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Keywords:

  • Arctic charr;
  • ecological speciation;
  • feeding behaviour;
  • profundal morph

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Abstract –  Arctic charr, Salvelinus alpinus (L.), is one of the several northern fishes that show resource polymorphisms in postglacial lakes. Two reproductively isolated morphs of Arctic charr coexist in distinct ecological niches in the subarctic lake Fjellfrøsvatn, North Norway. Offspring of the two morphs (termed littoral charr and profundal charr) were reared separately but under identical conditions. Their feeding behaviour was compared experimentally using different kinds of live prey. The fishes had no experience with natural prey before the experiments. The littoral morph were more effective in eating live plankton (Daphnia) and littoral benthos (Gammarus), and had a higher attack rate against pleuston (surface prey, Gerris) compared with the profundal morph. The two morphs behaved in accordance with expectations from their in situ niche utilisation towards the three prey types. This indicates a case of incipient ecological speciation where divergence in resource utilisation in contrasting niches has evolved adaptations in feeding behaviour by natural selection.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Postglacial lakes provide good examples of the importance of resource polymorphism as a diversifying force in vertebrates (Skúlason & Smith 1995; Schluter 2000). The occurrence and evolution of sympatric fish morphs in postglacial lakes of the northern hemisphere therefore attract much interest (Sandlund et al. 1992; Schluter & McPhail 1992; Adams et al. 1998; Lu & Bernatchez 1999; Skúlason et al. 1999; Robinson et al. 2000). Trophic adaptation and ecological speciation are proposed to occur, especially along resource gradients in the pelagic–benthic (littoral) axis (Schluter 1996). Distinct niche diversifications are common, and genetic differences and reproductive isolation are found in some cases (Schluter 2000). The actual selective forces are not well understood, but are believed to be niche-based divergent natural selection (Schluter 2001; Rundle & Nosil 2005).

Plasticity could play an important role in the high rates of divergence in fishes currently undergoing adaptive radiation in northern lakes (Smith & Skúlason 1996), but heritable variation is rarely tested (Robinson & Parsons 2002). Divergence in resource utilisation is likely to be based on genetic differences in behaviour, morphology and physiology, but we need to consider genetic changes in behaviour as distinct from other traits since behaviour is often the mechanism by which specialisation is exercised (Futuyama & Moreno 1988). Only a few studies have tested the genetic basis of feeding behaviour experimentally (Skúlason et al. 1993; Adams & Huntingford 2002; Klemetsen et al. 2002), although it is probably a key feature in polymorphic systems (Smith & Skúlason 1996). Moreover, behavioural change could precede morphological evolution (Wcislo 1989) and be amendable to more rapid change than morphology (Skúlason et al. 1999). Skulason et al. proposed that the Arctic charr occupy different niches of postglacial lakes (food and habitat) because they are genetically polymorphic for behavioural characters. Here, we present experimental results indicating that divergent natural selection on the feeding behaviour of two sympatric morphs of Arctic charr with distinct niches has taken place in Fjellfrøsvatn, a postglacial lake in North Norway. The morphs are termed littoral charr and profundal charr after their spawning habitats. The littoral charr performs ontogenetic habitat shifts between the littoral, pelagic and profundal zones, while the profundal charr lives in the profundal zone for its entire life.

