Journal of Fish Biology (2015) doi:10.1111/jfb.12677, available online at wileyonlinelibrary.com
Farmed Atlantic salmon Salmo salar L. parr may reduce early survival of wild fish L. Sundt-Hansen*†, J. Huisman‡, H. Skoglund§ and K. Hindar* *Norwegian Institute for Nature Research (NINA), N-7485 Trondheim, Norway, ‡Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway and §Laboratory of Freshwater Ecology and Inland Fisheries (LFI-Uni Environment), Uni Research, N-5006 Bergen, Norway (Received 22 September 2014, Accepted 26 February 2015) The study examined the density-mediated effects on growth, survival and dispersal of wild and farmed Atlantic salmon Salmo salar offspring in the period immediately following emergence, using a substitutive design. In small confined stream channels, wild parr coexisting with farmed parr had a significantly poorer survival, than wild parr alone. Density did not affect this relationship. In larger unconfined stream channels, wild parr coexisting with farmed parr entered a downstream trap in higher numbers than wild parr in allopatry. The results suggests that during the earliest life stages, farmed S. salar can outcompete wild S. salar, resulting in a reduced survival of wild S. salar. © 2015 The Fisheries Society of the British Isles
Key words: aquaculture; competition; density dependence; juvenile; salmonids; survival.
INTRODUCTION Wild Atlantic salmon Salmo salar L. 1758 populations have been greatly reduced in the past few decades and many populations worldwide have gone extinct (Limburg & Waldman, 2009). There is increasing evidence that escaped farmed S. salar threaten native and potentially locally adapted wild S. salar populations through interbreeding and competition (Hindar et al., 1991; Bourke et al., 1997; Garcia de Leaniz et al., 2007) and spreading diseases (Madhun et al., 2015). A large number of farmed S. salar escape annually (e.g. estimated at 198 000 in Norway in 2013; www.fiskeridir.no). These fish are considered potent invaders, as they may ascend rivers and breed with wild S. salar when they reach maturity (Fleming et al., 2000). Selective breeding of farmed S. salar has more than doubled individual growth rate in five generations, reducing the production cycle for farmed S. salar by c. 1⋅5 years (Thodesen et al., 1999) and has resulted in a rapid change in the genetic make-up compared with the wild origin (Karlsson et al., 2011). For wild S. salar, competition occurs predominantly during the early life stages in the river (Jonsson et al., 1998) and competition with farmed S. salar at this stage is with wild born offspring of escaped farmed S. salar. Intraspecific competition at sea is expected to be limited (Jonsson et al., 1998). An experimental study showed that the †Author to whom correspondence should be addressed. Tel.: +4798421195; email: [email protected]
1 © 2015 The Fisheries Society of the British Isles
2
L . S U N D T- H A N S E N E T A L.
offspring of farmed S. salar can be more aggressive and grow faster than wild offspring, but they also exhibit a more risky behaviour than wild S. salar and are more prone to predation (Einum & Fleming, 1997). In the wild, S. salar parr experience a high selection pressure at the earliest life stages, as a large proportion of the parr will starve or be preyed upon within the first weeks after emergence, when the yolk sack has been depleted (Garcia De Leaniz et al., 2000). At this point, the competition is tough and parr that do not establish territories are displaced, often downstream (Bujold et al., 2004). Displaced individuals often show poorer growth than those able to establish territories (Bujold et al., 2004). Farmed emerging alevins, with a high level of aggression, are expected to have a competitive advantage over wild emerging alevins, although they show poorer survival at a later juvenile life stage (McGinnity et al., 2003; Fraser et al., 2008). Previous studies of interactions between farmed and wild S. salar in controlled, whole-river experiments revealed a reduced smolt production of 30% (Fleming et al., 2000) and displacement of wild juveniles (McGinnity et al., 2003). Little empirical data exist on how farmed S. salar affects growth and survival of wild S. salar parr at different densities in a natural environment. Density-dependent effects constitute an important mechanism for population regulation, and it has become increasingly clear that density has a strong effect on growth, survival and dispersal of stream-dwelling juvenile salmonids (Jenkins et al., 1999; Post et al., 1999; Imre et al., 2005; Einum et al., 2006, 2011). The decline in average individual growth rate with density appears to occur over a narrow range of low densities, while average growth is relatively low at higher densities (Jenkins et al., 1999). A study on brown trout Salmo trutta L. 1758 by Jenkins et al. (1999), however, indicates that even though average growth rate declines with density, individuals with a large body size can maintain high growth rates even at high densities (Newman, 1993; Jenkins et al., 1999). The aim of this study was to examine density-mediated effects on growth, survival and dispersal of wild and farmed S. salar offspring in the period immediately following emergence, when mortality is high. The alevin density in the semi-natural environments was manipulated using a substitutive design (Weber & Fausch, 2003), keeping the frequency of each stock constant: This allowed for comparison of the competitive effect of farmed offspring relative to an equal number of wild offspring, at high and low densities. The experiments were based on the hypotheses that wild offspring in sympatry with farmed offspring will show poorer growth compared with wild in allopatry at equal densities, due to a more aggressive and dominant behaviour of farmed offspring. Secondly, a high population density will reinforce the negative influence of farmed offspring on growth and survival of wild offspring.
MATERIALS AND METHODS E X P E R I M E N TA L F I S H Wild adult S. salar were caught in a fish trap in the River Imsa (58∘ 59′ N; 5∘ 58′ E) in November 2008. On 10 November, seven males and 15 females were stripped and eggs were artificially fertilized, by mixing the milt and eggs, creating mixed family groups. The fertilized eggs were incubated in standard hatchery tanks. Farmed S. salar were obtained as eyed eggs from a commercial aquaculture breeding company (Aqua Gen AS; www.aquagen.no) on 20 January 2009 and incubated in the same hatchery as the eggs of wild origin, at the NINA Research Station Ims in south-western Norway (58∘ 59′ N; 5∘ 58′ E). The water supply to the hatchery and the confined and unconfined channels comes from a nearby lake.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
3
Table I. Experimental design of the study in the confined and unconfined stream channels, with an overview of treatment, strain, density, type [wild (W) and farmed (F)] and number of released alevins (n) Experimental arena
Treatment Type
Confined stream channels
Sympatry Sympatry Allopatry Allopatry Sympatry Sympatry Allopatry Allopatry
Unconfined stream channels
Aqua Gen (F), Imsa (W) Aqua Gen (F), Imsa (W) Imsa (W) Imsa (W) Aqua Gen (F), Imsa (W) Aqua Gen (F), Imsa (W) Imsa (W) Imsa (W)
Density n Low High Low High Low High Low High
12 (6 W + 6 F) 48 (24 W + 24 F) 12 48 50 (25 W + 25 F) 300 (150 W + 150 F) 50 300
The wild and farmed group had experienced different temperatures during the early incubation period and the development schedules were therefore synchronized by rearing the farmed group at a slightly higher temperature than the wild group for 12 days, using the models of Crisp (1981, 1988) to monitor development progression. Eggs were kept in the hatchery until the end of the yolk-sac stage (c. 3 weeks before swim-up), when both experiments started (30 March 2009). A sample of n = 50 fish were sampled for initial mass (farmed S. salar 140 ± 20 mg and wild S. salar 100 ± 20 mg; mean ± s.d.). In this study, the definitions of different juvenile life stages of S. salar are according to Allan & Ritter (1977), where alevin is the life stage from hatching until end of yolk-sac dependence and the parr stage is from emergence from the redd and until migration as a smolt.
CONFINED STREAM CHANNEL EXPERIMENT To examine the effect of high and low densities on competition between wild and farmed S. salar, an experiment was set up in 20 semi-natural stream channels, with two density regimes. The stream channels (485 cm × 25 cm) had a water level of 10–12 cm, a water discharge of 0⋅5 l s−1 and gravel substratum. Alevins were carefully released into the semi-natural stream channels and immediately took shelter in the gravel substratum. No food was added during the experiment and only natural food items entering through the inlet water or present in the substratum were available to the fish. The stream channels were closed to provide a confined environment that prevented outward migration. To compare growth and survival of the wild S. salar in sympatry with farmed S. salar, relative to that of wild S. salar in allopatry at equal densities, allopatry (wild S. salar alone) and sympatry (wild and farmed S. salar together) treatments were included in the experimental design. In addition, to test for the effect of high and low densities on the competition between farmed and wild S. salar, a high and a low density regime was created (Table I). There were five replicates of each treatment and a total of 600 experimental fish were used. The initial average biomass densities were 1⋅2 (sympatry, low density), 1⋅0 (allopatry, low density), 4⋅6 (sympatry, high density) and 3⋅8 g m−2 (allopatry, high density). The experiment was terminated on 27 May 2009, when fish were recaptured using dip-nets. All juvenile S. salar were sacrificed by administering an overdose of BenzoakVET (www.europharma.no) and subsequently frozen for processing in the laboratory. Samples of 39 fish were measured for fresh mass for later comparison to frozen mass. In the laboratory, fish were weighed, otoliths extracted and the caudal fins were sampled for DNA analysis. UNCONFINED STREAM CHANNEL EXPERIMENT Alevins from the same batches as used for the confined stream channel experiment were released into large semi-natural stream channels (width: 2⋅5 m, 21⋅6 m2 ) with gravel
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
4
L . S U N D T- H A N S E N E T A L.
substratum and constant water flow. A fish trap was located at the water outlet, allowing fish to migrate out of the stream channel. Alevins were transferred to artificial nests to stimulate natural emergence behaviour and to minimize immediate outmigration. The fish trap was monitored once a day and fish collected in the trap were sacrificed by administering an overdose of BenzoakVET and frozen for later measurements of body mass and DNA analysis. Two replicates of the treatments described in Table I were conducted and a total of 1400 fish were used. Initial biomass densities were, respectively, 0⋅23, 0⋅28, 2⋅8 and 3⋅3 g m−2 . The experiment was terminated on 4 June 2009 and remaining fish were recaptured by electrofishing. The experimental fish were sampled following the same procedure as the confined stream channels. In two of the stream channels, saltwater pockets were observed. Small amount of salt water is used during winter to prevent freezing and residuals of the water had remained in the two stream channels. In one of these stream channels (high density, sympatry), alevins were clearly affected; 61 alevins entered the trap in the days immediately after release (10%, compared with 0% in all other stream channels) and total mortality was 66% (non-affected stream channels: 6–38%). In the other affected stream channel (allopatry, high density), the saltwater pocket was relatively small and did not extend to the shallower regions, the main juvenile habitat. There was no early entering of the trap and the mortality was 61%.
