Risk taking and downstream migration in hatchery reared Atlantic salmon (Salmo salar) smolt
Fia Finn
Degree Thesis in Ecology 60 ECTS Master’s Level
Report passed: 01 June 2015 Supervisor: Tomas Brodin
Abstract
Individual variation and limited plasticity in behavior are factors that have been shown to shape populations and determine how well individuals are doing in different stages of life.
When salmon transform from parr to smolt and start the migration out to sea many factors together make an individual successful. The hypothesis of this study was that the boldness of individual smolt (1 and 2 year olds) is correlated to their inclination to migrate downstream.
The study also investigated difference in boldness and migration tendency between 1- and two year old smolt. Today, some hatcheries release smolt as both one and two year old and it is important to know whether there is any difference in behavior and migration intensity between age classes in order to make stocking programs more effective. To determine if the individuals differed in boldness, and/or displayed a bold behavioral type, two assays were performed in different contexts (novel environment and simulated predatory attack).
Downstream migratory intensity was, after behavior assays, quantified in an artificial stream.
I found that: i) the one year old smolts tended to be bolder in a predatory response assay than two year old smolt, ii) one year old smolts migrated less in the artificial stream compared to two year old smolt. Being bolder can have an effect on several aspects connected to fitness in the salmon life cycle and could affect the survival of a smolt migrating out to sea, even though no correlations to inclination to downstream migration were found in this study.
Key Words: Behavior, migration, risk taking, boldness, Salmo salar
Contents
1 Introduction 1
2 Materials and methods 3
2.1 Study system 3
2.2 Measuring boldness 3
2.2.1 Novel arena
4
2.2.2 Novel object
4
2.3 Downstream migration 4
2.4 Statistical methods 5
3 Results 5
3.1 Boldness in two contexts 5
3.2 Migration intensity and boldness 6
3.3 Effect of age on boldness 7
3.4 Effect of age on migration intensity 7
3.5 Condition and downstream migration 8
4 Discussion 9
4.1 Boldness in two contexts 9
4.2 Migration intensity and boldness 10
4.3 Difference in boldness and migration between 1- and 2
year old smolt 11
4.3.1 Boldness
11
4.3.2 Migration 11
5 Acknowledgments 12
6 References 14
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1 Introduction
Migration is a widespread behavior among animals which enables them to avoid competition and utilize new resources (Dodson 1997, Lucas and Baras 2001). It can be found in a number of different species from mammals and birds to zooplankton (Dingle and Drake 2007).
Migration has formative effects on populations as it effects the density of animals both spatially and temporally (Fryxell and Sinclair 1988). As a consequence of the importance of migration many aspects of it have been studied in order to understand the causes, mechanisms and consequences of migratory behavior. It has long been known that individuals within a species, or even within a population, differ in their migratory tendency (e.g. Skov et al. 2008). One well studied migrant is the Atlantic salmon (Salmo salar) that, when it reach a certain size, leave its rearing habitat in fresh water and start its migration towards the sea (Thorpe 1988, McCormick et al. 1998, Klemetsen et al. 2003). In order to tolerate the novel environment in the sea it goes through a number of physiological, morphological and behavioral changes before starting the downstream migration (Hoar 1988, Alexander et al. 1994, McCormick 1998). It changes position in the water column and goes from being bottom dwelling, solitary and fresh water tolerant to being pelagic, social and group living and physiologically adapted to life in the salty ocean (Hoar 1988, Iwata 1995).
This change is called smoltification and in the northern rivers of Sweden it takes place between the end of May and start of July (Alanärä et al 2014). An area that has gotten attention only in later years is the potential role played by individual behavior traits in controlling migration. However, the importance of individual variation in risk taking for downstream migration remains so far unknown.
