B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/biocon

An integrated comparison of captive-bred and wild Atlantic

salmon (Salmo salar): Implications for supportive breeding
programs

Simon Blancheta,b,*, David J. Páeza, Louis Bernatcheza, Julian J. Dodsona

a
CIRSA and Québec-Océan, Department of Biology, Pavillon Vachon, University Laval, Ste Foy, Québec, Canada G1K 7P4
b
Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – University Paul Sabatier, 118 route de Narbonne, F-31062,
Toulouse cedex 4, France

A R T I C L E I N F O A B S T R A C T

Article history: Supportive breeding is a strategy consisting in maintaining a pool of locally-adapted wild
Received 26 October 2007 genitors in captivity whose offspring are released in the wild at an early developmental
Received in revised form stage. In this study, we tested the utility of this strategy in preventing phenotypic and
21 May 2008 genetic divergences between captive-bred and wild animals that could be detrimental for
Accepted 25 May 2008 wild populations. Combining microsatellite analyses, morphological measurements and
Available online 10 July 2008 behavioural trials in the laboratory, we compared the progeny of Atlantic salmon (Salmo
salar) born in captivity with individuals born in the wild. At all these levels, we found sig-
Keywords: nificant differences between the progeny of the two groups. Specifically, allelic frequencies
Captive breeding significantly differed between groups, with captive-bred fish tending to be less variable
Salmonids conservation with lower heterozygosity and allelic richness values. The shape of wild-born fish was also
Population restoration different from that of the captive-group, particularly in the depth of the head and the
Microsatellite length of the pectoral fins. Finally, captive-bred individuals were, on average, more aggres-
Behaviour sive than wild-born fish. We demonstrated that this difference was strongly dependent
Morphometry upon the environment as captive-bred fish were more aggressive only when together with
their wild conspecifics or with an exotic competitor, the rainbow trout (Oncorhynchus
mykiss). Overall, our results showed that both phenotypic and genetic changes can arise
even if genitors share a common brood-stock and after only a few months of rearing in a
controlled environment. We conclude that the progeny produced in such supportive breed-
ing programs does not meet the criteria necessary to ensure preserving the genetic and
ecological integrity of wild populations.
 2008 Elsevier Ltd. All rights reserved.

1. Introduction eral authors have argued that captive breeding suffers impor-
tant limitations (reviewed in Snyder et al., 1996). Particularly,
Captive breeding is a widely used management practice that captive breeding often leads to genetic, morphological and
aims to restore, conserve and/or enhance wild populations. behavioural differences between captive-bred and wild popu-
In contrast to the potential benefits for species recovery, sev- lations which may pose major difficulties when attempting to

* Corresponding author: Address: Laboratoire Evolution et Diversité Biologique, U.M.R 5174, C.N.R.S – University Paul Sabatier, 118 route
de Narbonne, F-31062, Toulouse cedex 4, France. Tel.: +33 5 61 55 85 81; fax: +33 5 61 55 67 28.
E-mail addresses: [email protected] (S. Blanchet), [email protected] (D.J. Páez), [email protected] (L. Bernatchez),
[email protected] (J.J. Dodson).
0006-3207/$ - see front matter  2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2008.05.014
1990 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