O T O L I T H M A R K I N G A N D C L A S S I F I C AT I O N At the eyed-egg stage (c. 450 degree days), eggs were group marked to distinguish between farmed and wild S. salar sharing enclosures. The eggs of both wild and farmed origin were split into two equally sized batches, and the embryos from one batch for each of the groups were group marked with fluorescent dye by immersion of the eggs for 8 h in a solution of 175 mg l−1 alizarin red S (Baer & Rosch, 2008). To separate possible effects due to marking from origin of the fish, both marked and unmarked farmed and wild fish were used in the confined and the unconfined stream channel experiments, alternating between treatments. Both marked and unmarked alevins were used in the allopatry treatments. The otoliths were mounted on glass microscope slides with a transparent adhesive (Crystalbond; Buehler; www.buehler.com), polished with grit paper and analysed for dye marks with an epi-fluorescence microscope (Wright et al., 2002). In seven of the fish, the otolith markings were impossible to read. These fish were genotyped using microsatellite markers, as well as a sub-set of the parr from the unconfined stream channels (see Appendix S1, Supporting Information). The sub-set included all fish caught at termination of the experiment, and every third fish collected daily in the trap when the daily total of a specific stream channel exceeded 15 fish. When there were fewer than 15 fish for a specific day and stream channel, all were genotyped. This resulted in n = 230 fish being successfully classified to either wild or farmed, out of total n = 463 parr collected in the trap and caught at termination in the sympatry treatments. Statistical analysis The effects of density, origin and treatment on survival and body mass at termination of the experiment were analysed using the lme4 package in R 2.12.2 (R Development Core Team; www.r-project.org). Model selection was performed in a backward stepwise fashion, starting from the full model with all interactions. Non-significant terms were identified on the basis of 𝜒 2 tests of the deviance of models, using a threshold of P = 0⋅1. Average body mass, survival and total biomass per enclosure were compared between sympatry and allopatry treatments. The fit of models and possible violation of model assumptions were assessed using standard diagnostic plots. Possible effects of marking were tested by adding marked or unmarked as an additional explanatory variable to the full model, including two-way interactions with density and group. No significant effect on either survival or growth was found (P > 0⋅1). Channel was included as a random effect in all models. Survival For the confined stream channels, recapture rates at the end of the experiment were used as a proxy for survival, and analysed in a generalized linear mixed model with logit
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
5
link. Estimates were back-transformed to normal scale for }−1 easier interpretation, using { , where 𝛽 0 and 𝛽 A are the the survival probability for category ApA = 1 + e[−(𝛽0 +𝛽A )] intercept and slope (or difference) on the logit scale. The s.e. were back-transformed using the delta method (Powell, 2007), which approximates the curve of x v. p by a straight line at the estimate with the same slope (the tangent), and assumes the point estimate ± s.e. lie For a logit model, the s.e. (Y) on the real scale is calculated {[ on this line. ][ ] }2 ( ) 2 [−(𝛽0 +𝛽A )] [−(𝛽0 +𝛽A )] −1 1+e var𝛽0 + var𝛽A + 2cov𝛽0 𝛽A , where var𝛽 0 is as Y PA = e the square of the s.e. on the logit scale, and taking into account the covariance between the estimates [the variance–covariance matrix can be obtained in R using the command vcov()]. Note that for generalized linear models, this equation is built-in [command predict(model, se.fit = TRUE, type = “response”))”)], but not in the generalized linear mixed models. In the unconfined stream channels, the proportions of juveniles that entered the trap, were caught at termination of the experiment or died during the experiment were compared between treatments (allopatry or sympatry) and densities using t-tests. Because not all outmigrating individuals were classified, sympatric treatments were partly analysed combining the wild and farmed juveniles. The timing of outmigration did not fit any standard distribution, and could therefore not be analysed using standard regression methods or maximum likelihood methods.
Growth Differences in growth between the groups were assessed by the body mass at termination, measured on frozen fish: Frozen mass (M frozen ) was nearly identical to fresh mass (M fresh ) in a sub-sample of fish (M frozen = 1⋅006 M fresh − 0⋅013; r = 0⋅996, n = 39). Body mass at the end of the experiment and of parr collected daily in the traps of the unconfined stream channels were compared with the growth expected based on the starting mass and measured water temperatures using the growth model of Ratkowsky et al. (1983), with parameter values estimated for S. salar in the Norwegian River Imsa by Jonsson et al. (2001) (b = 0⋅31, d = 0⋅39, g = 0⋅134, T L = 4⋅9 and T U = 26⋅7, where b is the allometric mass exponent for the relationship between specific growth rate and body mass, d and g are constants and T L and T U are the estimated lower and upper temperatures for growth).
RESULTS CONFINED STREAM CHANNELS Survival
The survival of wild parr was negatively affected by the presence of farmed parr in the confined stream channels. The best model had both treatment (allopatry or sympatry) and origin (wild or farmed) as explanatory variables. Models including two-way interactions with density and group or density as main effect did not provide a significantly better fit (respectively 𝜒 2 = 0⋅144, P > 0⋅1; 𝜒 2 = 0⋅752, P > 0⋅05). The presence of farmed parr in the same channel significantly reduced survival of wild parr (𝜒 2 = 4⋅98, P < 0⋅05) from 74 ± 5 to 53 ± 7% (estimate ± s.e., both back-transformed from logit scale) [Fig. 1(a), (b)]. Farmed parr had significantly higher survival than sympatric wild parr (87 ± 13%, 𝜒 2 = 52⋅5, P < 0⋅001) (Figs 1 and 2). The random channel effect was estimated at s.d. = 0⋅658 on the logit scale. The total number of surviving parr per channel (wild + farmed) did not differ at either density between the allopatry and sympatry treatments (generalized linear model, P > 0⋅05). © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
6
L . S U N D T- H A N S E N E T A L.
Survival (proportion)
1·0
(a)
(b)
(c)
(d)
0·8 0·6 0·4 0·2 0
Body mass (mg)
800 600 400 200 0
Wildallopatry
Wildsympatry
Farmedsympatry
Wildallopatry
Wildsympatry
Farmedsympatry
Fig. 1. (a, b) Survival (proportion recaptured) of wild and farmed Salmo salar parr under (a) low (n = 12) and (b) high (n = 48) density and (c, d) body mass of wild and farmed S. salar under (c) low (n = 12) and (d) high (n = 48), in confined semi-natural stream channels. Three treatment groups: wild in allopatry, wild in sympatry and farmed in sympatry. , first to third quartile of the data; , median of data; lowest (highest) datum still within 1⋅5 interquartile range of the lower (upper) quartile; , outliers.
Body mass
The presence of farmed offspring did not affect the body mass of wild offspring (𝜒 2 = 0⋅055, P > 0⋅05; Fig. 1), and there were no interactive effects between origin or treatment and density (𝜒 2 = 3⋅15, P > 0⋅05). Farmed parr were heavier than wild parr (at high density: estimate ± s.e. = 385 ± 20 v. 276 ± 16 mg, P < 0⋅001), and fish of all groups were 88 ± 18 mg heavier (P < 0⋅001) at low than at high density (Figs 1 and 2). Body mass under both densities was lower than expected based on starting body mass and temperature, using the Ratkowksy et al. (1983) growth model. As fish were not individually marked, the distribution of end body mass was predicted based on the mean ± s.d. start body mass, giving for the wild fish a predicted average body mass of 449 mg (391–504 mg) and for farmed an average predicted 557 mg (504–608 mg). Biomass
Total biomass per channel differed significantly between both density and allopatry and sympatry treatments (linear model, interaction removed in model selection step). At termination, the biomass in the high-density channels with wild S. salar in allopatry was 7⋅57 ± 0⋅41 g m−2 (mean ± s.e.) compared with channels with a low initial density where biomass was 5⋅12 ± 0⋅47 g m−2 (P < 0⋅001). In sympatry channels, the biomass © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
7
Fig. 2. Mean ± s.e. body mass and total number (wild + farmed) of recaptured parr per confined semi-natural stream channel. Each channel is represented by one (allopatry) or two (sympatry) points: , high density (n = 48 released) and , low density (n = 12). (intercept = 537⋅9 ± 15⋅9, slope = −4⋅93 ± 0⋅65): farmed parr; (intercept = 390⋅2 ± 17⋅5, slope = −3⋅43 ± 0⋅69): wild parr in allopatry; (intercept = 406⋅8 ± 24⋅0, slope = −4⋅19 ± 0⋅98): wild parr in sympatry with farmed parr.
was 0⋅91 ± 0⋅47 g m−2 higher than in allopatry channels, caused by the higher survival rate and body mass of the farmed juveniles. UNCONFINED STREAM CHANNELS Mortality and outmigration
In the unconfined semi-natural channels, S. salar alevins either migrated out (entered fish trap), stayed (caught at termination) or died during the experiment. Overall, 61% left, 7% stayed and mortality was 32%. When excluding the channel with the small saltwater pocket, 71% left, 8% stayed and mortality was 21%. In the stream channels with wild offspring in allopatry, outmigration was lower and mortality was higher than in the sympatry treatment [Table II; 𝜒 2 = 155⋅2 (72⋅9 without slightly affected channel), P < 0⋅001]. These effects balanced each other, so that the number of S. salar parr remaining at the end of the experiment did not differ between allopatry and sympatry streams (two-sided t-test: t = 1⋅4, d.f. = 5, difference of means = 4⋅1, P > 0⋅05). The number of remaining parr was also independent of initial density (two-sided t-test: t = 1⋅6, d.f. = 4⋅2, difference in means = 4⋅66, P > 0⋅05). Within the sympatric channels, there were no significant difference in the number of wild and farmed parr that remained at the end of the experiment (paired two-sided t-test, d.f. = 2, t = 3⋅3, P > 0⋅05). Estimated mortality and outmigration rates did not differ between the groups (Table III). The timing of outmigration differed somewhat between treatments. At both densities, wild and farmed alevins and parr in the sympatry treatment entered the trap somewhat earlier than alevins and parr in the allopatry treatment. In sympatry, there was no clear
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
8
L . S U N D T- H A N S E N E T A L.
