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First published online January 19, 2006
Journal of Experimental Biology 209, 504-509 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02019
Early rearing environment impacts cerebellar growth in juvenile salmon
Section Neurobiology, Physiology and Behavior, UC Davis, Davis CA, USA
* Author for correspondence (e-mail: rlkihs{at}ucdavis.edu)
Accepted 29 November 2005
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Summary |
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Key words: salmon, Oncorhynchus mykiss, fish, brain, enrichment, development, conservation, hatchery
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). This study did not investigate to what degree these
differences reflected `nature' or `nurture', i.e. genetic selection for a type
of brain that is adaptive for captive living, or, developmental responses to
the hatchery environment within a single generation. Variation in brain size
is routinely observed among wild and domesticated strains of animals following
generations of artificial selection in captive environments. For example,
turkeys, rabbits, pigs, sheep, llamas, ferrets, cats and dogs all show
dramatic reductions in brain size in domesticated forms
(Ebinger and Rohrs, 1995; for
a review, see Kruska, 1988).
Because of this link to domestication, large neuroanatomical variation between
strains is often attributed to selection processes. In fishes, developmental
plasticity has also been cited as a potential contributing factor to neural
phenotype, but the degree to which brain growth can be influenced by proximate
environmental conditions is largely unknown (e.g.
Francis et al., 1993;
Huber et al., 1997;
Brandstatter and Kotrschal et al., 1998;
Hofman and Fernald, 2000;
Lema et al., 2005). In this
study, we examine how the early rearing environment influences neural and
behavioral development in steelhead trout O. mykiss.
A fish's brain grows continuously throughout its lifetime, suggesting that
brain growth may be impacted by the environmental conditions a fish
experiences. Such environmental feedback on brain development in teleost
fishes is likely to influence individual behavior and habitat preferences into
adult life (Zaunreiter et al.,
1991; Kotrschal and
Palzenberger, 1992). Salmon are an ideal model system for studying
environmentally induced changes because, in addition to brain size, many
phenotypic traits vary among individuals reared in wild and captive
environments. Differences include variation in growth rate, timing of sexual
maturity, and anti-predator, feeding and sexual behaviors
(Olla et al., 1994;
Fleming et al., 1997;
Gross, 1998;
Flagg et al., 2000). These
differences may influence the low survival observed in hatchery fish upon
release into the wild (Jonsson et al.,
2003). However, little is known about how the hatchery environment
itself may be playing a role in generating phenotypic differences between
strains.
In nature, salmon spend the first year of their life in dynamic and
heterogeneous fresh-water streams. Eggs are laid in gravel nests and hatch
into alevins (yolk-sac fry). Over a period of weeks, alevins absorb their yolk
sac before emerging from the gravel as free-swimming fry. By contrast, fish
reared domestically are nourished by clean, well-aerated water, but they are
also packed in rearing tanks, with little environmental variability or
enrichment, and no natural substrate. Previous studies suggest that the
structural environment experienced by alevins may initiate a trajectory for
later juvenile development. For example, alevins reared in standard hatchery
tanks enriched with naturalistic substrate are larger as fry than fish reared
without structure (Leon, 1975;
Hansen and Møller,
1985). Moreover, alevins reared with this type of enrichment (i.e.
gravel) may also develop into better swimmers that are more able to avoid
predators as fry (Bams, 1967).
These results indicate that structure influences alevin development, but
whether or not experiencing structure during ontogeny affects brain growth is
unknown.
Working in both laboratory and wild settings, we examine whether the structural environment fish experience immediately after hatching influences neural and behavioral development in steelhead trout (O. mykiss). In the laboratory, we reared hatchery-origin steelhead from the egg through the alevin life-stage in simple and structurally complex rearing treatments. For the field study, alevins were reared in a more naturalistic setting in artificial nests deployed in the American River (Sacramento County, CA, USA). For both experiments we measured total brain volume in addition to the relative volumes of four clearly defined structures (Fig. 1): the olfactory bulb (OB), the telencephalon (TE), the optic tectum (OT) and the cerebellum (CE).