preserve wild populations (Snyder et al., 1996; Price, 1999; and allelic richness) are important for populations to face
Heath et al., 2003). For instance, such deficiencies may have environmental changes (Frankham, 2008), and traits such as
harmful effects on wild populations (through ecological or ge- body size and competitive ability determine an individual’s
netic interactions) and may limit the settlement success of ability to exploit and survive in natural habitats (e.g. Håkans-
captive-bred animals in nature (Wang and Ryman, 2001; Ford, son and Jensen, 2005; Hill et al., 2006; Kraaijeveld-Smit et al.,
2002; McGinnity et al., 2003; Theodorou and Couvet, 2004; 2006). Although many studies have only considered one or
Håkansson and Jensen, 2005; Mathews et al., 2005; Frankham, two of these components (e.g. McPhee, 2004; Hill et al., 2006;
2008). Thus, researchers have attempted to develop captive Kraaijeveld-Smit et al., 2006), the information contained in
breeding strategies that aim to preserve both the genetic all of these components is needed to accurately forecast the
and phenotypic integrity of the target population (e.g. Duch- success of captive-bred animals in the wild and the effects
esne and Bernatchez, 2002; Fiumera et al., 2004; Theodorou they may have on wild populations (Kraaijeveld-Smit et al.,
and Couvet, 2004). 2006).
Recently, an alternative strategy to traditional captive Recent studies (Mathews et al., 2005; Kelley et al., 2006)
breeding has been developed to solve these potential prob- have highlighted the importance of considering several envi-
lems. This strategy (called ‘‘supportive breeding’’; Wang and ronments when attempting to compare the behaviour of cap-
Ryman, 2001) consists in maintaining a pool of locally- tive-bred and wild animals. For example, as density is
adapted wild genitors (i.e. genitors originating from the target generally higher in captivity and behaviour may vary accord-
population) in captivity whose offspring are released at an ing to density (Price, 1999; Blanchet et al., 2006; Kelley et al.,
early developmental stage. In theory, such a strategy may of- 2006), one can hypothesize that captive-bred animals behave
fer several advantages. First, the genetic integrity of the pop- differently according to the density they encounter in the
ulation is preserved through the use of randomly caught wild environment. Similarly, wild animals may also coexist with
breeders at each breeding season in combination with an ade- interspecific competitors that have been recently introduced
quate breeding design (e.g. Fiumera et al., 2000, 2004). Second, in their habitat (i.e., exotic species). Thus, if captive-bred ani-
the phenotypic and genotypic differences between captive- mals are unable to perform well (relative to their wild conspe-
bred and wild animals is limited by releasing first-generation cifics) in the presence of an exotic competitor, one can
captive animals at an early stage of development, thus limit- hypothesize that the exotic species may limit the settlement
ing exposure to the selective pressures imposed by captivity of the captive-bred animals.
(Salonen and Peuhkuri, 2006; Kraaijeveld-Smit et al., 2006). Currently, the enhancement of wild stocks of salmonid
Although this would be context-dependent and vary accord- fishes using hatchery-born fish to restore or supplement wild
ing to the census size of wild populations to be restocked, a populations is practiced worldwide, although the benefits re-
moderately high number of breeders (>20) should theoreti- main uncertain (Dodson et al., 1998). The question of the util-
cally be maintained in captivity to avoid undesirable genetic ity of supportive breeding strategies is therefore particularly
consequences that may negatively affect fitness of wild pop- relevant for this group of animals. For instance, Atlantic sal-
ulations (e.g. Tenhumberg et al., 2004; Theodorou and Couvet, mon (Salmo salar) is a cultural and economically important
2004; Favé et al., 2008). Typically, such a number is not always species. Atlantic salmon stocks are severely declining
obtainable due to logistical constraints or to the scarcity of throughout the species distribution, with some populations
the target population or species (Aho et al., 2006; Ramirez being considered endangered or nearly extinct (Klemetsen
et al., 2006). et al., 2003). Atlantic salmon naturally inhabit rivers of the
Evaluating the utility of captive breeding strategies is a North-Atlantic coastlines, where they spend their first two
prerequisite for future management decisions, and can be to five years of life. They then migrate to the ocean to feed
achieved through several approaches. A conservative ap- and grow for one year or more and then return to their natal
proach is to test for genetic and/or phenotypic differences be- rivers to spawn (see Klemetsen et al., 2003 for more informa-
fore releasing captive-bred animals into the wild (i.e., tests in tion). In this species, supportive breeding consists in produc-
the laboratory and/or in a controlled environment). To date, ing fish (from locally-adapted genitors) in a hatchery and
most studies that aim to compare captive-bred with wild ani- releasing them at the juvenile stage (usually within the first
mals consider captive populations that (i) were founded by year after hatching) into the wild (Tessier et al., 1997; Dodson
genitors from non-target wild populations and/or (ii) re- et al., 1998). Juvenile Atlantic salmon are territorial predators
mained captive for up to two generations (e.g. Mathews interacting through interference competition to defend profit-
et al., 2005; Kelley et al., 2006; Salonen and Peuhkuri, 2006). able territories that are rich in food and provide refuges
Therefore, the assumption that supportive breeding designs against predators (Klemetsen et al., 2003). In some rivers,
are useful for limiting genetic and phenotypic divergences juvenile salmon must also confront exotic competitors such
has, to our knowledge, rarely been tested. as the rainbow trout (Oncorhynchus mykiss), an anadromous
Evaluating the success of captive-bred animals in nature salmonid from the north-western coast of North America,
and their impacts on wild populations involves assessing representing an additional risk to declining populations
the genetic risks (e.g. inbreeding depression, change in allelic (Blanchet et al., 2007). The ability of captive-bred fish to adapt
frequencies and/or the introduction of deleterious alleles in to these competitive and unpredictable environments is cru-
wild populations, Ryman et al., 1995; Ford, 2002) as well as cial to forecast the benefits and also the genetic and ecologi-
the morphological, physiological and behavioural capabilities cal consequences of supportive breeding programs.
of captive-bred fish to survive in the wild. For instance, The main objective of this study was to assess the utility of
parameters linked to genetic diversity (e.g. heterozygosity a supportive breeding strategy in preventing potential diver-
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9 1991

gences between captive-bred and wild-born animals that are commercial fish food pellets before the beginning of the
usually considered detrimental for the target population. To experiments. Behavioural experiments were conducted dur-
do so, we compared the phenotypic and genetic characteris- ing the following winter (i.e., five months after fish capture).
tics of the progeny of wild breeders produced in captivity Mortality in the holding tank was relatively low (i.e. 10–20 fish
and in the wild. We posit the null hypothesis that no genetic per group) suggesting that no strong artificial selection (in-
or morphological changes occurred between captive-born duced by laboratory conditions) occurred during this period.
and wild-born Atlantic salmon sharing the same brood-stock.
We also compared the behaviour of captive-born and wild- 2.2. Genetic analyses
born Atlantic salmon in different competitive environments
to test the null hypotheses that (i) no behavioural changes oc- We selected 35 fish from each experimental group (n = 70). To-
curred between captive-born and wild-born Atlantic salmon tal DNA was extracted from muscle tissue using a salt extrac-
(ii) the behaviour of captive-born animals is not density- tion method described in Aljanabi and Martinez (1997). Ten
dependent and (iii) captive-born and wild-born conspecifics nuclear microsatellite loci were amplified using polymerase
behave similarly in the presence of an exotic competitor. chain reaction (PCR) (Table 1). PCR products were run on an
ABI 3100 automated capillary sequencer (Applied Biosys-
TM