Table II. Observed proportions of parr collected in the trap, dead (mortality) and caught at the end of experiment (stay) in the unconfined stream channels with wild in allopatry and with wild and farmed in sympatry, at high and low densities Proportions Treatment
Density
Outmigration
Mortality
Stay
Sympatry Sympatry* Allopatry Allopatry Allopatry†
Low High Low High High
0⋅65 0⋅90 0⋅50 0⋅47 0⋅60
0⋅19 0⋅06 0⋅30 0⋅48 0⋅34
0⋅16 0⋅03 0⋅20 0⋅05 0⋅06
*Based on a single replicate due to saltwater pocket in one of the two replicates. †Excluding one replicate with small saltwater pocket.
difference between the peak and length of the outmigration period of wild and farmed juveniles (Fig. 3). Body mass
Farmed parr entering the trap were on average larger than wild parr at any given day (Fig. 4). The average body mass of wild parr in the trap matches approximately the Ratkowsky growth model, particularly at the start and end of the experiment. The body mass of the farmed juveniles exceeded the prediction based on starting body mass, temperature and parameter estimates for wild S. salar (Fig. 4). Table III. Number of individual experimental fish; released (start), outmigrated (trap), electrofished at termination (stay) and unaccounted for (dead; for sympatric treatments estimated and minimum–maximum) in unconfined stream channels. The numbers are estimates, as not all individuals were classified to either group Treatment
Channel
Type
Start
Trap
Stay
Dead (estimate)
Dead (minimum–maximum)
Sympatry
1*
Sympatry
2
Sympatry
3
Allopatry Allopatry Allopatry Allopatry
4 5 6 7
Wild Farmed Wild Farmed Wild Farmed Wild Wild Wild Wild
150 150 25 25 25 25 300 300 50 50
150⋅4 119⋅6 13⋅0 19⋅0 17⋅8 15⋅2 103⋅0 181⋅0 18⋅0 32⋅0
8⋅0 2⋅0 6⋅5 4⋅5 4⋅0 1⋅0 13⋅0 18⋅0 13⋅0 7⋅0
−8⋅4† 28⋅4 5⋅4 1⋅6 3⋅2 8⋅8 184⋅0‡ 101⋅0 19⋅0 11⋅0
0–72 0–89 1–12 0–6 2–5 7–10 – – – –
*Replicate of high density sympatry treatment excluded due to saltwater pocket causing high mortality at start of experiment. †This should be interpreted as an overestimation of the proportion of wild amongst unclassified individuals in the trap. ‡Saltwater pocket found in stream channel.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
Wild
10
9
(d)
5
Farmed
0 −5 −10
Farmed
Wild
40
10
20
5
0
0
−20
−5
−40
−10
40
(b)
10
(f)
6 20 4 10
2 0
0 40
(c)
10
(g)
8
30
Wild
(e)
8
30
Wild
Frequency (fry day–1)
(a)
6 20 4 10 0
2 15 19 23 27 31 35 39 43 47 51 55 59 63
0
15 19 23 27 31 35 39 43 47 51 55 59 63
Days since start Fig. 3. Number of fry collected in the traps of the unconfined stream channels day−1 since the start of the experiment (30 March 2009 = 0, no outmigration during first 15 days). For the sympatry channels, (a, d, e), the wild ( ):farmed ( ) ratio was estimated from a genotyped sub-sample when the total number of fry per day exceeded 15 or when not all individuals could be classified. High density (a) n = 150 + 150 wild + farmed or (b, c) n = 300 wild and low density (d, e) n = 25 + 25 wild + farmed or (f, g) n = 50 wild.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
10
L . S U N D T- H A N S E N E T A L.
Mean body mass (mg)
1500
1000
500
0 15 April
22 April
29 April
06 May
13 May
20 May
27 May
03 June
Date Fig. 4. Mean ± range body mass of outmigrants from the unconfined stream channels. Frozen body mass of parr collected were averaged group−1 day−1 (released as alevins on 30 March) and averaged over replicates and density treatments. Treatment: , farmed; , wild in allopatry; , wild in sympatry with farmed (symbol size is proportional to sample size). , fitted values from the Ratkowsky et al. (1983) growth model, with parameters for the Imsa stock from Jonsson et al. (2001) and observed daily temperatures. The initial body mass of wild fish was 0⋅1 g ( ) and 0⋅14 g for the farmed ( ), starting at median swim-up time ( ). , parr caught at termination of experiment.
The body mass of parr that remained in the unconfined stream channels at the end of the experiment was not affected by initial density or interactions with density (𝜒 2 = 0⋅80, P > 0⋅05 and 𝜒 2 = 1⋅55, P > 0⋅05, respectively). When including the channel with the small saltwater pocket, no effect of treatment was found (𝜒 2 = 1⋅34, P > 0⋅05). When excluding this channel, however, wild parr remaining in the allopatry treatment were found to be 119 ± 62 mg (mean ± s.e., 𝜒 2 = 3⋅86, P < 0⋅05) smaller than the wild parr remaining in sympatry with farmed parr (mean ± s.e. = 913 ± 74 mg). As expected, farmed parr were larger than wild parr (mean ± s.e. = 437 ± 81 mg, 𝜒 2 = 38⋅0, P < 0⋅001). As the number of individuals remaining in the pool until termination was found to be independent of initial density or treatment, this number was included as an extra explanatory variable. Individual body mass decreased slightly with the number of individuals staying in a pool, when the slightly affected pool was included (slope ± s.e. = −18 ± 7 mg, 𝜒 2 = 5⋅71, P < 0⋅05), but not when excluded (−12 ± 7 mg, 𝜒 2 = 3⋅45, P > 0⋅05). Total biomass at termination ranged from 0⋅21 to 0⋅49 g m−2 , with no consistent differences between initial densities or treatments.
DISCUSSION This study demonstrated that competition from offspring of farmed S. salar may reduce the survival of wild S. salar during an early juvenile life stage. In confined semi-natural stream channels, wild parr showed significantly lower survival when in sympatry with farmed parr compared with the same densities with only wild parr
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
11
present. In the larger unconfined stream channels, however, there was no difference in survival or dispersal between farmed and wild offspring. The early juvenile period, when the alevins emerge from nests and establish feeding territories, is typically characterized by high mortality and intense competition for resources (Einum & Fleming, 2000). Differences in competitive ability during this critical period have been found to affect survival (Einum & Fleming, 2000; Skoglund et al., 2011, 2012). Studies on the behaviour of farmed parr have shown that they display a higher level of aggression (Einum & Fleming, 1997; Houde et al., 2010a). This may be due to higher level of growth hormone (Fleming et al., 2002), which can lead to a more aggressive and bolder behaviour (Johnsson & Björnsson, 1994; Fleming et al., 2002). Such behavioural characteristics may prove to be advantageous during territorial contests immediately after emergence. Juvenile S. salar in streams are typically territorial (Keeley & Grant, 1995), and the primary cause of density dependence is thought to be an increase in interference competition at higher population densities (Sinclair, 1989). In the confined stream channels, increasing the density of wild parr resulted in a reduction in body mass and a slight, but non-significant, decrease in survival rate. The reduced growth with increased population density is well supported in the literature (Jenkins et al., 1999; Post et al., 1999; Imre et al., 2005; Einum et al., 2006, 2011). In contrast, the presence of farmed parr did not affect the body mass of wild parr. Such a pattern could occur if initial mortality is higher in the sympatric streams, resulting in lower density during the remainder of the experiment. This was, however, not the case; the decreased survival of wild parr in sympatry was offset by the high survival of farmed parr, resulting in comparable final densities. By not allowing fish in the stream channels to migrate out, the intensity of the competition may have been considerably increased, compared with the unconfined stream channels. The low numbers of parr remaining in each of the large stream channels at termination of the experiment (0⋅2–0⋅8 parr m−2 , compared with 4⋅0–33⋅0 parr m−2 in the confined stream channels) may indicate that the habitat conditions were unsatisfactory, i.e. due to little shelter, which is strongly correlated with carrying capacity (Finstad et al., 2009), or low food availability. I M P L I C AT I O N S F O R W I L D P O P U L AT I O N S
An important factor in the odds to establish and hold a territory is the timing of emergence, as early emerging alevins may have a competitive advantage owing to the prior residency effect (Hodge et al., 1996; Cutts et al., 1999; Kvingedal & Einum, 2011; Skoglund et al., 2012). In this study, hatching and emergence of farmed and wild S. salar offspring were intentionally synchronized by manipulating incubation temperature, to exclude prior residency effects. Differences due to the possibility that the two strains may have different developmental rate (Fraser et al., 2010), however, cannot be excluded. In the wild, timing of emergence can differ due to a number of reasons, such as timing of spawning. Escaped farmed S. salar are often found to differ from wild S. salar in spawning time, and previous studies have shown that escaped farmed S. salar commonly spawn earlier (Lura et al., 1993; Fleming et al., 2000) but can also spawn later (Webb et al., 1991) than wild S. salar. Whether prior residency effects will favour wild or farmed offspring may vary between rivers and years, depending on relative differences in spawning time and genetic origin of wild and farmed fish.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
12
L . S U N D T- H A N S E N E T A L.
In this study, the presence of farmed juveniles did not alter the total density, relative to a situation with only wild juveniles; the decreased survival of wild juveniles being balanced by the higher survival of farmed juveniles. Studies from later juvenile stages have shown that offspring of farmed S. salar exhibit reduced anti-predator behaviour relative to wild juveniles (Einum & Fleming, 1997; Johnsson et al., 2001; Houde et al., 2010b) reducing their survival in the wild if predators are present. The absence of predators in this study may have given the farmed parr an artificial advantage and allowed them to win more territories than wild parr, allowing the farmed parr to have both higher survival and growth. In older parr, McGinnity et al. (2003) observed a displacement of wild parr due to competition from farmed parr in a natural environment. The presence of farmed juveniles may decrease the total density (wild + farm) at these later life stages, and thereby affect density-dependent selection processes. By changing the selection regime, the offspring of escaped farmed S. salar may affect the genetic composition of wild populations. Thus, even though farmed parr may not be adapted to the wild environment in the same degree as wild parr, they can still outcompete wild S. salar at this critical early stage. The authors thank the staff at NINA research station Ims for technical assistance and A. Finstad, T. Forseth and S. Einum for scientific advice when planning the experiment. The authors also thank I. A. Fleming and P. McGinnity for valuable comments on the manuscript. The authors thank Aqua Gen AS for providing eggs for the experiment. This work was supported by the Norwegian Environment Agency and the QuantEscape knowledge platform of the Research Council of Norway.