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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12°C), flow-through (20 l min-1)
rearing tanks (1.2 mx0.6 mx0.6 m, density 2000 eggs/tank). These
two rearing environments were identical except that the bottom surface of
complex tanks was scattered with small stones (4 cm diameter, 1 stone/10
cm2). The photoperiod matched ambient conditions. Hatching began on
day 35 post-spawn and all fish were hatched by day 37 post-spawn. The alevin
life-stage lasted 12 days, at which time the fish began to emerge from the
bottom of the tank. Each day from hatching to emergence, a video recording (Sony Mini-DV video camera DCR-TRV18; Tokyo, Japan) was made of a tank, from above. The recordings were for 2 s at 10 min intervals during daylight hours (08:00 h to 16:30 h) for each treatment (one treatment tank/day). To assess differences in movement between treatments, we counted the number of alevins swimming along the bottom of the tank during each 2 s period (50 periods/tank/day). For both treatments, the number of moving fish per day did not change across the 10-day sampling period (regression, linear fit, F=0.0395, d.f.=9, P=0.8475). Data were normalized to area (number of moving fish m-2) because the video camera could not record the entire tank at once. On day 47 post-spawn, 30 fish from each tank were collected, over-anesthetized with MS222 (tricaine methane sulfonate: 10 mg kg-1 water), weighed and measured. Five fish from each tank were sampled for subsequent neural analysis. These fish were immersed in Bouin's fixative overnight, dehydrated in a graded ethanol series, and embedded in paraffin.
Field study
We next evaluated how brain growth compared between fish reared in the
laboratory and in a more typical setting in nature. Eggs were again obtained
from the Nimbus Salmon/Steelhead Hatchery on day 27 post-spawn and positioned
in two artificially constructed redds (i.e. nests) at sites chosen to
approximate natural steelhead nests in the American River, CA, USA (sites A:
38°37.8'N, 121°17.6'W and B: 38°35.4'N,
121°19.8'W). Within each redd we placed six egg incubation tubes
containing 25 eggs each and stones (3 cm diameter) collected from the
river. Egg tubes were constructed from PVC pipe (44.5 mm diameter, 300 mm
long), drilled with 18x 19 mm holes that were covered with mesh (0.35
mm). For each redd, a 22 cm deep depression was made in the gravel and tubes
were buried in an upstream progression. The temperature and flow rate of the
river varied throughout the course of the rearing period (0.76-1.17 m
s-1), but both were consistently higher than the laboratory
conditions. Alevins were reared in the river for 13 days until yolk sac
absorption. All fish were then removed and sacrificed (MS222: 10 mg
kg-1 water) on site. Of these fish, 36 individuals were randomly
selected for neural analysis. These fish were immersed in Bouin's fixative
overnight, dehydrated in a graded ethanol series, and embedded in
paraffin.
Neural analysis
Sections were cut transversely at 10 µm, mounted on charged slides,
Nissl stained and mounted with Permount® under a coverslip.
Cross-sectional area of the total brain and identified structures [the
olfactory bulb (OB), telencephalon (TE), optic tectum (OT) and cerebellum
(CE)] were measured serially and analyzed at regular 40 µm intervals using
Zeiss AxioVision® Software (Fig.
1). Volumes (including total brain volume) were calculated by
multiplying the area of each section by the section thickness and summing the
results. Measurements of total brain volume began on the section where the
first cells of the olfactory bulb were observed in the brain case, and ended
at the caudal pole of the corpus cerebella. Total brain volume measurements
included the medulla through to the termination of the cerebellum. Subdivision
demarcations followed published descriptions
(Northcutt and Davis, 1983;
Wullimann et al., 1996). All
measurements were done blind to the treatment groups being examined.