tems). Allelic sizes were scored using GENESCAN analysis

TM

2. Methods v.3.7 and GENOYPER v.3.7 NT software.

TM

2.1. Study populations 2.3. Morphometric analysis

The two groups of young-of-the-year (YOY) fish we compared For the morphometric analysis, we selected 30 fish from each
were produced from adult Atlantic salmon from the river Mal- experimental group (n = 60). Fish were euthanized with an ex-
baie (Québec, Canada, 47 67 0 N; 70 16 0 W). The Atlantic sal- cess of the sedative eugenol and each was positioned on their
mon population in this river was relatively small until a left side on a measuring board with the lower jaw closed and
restoration program began in 1992. Presently, about 400–500 caudal fin extended. Each individual was photographed using
adults enter this river annually to spawn. A pool of genitors an Olympus digital camera. From each image, 16 morpholog-
(i.e., 10 anadromous males and 10 females) is maintained at ical traits (Fig. 1) were measured to the nearest 0.001 mm
the provincial hatchery of Tadoussac. Each year, this pool is using the free software IMAGE J (U.S. National Institute of
renewed by haphazardly capturing approximately 10 wild Health, http://rsb.info.nih.gov/ij/). We focused on these traits
genitors (five anadromous males and five females) in a fish because they have been associated with swimming perfor-
ladder installed on an insurmountable dam during the sum- mance and habitat selection (Letcher, 2003; Páez et al., 2008).
mer spawning migration. An effective breeder’s pool of 20
genitors (with an equal sex-ratio) renewed at 50% each gener- 2.4. Behavioural analyses
ation falls within the range theoretically predicted for pre-
serving wild populations for a population with such census Behavioural tests were conducted using 12 artificial channels
size (Duchesne and Bernatchez, 2002; Favé et al., 2008) and fitted with a re-circulating water system. Each channel mea-
in the range used in other programs (Aho et al., 2006; Ramirez sured 1.90 m long, 0.30 m wide and 0.30 m deep. One pool/rif-
et al., 2006). At the hatchery, the genitors are mated and the fle succession was simulated using small pebbles (see
progeny is reared in tanks. Fish densities at this hatchery Blanchet et al., 2006 for more details). Water depth and water
are relatively low (500 YOYs m3 compared to velocity were consistent with natural habitat conditions
3
2000 YOYs m in commercial hatcheries, see McDonald experienced by juvenile Atlantic salmon (Klemetsen et al.,
et al., 1998), and water temperature is free to fluctuate natu- 2003; Blanchet et al., 2007). Two large pebbles (7–10 cm diam-
rally as the hatchery receives its water supply from a neigh- eter) were added in each riffle and each pool as refuges. Pho-
bouring lake. Fish are reared until the age of about four toperiod was controlled with two 60-W lights above each
months before being released in September. Thus, the salmon channel at 80% and 7% of the available intensity during day,
population in the river Malbaie consists of wild-born and dawn, dusk, and night, respectively. Light-to-dark cycle was
hatchery-born fish. In the downstream part of this river (i.e., 9:14 h plus 30 min of dawn and of dusk. Light intensity and
below the fish ladder) a self-sustaining population of exotic photoperiod were automatically set with a photoperiod mon-
rainbow trout cohabits with the Atlantic salmon. itor (SunMatch, Aquabiotech Inc.). We maintained water tem-
During August 2005, before hatchery-born fish were re- perature constant at 14 ± 1 C. Fish were fed with commercial
leased in the river, we sampled (by electrofishing) 250 YOY food pellets. Daily food ration (4% of the total wet biomass per
Atlantic salmon at two locations above the dam (these fish channel and per day) was dispensed at the upstream end of
are hereafter referred to as the ‘‘wild group’’). In addition, the channel.
we sampled 100 YOY rainbow trout in the downstream part The behavioural experiment involved seven competitive
of the river. During the same period, we haphazardly sampled treatments (Table 2) designed to separate the effect of adding
25 YOYs from each of 10 families produced in 2005 for the a given competitor from a simple density effect (see Weber
supportive breeding program. These 250 fish are hereafter re- and Fausch, 2003). Firstly, we tested each group indepen-
ferred to as the ‘‘hatchery group’’. dently, only varying their intraspecific densities (i.e. in treat-
We transferred all fish groups to the laboratory and raised ments 1 and 3, we observed three fish per channel and in
them in separate holding tanks. They were fed ad-libitum with treatments 2 and 4 we observed six fish per channel).
1992 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

Secondly, we assessed behaviour when the two salmon

comprised 10 mM Tris–HCl [pH 9.0], 1.5 mM MgCl2, 0.1% Triton X-100, 50 mM KCl. The concentration of dNTPs was 10 mM each. References denoted with * correspond to loci that were directly
Description of the ten microsatellites markers used to compare genetic parameters between captive-born and wild-born Atlantic salmon. Number of alleles (A) is presented for each locus. The buffer
Poteaux et al. (1999)
Cairney et al. (2000)
Cairney et al. (2000)
groups were in contact together (i.e. in treatment 5 we ob-

Eackles and King*

King et al. (2005)

King et al. (2005)

Rise et al. (2004)
Rise et al. (2004)
Reference
served three fish of each group per channel, Table 2). Finally,

O’Reilly et al.*
Slettan et al.*
we assessed behaviour when the two salmon groups were
in contact with the rainbow trout (i.e. we independently ob-
served three fish of each group together with three rainbow
trout per channel in treatments 6 and 7, Table 2). Each treat-
ment lasted five days, including a three-day acclimatisation
period followed by two days of observation. Each treatment
5 min at 94, 34 · (45 s at 94, 45 s at 60, 120 s at 68), 10 min at 68