Supporting Information Supporting Information may be found in the online version of this paper: Appendix S1. Genotyping and classification. References Allan, I. R. H. & Ritter, J. A. (1977). Salmonid terminology. Journal du Conseil pour l’Exploration de la Mer 37, 293–299. doi: 10.1093/icesjms/37.3.293 Baer, J. & Rosch, R. (2008). Mass-marking of brown trout (Salmo trutta L.) larvae by alizarin: method and evaluation of stocking. Journal of Applied Ichthyology 24, 44–49. Bourke, E. A., Coughlan, J., Jansson, H., Galvin, P. & Cross, T. F. (1997). Allozyme variation in populations of Atlantic salmon located throughout Europe: diversity that could be compromised by introductions of reared fish. ICES Journal of Marine Science 54, 974–985. Bujold, V., Cunjak, R. A., Dietrich, J. P. & Courtemanche, D. A. (2004). Drifters versus residents: assessing size and age differences in Atlantic salmon (Salmo salar) fry. Canadian Journal of Fisheries and Aquatic Sciences 61, 273–282. Crisp, D. T. (1981). A desk study of the relationship between temperature and hatching time for the eggs of five species of salmonid fishes. Freshwater Biology 11, 361–368. Crisp, D. T. (1988). Prediction, from temperature, of eyeing, hatching and ‘swim-up’ times for salmonid embryos. Freshwater Biology 19, 41–48. Cutts, C. J., Metcalfe, N. B. & Taylor, A. C. (1999). Competitive asymmetries in territorial juvenile Atlantic salmon, Salmo salar. Oikos 86, 479–486. Einum, S. & Fleming, I. A. (1997). Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. Journal of Fish Biology 50, 634–651. Einum, S. & Fleming, I. A. (2000). Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54, 628–639.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
13
Einum, S., Sundt-Hansen, L. & Nislow, K. H. (2006). The partitioning of density-dependent dispersal, growth and survival throughout ontogeny in a highly fecund organism. Oikos 113, 489–496. Einum, S., Robertsen, G., Nislow, K. H., McKelvey, S. & Armstrong, J. D. (2011). The spatial scale of density-dependent growth and implications for dispersal from nests in juvenile Atlantic salmon. Oecologia 165, 959–969. Finstad, A. G., Einum, S., Ugedal, O. & Forseth, T. (2009). Spatial distribution of limited resources and local density regulation in juvenile Atlantic salmon. Journal of Animal Ecology 78, 226–235. Fleming, I. A., Hindar, K., Mjølnerød, I. B., Jonsson, B., Balstad, T. & Lamberg, A. (2000). Lifetime success and interactions of farm salmon invading a native population. Proceedings of the Royal Society B 267, 1517–1523. Fleming, I. A., Agustsson, T., Finstad, B., Johnsson, J. I. & Bjornsson, B. Th. (2002). Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 59, 1323–1330. Fraser, D. J., Cook, A. M., Eddington, J. D., Bentzen, P. & Hutchings, J. A. (2008). Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evolutionary Applications 1, 501–512. Fraser, D. J., Minto, C., Calvert, A. M., Eddington, J. D. & Hutchings, J. A. (2010). Potential for domesticated-wild interbreeding to induce maladaptive phenology across multiple populations of wild Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 67, 1768–1775. Garcia De Leaniz, C., Fraser, N. & Huntingford, F. A. (2000). Variability in performance in wild Atlantic salmon, Salmo salar L., fry from a single redd. Fisheries Management and Ecology 7, 489–502. Garcia de Leaniz, C., Fleming, I. A., Einum, S., Verspoor, E., Jordan, W. C., Consuegra, S., Aubin-Horth, N., Lajus, D., Letcher, B. H., Youngson, A. F., Webb, J. H., Vollestad, L. A., Villanueva, B., Ferguson, A. & Quinn, T. P. (2007). A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biological Review of the Cambridge Philosophical Society 82, 173–211. Hindar, K., Ryman, N. & Utter, F. (1991). Genetic effects of cultured fish on natural fish populations. Canadian Journal of Fisheries and Aquatic Sciences 48, 945–957. Hodge, S., Arthur, W. & Mitchell, P. (1996). Effects of temporal priority on interspecific interactions and community development. Oikos 76, 350–358. Houde, A. L. S., Fraser, D. J. & Hutchings, J. A. (2010a). Fitness-related consequences of competitive interactions between farmed and wild Atlantic salmon at different proportional representations of wild-farmed hybrids. ICES Journal of Marine Science 67, 657–667. Houde, A. L. S., Fraser, D. J. & Hutchings, J. A. (2010b). Reduced anti-predator responses in multi-generational hybrids of farmed and wild Atlantic salmon (Salmo salar L.). Conservation Genetics 11, 785–794. Imre, I., Grant, J. W. A. & Cunjak, R. A. (2005). Density-dependent growth of young-of-the-year Atlantic salmon Salmo salar in Catamaran Brook, New Brunswick. Journal of Animal Ecology 74, 508–516. Jenkins, T. M., Diehl, S., Kratz, K. W. & Cooper, S. D. (1999). Effects of population density on individual growth of brown trout in streams. Ecology 80, 941–956. Johnsson, J. I. & Björnsson, B. Th. (1994). Growth hormone increases growth rate, appetite and dominance in juvenile rainbow trout, Oncorhynchus mykiss. Animal Behaviour 48, 177–186. Johnsson, J. I., Hojesjo, J. & Fleming, I. A. (2001). Behavioural and heart rate responses to predation risk in wild and domesticated Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 58, 788–794. Jonsson, N., Jonsson, B. & Hansen, L. P. (1998). The relative role of density-dependent and density-independent survival in the life cycle of Atlantic salmon Salmo salar. Journal of Animal Ecology 67, 751–762. Jonsson, B., Forseth, T., Jensen, A. J. & Næsje, T. F. (2001). Thermal performance of juvenile Atlantic Salmon, Salmo salar L. Functional Ecology 15, 701–711. doi: 10.1046/j.0269-8463.2001.00572.x
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
14
L . S U N D T- H A N S E N E T A L.
Karlsson, S., Moen, T., Lien, S., Glover, K. A. & Hindar, K. (2011). Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP-chip. Molecular Ecology Resources 11, 247–253. Keeley, E. R. & Grant, J. W. A. (1995). Allometric and environmental correlates of territory size in juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 52, 186–196. Kvingedal, E. & Einum, S. (2011). Prior residency advantage for Atlantic salmon in the wild: effects of habitat quality. Behavioral Ecology and Sociobiology 65, 1295–1303. Limburg, K. E. & Waldman, J. R. (2009). Dramatic declines in North Atlantic diadromous fishes. Bioscience 59, 955–965. doi: 10.1525/bio.2009.59.11.7 Lura, H., Barlaup, B. T. & Sægrov, H. (1993). Spawning behaviour of a farmed escaped female Atlantic salmon (Salmo salar). Journal of Fish Biology 42, 311–313. Madhun, A. S., Karlsbakk, E., Isachsen, C. H., Omdal, L. M., Eide Sørvik, A. G., Skaala, Ø., Barlaup B. T. & Glover, K. A. (2015). Potential disease interaction reinforced: double-virus-infected escaped farmed Atlantic salmon, Salmo salar L., recaptured in a nearby river. Journal of Fish Diseases 38, 209–219. doi: 10.1111/jfd.12228 McGinnity, P., Prodohl, P., Ferguson, K., Hynes, R., O’Maoileidigh, N., Baker, N., Cotter, D., O’Hea, B., Cooke, D., Rogan, G., Taggart, J. & Cross, T. (2003). Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society B 270, 2443–2450. Newman, R. M. (1993). A conceptual model for examining density dependence in the growth of stream trout. Ecology of Freshwater Fish 2, 121–131. Post, J. R., Parkinson, E. A. & Johnston, N. T. (1999). Density dependent processes in structured fish populations: interaction strengths in whole-lake experiments. Ecological Monographs 69, 155–175. Powell, L. A. (2007). Approximating variance of demographic parameters using the delta method: a reference for avian biologists. Condor 109, 949–954. Ratkowsky, D., Lowry, R., McMeekin, T., Stokes, A. & Chandler, R. (1983). Model for bacterial culture growth rate throughout the entire biokinetic temperature range. Journal of Bacteriology 154, 1222–1226. Sinclair, A. R. E. (1989). Ecological concepts: the contribution of ecology to an understanding of the natural world. In The Regulation of Animal Populations (Cherrett, M., ed.), pp. 197–241. Oxford: Blackwell Scientific Publications. Skoglund, H., Einum, S. & Robertsen, G. (2011). Competitive interactions shape offspring performance in relation to seasonal timing of emergence in Atlantic salmon. Journal of Animal Ecology 80, 365–374. Skoglund, H., Einum, S., Forseth, T. & Barlaup, B. T. (2012). The penalty for arriving late in emerging salmonid juveniles: differences between species correspond to their interspecific competitive ability. Functional Ecology 26, 104–111. Thodesen, J., Grisdale-Helland, B., Helland, S. J. & Gjerde, B. (1999). Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture 180, 237–246. Webb, J. H., Hay, D. W., Cunningham, P. D. & Youngson, A. F. (1991). The spawning behaviour of escaped farmed and wild adult Atlantic salmon (Salmo salar) in a northern Scottish river. Aquaculture 98, 97–110. Weber, E. D. & Fausch, K. D. (2003). Interactions between hatchery and wild salmonids in streams: differences in biology and evidence for competition. Canadian Journal of Fisheries and Aquatic Sciences 60, 1018–1036. Wright, P. J., Panfili, J., Folkvord, A., Mosegaard, H. & Meunier, F. J. (2002). Direct validation. In Manual of Fish Sclerochronoloy (Panfili, H., de Pontual, H., Troadec, H. & Wright, P. J., eds), pp. 114–127. Brest: Ifremer–IRDcoedition.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
Farmed Atlantic salmon Salmo salar L. parr may reduce early survival of wild fish L. Sundt-Hansen*†, J. Huisman‡, H. Skoglund§ and K. Hindar* *Norwegian Institute for Nature Research (NINA), N-7485 Trondheim, Norway, ‡Department of Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway and §Laboratory of Freshwater Ecology and Inland Fisheries (LFI-Uni Environment), Uni Research, N-5006 Bergen, Norway (Received 22 September 2014, Accepted 26 February 2015) The study examined the density-mediated effects on growth, survival and dispersal of wild and farmed Atlantic salmon Salmo salar offspring in the period immediately following emergence, using a substitutive design. In small confined stream channels, wild parr coexisting with farmed parr had a significantly poorer survival, than wild parr alone. Density did not affect this relationship. In larger unconfined stream channels, wild parr coexisting with farmed parr entered a downstream trap in higher numbers than wild parr in allopatry. The results suggests that during the earliest life stages, farmed S. salar can outcompete wild S. salar, resulting in a reduced survival of wild S. salar. © 2015 The Fisheries Society of the British Isles
Key words: aquaculture; competition; density dependence; juvenile; salmonids; survival.
