed in other teleost species in general.