5 min at 94, 34 · (45 s at 94, 30 s at 60, 120 s at 68), 10 min at 68

5 min at 94, 34 · (45 s at 94, 30 s at 60, 120 s at 68), 10 min at 68
3 min at 94, 35 · (50 s at 95, 50 s at 60, 50 s at 72), 3 min at 72

3 min at 96, 32 · (50 s at 95, 50 s at 60, 50 s at 72), 5 min at 72

3 min at 94, 32 · (45 s at 94, 45 s at 57, 60 s at 72), 5 min at 72

3 min at 94, 32 · (45 s at 94, 45 s at 57, 60 s at 72), 5 min at 72
3 min at 94, 32 · (45 s at 94, 45 s at 57, 60 s at 72), 5 min at 72
was replicated four times over a period of 24 days, with new
2 min at 94, 35 · (30s at 94, 30s at 55, 30 s at 72), 5 min at 72

2 min at 95, 35 · (45 s at 95, 1 s at 59, 45 s at 72), 5 min at 72

fish used for each replicate (i.e. no fish was ever used twice).
During the experiment, fish body weight was 3.22 ± 0.92 g
Cycle (temperature in Celsius degrees)

(mean ± SD), but it varied among replicates (one-way ANOVA,

p = 0.03), with fish from the last replicate being bigger. How-
ever, within replicates, there were no size differences be-
tween treatments (nested ANOVA, p = 0.21) or among groups
and/or species (nested ANOVA, p = 0.83). When wild and
Table 1 – Microsatellites used to compare the genetic characteristics of wild-born versus hatchery-born Atlantic salmon

hatchery salmon were observed together, fin erosion (particu-

larly of the pectoral fins) of hatchery fish permitted the obser-
ver to easily distinguish the two groups without specific
marking.
Each channel was observed for a 10 min period in the
morning (i.e. between 9 a.m. and 11 a.m.). We measured three
individual behavioural variables: (1) the proportion of time
spent in the pool (by default, the time spent in the riffle is
the total time of observation minus the time spent in the
pool) (2) the proportion of time being active (a fish was consid-
ered active when it was out of the substrate, facing the cur-
rent, and propped up on its pectoral fins) and (3) number of
aggressive interactions (chases, displays and nipping) initi-
Taq (U)

ated by each fish.

0.5
0.5
1.5
0.5
0.4
0.3
0.2
0.2
0.2
0.2

2.5. Statistical analyses

2.5.1. Genetic analyses

dNTPs (ll)

Individual heterozygosity (multilocus heterozygosity) levels

0.45
0.45
0.5
0.3
0.3
0.3
0.3
1
1
1

were scored as either heterozygous (1) or homozygous (0),

and these scores were averaged for all 10 loci for each individ-
ual. Differences between the two groups were then assessed
using a Mann–Whitney U-test. To compare the allelic richness
Rx buffer (ll)

(number of alleles per locus) between groups, a correction for

sample size was made using the allelic richness option in
1.9
1.9
1
1
1
1
1
1
1
1

FSTAT 2.9.3 software (Goudet, 1995). We also used a Mann–

Whitney U-test to compare the number of alleles between
the two groups. Furthermore, we compared allele frequencies
between the two groups using Fisher’s exact test as described
Rx volume (ll)

by Raymond and Rousset (1995a). This test was applied for

each locus independently (Bonferroni corrections were ap-
13.5
13.5

plied to account for multiple comparisons) and for all the loci
10
10
10
10
10
10
10
10

submitted by authors to GeneBank.

together. These tests were performed using GENEPOP version

3.4 (Raymond and Rousset, 1995b). Finally, we tested whether
bottleneck (i.e., a drastic reduction in the number of effective
breeders) effects occurred in each of the two groups. Indeed,
14
20
20
11
12
11
23
24
A

because of the small wild population size in river Malbaie, it

5
4

is possible that this population suffered a bottleneck well be-

fore the restoration program was initiated. In the captive-
Ssa 401UOS
Ssa 417UOS

SSSOSl 417
CA 054978
CA 054565

group, a bottleneck is expected as only a small portion of

Strutta-12
SSAD 237

SSAD 71
SsaD 85
Ssa 197

the total pool of genitors is used to produce progeny. After a

Locus

bottleneck event, the allelic diversity is expected to decline

faster than heterozygosity. Thus, the observed heterozygosity
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9 1993

Fig. 1 – Landmarks used for morphological measurements. 1–2 Fork length (FL), 3–4 maximum body depth (BD), 1–7 head
length (HL), 5–6 head depth (HD), 8–9 orbital length (OL), 10–11 orbital depth (OD), 1–5 distance between tip of the snout and
highest head height (SHL), 12–13 pectoral fin length (PCL), 1–3 predorsal length (PDL), 1–14 prepelvic length (PPL), 3–15 distance
between origins of the dorsal and anal fins (ODAFL), 3–16 distance between the origins of the dorsal and adipose fins
(ODADFL), 17–18 distance between insertions of the adipose and anal fins (OAAFL), 18–19 caudal peduncle length (DPL), 20–21
caudal peduncle depth (CPD), 22–23 minimum caudal fin height (MinCFH), 24–25 maximum caudal fin height (MaxCFH).