Deep postglacial lakes have four main resource habitats (the lake surface and the pelagic, littoral and profundal zones) that are very different physical environments. They have characteristic invertebrate prey types: pleuston (terrestrial and aquatic insects), plankton (small crustaceans, <2 mm), littoral benthos (larger gastropods, insects and crustaceans, >7 mm, often hard-shelled and commonly swift moving) and profundal benthos (smaller and more slow-moving oligochaetes, chironomids, crustaceans and Pisidium bivalves). By experimenting with limnetic and littoral benthic morphs of Arctic charr, Skúlason et al. (1993) found genetically based differences in the feeding behaviour with plankton prey (Daphnia), and Adams & Huntingford (2002) found differences with plankton (Artemia) and benthos (Tubifex). In previous experiments, offspring of the profundal Fjellfrøsvatn charr were more effective than the littoral charr in eating live profundal prey (chironomid larvae), but the littoral charr were more aggressive, more active and more pelagic than the profundal charr (Klemetsen et al. 2002). In the present report, we extended the experiments to live prey types that are characteristic of the three other resource habitats. We hypothesised that the two morphs have genetically based differences in feeding performance due to divergent selection in their natural habitats, and predicted that offspring of the littoral morph should be more effective in eating pleuston, plankton and littoral benthos than offspring of the profundal morph.

The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

The circumpolar Arctic charr is perhaps the most variable of all northern fishes, with strong variation in size at maturation, form, colour, life history, migration, habitat and ecological niche (reviewed by Jonsson & Jonsson 2001 and Klemetsen et al. 2003a). Polymorphisms with sympatric morphs have repeatedly been reported (e.g., Hindar & Jonsson 1982; Klemetsen et al. 1985; Sandlund et al. 1992; Reist et al. 1995; Adams et al. 1998; Alekseyev et al. 2002). The reproduction of the littoral and profundal morphs of Fjellfrøsvatn is strongly isolated in time and space (Klemetsen et al. 1997; Knudsen et al. 1997). The littoral morph spawns in shallow water (c. 1–5 m depth) in September on substrates of stones and rocks. The profundal morph spawns in deep water (20–40 m) in early March, under thick ice and snow. The profundal morph differs from the littoral morph in phenotype, life history and ecology. A range of head, body and fin measurements were different in the wild phenotypes and the majority of these persisted in the offspring (Klemetsen et al. 2002). Snout length, maxilla length and eye diameter were, for instance, all larger in the profundal charr. Small but significant genetic differences were found by microsatellite DNA analysis (Westgaard et al. 2004; Wilson et al. 2004).

The profundal morph grows slowly to a maximum size of 14 cm and both sexes mature from 7 cm and age 3. The fecundity of seven females was 18–69 eggs (Klemetsen et al. 2002) and the average egg diameter was 3.8 mm (Klemetsen et al. 2003a). The littoral morph grows to 40 cm and matures from 16 cm and age 5. The fecundity of 11 females was 278–480 eggs and the average egg diameter was 5.3 mm (N = 16, 15 eggs measured per fish, unpublished results, A. Klemetsen). Mature littoral charr are brightly coloured, while mature profundal charr are cryptic. Hatchery-reared offspring of the profundal morph are coloured like their parents. This indicates that the cryptic coloration is under genetic control (Klemetsen et al. 2003a). Almost all littoral charr congregate in the littoral zone in the winter, but feed both in the littoral and pelagic zones in the ice-free season (Klemetsen et al. 2003b). Some young fish also feed in the profundal zone in late summer and autumn, mainly on deep-water zooplankton (Knudsen et al. 1997). In contrast, profundal charr perform no habitat shifts but are confined to the profundal zone their entire life. Apart from some habitat overlap in the profundal zone in late summer and autumn, the morphs have explicit niche segregation (Klemetsen et al. 1997; Knudsen et al. 1997).

Material and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Fjellfrøsvatn is a dimictic, oligotrophic lake situated at 125 m.a.s.l. north of the Arctic Circle (69°05′N, 19°20′E) in the Målselv River System, Norway. The surface area is 6.5 km2, two-thirds are deeper than 20 m (profundal) and the maximum depth is 88 m (Klemetsen et al. 1997). It is ice-covered for about 6 months a year. Brown trout Salmo trutta L. and the two morphs of Arctic charr are the only fishes.