The Atlantic salmon is not only a migrant with great impacts on the systems it inhabits (Kulmala et al. 2015) but also one of the most appreciated fish utilized to feed humans. To the demise of natural populations, salmon has been harvested for hundreds of years and more intensely so over the last century with the use of larger, more efficient equipment leading to a bigger human impact than ever. Although compensatory measures are being taken, such as rearing and releasing of smolt, the increased fishing, in combination with other detrimental factors such as increased damming for hydro power plants, has led to major decline in smolt- to-adult return rates (McKinnell and Karlström 1999, Kallio-Nyberg et al. 2011a, 2011b, Kulmala et al. 2015). With this in mind, it is clear that all new information about this species and the mechanisms behind what determines the successful completion of an individual's lifecycle are not only valuable from an ecological point of view but may also have great economic importance. For example, identifying behavioral variation and possible connection to individual’s inclination to migrate downstream could affect how we use habitat restoration and conservation measurements for fish populations in general and for potential threats to the Atlantic salmon in particular.
Consistent difference in behavior between individuals has been shown in a wide variety of taxa, even though they still display behavioral plasticity in some contexts or situations (Stamps 2007). These behavioral consistencies, across time or contexts, are referred to as either temperaments (Réale et al. 2007), coping styles (Koolhaas et al 1999), behavioral profiles (Groothuis and Trillmich 2011), animal personalities (Dall et al. 2004) or behavioral syndromes (Sih et al. 2004a, 2004b). Fish was among the first groups of animals used in the study of animal personality. The early work was performed on sticklebacks (e.g. Ehlinger and Wilson 1988) and sunfish (Wilson et al. 1993). For example, Wilson (1993) observed that individuals that were relatively risk-taking in comparison to others in one situation or context would also be more risk-taking in another context and suggested that the behavior displayed by these individuals was not random variability, but instead a result of selection.
Consistent between individual differences, i.e. getting the same rank-order of a behavioral trait between situations within a group of conspecifics that experience both situations, is nowadays discussed as an adaptive strategy (e.g. Wolf and McNamara 2012). In the last decades the number of studies investigating consistent individual differences have grown rapidly and many reviews have been published (e.g., Sih et al. 2004a, 2004b, Réale et al.
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2007, Sih and Bell 2008, Wolf and Weissing 2012) including some specifically focusing on fish (Toms et al. 2010, Budaev and Brown 2011, Conrad et al. 2011).
Consistent individual differences in behavior have been studied in the lab to a great extent and a question that has been raised in later years is, what ecological consequences do behavioral differences have for individuals and populations in the natural environment (Dingemanse and Réale 2005, Bolnick et al. 2011, Adriaenssens and Johnsson 2011a, Sih et al. 2012). Some of the consequences studied were the potential effects on an individual's reproductive success, community structure and population dynamics. Consistent individual differences in behavior may also in the end have an effect on our natural resources and how we should manage them (Mittelbach et al. 2014).
In this thesis focus lie on the bold-shy continuum. It describes the tradeoff individuals face between risk and reward when e.g. foraging, inspecting predators and in intraspecific competition (Wilson et al. 1994, Sih et al. 1994a). To feed in open water, for example, will put the individual in higher risk of predation but may also let it access richer food sources (Gliwicz et al. 2006). Similarly, to feed during daytime will expose prey to a higher degree of visually searching predators compared to night time but might increase your feeding rate (Fraser and Metcalfe 1997, Metcalfe et al. 1999, Ryer and Hurst 2008). Also, a more active individual may encounter more prey but also more predators (Fraser et al. 2001, Biro et al.
2004, Sundström et al. 2004). Many studies have shown correlations between behavior and performance. Bolder bighorn sheep (Ovis canadensis) tend to survive better in the wild (Reale et al. 2000). Bolder sunfish approach predators, get used to laboratory environment and feed more on prey (Wilson et al. 1994). Bold mosquitofish (Gambusia affinis) have been shown to be more risk taking and disperse more (Cote et al. 2010). Bolder killifish (Rivulus hartii) disperse further and grow faster (Fraser et al. 2001). Further, a study looking at partial migration in European roach (Rutilus rutilus) found that bolder individuals migrated (from lake to stream) to a higher degree (Chapman et al. 2011).