Table 2 – Design of the experiment used to compare the using a Bonferroni procedure (so that the acceptable signifi-
behaviours of wild-born versus hatchery-born Atlantic cance level was reduced to a < 0.05/16 = 0.003).
salmon
Wild-born Hatchery-born Rainbow 2.5.3. Behavioural analyses
salmon salmon trout A two-way MANCOVA was computed to test whether the gen-
eral behaviour of the fish changed according to origin (wild or
Low intraspecific W 3 – –
High intraspecific W 6 – –
hatchery) and competitive treatments (see Table 2). We used
Low intraspecific H – 3 – the averaged body length of Atlantic salmon in each replicate
High intraspecific H – 6 – and for each group as the covariate. All two-term interactions
Mixed intraspecific 3 3 – were considered in this analysis. If the MANCOVA was signif-
Interspecific W 3 – 3 icant, we performed three independent ANCOVAs to compare
Interspecific H – 3 3
(i) the aggression rate, (ii) the time spent in the pool and (iii)
Experimental design used to evaluate the effects of intraspecific the time spent being active. The aggression rate was log(x + 1)
and interspecific competition on the behaviour of hatchery-born transformed and the two other behaviours were arcsine
and wild-born Atlantic salmon. The number of fish introduced in
transformed to meet the assumption of normality and homo-
each treatment (seven treatments) is indicated. ‘‘W’’ means wild-
scedasticity. Initially, a ‘‘trial’’ factor was included in the mod-
born fish and ‘‘H’’ means hatchery-born fish. Each treatment was
replicated four times (n = 4) and new fish were used for each el to account for possible temporal effects. As it was not
replicate. significant, this term was excluded from the final models.
All statistical analyses were performed using R version
should be larger than the heterozygosity expected from the 2.2.1 (R Development Core Team, 2005).
observed allele number at mutation-drift equilibrium (Cornu-
et and Luikart, 1996). We tested this assumption using the 3. Results
BOTTLENECK software (Cornuet and Luikart, 1996). This soft-
ware used sign test to compare the observed number of loci 3.1. Genetic analyses
with heterozygosity excess to the number expected under
the mutation-drift equilibrium (Cornuet and Luikart, 1996). When all loci were pooled, allele frequencies significantly var-
ied between the two groups (Fisher exact test, v2 = +1,
2.5.2. Morphometric analyses p = 0.000, Table 3A). Seven out of the ten loci we compared
We used ANCOVAs (analyses of covariance) to asses shape showed different frequencies between the two groups after
differences between the two groups of fish while controlling the Bonferroni correction (Table 3A). As illustrated in Fig. 2,
for the allometric effect of body size on each morphological some of these loci showed marked differences, with each
trait. We first computed a multivariate ANCOVA (MANCOVA) group being characterized by specific patterns of allelic fre-
with the total body length of each fish as the covariate and quencies and sometimes by private alleles with high frequen-
the origin of the fish as categorical predictor. The resulting cies. The allele frequencies for all the ten loci used in this
two-term interaction was also included to test for allometric experiment are available upon request to the corresponding
differences between the two groups of fish. If the MANCOVA author. We also found that these frequency differences trans-
was significant, we then used a univariate ANCOVA to assess lated into a trend whereby both individual heterozygosity and
how each trait independently differed between each group. allelic richness tended to be lower in the hatchery than in the
Significant p-values were corrected for multiple comparison wild group (Table 3B). These differences, however, were
1994 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

Table 3 – Genetic parameters of wild-born versus hatch- SSAD 237

390
ery-born Atlantic salmon

Fisher exact test 370

(A) Allelic frequencies 350

CA054978 0.001 ± 0.000
CA 054565 0.198 ± 0.002 330
Ssa 401UOS 0.000 ± 0.000
Ssa 417UOS 0.000 ± 0.000 310
SSAD 237 0.000 ± 0.000
Strutta-12 0.000 ± 0.000 290
Ssa 197 0.031 ± 0.001
SSSOSl 417 0.053 ± 0.002 270
SsaD 85 0.000 ± 0.000
SSAD 71 0.000 ± 0.000 250
All loci 0.000
225
Hatchery fish Wild fish Strutta-12
(B) Genetic diversity 220
Allelic richness 8.61 ± 1.00 14.87 ± 4.08
Multilocus heterozygosity 0.75 ± 0.02 0.81 ± 0.02 215

Alleles size(bp)
Results of several tests used to compare genetic parameters
between hatchery-born (‘‘Hatchery fish’’) and wild-born (‘‘Wild
210
fish’’) Atlantic salmon. Table (A) – results (p-value ± SD) of Fisher
exact tests used to compare the allelic frequencies, for each mar- 205
ker independently and for all the loci combined, between the
hatchery and wild groups. Table (B) – genetic diversity (mean ± S.E. 200
for allelic richness and multilocus heterozygosity respectively) for
both groups of salmon. Bold p-values are significant after Bon- 195
feronni corrections.
190