Eggs of the littoral morph were fertilised in the field in September 2001 (15 females and 15 males) and brought to Kårvika Research Station near Tromsø. Eggs of the profundal morph were fertilised in the hatchery in March 2002. Because of low catches and high mortality under severe winter conditions, we were only able to get eggs from seven females. Mortality also prevented the use of wild-caught males in 2002, and we therefore used three mature male F1 offspring of profundal charr from an earlier experiment for this fertilisation. The procedure is described in detail by Klemetsen et al. (2002). Eggs and offspring from the two morphs were treated similarly but kept separately and fed with commercial dry pellets. We observed no differences in their feeding rates with pellets. After start-feeding, the mortality was negligible for both morphs. The individuals of the two morphs were also kept separate during the experimental trials. The experiments were conducted during February to April 2003 using 9- to 12-cm long fish of both morphs. An essential feature of the experiments was to use fish that were naïve in the sense that they had not previously been exposed to any kind of live prey. We used 1–2 mm Daphnia longispina (Crustacea: Cladocera) as plankton prey, 6- to 11-mm long Gammarus sp. (Crustacea: Amphipoda) as littoral prey and 5- to 8-mm long pond skaters Gerris sp. (Insecta: Heteroptera) as pleuston prey. The fish were acclimatised to 7 ± 0.5 °C in 65 l glass aquaria for 2 days without food prior to the experiments. The aquaria had slow, separate flows of water of 7 ± 0.5°. The water flow was turned off during the experiments. There were separate aquaria for the two morphs. A red light with an intensity of 10 W m−2 at the surface allowed observation of prey and fish without disturbing the fish. A general account of the experimental protocol is given by Klemetsen et al. (2002).

In each plankton experiment, 30 Daphnia were given to four naïve fishes of one morph and then repeated with 30 new Daphnia and four naïve fishes of the other morph. This was done three times with both morphs and with new naïve fishes each time. All Daphnia were consumed during the experiments, giving a total of 3 × 30 = 90 feeding observations for each morph. The times for each successful predation (prey swallowed) were noted until all prey were eaten. All fishes were actively feeding except for two experiments with littoral charr and one experiment with profundal charr, where only three of the fishes were observed feeding.

In the experiments with littoral benthos, six Gammarus were given to two naïve fishes of one morph in each trial. This was done four times with new naïve fishes, giving a total of 4 × 6 = 24 potential prey ingestions per morph. Four stages in a feeding attempt were noted and timed: approached but ignored, attacked but missed, taken but ejected, and taken and swallowed. If not all prey were taken, the experiment was terminated after 90 min. All littoral fishes were active and performed feeding attempts, but only one individual was successfully ingesting prey in two experiments. All profundal fishes were also active and made feeding attempts, except for one fish in one experiment.

With pleuston prey, the water depth was lowered to 23 cm to give a short distance to the surface for all fish. Four Gerris were presented to two naïve fishes of the same morph. Each experiment lasted for 60 min and was done three times with each morph and with new fish each time. As with Gammarus prey, four potential stages in a feeding attempt, including ignored, missed, ejected and swallowed, were noted and timed. All fishes of both morphs showed some feeding activity in all Gerris experiments.

The data obtained from the feeding experiments on Daphnia and Gammarus were analysed using generalised linear models (GLM) with exponential error distribution (Crawley 2002). The significant contribution of the relevant predictor (morph affiliation) to variation in ingestion time was tested by analysis of deviance. Mean ingestion time during a feeding experiment, a measure of fish-feeding efficiency, was estimated from the GLM. All the analyses were performed with the statistical software R (version 2.1.0; R Foundation for Statistical Computing, Vienna, Austria), using the survival analysis package ‘Survival’.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Littoral and profundal charr differed greatly in their efficiency while feeding on Daphnia (Fig. 1a). The littoral charr reacted shortly after being presented with plankton and the first prey was taken during the first minute in all three replicates. The profundal charr reacted more slowly as the first prey was taken after 1, 3 and 3 min. The estimated mean ingestion time for the littoral morph was 4 min 12 s, with small differences among trials (4 min 6 s, 4 min 12 s and 4 min 30 s) and the last Daphnia was taken after 12, 13 and 20 min. The mean ingestion time for the profundal morph was 22 min, with substantial variation among trials (12 min 3 s, 13 min 36 s and 42 min 20 s) and the last Daphnia was taken after 30, 40 and 80 min. The difference in ingestion time between the morphs was highly significant (analysis of deviance, P < 0.0001).

image

Figure 1.  Comparisons of feeding efficiency between naïve offspring of the littoral and profundal morphs from experiments with (a) Daphnia and (b) Gammarus as prey (dotted lines, 95% CL).