INTRODUCTION Wild Atlantic salmon Salmo salar L. 1758 populations have been greatly reduced in the past few decades and many populations worldwide have gone extinct (Limburg & Waldman, 2009). There is increasing evidence that escaped farmed S. salar threaten native and potentially locally adapted wild S. salar populations through interbreeding and competition (Hindar et al., 1991; Bourke et al., 1997; Garcia de Leaniz et al., 2007) and spreading diseases (Madhun et al., 2015). A large number of farmed S. salar escape annually (e.g. estimated at 198 000 in Norway in 2013; www.fiskeridir.no). These fish are considered potent invaders, as they may ascend rivers and breed with wild S. salar when they reach maturity (Fleming et al., 2000). Selective breeding of farmed S. salar has more than doubled individual growth rate in five generations, reducing the production cycle for farmed S. salar by c. 1⋅5 years (Thodesen et al., 1999) and has resulted in a rapid change in the genetic make-up compared with the wild origin (Karlsson et al., 2011). For wild S. salar, competition occurs predominantly during the early life stages in the river (Jonsson et al., 1998) and competition with farmed S. salar at this stage is with wild born offspring of escaped farmed S. salar. Intraspecific competition at sea is expected to be limited (Jonsson et al., 1998). An experimental study showed that the †Author to whom correspondence should be addressed. Tel.: +4798421195; email: [email protected]
1 © 2015 The Fisheries Society of the British Isles
2
L . S U N D T- H A N S E N E T A L.
offspring of farmed S. salar can be more aggressive and grow faster than wild offspring, but they also exhibit a more risky behaviour than wild S. salar and are more prone to predation (Einum & Fleming, 1997). In the wild, S. salar parr experience a high selection pressure at the earliest life stages, as a large proportion of the parr will starve or be preyed upon within the first weeks after emergence, when the yolk sack has been depleted (Garcia De Leaniz et al., 2000). At this point, the competition is tough and parr that do not establish territories are displaced, often downstream (Bujold et al., 2004). Displaced individuals often show poorer growth than those able to establish territories (Bujold et al., 2004). Farmed emerging alevins, with a high level of aggression, are expected to have a competitive advantage over wild emerging alevins, although they show poorer survival at a later juvenile life stage (McGinnity et al., 2003; Fraser et al., 2008). Previous studies of interactions between farmed and wild S. salar in controlled, whole-river experiments revealed a reduced smolt production of 30% (Fleming et al., 2000) and displacement of wild juveniles (McGinnity et al., 2003). Little empirical data exist on how farmed S. salar affects growth and survival of wild S. salar parr at different densities in a natural environment. Density-dependent effects constitute an important mechanism for population regulation, and it has become increasingly clear that density has a strong effect on growth, survival and dispersal of stream-dwelling juvenile salmonids (Jenkins et al., 1999; Post et al., 1999; Imre et al., 2005; Einum et al., 2006, 2011). The decline in average individual growth rate with density appears to occur over a narrow range of low densities, while average growth is relatively low at higher densities (Jenkins et al., 1999). A study on brown trout Salmo trutta L. 1758 by Jenkins et al. (1999), however, indicates that even though average growth rate declines with density, individuals with a large body size can maintain high growth rates even at high densities (Newman, 1993; Jenkins et al., 1999). The aim of this study was to examine density-mediated effects on growth, survival and dispersal of wild and farmed S. salar offspring in the period immediately following emergence, when mortality is high. The alevin density in the semi-natural environments was manipulated using a substitutive design (Weber & Fausch, 2003), keeping the frequency of each stock constant: This allowed for comparison of the competitive effect of farmed offspring relative to an equal number of wild offspring, at high and low densities. The experiments were based on the hypotheses that wild offspring in sympatry with farmed offspring will show poorer growth compared with wild in allopatry at equal densities, due to a more aggressive and dominant behaviour of farmed offspring. Secondly, a high population density will reinforce the negative influence of farmed offspring on growth and survival of wild offspring.
MATERIALS AND METHODS E X P E R I M E N TA L F I S H Wild adult S. salar were caught in a fish trap in the River Imsa (58∘ 59′ N; 5∘ 58′ E) in November 2008. On 10 November, seven males and 15 females were stripped and eggs were artificially fertilized, by mixing the milt and eggs, creating mixed family groups. The fertilized eggs were incubated in standard hatchery tanks. Farmed S. salar were obtained as eyed eggs from a commercial aquaculture breeding company (Aqua Gen AS; www.aquagen.no) on 20 January 2009 and incubated in the same hatchery as the eggs of wild origin, at the NINA Research Station Ims in south-western Norway (58∘ 59′ N; 5∘ 58′ E). The water supply to the hatchery and the confined and unconfined channels comes from a nearby lake.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
3
Table I. Experimental design of the study in the confined and unconfined stream channels, with an overview of treatment, strain, density, type [wild (W) and farmed (F)] and number of released alevins (n) Experimental arena
Treatment Type
Confined stream channels
Sympatry Sympatry Allopatry Allopatry Sympatry Sympatry Allopatry Allopatry
Unconfined stream channels
Aqua Gen (F), Imsa (W) Aqua Gen (F), Imsa (W) Imsa (W) Imsa (W) Aqua Gen (F), Imsa (W) Aqua Gen (F), Imsa (W) Imsa (W) Imsa (W)
Density n Low High Low High Low High Low High
12 (6 W + 6 F) 48 (24 W + 24 F) 12 48 50 (25 W + 25 F) 300 (150 W + 150 F) 50 300
The wild and farmed group had experienced different temperatures during the early incubation period and the development schedules were therefore synchronized by rearing the farmed group at a slightly higher temperature than the wild group for 12 days, using the models of Crisp (1981, 1988) to monitor development progression. Eggs were kept in the hatchery until the end of the yolk-sac stage (c. 3 weeks before swim-up), when both experiments started (30 March 2009). A sample of n = 50 fish were sampled for initial mass (farmed S. salar 140 ± 20 mg and wild S. salar 100 ± 20 mg; mean ± s.d.). In this study, the definitions of different juvenile life stages of S. salar are according to Allan & Ritter (1977), where alevin is the life stage from hatching until end of yolk-sac dependence and the parr stage is from emergence from the redd and until migration as a smolt.
CONFINED STREAM CHANNEL EXPERIMENT To examine the effect of high and low densities on competition between wild and farmed S. salar, an experiment was set up in 20 semi-natural stream channels, with two density regimes. The stream channels (485 cm × 25 cm) had a water level of 10–12 cm, a water discharge of 0⋅5 l s−1 and gravel substratum. Alevins were carefully released into the semi-natural stream channels and immediately took shelter in the gravel substratum. No food was added during the experiment and only natural food items entering through the inlet water or present in the substratum were available to the fish. The stream channels were closed to provide a confined environment that prevented outward migration. To compare growth and survival of the wild S. salar in sympatry with farmed S. salar, relative to that of wild S. salar in allopatry at equal densities, allopatry (wild S. salar alone) and sympatry (wild and farmed S. salar together) treatments were included in the experimental design. In addition, to test for the effect of high and low densities on the competition between farmed and wild S. salar, a high and a low density regime was created (Table I). There were five replicates of each treatment and a total of 600 experimental fish were used. The initial average biomass densities were 1⋅2 (sympatry, low density), 1⋅0 (allopatry, low density), 4⋅6 (sympatry, high density) and 3⋅8 g m−2 (allopatry, high density). The experiment was terminated on 27 May 2009, when fish were recaptured using dip-nets. All juvenile S. salar were sacrificed by administering an overdose of BenzoakVET (www.europharma.no) and subsequently frozen for processing in the laboratory. Samples of 39 fish were measured for fresh mass for later comparison to frozen mass. In the laboratory, fish were weighed, otoliths extracted and the caudal fins were sampled for DNA analysis. UNCONFINED STREAM CHANNEL EXPERIMENT Alevins from the same batches as used for the confined stream channel experiment were released into large semi-natural stream channels (width: 2⋅5 m, 21⋅6 m2 ) with gravel
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
4
L . S U N D T- H A N S E N E T A L.
substratum and constant water flow. A fish trap was located at the water outlet, allowing fish to migrate out of the stream channel. Alevins were transferred to artificial nests to stimulate natural emergence behaviour and to minimize immediate outmigration. The fish trap was monitored once a day and fish collected in the trap were sacrificed by administering an overdose of BenzoakVET and frozen for later measurements of body mass and DNA analysis. Two replicates of the treatments described in Table I were conducted and a total of 1400 fish were used. Initial biomass densities were, respectively, 0⋅23, 0⋅28, 2⋅8 and 3⋅3 g m−2 . The experiment was terminated on 4 June 2009 and remaining fish were recaptured by electrofishing. The experimental fish were sampled following the same procedure as the confined stream channels. In two of the stream channels, saltwater pockets were observed. Small amount of salt water is used during winter to prevent freezing and residuals of the water had remained in the two stream channels. In one of these stream channels (high density, sympatry), alevins were clearly affected; 61 alevins entered the trap in the days immediately after release (10%, compared with 0% in all other stream channels) and total mortality was 66% (non-affected stream channels: 6–38%). In the other affected stream channel (allopatry, high density), the saltwater pocket was relatively small and did not extend to the shallower regions, the main juvenile habitat. There was no early entering of the trap and the mortality was 61%.