marginally non-significant (multilocus heterozygosity; Mann– 380

Whitney U-test, z = 1.87, p = 0.06 and allelic richness; SSAD 71
z = 1.68, p = 0.09).
350
The number of loci showing heterozygosity excess was sig-
nificantly higher than what expected by chance for the cap-
320
tive-born group (10 out of the 10 loci; sign test, p = 0.006),
indicating that the small number of genitors used in the cap-
tive pool created a recent genetic bottleneck. In contrast, the 290
number of loci showing heterozygosity excess did not differ
significantly from what was expected by chance in the wild- 260
born group (7 out of the 10 loci; sign test, p = 0.373).
230
3.2. Morphometric analyses
200
The shape of wild-born fish significantly differed from that of Wild fish Hatchery fish
the hatchery group (MANCOVA, effect of the fish body length,
Fig. 2 – Allelic frequencies of wild-born versus hatchery-
Wilks’ k (1, 16) = 0.008, p < 0.001; effect of the origin of the fish,
born Atlantic salmon. Schematic illustration of relative
Wilks’ k (1, 16) = 0.274, p < 0.001; interaction term, Wilks’ k
allelic frequencies of three out of seven loci (SSAD 237,
(1, 16) = 0.550, p = 0.055). At the univariate level, 6 out of the
Strutta-12 and SSAD 71, see Table 3) that showed significant
16 traits we measured significantly differed between the two
frequency differences between hatchery-born (‘‘Hatchery
groups (Table 4). When ranked according to the F value, the
fish’’) and wild-born (‘‘Wild fish’’) Atlantic salmon. These
greatest differences between the two groups involved the
three loci were chosen for illustration as they displayed the
depth of the head and the length of the pectoral fins (Table
highest differences between groups. Allele frequencies for
4). Specifically, for a given length, wild fish had the deepest
all the loci are available upon request to the corresponding
heads and the longest pectoral fins. Other functionally impor-
author.
tant traits, which remained larger in the wild group following
size correction, were the maximum span of the caudal fin and
the depth of the caudal peduncle (see Table 4). It is worth not- the two groups. Specifically, the slope of the relationship be-
ing that for one trait (the orbital depth, see Table 4) we de- tween the orbital depth and the body length of Atlantic sal-
tected a significant interaction term (p < 0.003) indicating mon was higher in the hatchery group (slope = 0.074) than
that the allometric relationship of this trait differed between in the wild group (slope = 0.039).
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9 1995

Table 4 – Morphological characteristics of wild-born versus hatchery-born Atlantic salmon

Response variable Hatchery fish Wild fish F value p-value

Pectoral fin length 0.058 (±0.020) 0.057 (±0.008) 53.29 0.000

Head depth 0.007 (±0.003) 0.007 (±0.002) 22.18 0.000
Head length 0.005 (±0.003) 0.005 (±0.003) 17.43 0.000
Maximum caudal fin height 0.014 (±0.006) 0.013 (±0.008) 12.05 0.001
Minimum caudal fin height 0.007 (±0.005) 0.007 (±0.005) 10.56 0.002
Caudal peduncle depth 0.005 (±0.004) 0.005 (±0.003) 8.77 0.003
Distance origins of the dorsal and anal fins 0.004 (±0.003) 0.004 (±0.003) 5.08 0.028
Prepelvic length 0.002 (±0.002) 0.002 (±0.001) 4.46 0.039
Orbital depth 0.004 (±0.005) 0.004 (±0.004) 2.30 0.134*
Predorsal length 0.006 (±0.011) 0.006 (±0.003) 1.85 0.179
Caudal peduncle length 0.004 (±0.009) 0.004 (±0.005) 0.99 0.330
Distance insertions of the adipose and anal fins 0.002 (±0.005) 0.002 (±0.005) 0.49 0.483
Maximum body depth 0.002 (±0.003) 0.002 (±0.007) 0.27 0.601
Distance outer tip of the snout/highest head height 0.001 (±0.006) 0.001 (±0.005) 0.19 0.657
Orbital length 0.001 (±0.005) 0.001 (±0.004) 0.14 0.701
Distance the origins of the dorsal and adipose fins 0.001 (±0.002) 0.001 (±0.002) 0.14 0.705

Results of ANCOVAs used to compare each morphological trait (see Fig. 1 for a description of the traits) independently between hatchery-born
(‘‘Hatchery fish’’) and wild-born (‘‘Wild fish’’) Atlantic salmon. The means corrected for fish body length (±SE) for each trait and each group are
given for comparison. Bold p-values are significant after Bonferoni corrections. A star (*) indicated trait(s) for which a significant interaction
term between fish body length and origin of the fish was detected.

3.3. Behavioural analyses different patterns according to the behaviour we considered

(Table 5B). For the two variables related to habitat use (time
The general behaviour differed significantly between wild spent in the pool and time spent in active swimming), we
and hatchery fish and also between competitive treatments found significant differences among the competitive treat-
(Table 5A). When all the behaviours were considered together ments but no differences between hatchery-born and wild-
in a single analysis, differences between wild and hatchery born fish (Table 5B). For both groups, fish were found more of-
fish were consistent across competitive treatments as the ten in pools and were more active when rainbow trout was
interaction between ‘‘groups’’ and ‘‘competitive treatments’’ also present in the channels (Fig. 3a and b). Concerning the
was not significant (Table 5A). Univariate analyses revealed aggression rate, we found a significant effect of individual

Table 5 – Statistical comparison of the behaviours of wild-born versus hatchery-born Atlantic salmon

Source of variation d.f. Wilks’ k p-value

(A) Multivariate analysis

Body length 3,19 0.79 0.248
Groups 3,19 0.50 0.007
Competitive treatments 9,19 0.36 0.027
Body length * groups 3,19 0.91 0.627
Body length * competitive treatments 9,19 0.67 0.602
Groups * competitive treatments 9,19 0.65 0.534

Response variables

Time spent in the pool Time spent being active Aggression rate

(B) Univariate analyses

Body length F1,19 0.17 2.51 4.83
P-value 0.678 0.129 0.043
Groups F1,19 1.08 0.01 31.92
P-value 0.309 0.907 <0.001
Competitive treatments F3,19 4.39 3.14 2.33
P-value 0.016 0.049 0.112
Body length * groups F1,19 0.39 0.97 1.25
P-value 0.539 0.335 0.280
Body length * competitive treatments F3,19 0.61 0.44 2.29
P-value 0.610 0.726 0.116
Groups * competitive treatments F3,19 0.37 0.17 3.82
P-value 0.777 0.915 0.011