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Naïve offspring of littoral charr ate more Gammarus more quickly and with fewer attempts than the naïve offspring of profundal charr (Fig. 1b). Littoral charr reacted immediately to the presence of the amphipods and made the first feeding attempts during the first minute in all parallels. The profundal charr also made the first attempts during the first minute in three parallels, but took longer time to catch the prey. The littoral charr ate all 24 amphipods, with the last ones being taken after 2–11 min in the four parallels. The profundal charr ate 17 of the 24 amphipods. Six were eaten in two parallels, five in one parallel and none in the last parallel. The last were eaten after 13, 26 and 75 min. The two morphs differed significantly in ingestion time, with the profundal morph being the slower forager (analysis of deviance, P < 0.0001). Littoral offspring made 64 attempts to swallow the 24 Gammarus, whereas profundal offspring performed 169 attempts to swallow 17 Gammarus, showing a significantly lower capture efficiency (Table 1; chi-squared test, P < 0.001). The profundal charr approached and ignored the prey far more frequently than the other morph (Table 1). Furthermore, profundal charr ejected Gammarus prey far more often than the littoral offspring because the amphipods struggled to get out of the mouth, giving a successful ingestion rate of 20% for profundal charr and 44% for littoral charr.

Table 1.   Feeding attempts on Gammarus (littoral prey) by naïve offspring of littoral (L) and profundal charr (P).
 IgnoreMissRejectSwallow
  1. Two naïve fish were used in each trial.

L112166
L21066
L30036
L42366
Ltot453124
P1243175
P2102236
P340116
P4357160
Ptot73126717

Littoral offspring made the first attempts to feed on Gerris during the first minute in all trials, compared to 1, 11 and 18 min in the trails of profundal offspring. The littoral charr had 154 attempts to take Gerris, while only 38 feeding attempts were observed for the profundal charr. The Gerris effectively jumped away when attacked; only one was eventually swallowed, by a littoral charr (Table 2). There was no difference in the relative distribution of Ignore and Attack (taken as the sum of miss, reject and swallow) between the morphs (Table 2; chi-squared test, P > 0.1), but littoral offspring had four times more feeding attempts than profundal offspring (0.86 vs. 0.21 attempts min−1). These results show that offspring of the littoral morph were much more inclined to react towards prey at the water surface than the profundal morph.

Table 2.   Feeding attempts on Gerris (surface prey) by naïve offspring of littoral (L) and profundal charr (P).
 IgnoreMissRejectSwallowTotal attempts
  1. Two naïve fish were used in each trial.

L123535182
L214120026
L327190046
Ltot648451154
P135008
P2590014
P36100016
Ptot14240038

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

The prediction that offspring of the littoral charr should be more effective in eating pleuston, plankton and littoral benthos was supported by the experiments. They reacted to the presence of Daphnia and Gammarus by approaching the prey within seconds and made the first successful capture within the first minute. The profundal fish reacted more slowly and took longer time to take both the plankton and Gammarus prey. The littoral charr attacked the amphipods more quickly and with more aggression, and consumed all of them. The profundal charr also approached the amphipods, but then often broke the feeding sequence and ignored the prey. If they caught one, they had problems swallowing the struggling prey and ended up ejecting it far more often than the littoral charr did, and did not consume all the Gammarus. Both Daphnia and Gammarus are important prey types in Fjellfrøsvatn and many other postglacial lakes (Klemetsen et al. 2003b). Clear differences between the morphs were also observed when they were tested against pleuston (Gerris) as prey. Because Gerris had an effective anti-predator behaviour, full predation sequences could not be recorded with this prey. Nevertheless, the littoral offspring reacted more quickly to the presence of prey at the surface and made far more feeding attempts than the profundal offspring.