During migration to the sea the Atlantic salmon smolt will face many challenges having to deal with novel environments, predation by fish, birds and mammals (Serrano et al 2009).
The timing is important for the smolt that need to hit the time-window, or risk being mismatched with suitable temperatures and food availability in the oceans (Hansen 1987).
All though behaviors repeatedly has been shown important for dispersal, the importance of individual variation in risk taking behaviors for downstream migration remains unknown.
Identifying behavioral variation and possible connections to individual inclination to migrate downstream could provide valuable information for habitat restoration and conservation measurements and how to identify potential threats to Atlantic salmon populations.
Moreover, depending on where the population of Atlantic salmon is located they start their migration at different ages. Populations in southern latitudes commonly start migrating out to sea as one year olds. This is a result of warmer temperatures and thereby increased resources and a faster growth. In the northern waters however, smolt of the Atlantic salmon can be up to 3-4 years before starting to smoltify (McCormick 1998). In Swedish compensatory hatcheries salmon are fed more than the natural abundance and will therefore grow more in accordance to southern populations and smoltify both as one and two- year old.
After the first year the one year old smolt are sorted into those who smoltify and those who stay as parr creating two groups of smolt (one- and two year old). The one year old smolt will therefore be individuals with a higher growth rate. High growth rates have been connected to risk taking behavior in salmonidae (Biro et al. 2003a, 2003b, 2004, 2006) and in this thesis these potential differences between fast growing (1-year old) and slower growing (2-year old) smolt will also be investigated.
3 The aims of my thesis were:
1) Investigate if one- and two year old salmon smolt display consistant between individual variation in the shy/bold behavioral dimension over two different contexts.
2) Examine if individual boldness score predicts how actively individual salmon migrate downstream.
3) Examine if the two age classes of smolt differed in boldness and/or migration rate.
My main hypotheses were that i) there would be consistent individual variation in the bold- shy spectrum over contexts, ii) that bolder individuals would display a more active migratory behavior. iii) 1- year olds will display a bolder behavior and more actively migrate downstream than 2 -year old smolt
2 Materials and methods
2.1 Study system
The study was conducted at Norrfors compensatory hatchery (Vattenfall AB) (63°52´ N;
20°01´ E) which is located at the river Umeälven 10km east of Umeå, Sweden, between the 15th of April and the 18th of June. The experimental period was chosen to match the peak in downstream migration of salmon. The hatchery yearly produces 80 000 Atlantic salmon to compensate for the obstruction of the migration pathways of the salmon to and from the Baltic sea by the hydropower plant. The fish are reared in round indoor pools (Ø 8m, depth 1 m) supplied with water via a flow through system from the river, this means the fish at the hatchery experience the same temperature regime and water chemistry as the natural fauna in the river. The light conditions are also set to follow the natural regime. The fish are fed according to standard commercial protocol.
80 1-year olds were randomly sampled from the hatchery in Norrfors in april the 15th 2013.
They were tagged with pit-tags (12mm half duplex PIT tag (Biomark) inserted into the abdominal cavity), measured for weight (to nearest gram, mean±sd = 16 ± 5g) length (fork length, mean±sd = 115 ± 14mm. 60 2-year old smolt were additionally sampled and put through the same procedure (mean weight ±sd = 37 ±8g, mean fork length ±sd = 145
±12mm). All handling were done under anesthetic (MS222). From the length and weight, Fulton's condition factor (K = W/L3 , where W=the weight of the fish (g) and L is the length (here, fork length, in cm), (Ricker 1975)) was calculated. Fulton's condition factor is widely used in fisheries and general fish biology as an indicator of tissue energy reserves.