O T O L I T H M A R K I N G A N D C L A S S I F I C AT I O N At the eyed-egg stage (c. 450 degree days), eggs were group marked to distinguish between farmed and wild S. salar sharing enclosures. The eggs of both wild and farmed origin were split into two equally sized batches, and the embryos from one batch for each of the groups were group marked with fluorescent dye by immersion of the eggs for 8 h in a solution of 175 mg l−1 alizarin red S (Baer & Rosch, 2008). To separate possible effects due to marking from origin of the fish, both marked and unmarked farmed and wild fish were used in the confined and the unconfined stream channel experiments, alternating between treatments. Both marked and unmarked alevins were used in the allopatry treatments. The otoliths were mounted on glass microscope slides with a transparent adhesive (Crystalbond; Buehler; www.buehler.com), polished with grit paper and analysed for dye marks with an epi-fluorescence microscope (Wright et al., 2002). In seven of the fish, the otolith markings were impossible to read. These fish were genotyped using microsatellite markers, as well as a sub-set of the parr from the unconfined stream channels (see Appendix S1, Supporting Information). The sub-set included all fish caught at termination of the experiment, and every third fish collected daily in the trap when the daily total of a specific stream channel exceeded 15 fish. When there were fewer than 15 fish for a specific day and stream channel, all were genotyped. This resulted in n = 230 fish being successfully classified to either wild or farmed, out of total n = 463 parr collected in the trap and caught at termination in the sympatry treatments. Statistical analysis The effects of density, origin and treatment on survival and body mass at termination of the experiment were analysed using the lme4 package in R 2.12.2 (R Development Core Team; www.r-project.org). Model selection was performed in a backward stepwise fashion, starting from the full model with all interactions. Non-significant terms were identified on the basis of 𝜒 2 tests of the deviance of models, using a threshold of P = 0⋅1. Average body mass, survival and total biomass per enclosure were compared between sympatry and allopatry treatments. The fit of models and possible violation of model assumptions were assessed using standard diagnostic plots. Possible effects of marking were tested by adding marked or unmarked as an additional explanatory variable to the full model, including two-way interactions with density and group. No significant effect on either survival or growth was found (P > 0⋅1). Channel was included as a random effect in all models. Survival For the confined stream channels, recapture rates at the end of the experiment were used as a proxy for survival, and analysed in a generalized linear mixed model with logit
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
5
link. Estimates were back-transformed to normal scale for }−1 easier interpretation, using { , where 𝛽 0 and 𝛽 A are the the survival probability for category ApA = 1 + e[−(𝛽0 +𝛽A )] intercept and slope (or difference) on the logit scale. The s.e. were back-transformed using the delta method (Powell, 2007), which approximates the curve of x v. p by a straight line at the estimate with the same slope (the tangent), and assumes the point estimate ± s.e. lie For a logit model, the s.e. (Y) on the real scale is calculated {[ on this line. ][ ] }2 ( ) 2 [−(𝛽0 +𝛽A )] [−(𝛽0 +𝛽A )] −1 1+e var𝛽0 + var𝛽A + 2cov𝛽0 𝛽A , where var𝛽 0 is as Y PA = e the square of the s.e. on the logit scale, and taking into account the covariance between the estimates [the variance–covariance matrix can be obtained in R using the command vcov()]. Note that for generalized linear models, this equation is built-in [command predict(model, se.fit = TRUE, type = “response”))”)], but not in the generalized linear mixed models. In the unconfined stream channels, the proportions of juveniles that entered the trap, were caught at termination of the experiment or died during the experiment were compared between treatments (allopatry or sympatry) and densities using t-tests. Because not all outmigrating individuals were classified, sympatric treatments were partly analysed combining the wild and farmed juveniles. The timing of outmigration did not fit any standard distribution, and could therefore not be analysed using standard regression methods or maximum likelihood methods.
Growth Differences in growth between the groups were assessed by the body mass at termination, measured on frozen fish: Frozen mass (M frozen ) was nearly identical to fresh mass (M fresh ) in a sub-sample of fish (M frozen = 1⋅006 M fresh − 0⋅013; r = 0⋅996, n = 39). Body mass at the end of the experiment and of parr collected daily in the traps of the unconfined stream channels were compared with the growth expected based on the starting mass and measured water temperatures using the growth model of Ratkowsky et al. (1983), with parameter values estimated for S. salar in the Norwegian River Imsa by Jonsson et al. (2001) (b = 0⋅31, d = 0⋅39, g = 0⋅134, T L = 4⋅9 and T U = 26⋅7, where b is the allometric mass exponent for the relationship between specific growth rate and body mass, d and g are constants and T L and T U are the estimated lower and upper temperatures for growth).
RESULTS CONFINED STREAM CHANNELS Survival
The survival of wild parr was negatively affected by the presence of farmed parr in the confined stream channels. The best model had both treatment (allopatry or sympatry) and origin (wild or farmed) as explanatory variables. Models including two-way interactions with density and group or density as main effect did not provide a significantly better fit (respectively 𝜒 2 = 0⋅144, P > 0⋅1; 𝜒 2 = 0⋅752, P > 0⋅05). The presence of farmed parr in the same channel significantly reduced survival of wild parr (𝜒 2 = 4⋅98, P < 0⋅05) from 74 ± 5 to 53 ± 7% (estimate ± s.e., both back-transformed from logit scale) [Fig. 1(a), (b)]. Farmed parr had significantly higher survival than sympatric wild parr (87 ± 13%, 𝜒 2 = 52⋅5, P < 0⋅001) (Figs 1 and 2). The random channel effect was estimated at s.d. = 0⋅658 on the logit scale. The total number of surviving parr per channel (wild + farmed) did not differ at either density between the allopatry and sympatry treatments (generalized linear model, P > 0⋅05). © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
6
L . S U N D T- H A N S E N E T A L.
Survival (proportion)
1·0
(a)
(b)
(c)
(d)
0·8 0·6 0·4 0·2 0
Body mass (mg)
800 600 400 200 0
Wildallopatry
Wildsympatry
Farmedsympatry
Wildallopatry
Wildsympatry
Farmedsympatry
Fig. 1. (a, b) Survival (proportion recaptured) of wild and farmed Salmo salar parr under (a) low (n = 12) and (b) high (n = 48) density and (c, d) body mass of wild and farmed S. salar under (c) low (n = 12) and (d) high (n = 48), in confined semi-natural stream channels. Three treatment groups: wild in allopatry, wild in sympatry and farmed in sympatry. , first to third quartile of the data; , median of data; lowest (highest) datum still within 1⋅5 interquartile range of the lower (upper) quartile; , outliers.
Body mass
The presence of farmed offspring did not affect the body mass of wild offspring (𝜒 2 = 0⋅055, P > 0⋅05; Fig. 1), and there were no interactive effects between origin or treatment and density (𝜒 2 = 3⋅15, P > 0⋅05). Farmed parr were heavier than wild parr (at high density: estimate ± s.e. = 385 ± 20 v. 276 ± 16 mg, P < 0⋅001), and fish of all groups were 88 ± 18 mg heavier (P < 0⋅001) at low than at high density (Figs 1 and 2). Body mass under both densities was lower than expected based on starting body mass and temperature, using the Ratkowksy et al. (1983) growth model. As fish were not individually marked, the distribution of end body mass was predicted based on the mean ± s.d. start body mass, giving for the wild fish a predicted average body mass of 449 mg (391–504 mg) and for farmed an average predicted 557 mg (504–608 mg). Biomass
Total biomass per channel differed significantly between both density and allopatry and sympatry treatments (linear model, interaction removed in model selection step). At termination, the biomass in the high-density channels with wild S. salar in allopatry was 7⋅57 ± 0⋅41 g m−2 (mean ± s.e.) compared with channels with a low initial density where biomass was 5⋅12 ± 0⋅47 g m−2 (P < 0⋅001). In sympatry channels, the biomass © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
7
Fig. 2. Mean ± s.e. body mass and total number (wild + farmed) of recaptured parr per confined semi-natural stream channel. Each channel is represented by one (allopatry) or two (sympatry) points: , high density (n = 48 released) and , low density (n = 12). (intercept = 537⋅9 ± 15⋅9, slope = −4⋅93 ± 0⋅65): farmed parr; (intercept = 390⋅2 ± 17⋅5, slope = −3⋅43 ± 0⋅69): wild parr in allopatry; (intercept = 406⋅8 ± 24⋅0, slope = −4⋅19 ± 0⋅98): wild parr in sympatry with farmed parr.
was 0⋅91 ± 0⋅47 g m−2 higher than in allopatry channels, caused by the higher survival rate and body mass of the farmed juveniles. UNCONFINED STREAM CHANNELS Mortality and outmigration
In the unconfined semi-natural channels, S. salar alevins either migrated out (entered fish trap), stayed (caught at termination) or died during the experiment. Overall, 61% left, 7% stayed and mortality was 32%. When excluding the channel with the small saltwater pocket, 71% left, 8% stayed and mortality was 21%. In the stream channels with wild offspring in allopatry, outmigration was lower and mortality was higher than in the sympatry treatment [Table II; 𝜒 2 = 155⋅2 (72⋅9 without slightly affected channel), P < 0⋅001]. These effects balanced each other, so that the number of S. salar parr remaining at the end of the experiment did not differ between allopatry and sympatry streams (two-sided t-test: t = 1⋅4, d.f. = 5, difference of means = 4⋅1, P > 0⋅05). The number of remaining parr was also independent of initial density (two-sided t-test: t = 1⋅6, d.f. = 4⋅2, difference in means = 4⋅66, P > 0⋅05). Within the sympatric channels, there were no significant difference in the number of wild and farmed parr that remained at the end of the experiment (paired two-sided t-test, d.f. = 2, t = 3⋅3, P > 0⋅05). Estimated mortality and outmigration rates did not differ between the groups (Table III). The timing of outmigration differed somewhat between treatments. At both densities, wild and farmed alevins and parr in the sympatry treatment entered the trap somewhat earlier than alevins and parr in the allopatry treatment. In sympatry, there was no clear
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
8
L . S U N D T- H A N S E N E T A L.