The experimental fish were naïve in relation to live prey. Their previous feeding experience consisted of dead food particles (pellets) with a uniform size, shape, colour, smell and taste that were given at the surface and sank slowly to the bottom of the rearing tanks. Differences in the naïve behaviour between offspring of the two charr morphs when feeding on live and dissimilar prey with specific behaviour patterns are therefore likely to have a genetic basis. We are aware that the few brood fishes of the profundal morph (caused by difficult winter sampling in deep water) could potentially give a genetic bias. There were, however, no indications of selective mortality in brood fish or offspring; and we find the present results so clear that genetic bias is unlikely. This is also supported by earlier studies of the two morphs (Klemetsen et al. 2002), where offspring from a higher number of wild brood fish of each sex of the profundal morph were used.

Combined experimental and field studies from Iceland and Scotland have demonstrated genetic differences in morphometry and in two cases also in the feeding behaviour of Arctic charr (Skúlason et al. 1993; Adams & Huntingford 2002). These studies mainly concern differentiation between limnetic and littoral–benthic forms, commonly found among lacustrine fish morphs (Schluter 2000; Robinson & Parsons 2002). In combination, the present findings and the results of Klemetsen et al. (2002) put Fjellfrøsvatn as the first case where genetic differences in the feeding behaviour of two sympatric charr morphs against all major lacustrine prey types (pleuston, plankton, littoral benthos, profundal benthos) have been found. It is also the first case that demonstrates genetic differences in morphometry (Klemetsen et al. 2002) and behaviour of sympatric postglacial fish morphs where one morph is segregated in the profundal habitat.

Arctic charr probably immigrated to Fjellfrøsvatn in early postglacial times when the sea level was high. The geography of the area makes a second invasion unlikely. The two morphs therefore probably diverged in sympatry (Klemetsen et al. 1997). The habitat dimension makes up an important difference between the niches of the charr morphs of Fjellfrøsvatn because their strongly contrasting environments must exert different selective forces. Profundal charr spend their entire life cycle in one habitat only (the profundal zone), while littoral charr perform marked seasonal and ontogenetic habitat shifts, primarily between the littoral and pelagic zones (Klemetsen et al. 1997, 2003b; Knudsen et al. 1997). The profundal charr can therefore be regarded as a specialist, living in a physically homogeneous environment with little predation and a benthic prey community of few, small, slow-moving and often half-burrowed animals. In contrast, the littoral charr is a generalist, exposed to several, physically highly variable habitats with predators (brown trout and fish-eating birds) and complex prey communities (pleuston, plankton and littoral benthos) with high diversities and high densities of prey animals with variable sizes and mobility. Skúlason et al. (1999) found that the importance of phenotypic plasticity and genetic influence on phenotypes differ between and within systems, and that the relative importance of these effects depends on selective environments and developmental constraints. The reproductive isolation (Klemetsen et al. 1997) and genetic differences (Klemetsen et al. 2002; present study; Westgaard et al. 2004; Wilson et al. 2004) found in Fjellfrøsvatn indicate that the profundal charr has evolved adaptations to its narrow niche that might represent an incipient step in ecological speciation by natural selection in this postglacial lake.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

We thank Sten Siikavuopio for his skilled help with setting up the experiments at the Kårvika Research Station, and Laina Dalsbøe and Jan Evjen for their skilled help in catching brood fish in Fjellfrøsvatn during the winter.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. The littoral and profundal charr morphs of the subarctic lake Fjellfrøsvatn
  5. Material and methods
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References
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