Statistical analysis
Differences in body weight and length between laboratory rearing treatments
were analyzed using a two-level nested analysis of variance (ANOVA), where
tanks were nested within treatments. Movement behavior was analyzed using a
Z-test. Variation among treatments in relative total brain volume was
analyzed using a Student's t-test. The relative volume of each
structure (olfactory bulb, telencephalon, optic tectum and cerebellum) was
analyzed using either a Student's t-test or a Wilcoxon Signed Ranks
test if the data did not conform to the assumptions of a parametric test. Body
and brain size comparisons among field sites were analyzed using a Student's
t-test. Comparisons of body size and the relative volume of each
brain structure between laboratory and wild-reared fish were analyzed using a
one-way ANOVA. If the model was significant, then this analysis was followed
by a Tukey-Kramer HSD to determine which groups differed from each other. The
relative total brain volume between laboratory and wild-reared fish was
analyzed with a Wilcoxon Signed Ranks test.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Field study
Seventy-three percent (N=110/150) and 69% (N=104/150) of
river-reared fish hatched and survived to collection in nest 1 and 2,
respectively. There were no body or brain size differences between the two
nest sites (length: site A 26.46±0.18 mm, site B 26.49±0.18 mm,
t1,10=-0.122, P=0.905; body mass: site A
15.29±0.31 mg, site B 14.95±0.31 mg,
t1,10=0.764, P=0.463; relative total brain
volume: site A 23.11±0.42 mm3 g-1, site B
24.27±0.34 mm3 g-1,
t1,8=-2.152, P=0.0636), even though the
temperatures varied between sites by as much as 1.2°C (site A
13-13.8°C and site B 13.62-15.0°C).
We found significant phenotypic variation in river-reared fish compared to their lab-reared counterparts. River-reared fish were larger than fish reared in both laboratory treatments (length: river 26.48±0.09 mm, F2,15=83.3585, P<0.0001; body mass: river 15.12±0.17 mg, F2,15=55.2434, P<0.0001). With respect to brain growth, fish reared in the river had larger total brain volumes than those reared in the laboratory (river: 23.8050±0.84 mm3 g-1, laboratory: 21.40±0.59 mm3 g-1, Z2,28=2.39168, P=0.016). However, river-reared fish had similar relative cerebellar volumes to fish reared with stones and both of these groups had larger relative cerebella than fish reared in simple tanks (Fig. 3; F2,28=7.7342, P=0.002). River-reared fish had larger relative telencephalon volumes than fish reared with stones, but they were not larger than those of fish reared in simple tanks (TE: river 0.083±0.001, F2,28=4.4309, P=0.022). We did not find differences among treatments in relative OB or OT volumes (OB: river 0.012±0.0003, F2,28=0.2605, P=0.773, OT: river 0.32±0.016, F2,28=1.1802, P=0.323).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Quester
and Schröder, 1997), which might, in turn, obscure
differences in other brain regions such as the OB and the TE
(Marchetti and Nevitt, 2003).
Because we used the same fixation techniques for both treatments, the
differences we observe in the cerebellum appear to be robust.
In other groups of fishes, cerebellar size among different species
correlates strongly with habitat type (pelagic or benthic), prey
maneuverability, as well as swimming ability
(Huber et al., 1997). However,
this is the first study in fish to show that variation in captive rearing
environments can result in brain differences that are on the same scale as
those commonly attributed to selection. Our results thus suggest that
proximate mechanisms can shape brain structures in fishes, and also initiate a
developmental trajectory that may facilitate survival in their local
environment (Fig. 4).
|
;
Broglio et al., 2003). In our
experiment, alevins moved less if stones were present, suggesting that the act
of negotiating a more complex habitat influences the development of the
cerebellum. It follows that, if alevins can establish a position in the tank,
they may also utilize yolk reserves more efficiently because they are less
active. More efficient energy consumption is likely to enhance growth,
including brain growth, and allow fish reared with cobble to get a `head
start' when they emerge from the gravel to become free-swimming fry. This idea
is attractive since results from several other studies suggest that alevins
reared with structure experience enhanced growth well into juvenile life
(Leon, 1975;
Hansen and Møller,
1985). In our study, structure, at least in the laboratory, did
not seem to promote enhanced growth since fish grew at similar rates
regardless of how they were reared. In addition, the presence or absence of
structure did not affect total brain volume, which suggests that the effect of
structure on the size of the cerebellum may not be solely the result of
changes in energy consumption.