Table II. Observed proportions of parr collected in the trap, dead (mortality) and caught at the end of experiment (stay) in the unconfined stream channels with wild in allopatry and with wild and farmed in sympatry, at high and low densities Proportions Treatment
Density
Outmigration
Mortality
Stay
Sympatry Sympatry* Allopatry Allopatry Allopatry†
Low High Low High High
0⋅65 0⋅90 0⋅50 0⋅47 0⋅60
0⋅19 0⋅06 0⋅30 0⋅48 0⋅34
0⋅16 0⋅03 0⋅20 0⋅05 0⋅06
*Based on a single replicate due to saltwater pocket in one of the two replicates. †Excluding one replicate with small saltwater pocket.
difference between the peak and length of the outmigration period of wild and farmed juveniles (Fig. 3). Body mass
Farmed parr entering the trap were on average larger than wild parr at any given day (Fig. 4). The average body mass of wild parr in the trap matches approximately the Ratkowsky growth model, particularly at the start and end of the experiment. The body mass of the farmed juveniles exceeded the prediction based on starting body mass, temperature and parameter estimates for wild S. salar (Fig. 4). Table III. Number of individual experimental fish; released (start), outmigrated (trap), electrofished at termination (stay) and unaccounted for (dead; for sympatric treatments estimated and minimum–maximum) in unconfined stream channels. The numbers are estimates, as not all individuals were classified to either group Treatment
Channel
Type
Start
Trap
Stay
Dead (estimate)
Dead (minimum–maximum)
Sympatry
1*
Sympatry
2
Sympatry
3
Allopatry Allopatry Allopatry Allopatry
4 5 6 7
Wild Farmed Wild Farmed Wild Farmed Wild Wild Wild Wild
150 150 25 25 25 25 300 300 50 50
150⋅4 119⋅6 13⋅0 19⋅0 17⋅8 15⋅2 103⋅0 181⋅0 18⋅0 32⋅0
8⋅0 2⋅0 6⋅5 4⋅5 4⋅0 1⋅0 13⋅0 18⋅0 13⋅0 7⋅0
−8⋅4† 28⋅4 5⋅4 1⋅6 3⋅2 8⋅8 184⋅0‡ 101⋅0 19⋅0 11⋅0
0–72 0–89 1–12 0–6 2–5 7–10 – – – –
*Replicate of high density sympatry treatment excluded due to saltwater pocket causing high mortality at start of experiment. †This should be interpreted as an overestimation of the proportion of wild amongst unclassified individuals in the trap. ‡Saltwater pocket found in stream channel.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
Wild
10
9
(d)
5
Farmed
0 −5 −10
Farmed
Wild
40
10
20
5
0
0
−20
−5
−40
−10
40
(b)
10
(f)
6 20 4 10
2 0
0 40
(c)
10
(g)
8
30
Wild
(e)
8
30
Wild
Frequency (fry day–1)
(a)
6 20 4 10 0
2 15 19 23 27 31 35 39 43 47 51 55 59 63
0
15 19 23 27 31 35 39 43 47 51 55 59 63
Days since start Fig. 3. Number of fry collected in the traps of the unconfined stream channels day−1 since the start of the experiment (30 March 2009 = 0, no outmigration during first 15 days). For the sympatry channels, (a, d, e), the wild ( ):farmed ( ) ratio was estimated from a genotyped sub-sample when the total number of fry per day exceeded 15 or when not all individuals could be classified. High density (a) n = 150 + 150 wild + farmed or (b, c) n = 300 wild and low density (d, e) n = 25 + 25 wild + farmed or (f, g) n = 50 wild.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
10
L . S U N D T- H A N S E N E T A L.
Mean body mass (mg)
1500
1000
500
0 15 April
22 April
29 April
06 May
13 May
20 May
27 May
03 June
Date Fig. 4. Mean ± range body mass of outmigrants from the unconfined stream channels. Frozen body mass of parr collected were averaged group−1 day−1 (released as alevins on 30 March) and averaged over replicates and density treatments. Treatment: , farmed; , wild in allopatry; , wild in sympatry with farmed (symbol size is proportional to sample size). , fitted values from the Ratkowsky et al. (1983) growth model, with parameters for the Imsa stock from Jonsson et al. (2001) and observed daily temperatures. The initial body mass of wild fish was 0⋅1 g ( ) and 0⋅14 g for the farmed ( ), starting at median swim-up time ( ). , parr caught at termination of experiment.
The body mass of parr that remained in the unconfined stream channels at the end of the experiment was not affected by initial density or interactions with density (𝜒 2 = 0⋅80, P > 0⋅05 and 𝜒 2 = 1⋅55, P > 0⋅05, respectively). When including the channel with the small saltwater pocket, no effect of treatment was found (𝜒 2 = 1⋅34, P > 0⋅05). When excluding this channel, however, wild parr remaining in the allopatry treatment were found to be 119 ± 62 mg (mean ± s.e., 𝜒 2 = 3⋅86, P < 0⋅05) smaller than the wild parr remaining in sympatry with farmed parr (mean ± s.e. = 913 ± 74 mg). As expected, farmed parr were larger than wild parr (mean ± s.e. = 437 ± 81 mg, 𝜒 2 = 38⋅0, P < 0⋅001). As the number of individuals remaining in the pool until termination was found to be independent of initial density or treatment, this number was included as an extra explanatory variable. Individual body mass decreased slightly with the number of individuals staying in a pool, when the slightly affected pool was included (slope ± s.e. = −18 ± 7 mg, 𝜒 2 = 5⋅71, P < 0⋅05), but not when excluded (−12 ± 7 mg, 𝜒 2 = 3⋅45, P > 0⋅05). Total biomass at termination ranged from 0⋅21 to 0⋅49 g m−2 , with no consistent differences between initial densities or treatments.
DISCUSSION This study demonstrated that competition from offspring of farmed S. salar may reduce the survival of wild S. salar during an early juvenile life stage. In confined semi-natural stream channels, wild parr showed significantly lower survival when in sympatry with farmed parr compared with the same densities with only wild parr
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
11
present. In the larger unconfined stream channels, however, there was no difference in survival or dispersal between farmed and wild offspring. The early juvenile period, when the alevins emerge from nests and establish feeding territories, is typically characterized by high mortality and intense competition for resources (Einum & Fleming, 2000). Differences in competitive ability during this critical period have been found to affect survival (Einum & Fleming, 2000; Skoglund et al., 2011, 2012). Studies on the behaviour of farmed parr have shown that they display a higher level of aggression (Einum & Fleming, 1997; Houde et al., 2010a). This may be due to higher level of growth hormone (Fleming et al., 2002), which can lead to a more aggressive and bolder behaviour (Johnsson & Björnsson, 1994; Fleming et al., 2002). Such behavioural characteristics may prove to be advantageous during territorial contests immediately after emergence. Juvenile S. salar in streams are typically territorial (Keeley & Grant, 1995), and the primary cause of density dependence is thought to be an increase in interference competition at higher population densities (Sinclair, 1989). In the confined stream channels, increasing the density of wild parr resulted in a reduction in body mass and a slight, but non-significant, decrease in survival rate. The reduced growth with increased population density is well supported in the literature (Jenkins et al., 1999; Post et al., 1999; Imre et al., 2005; Einum et al., 2006, 2011). In contrast, the presence of farmed parr did not affect the body mass of wild parr. Such a pattern could occur if initial mortality is higher in the sympatric streams, resulting in lower density during the remainder of the experiment. This was, however, not the case; the decreased survival of wild parr in sympatry was offset by the high survival of farmed parr, resulting in comparable final densities. By not allowing fish in the stream channels to migrate out, the intensity of the competition may have been considerably increased, compared with the unconfined stream channels. The low numbers of parr remaining in each of the large stream channels at termination of the experiment (0⋅2–0⋅8 parr m−2 , compared with 4⋅0–33⋅0 parr m−2 in the confined stream channels) may indicate that the habitat conditions were unsatisfactory, i.e. due to little shelter, which is strongly correlated with carrying capacity (Finstad et al., 2009), or low food availability. I M P L I C AT I O N S F O R W I L D P O P U L AT I O N S
An important factor in the odds to establish and hold a territory is the timing of emergence, as early emerging alevins may have a competitive advantage owing to the prior residency effect (Hodge et al., 1996; Cutts et al., 1999; Kvingedal & Einum, 2011; Skoglund et al., 2012). In this study, hatching and emergence of farmed and wild S. salar offspring were intentionally synchronized by manipulating incubation temperature, to exclude prior residency effects. Differences due to the possibility that the two strains may have different developmental rate (Fraser et al., 2010), however, cannot be excluded. In the wild, timing of emergence can differ due to a number of reasons, such as timing of spawning. Escaped farmed S. salar are often found to differ from wild S. salar in spawning time, and previous studies have shown that escaped farmed S. salar commonly spawn earlier (Lura et al., 1993; Fleming et al., 2000) but can also spawn later (Webb et al., 1991) than wild S. salar. Whether prior residency effects will favour wild or farmed offspring may vary between rivers and years, depending on relative differences in spawning time and genetic origin of wild and farmed fish.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
12
L . S U N D T- H A N S E N E T A L.
In this study, the presence of farmed juveniles did not alter the total density, relative to a situation with only wild juveniles; the decreased survival of wild juveniles being balanced by the higher survival of farmed juveniles. Studies from later juvenile stages have shown that offspring of farmed S. salar exhibit reduced anti-predator behaviour relative to wild juveniles (Einum & Fleming, 1997; Johnsson et al., 2001; Houde et al., 2010b) reducing their survival in the wild if predators are present. The absence of predators in this study may have given the farmed parr an artificial advantage and allowed them to win more territories than wild parr, allowing the farmed parr to have both higher survival and growth. In older parr, McGinnity et al. (2003) observed a displacement of wild parr due to competition from farmed parr in a natural environment. The presence of farmed juveniles may decrease the total density (wild + farm) at these later life stages, and thereby affect density-dependent selection processes. By changing the selection regime, the offspring of escaped farmed S. salar may affect the genetic composition of wild populations. Thus, even though farmed parr may not be adapted to the wild environment in the same degree as wild parr, they can still outcompete wild S. salar at this critical early stage. The authors thank the staff at NINA research station Ims for technical assistance and A. Finstad, T. Forseth and S. Einum for scientific advice when planning the experiment. The authors also thank I. A. Fleming and P. McGinnity for valuable comments on the manuscript. The authors thank Aqua Gen AS for providing eggs for the experiment. This work was supported by the Norwegian Environment Agency and the QuantEscape knowledge platform of the Research Council of Norway.