2.2 Measuring boldness
Two assays were preformed to measure boldness in two different contexts during three consecutive hours. The first explored how the individuals reacted to a novel environment (un-informed risk) and the second, performed on the same day, recorded response to a
"attack" by a novel object (informed risk). The assays were performed in 10 600 liter aquariums (184.1 x 46.9 x 72.4 cm) parted in two, resulting in two arenas of each 92.1 x 46.9 x 72.4 cm. Each day 2 individuals were screened in every arena (4 per aquaria), adding up to 40 individuals per day, and between trials the water was changed to avoid chemical cues and stress transfer between individuals.
4 2.2.1 Novel arena
The first behavioral assay was used to measure boldness in a situation where the fish had no information about the potential risk (un- informed) using a standard refuge emergence protocol (Yoshida et al.
2005, Brown et al. 2007). Each fish was individually placed in a black plastic refuge (46,9 x 20 x 30), and left to acclimatize for 30 min. Then the front wall of the refuge was lifted (fig. 1a) and the behavior of each
individual was recorded for 60 min using a web-cam. From this assay two behavioral measurements were extracted 1) "latency to enter novel arena" (in seconds) and 2)
"proportion of time spent in novel arena" (in seconds).
2.2.2 Anti-predation response
After the first assay the fish were caught with a small net and put in another refuge (a pipe, Ø= 20cm) to acclimatize for 30 min. Then the refuge was slowly lifted to make sure that the fish stayed in place. Following the removal of the refuge an orange bag filled with sand, Ø=8cm, was dropped from above the fish (fig. 1b) to simulate a predatory attack, similar methods was used by Johnsson et al (2001). After the drop the behavior of the fish was recorded from above for 30 min using a web-cam. Based on earlier experience I extracted two measurements that should accurately represent how boldness in the face of predation risk 1) time spent swimming in response to attack 2) duration of freezing response.
2.3 Downstream migration
Three days after the boldness assays the individuals were assayed for downstream migratory tendency in an artificial stream (fig. 2). Migration tests ran for four days in groups of 20, with two antennas placed in the artificial stream recording how many laps the pit-tagged fish made. The two year old fish was tested between June 4th and June 10th and the one year old fish between June 13th and June 25th. The time-periods were chosen to match natural migration peak of the two age classes in this river (Alanärä et al. 2014).
Three days after the boldness assay the fish were moved from their holding tanks into the migration study-pool (Ø 8 m, depth 1 m). Two pools were used simultaneously and as with the rearing-pools, the study-pools were continuously supplied with water from river Umeälven. The flow-through creates a current in the pool, with water circulating alongside the wall (fig. 2). The center of the study pools were sealed off, restricting fish from entering the area (fig. 2). A refuge from the current was created close to the middle of the pool so that fish could choose to rest from swimming the current or hide if they felt threatened. At the narrow passage between the enclosed area and the tank wall, two PIT-tag antennas was installed and connected to a Biomark half duplex reader. Fish passing the antenna were registered on the reader. Each
registration recorded the tag ID and the time and date of detection. The use of two antennas allowed to distinguishing between upstream and downstream movements. The reader collected data non-stop during the study period and inclination to run downstream was
Fig.1. The aquarium set-up used in our study to measure boldness in 1- and 2 year old smolt. In the left part (a) the "novel arena" is shown and in the right (b) simulated predatory attack.
Fig. 2. The pool with the artificial stream in which migratory intensity was measured.
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calculated as laps/96 hours (trial-period). After the experiment, the fish were released into river Umeälven.
2.4 Statistical methods
Since I collected four measurements of boldness measured in the two assays I used principal component analysis (PCA) to sum up the variation in all four variables along a reduced number of uncorrelated components. Only principal components (PC) with eigenvalue greater than one (Kaiser–Guttman criterion) were selected for further analysis. This resulted in two PC components describing individual levels of boldness.
The tag readings of the antenna (migration intensity) were sorted so that true downstream movement was used for the analysis. This was defined by an individual being detected at the upstream antenna and then shortly after being detected in the downstream antenna.