Multivariate (A) and univariate (B) analyses of variance used to compare the behavioural responses (time spent in the pool, time spent being
active and aggressive rate) between hatchery-bred and wild Atlantic salmon under different competitive treatments. Analysis of variance
included the fixed effects of groups and competitive treatments. Significant p-values (p < 0.05) are in bold.
1996 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

1.4 tion indicated that hatchery fish differed from wild fish but
a Wild fish only in some of the treatments (Table 5B, Fig. 3c). Particularly,
Arcsine (time spent in a pool)

1.2 Hatchery fish hatchery fish were more aggressive than wild fish only in
presence of their wild conspecifics or with the rainbow trout
1.0 (Fig. 3c).

0.8

0.6 4. Discussion

0.4 Here, we applied an integrated approach to assess phenotypic

and genetic differences between wild- and captive-born sal-
0.2 mon in the context of a supportive breeding program. We
highlighted significant genetic, morphological, and behav-
0.0 ioural differences between the progeny of captive-bred and
1.2 wild-born Atlantic salmon. Moreover, we showed that both
Wild fish
Arcsine (time spent being active)

b phenotypic and genetic changes can arise even if the genitors

1.0 Hatchery fish share the same brood-stock and after only a few months of
rearing in a controlled environment.
0.8 Taken individually, our results are consistent with previ-
ous observations concerning the effects of captivity on the ge-
netic and phenotypic integrity of wild species. For instance,
0.6
we found that the captive-bred salmon (i) had allelic frequen-
cies that significantly varied from the wild-born progeny and
0.4
(ii) tended to have lower genetic variability. Thus, even if the
genitors share the same brood-stock, the single breeding
0.2
event that separated the two experimental groups impacted
the genetic integrity of the target wild population. The obser-
0.0 vation that observed heterozygosity was larger than the het-
1.0 erozygosity expected from the observed allele number at
c Wild fish mutation-drift equilibrium in the captive-group probably re-
Log (aggression rate + 1)

0.8
Hatchery fish sults from a bottleneck inherent in the low number of geni-
tors used in captivity (Ryman et al., 1995; Tessier et al., 1997;
Kraaijeveld-Smit et al., 2006). It is worth noting that before
0.6 the restoration program began in river Malbaie, the popula-
tion size was relatively small, as for most populations that
are endangered or exploited (Smith and Bernatchez, 2008).
0.4 However, it did not seem that this low population size was
sufficient to induce a detectable bottleneck in the wild-born
0.2 group. These results suggest that the number of breeders (or
refreshment rate) used in supportive design should be care-
fully estimated to avoid undesirable genetic effects.
0.0 Similarly, significant morphological and allometric differ-
Low intra High intra Mixed Interspe. ences were detected between captive-bred and wild-born sal-
density density intra mon, with the strongest changes observed for fin lengths and
other aspects of body shape, that are functionally important
Fig. 3 – Behavioural repertory of wild-born versus hatchery- for swimming. These results concur with those obtained for
born Atlantic salmon. Patterns of behavioural responses [(a) other animal species (e.g. Håkansson and Jensen, 2005) and
time spent in a pool, (b) time spent being active and (c) particularly with those obtained for salmonids (Kostow,
aggression rate] of hatchery-born (‘‘Hatchery fish’’, white 2004; Dahl et al., 2006, reviewed in Weber and Fausch, 2003).
bars) and wild-born (‘‘Wild fish’’, black bars) Atlantic salmon As demonstrated by Kostow (2004) in rainbow trout, the mor-
when reared under four different competitive treatments phological differences seen in captive-bred individuals were
see Table 2 for a description of the treatments. Data are the directly associated with a higher mortality rate in the wild.
mean (±S.E.). Each treatment was replicated four times This link has been interpreted as a consequence of the re-
(n = 4) and new fish were used for each replicate. duced ability of captive animals to occupy favourable habitats
(Weber and Fausch, 2003). Although we failed to detect signif-
icant differences in habitat use by captive-bred and wild-born
body length (Table 5B) with bigger fish being on average more animals in our laboratory setting, an association between
aggressive (results not shown). Irrespectively of individual morphology and habitat use seems highly plausible in the
body length, we found a significant interaction between wild. Indeed, morphological traits such as long paired fins
groups and competitive treatments (Table 5B). This interac- and a large caudal peduncle and caudal fin facilitate the
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9 1997