Supporting Information Supporting Information may be found in the online version of this paper: Appendix S1. Genotyping and classification. References Allan, I. R. H. & Ritter, J. A. (1977). Salmonid terminology. Journal du Conseil pour l’Exploration de la Mer 37, 293–299. doi: 10.1093/icesjms/37.3.293 Baer, J. & Rosch, R. (2008). Mass-marking of brown trout (Salmo trutta L.) larvae by alizarin: method and evaluation of stocking. Journal of Applied Ichthyology 24, 44–49. Bourke, E. A., Coughlan, J., Jansson, H., Galvin, P. & Cross, T. F. (1997). Allozyme variation in populations of Atlantic salmon located throughout Europe: diversity that could be compromised by introductions of reared fish. ICES Journal of Marine Science 54, 974–985. Bujold, V., Cunjak, R. A., Dietrich, J. P. & Courtemanche, D. A. (2004). Drifters versus residents: assessing size and age differences in Atlantic salmon (Salmo salar) fry. Canadian Journal of Fisheries and Aquatic Sciences 61, 273–282. Crisp, D. T. (1981). A desk study of the relationship between temperature and hatching time for the eggs of five species of salmonid fishes. Freshwater Biology 11, 361–368. Crisp, D. T. (1988). Prediction, from temperature, of eyeing, hatching and ‘swim-up’ times for salmonid embryos. Freshwater Biology 19, 41–48. Cutts, C. J., Metcalfe, N. B. & Taylor, A. C. (1999). Competitive asymmetries in territorial juvenile Atlantic salmon, Salmo salar. Oikos 86, 479–486. Einum, S. & Fleming, I. A. (1997). Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. Journal of Fish Biology 50, 634–651. Einum, S. & Fleming, I. A. (2000). Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54, 628–639.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
C O M P E T I N G W I L D A N D FA R M E D S A L M O S A L A R PA R R
13
Einum, S., Sundt-Hansen, L. & Nislow, K. H. (2006). The partitioning of density-dependent dispersal, growth and survival throughout ontogeny in a highly fecund organism. Oikos 113, 489–496. Einum, S., Robertsen, G., Nislow, K. H., McKelvey, S. & Armstrong, J. D. (2011). The spatial scale of density-dependent growth and implications for dispersal from nests in juvenile Atlantic salmon. Oecologia 165, 959–969. Finstad, A. G., Einum, S., Ugedal, O. & Forseth, T. (2009). Spatial distribution of limited resources and local density regulation in juvenile Atlantic salmon. Journal of Animal Ecology 78, 226–235. Fleming, I. A., Hindar, K., Mjølnerød, I. B., Jonsson, B., Balstad, T. & Lamberg, A. (2000). Lifetime success and interactions of farm salmon invading a native population. Proceedings of the Royal Society B 267, 1517–1523. Fleming, I. A., Agustsson, T., Finstad, B., Johnsson, J. I. & Bjornsson, B. Th. (2002). Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 59, 1323–1330. Fraser, D. J., Cook, A. M., Eddington, J. D., Bentzen, P. & Hutchings, J. A. (2008). Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evolutionary Applications 1, 501–512. Fraser, D. J., Minto, C., Calvert, A. M., Eddington, J. D. & Hutchings, J. A. (2010). Potential for domesticated-wild interbreeding to induce maladaptive phenology across multiple populations of wild Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 67, 1768–1775. Garcia De Leaniz, C., Fraser, N. & Huntingford, F. A. (2000). Variability in performance in wild Atlantic salmon, Salmo salar L., fry from a single redd. Fisheries Management and Ecology 7, 489–502. Garcia de Leaniz, C., Fleming, I. A., Einum, S., Verspoor, E., Jordan, W. C., Consuegra, S., Aubin-Horth, N., Lajus, D., Letcher, B. H., Youngson, A. F., Webb, J. H., Vollestad, L. A., Villanueva, B., Ferguson, A. & Quinn, T. P. (2007). A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biological Review of the Cambridge Philosophical Society 82, 173–211. Hindar, K., Ryman, N. & Utter, F. (1991). Genetic effects of cultured fish on natural fish populations. Canadian Journal of Fisheries and Aquatic Sciences 48, 945–957. Hodge, S., Arthur, W. & Mitchell, P. (1996). Effects of temporal priority on interspecific interactions and community development. Oikos 76, 350–358. Houde, A. L. S., Fraser, D. J. & Hutchings, J. A. (2010a). Fitness-related consequences of competitive interactions between farmed and wild Atlantic salmon at different proportional representations of wild-farmed hybrids. ICES Journal of Marine Science 67, 657–667. Houde, A. L. S., Fraser, D. J. & Hutchings, J. A. (2010b). Reduced anti-predator responses in multi-generational hybrids of farmed and wild Atlantic salmon (Salmo salar L.). Conservation Genetics 11, 785–794. Imre, I., Grant, J. W. A. & Cunjak, R. A. (2005). Density-dependent growth of young-of-the-year Atlantic salmon Salmo salar in Catamaran Brook, New Brunswick. Journal of Animal Ecology 74, 508–516. Jenkins, T. M., Diehl, S., Kratz, K. W. & Cooper, S. D. (1999). Effects of population density on individual growth of brown trout in streams. Ecology 80, 941–956. Johnsson, J. I. & Björnsson, B. Th. (1994). Growth hormone increases growth rate, appetite and dominance in juvenile rainbow trout, Oncorhynchus mykiss. Animal Behaviour 48, 177–186. Johnsson, J. I., Hojesjo, J. & Fleming, I. A. (2001). Behavioural and heart rate responses to predation risk in wild and domesticated Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 58, 788–794. Jonsson, N., Jonsson, B. & Hansen, L. P. (1998). The relative role of density-dependent and density-independent survival in the life cycle of Atlantic salmon Salmo salar. Journal of Animal Ecology 67, 751–762. Jonsson, B., Forseth, T., Jensen, A. J. & Næsje, T. F. (2001). Thermal performance of juvenile Atlantic Salmon, Salmo salar L. Functional Ecology 15, 701–711. doi: 10.1046/j.0269-8463.2001.00572.x
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
14
L . S U N D T- H A N S E N E T A L.
Karlsson, S., Moen, T., Lien, S., Glover, K. A. & Hindar, K. (2011). Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP-chip. Molecular Ecology Resources 11, 247–253. Keeley, E. R. & Grant, J. W. A. (1995). Allometric and environmental correlates of territory size in juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 52, 186–196. Kvingedal, E. & Einum, S. (2011). Prior residency advantage for Atlantic salmon in the wild: effects of habitat quality. Behavioral Ecology and Sociobiology 65, 1295–1303. Limburg, K. E. & Waldman, J. R. (2009). Dramatic declines in North Atlantic diadromous fishes. Bioscience 59, 955–965. doi: 10.1525/bio.2009.59.11.7 Lura, H., Barlaup, B. T. & Sægrov, H. (1993). Spawning behaviour of a farmed escaped female Atlantic salmon (Salmo salar). Journal of Fish Biology 42, 311–313. Madhun, A. S., Karlsbakk, E., Isachsen, C. H., Omdal, L. M., Eide Sørvik, A. G., Skaala, Ø., Barlaup B. T. & Glover, K. A. (2015). Potential disease interaction reinforced: double-virus-infected escaped farmed Atlantic salmon, Salmo salar L., recaptured in a nearby river. Journal of Fish Diseases 38, 209–219. doi: 10.1111/jfd.12228 McGinnity, P., Prodohl, P., Ferguson, K., Hynes, R., O’Maoileidigh, N., Baker, N., Cotter, D., O’Hea, B., Cooke, D., Rogan, G., Taggart, J. & Cross, T. (2003). Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society B 270, 2443–2450. Newman, R. M. (1993). A conceptual model for examining density dependence in the growth of stream trout. Ecology of Freshwater Fish 2, 121–131. Post, J. R., Parkinson, E. A. & Johnston, N. T. (1999). Density dependent processes in structured fish populations: interaction strengths in whole-lake experiments. Ecological Monographs 69, 155–175. Powell, L. A. (2007). Approximating variance of demographic parameters using the delta method: a reference for avian biologists. Condor 109, 949–954. Ratkowsky, D., Lowry, R., McMeekin, T., Stokes, A. & Chandler, R. (1983). Model for bacterial culture growth rate throughout the entire biokinetic temperature range. Journal of Bacteriology 154, 1222–1226. Sinclair, A. R. E. (1989). Ecological concepts: the contribution of ecology to an understanding of the natural world. In The Regulation of Animal Populations (Cherrett, M., ed.), pp. 197–241. Oxford: Blackwell Scientific Publications. Skoglund, H., Einum, S. & Robertsen, G. (2011). Competitive interactions shape offspring performance in relation to seasonal timing of emergence in Atlantic salmon. Journal of Animal Ecology 80, 365–374. Skoglund, H., Einum, S., Forseth, T. & Barlaup, B. T. (2012). The penalty for arriving late in emerging salmonid juveniles: differences between species correspond to their interspecific competitive ability. Functional Ecology 26, 104–111. Thodesen, J., Grisdale-Helland, B., Helland, S. J. & Gjerde, B. (1999). Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture 180, 237–246. Webb, J. H., Hay, D. W., Cunningham, P. D. & Youngson, A. F. (1991). The spawning behaviour of escaped farmed and wild adult Atlantic salmon (Salmo salar) in a northern Scottish river. Aquaculture 98, 97–110. Weber, E. D. & Fausch, K. D. (2003). Interactions between hatchery and wild salmonids in streams: differences in biology and evidence for competition. Canadian Journal of Fisheries and Aquatic Sciences 60, 1018–1036. Wright, P. J., Panfili, J., Folkvord, A., Mosegaard, H. & Meunier, F. J. (2002). Direct validation. In Manual of Fish Sclerochronoloy (Panfili, H., de Pontual, H., Troadec, H. & Wright, P. J., eds), pp. 114–127. Brest: Ifremer–IRDcoedition.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12677