Antennas were positioned so the downstream lap would be faster so that I could determine which direction fish were swimming. The first 30 minutes of each migration trial were removed from analyses as it represented acclimatization. 6 1-year old and 27 2-year old smolt were excluded from the migration trial due to malfunctioning equipment resulting in 74 1- year old and 33 2-year old smolt.
To test for correlations between boldness and migration intensity I used linear mixed effect models where detection frequency (migration intensity) was treated as a normal distributed response variable, the PCA scores as continuous explanatory variables and aquaria and trial- set as random factors. The random factors were set to account for pseudo replication due to repeated measures within each trial-set and aquaria. Trial-set is the groups in which the migration intensity was measured (4 set of trials in 2 pools for 1 year old fish and 3 set of trialsfor the 2 year old fish). This generated a model like the following:
FreqDetection~ PC (1 or 2), random = Aquaria and trial-set
A linear mixed effect model was also used to test for difference in boldness (PC1 and PC2) between one and two year old fish, treating the PCA-components as normally distributed response variables, age as a two level fixed effect and aquaria as a random effect.
PC (1 or 2) ~ Age, random = Aquaria
Difference in migration intensity between one and two year old fish were tested using a mixed effect model where detection frequency was used as a normal distributed response variable, age as a nominal two level factor and trial-set as a random effect.
FreqDetection ~ Age, random = trial set
Then it was tested if condition had an impact on an individual's inclination to migrate downstream by a mixed effect model where detection frequency was used as a normal distributed response variable, condition as a nominal two level factor and trial-set as a random effect.
FreqDetection ~ Condition, random = trial set
All experiments in this study were approved by the Animal Review Board at the Court of Appeal of Northern Norrland in Umeå (Dnr A-11-13 to Tomas Brodin).
3 Results
3.1 Boldness in two contexts
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The two principal components explained 40.2% and 26.6% of the total variation in the data respectively (table1). Latency to enter novel arena and time spent in the open was equally influencing the loadings of the first principal component, whereas time spent swimming in panic and time spent frozen contributed equally to the second principal component. As PC1 and PC2 were the only components with an eigenvalue over or equal to 1 all other tests were based on PC1 and PC2. For PC1, positive score specify more time in the open and shorter latency to enter novel arena. Negative scores indicate less time in the open and a long latency to enter novel arena. For PC2, an individual with high scores spent more time swimming in panic and more time frozen (i.e. lower boldness). I defined PC1 scores to be a measure of moving in a risky situation and PC2 as a measure of response to a simulated predatory attack.
Table 1. Loadings of different measures of boldness, (time in the open, latency to enter from shelter, latency to move after freezing and time spent swimming in panic), estimated for individual smolt, included in the principal component analysis, for the two principal components PC1 and PC2.
PC1 PC2
% Variance 40.2 26.6 EigenValue 1.61 1.1 Variable
contribution
Out Novel 49.9 0.25 Latency Open -50 0 Time First Move 0.2 49.4
Time Panic 0 50.3
3.2 Migration intensity and boldness
There were no correlations between migration intensity and either PC1 (1-year old; p=0.97, fig 3a, 2-year old; p=0.67, fig 3c) or PC2 (1-year old; p=0.59, fig 3b 2-year old; p=0.57, fig 3d). Meaning that individuals that were fast at emerging from the shelter and spend more time in the open area of the new environment did not swim more laps in the artificial stream than individuals that emerged later and spend more time in the shelter. Similarly there were no correlation between individuals that reacted less to the simulated predator attack (panicked less and resumed swimming earlier) and the number of laps they swam during the migration trial.
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a b
c d
Fig.3. Effect of PC- scores on downstream migration intensity for a) PC1 and 1-year old smolt ( n= 74) b) PC2 and 1-year old smolt c) Pc1 and 2-year old smolt (n=33) and d) PC2 and 2-year old smolt.
3.3 Effect of age on boldness
There were no significant difference in PC1 between one year old and two year old smolt (p=0.73, df =129) however for PC2 there was a trend for the two year olds to have a higher score (p =0.08 , df = 129, fig. 4), which means that the one year olds showed a tendency to be more bold in this assay.