exploitation of habitats such as high current velocity zones, at environments and when they interbred with wild conspecif-
lower energetic costs (Arnold et al., 1991; Letcher, 2003; Páez ics. This implies that further studies should be specifically de-
et al., 2008). signed to elucidate the relative importance of genetic versus
Changes in behavioural characteristics such as activity or environmental factors (and their interaction) on the pheno-
aggression rate have also been associated with poor survival typic differentiation of captive-bred and wild animals during
rate of captive fish in the wild (i.e. a high predation rate, see Biro early ontogeny.
et al., 2004). Here, in accordance with many other studies, we The number of breeding events in captivity separating our
found that captive-bred animals were on average more aggres- two groups of fish was difficult to evaluate. Indeed, the wild-
sive than wild-born conspecifics. This suggests that the proto- born fish we used here might have originated from captive-
col used to raise fish under hatchery conditions induces reared fish previously released in the River Malbaie. Similarly,
behaviours that may be maladapted for surviving in the wild the genitors that were used by the hatchery to produce the
or that may be detrimental for wild populations (Biro et al., captive-bred fish might themselves have originated from cap-
2004; McPhee, 2004; Mathews et al., 2005; Kelley et al., 2006). tive-bred fish, signifying in this case that more than a single
We also demonstrated that such a behavioural difference breeding event could have separated purely-wild fish from
between groups was highly dependent on the social environ- captive-bred fish. Araki et al. (2007b) recently demonstrated
ment (i.e. density and type of competitors). Indeed, captive- that the effect of captivity on fitness was cumulative with a
bred fish were more aggressive only when together with their fitness decline of 37.5% per captive-reared generation. Thus,
wild-born conspecifics or when together with rainbow trout. the phenotypic and genetic differences we report might
It is worth noting that this difference was due to a concomi- directly reflect this cumulative effect of captivity. These
tant decrease and increase in aggression of the wild and differences are expected to increase if measures are not taken
hatchery group, respectively. This also indicates that wild- to ensure that genitors used in captivity have not been them-
born salmon strongly modify their natural behaviour (i.e. in selves bred in captivity.
comparison to the purely intraspecific treatments) when fac-
ing captive-bred salmon and/or rainbow trout. This behav-
ioural plasticity has several important implications for 5. Conclusions and implications
supportive breeding programs. First, by being more aggressive
when together with wild-born salmon, captive-raised ani- We showed that using genitors from a ‘‘local’’ brood-stock and
mals could exert a new selective pressure on wild-born indi- a limited rearing period in captivity did not prevent the mor-
viduals, as suggested by Blanchet et al. (2007) in the case of phological, behavioural and genetic divergences that have
competition between exotic and native salmonids. Second, commonly been identified as detrimental for target popula-
the behavioural response of Atlantic salmon differed between tions. Therefore, the progeny produced in such supportive
groups when facing an exotic competitor. This result suggests breeding programs does not meet the criteria necessary to en-
that the captive environment can change behavioural charac- sure preserving the genetic and ecological integrity of wild
teristics that are relevant to biological interactions such as populations. In view of these results and following the pre-
interspecific competition. cautionary principle, we argue that such supportive breeding
Taken as a whole, our results provide insight into the programs cannot be considered as acceptable conservation
mechanisms underlying the different phenotypic changes strategies, at least in their present form. However, such pro-
we documented. In the absence of genetic data, many authors grams could easily be improved. For instance, the first aim
have hypothesized that because of a common brood-stock of these programs should be maintaining the genetic diversity
(hence a common genetic background) phenotypic plasticity and allelic frequencies of the native population rather than
predominantly determines phenotypic differences between maximizing production. To do so, the genetic structure of
captive-bred and wild animals (Kostow, 2004; Dahl et al., the native population must be well known, the census size
2006). This hypothesis is particularly attractive when consid- of the captive breeders must be adequately calculated and
ering animals that phenotypically diverge within a single frequently refreshed, and factorial breeding designs should
generation of captivity. In our case, phenotypic plasticity be favoured (Fiumera et al., 2000, 2004; Duchesne and Bernat-
probably contributes in part to the phenotypic differentiation chez, 2002; Wedekind, 2002). Also, it has recently been dem-
we observed between groups. However, since we observed ge- onstrated that equalizing milt volume of males reduces the
netic differences between both groups, we can also suggest loss of genetic variation in a captive population (Wedekind
that these phenotypic differences also result from the pheno- et al., 2007). Efforts should also be devoted to avoid using gen-
typic expression of functional alleles present in the wild-born itors that are themselves issued from captive brood-stock and
group that are not expressed in captivity (or vice versa) hence to limit the cumulative effects of captivity (Araki et al.,
(Wedekind, 2002; Heath et al., 2003). Thus, if genetic factors 2007b). Second, selection and/or plasticity acting during cap-
contribute to the differentiation of captive-bred and wild- tivity must be reduced to avoid phenotypic differentiation.
born animals, one can expect potential detrimental effects This can be achieved by reducing the captive period. Metcalfe
for wild populations in the case of interbreeding between cap- et al. (2003) proposed to limit the period of captivity to egg
tive-bred and wild-born animals (Araki et al., 2007b; Roberge production with release at the egg stage. Another possibility,
et al., 2008). For instance, Araki et al. (2007b) used pedigree albeit more costly, would be to rear captive juveniles in more
analyses to demonstrate that in the rainbow trout the genetic natural conditions by increasing the physical heterogeneity of
effects of domestication strongly reduced subsequent repro- the captive habitat or by building artificial nursery habitat
ductive capabilities when captive fish were moved to natural (see Berejikian et al., 2000). Once this has been achieved,
1998 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 1 9 8 9 –1 9 9 9

short-term and long-term assessment of the costs (both eco- recruit at higher rates than hacked falcons in a common
logical and economical) and benefits of supportive programs environment. Biological Conservation 131, 453–458.
can be performed in the wild through the use of parentage Cairney, M., Taggart, J.B., Hoyheim, B., 2000. Characterization of
microsatellite and minisatellite loci in Atlantic salmon (Salmo
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et al., 1997; Hansen, 2002; Brown et al., 2006; Adamski and Cornuet, J.M., Luikart, G., 1996. Description and power analysis of
Witkowski, 2007; Araki et al., 2007a, b). two tests for detecting recent population bottlenecks from
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Acknowledgments
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lane Rossignol who helped on several aspects of the work. Leaniz, C., Gross, M.R., Newbury, R., Nielsen, J.L., Power, M.E.,
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