We also found significant variation in brain growth between river and laboratory rearing environments. Fish reared in the river were larger and had larger total brain volumes than laboratory-reared fish, perhaps because of slightly warmer and more variable temperatures in the river. However, relative cerebellar volumes were similar between river-reared fish and those reared in the complex treatment. River-reared fish also had larger telencephalon volumes than fish reared with stones, but their telencephalon volumes were similar to fish reared in simple tanks. Thus, while offering fish a physically complex environment early on appears to alter cerebellar growth, our laboratory rearing environments did not produce brain growth comparable to that in the wild.
It is probable that a suite of factors contributed to the brain differences
we observed in the laboratory-reared fish. For example, in other fish species,
it has been shown that rearing density impacts on dendritic growth and
arborization. Jewel fish reared under crowded conditions develop fewer
dendritic spines on pyriform interneurons in the optic tectum
(Burgess and Coss, 1981).
However, in our study, rearing density was similar in both laboratory and
field experiments. Social status and other environmental factors (e.g.
temperature) also have been shown to influence the size or number of
neuroendocrine cells in the forebrain
(Miranda et al., 2003;
Semsar and Godwin, 2003),
suggesting that these factors also contribute to shaping the wild brain
phenotype. For example, in cichlid fish, changes in social status alter the
size of gonadotropin-releasing and somatostatin-containing neurons in the
preoptic area of the hypothalamus. These neurons are presumed to be involved
in growth and reproduction (Francis et
al., 1993; Hofman and Fernald,
2000).
While the mechanisms are unclear, in other taxa that have been more
rigorously studied, environmental enrichment is known to affect brain growth
and morphology (Rosenweig and Bennett,
1996; Kempermann et al.,
1997). In mice, for example, environmental enrichment has been
shown to influence neurotrophin protein and mRNA levels in the brain.
Neurotrophins, in turn, impact on neuronal cell proliferation and survival, as
well as structural changes, including synaptic connectivity
(Ickes et al., 2000;
Branchi et al., 2004;
Sale et al., 2004).
Alternatively, maternal deprivation and other forms of environmental stress
during juvenile development have been linked to reduction in the size of
specific brain structures as well as inhibition of cell proliferation as
animals mature (Coe et al.,
2003; Buchanan et al.,
2004; Mirescu et al.,
2004). For instance, male song birds that experience poor
nutrition during early rearing have smaller song control centers in the brain
as adult birds, and also have poorer song quality compared to birds that were
reared with proper nutrition (Buchanan et
al., 2003; Buchanan et al.,
2004).
We have not yet determined how morphological variation in cerebellar size
correlates with behavior as the fish age, but previous experiments indicate
that some types of hatchery enrichment strategies can influence the behavior
and survival of salmon. For example, steelhead reared in environments that
include underwater feeding, in-stream structure and overhead cover, were
socially dominant to fish reared in conventional environments
(Berejikian et al., 2000).
Further, in some studies, hatchery programs that include enrichment produce
fish that survive better during downstream migration than fish reared in
conventional hatchery environments, but results are inconsistent
(Maynard et al., 2003). In all
of these enrichment studies, fish were reared in standard hatchery conditions
until the first few months of life, thus enrichment protocols bypassed the
alevin life-stage altogether. In the current study, we noted that alevins
reared in tanks with structure were able to establish a position in the
stones, which allowed them to interact with neighbors in a more predictable
way than fish in tanks without stones. This observation suggests that natural
substrate may promote social learning in alevins, and may help to explain some
of the differences in behavior observed between hatchery and wild fish
(Metcalfe et al., 2003; for
North Sea cod, see Braithwaite and
Salvanes, 2005).
Potential neural correlates to these behavioral differences clearly need to
be explored. Because habitat manipulations are easy to implement, fishes may
serve as effective model systems for studying underlying mechanisms
contributing to these processes. Just as importantly, captive rearing is used
to propagate a variety of threatened and endangered fish species for release
into the wild. Until recently, little attention has been paid to the proximate
effects of the hatchery environment on the phenotype development and survival
ability of fish reared in captivity
(Braithwaite and Salvanes,
2005). Here, we have shown that rearing conditions dramatically
impact upon both behavior and brain growth, and that these effects begin very
early in life. These results point to new avenues for conservation researchers
to explore.
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Acknowledgments |
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