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Fig. 4. Boldness scores for 1 year old and two year old salmon based on PC2 (mean ±95% CI) estimated by Principal Component Analysis on 140 individuals. High scores indicate longer time swimming in panic and longer time spent frozen (i.e. lower boldness).
3.4 Effect of age on migration intensity
The two age groups differed significantly in mean migration intensity , (p = 0.0014, df= 101, fig 5), with two year old smolt migrating to a higher degree.
Fig. 5. Migration intensity (mean±95%CI) during the four day trial period for 1- and 2 year old smolt (n1-year old= 74, n2-year old=33 ).
3.5 Condition and downstream migration
The condition of the 1-year old and 2-year old smolt were not significantly different but a trend could be seen for the one year olds having better condition (fig. 6).
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Fig. 6. Fultons condition factor for 1- and 2-year old salmon (mean ±95% CI) (n1-year old= 74, n2-year old=33 ).
Body condition did not have an effect on the downstream migration of the one year old fish (p=0.97 fig. 7a). Condition was a significant factor for the two year old smolt, however (p<0.001 fig 7b) and the individuals who had better condition were less active in their downstream movement.
a b
Fig. 7. Effect of Fulton's body condition on the downstream migration intensity for a) 1-year old smolt ( n= 74) and b) 2-year old smolt (n=33).
4 Discussion
4.1 Boldness in two contexts
My results show that how bold an individual hatchery reared smolt are in an uninformed situation does not predict how bold it is when it respond to an actual visual threat. This means that my first hypothesis appears invalid because no consistency in bold behavior over contexts was found. Previously, consistent difference in boldness have been observed in Atlantic salmon fry (Serrano et al. 2010), and trout parr (Salmo trutta) (Adriaenssens and Johnsson 2011). One reason for the lack of consistency in behavioral variation could be that
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this study screened individuals during smotlification, unlike previous mentioned studies performed on fry and parr, when the salmon goes through severe changes in morphology (McCormick 1998), physiology (Hoar 1988, Alexander et al. 1994) and behavior (McCormick 1998). If parr go through these changes at different rates it might lead to uncoupling effects on behaviors disrupting prior behavioral consistency during smotlification. Sih et al. (2012) mention the possibility of uncoupling of behaviour when animals have complex life cycles where one behavioral type is successful for the juvenile but not for the adult. A way to test this could be to do behavioral tests on parr the year before, then again during smoltification and after smoltification. One major challenge when assessing personality is the behavioral plasticity that might be present for one trait but not the other depending on species, populations and conditions. This means that individuals can be consistent over contexts in one trait (e.g. activity) but not in others (Sih et al. 2004a). For this study it is possible that the fish are very plastic during smoltification and hence loose consistency over contexts. Another confounding factor could be that individuals may differ in their plasticity, which would have the effect that part of the group might be constant over contexts but their ranking would still change as a result of plastic conspecifics. This is because consistency is a relative measurement in the assays used in screening levels of boldness and other behavioral traits (Nussey et al. 2007, Dingemanse et al. 2010). The process of going through smoltification could also affect the stability and population persistence of personality traits as the change in physiology possibly could affect different individuals in different ways (Dingemanse and Wolf 2013). All of the above mentioned factors may contribute to the lack of consistency in boldness found here.
The two behavioral scores from the two boldness-tests loaded on separated PC-axis indicating that the tests might not actually score the same behavior (i.e. boldness). This because boldness is measured in a number of different ways and it has been discussed that it might be problematic to use the results from all of these methods and claim that they represent the same behavior (Carter et al. 2012, Garamszegi et al. 2013). Carter et al. (2012) found that baboons who reacted strongly and most alarmed by a model snake also were the ones that inspected it for the longest. They also suggest using many different assays to measure the same personality trait to come as close as possible to the trait of actual interest.
Toms et al. (2013) also discuss inconsistencies in behavior over contexts when wanting to draw conclusions from animal personality. In their study they argue that lack of correlations does not necessarily mean that there is a lack of consistency in behavior between individuals but instead could be a result of the methods used when screening. Toms et al (2013) use an example with human personality where aggression, for example, would be consistently high in aggressive situations such as in a heated discussion or in traffic, but if measured in other situations, when eating dinner or watching television, might not score with the same +consistency. Sih et al (2004) also comments on this; “the insight for behavioral ecologists is that expression of [personality] might depend on the situations studied, and that our goal should be to understand which situations allow [personality] to emerge”. Réale et al (2007) even separates the novel environment assays from the others when measuring boldness and suggests that it is actually measuring exploratory behavior.
Conclusively there are many things that could affect consistency of boldness between the two contexts for the individual smolt and further studies are needed to identify the most important explanations for the lack of correlations found here.
4.2 Migration intensity and boldness
There were no correlations between boldness and migratory intensity, which suggests that my second hypothesis should be rejected. Individual differences in migration tendency have been documented in many taxa and have been connected to both morphology, physiology and behavior. The connection to individual behavioral trait, however, have only been found in a few studies. In a study comparing migrant and resident Blue tits (Cyanistes caeruleus) from the same population Nilsson et al. (2010) found that the migrants were bolder when
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approaching a novel object. Similarly, Chapman et al (2011) found that migrating European roach (Rutilus rultilus) displayed a significantly bolder behavior when tested in a standardized novel arena assay. Boldness have also been connected to dispersal, another mechanism requiring active movement from one habitat to another. Fraser et al. (2001) observed that bolder Trinidad killifish (Rivulus hartii) displayed a more active dispersing behavior when released in their native stream. Further, in Great tits (Parus major) degree of native dispersal was correlated to how actively individuals behaved in a novel arena assay.
The process of smoltifying is a comprehensive change physiologically, morphologically and behavioral which might leave the impact of boldness level on how actively an individual migrate downstream comparatively low. Migration downstream is evolutionary driven by a change in predation risk or more favorable food availability in alternative habitat (Gross et al.
1988; Brönmark et al. 2008) and the effect of an individual's condition on how actively it migrates have especially been studied in salmonidae smolt reared for compensatory release.
A result of smolt-to-adult return rates being historically low (e.g., McKinnell and Karlström 1999, Kallio-Nyberg et al. 2011a, 2011b) compared to great efforts. What studies find is that individuals in better condition have less motivation to instigate downstream migration (Rowe et al. 1991, Wysujack et al. 2009 and Lans et al. 2011). It is also possible that other behavioral traits are more significant in the shift from a stream-dwelling and territorial defending life style to an actively swimming and schoaling in the ocean. How dominant individuals are have, for example, been shown to have an effect on how actively they migrate (Metcalfe 2006).
4.3 Difference in boldness and migration between 1- and 2 year old smolt
4.3.1 BoldnessThere was a tendency (close to significance) for one- and two year old smolt to differ in boldness, with 1 year old smolt behaving bolder, but it was not significant which means that my third hypothesis should be discarded. The tendency, however could be explained by the fact that one year olds in this hatchery are sorted in the spring according to smoltification stage. The one year olds that are close to or have started smoltifying will be released that year and the others will stay in the hatchery and be released the year after. This result in the one year olds in the hatchery, after sorting, being the ones that grow fastest in these particular conditions. One way to grow fast in a hatchery is accessing food effectively by behaving in a bold (risk taking) way. As there are no predators a bold individual will get more access to food without the negative impacts expected in a natural system. High growth rate have been connected to risk taking behavior in, for example, transgenic salmon (modified to grow faster) that were more risk taking in laboratory experiments (Sundström et al. 2003). The connection between growth rate and risk taking behavior has also been observed in domestic rainbow trout (Oncorhynchus mykiss) where age 1 gained 20% more mass in the wild and young of the year 100% more compared to wild rainbow trout (Biro et al. 2003a, 2003b, 2004, 2006). However domestic trout in both age classes suffered 50-60% greater mortality in the presence of avian predators (loons (Gavia immer)). In a field experiment they also observed that the domestic individuals used riskier habitats and responded less to presence of predators (Biro et al 2003a). However, other studies have found no such connections.
Adrianssens and Johansson (2011a) for example found that trout with low exploring tendencies in the lab grew faster than bolder when released into the wild. They also showed that activity in the lab and survival in the wild was un-correlated. Other connections between behavioral traits observed in the lab and behaviors in the wild in fish are between boldness (predator inspection) and how they interacted when shoaling in the wild (Croft et al 2009).
Bolder guppies had weaker and fewer social connections in the field (Croft et al 2009). This could also result in less protection from conspecifics in the presence of a predator and also lead to greater dispersal and activity. When smolts of the Atlantic salmon migrate out to sea the mean migrational period usually extends over three to seven weeks (Antonsson and Gudjonsson 2002, Stewart et al. 2006, Orell et al. 2007). However, in many populations the time for the smolt to reach the ocean can be faster (1-2 weeks). If this time is prolonged due
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to shy individuals it is possible that local predation can have a detrimental effect on the number of individuals making it out to sea (Finstad and Jonsson 2001). What also have been observed is a synchronized entry into the sea, predator swamping, with parts of the population waiting in the estuary, and individuals that has longer to migrate start earlier to avoid being eaten (Finstad and Jonsson 2001, Stewart et al. 2006). The difference found in boldness in this study might lead to a disruption of the predator swamping and increase mortality in the smolt.
Smolt that display a shy behavior could miss the optimal window and get stuck in the river with increased predation and poor resources. Contrary, the one year old might display so high boldness levels that it becomes maladaptive and the cost of increased predation-risk outweighs the benefits of potential increased migration intensity.
4.3.2 Migration
Mean migratory intensity (amount of laps swimming downstream in the artificial stream) was different between the two age classes, however contrary to my hypothesis, the two year old smolt migrated downstream to a higher extent. The two age groups in this study (1- and 2 year old) were both smoltifying and would be released in the spring, however they differed in condition (fig.6). Condition is a parameter that have been observed to affect downstream migration (Berglund 1995, Hutchings and Jones 1998, Brodersen et al. 2008) in Atlantic salmon. As mentioned previous, condition have been found to have a negative effect on how actively an individual migrates downstream (Rowe et al. 1991, Berglund 1995, Hutchings and Jones 1998, Brodersen et al. 2008, Wysujack et al. 2009 and Lans et al. 2011). This is in line with the results found in this study. The two year old smolt who were in better condition were significantly less active in their downstream migration.
The fast growing individuals who smoltify after their first year and subsequently are slower at instigating downstream migration, which have been observed in other hatchery reared individuals (Kekäläinen et al. 2008, Johnson et al. 2010), might suffer from increased mortality (Chittenden et al. 2008, Lacroix 2008, Romakkaniemi 2008). Therefore, a slow growing 2-year old smolt might be most suited for compensatory release, which has been suggested in other studies (e.g., Lans et al. 2011).
In conclusion, I found between individual variation in boldness expressed under visual threat. Individual boldness could not predict how actively the smolt migrated downstream which might be a result of a) uncoupling mechanisms of behaviors across complex life cycle b) high variation in timing and speed of which individuals go through the smoltification process or c) the use of methodology that potentially measured different behaviors. One year old smolt were bolder but displayed a less active downstream migration. High condition could have a negative effect on downstream migratory activity. These findings suggest the potential for differential migration success, driven by asymmetric survival, between one and two year old hatchery reared smolt during downstream migration, that could have significant effects on restocking success.
5 Acknowledgments
Thanks to my supervisor Tomas Brodin, and Gustav Hellström, Anders Alanärä and Lo Persson at SLU, for letting me be a part of this interesting project, for constant support and great discussions. Also, big thanks to Martina Heynen for inspiration and good talks.
13
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