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Temperature preference of juvenile lumpfish (Cyclopterus lumpus) originating from the southern and northern parts of Norway
Journal of Thermal Biology 89 (2020) 102562
Contents lists available at ScienceDirect
Journal of Thermal Biology journal homepage: http://www.elsevier.com/locate/jtherbio
Temperature preference of juvenile lumpfish (Cyclopterus lumpus) originating from the southern and northern parts of Norway Atle Mortensen a, b, Richard B. Johansen b, Øyvind J. Hansen a, b, Velmurugu Puvanendran a, b, * a b
Nofima AS, Muninbakken 13, 9291, Tromsø, Norway Center for Marine Aquaculture, Salarøyvegen 979, 9103, Kvaløya, Norway
A R T I C L E I N F O
A B S T R A C T
Keywords: Temperature preference Lumpfish Growth
Fish are ectothermic animals and have body temperatures close to that of the water they inhabit. They can still control their body temperatures by selecting habitats with temperatures that maximize their growth, feed con version and wellbeing. Lumpfish, Cyclopterus lumpus, is widely distributed in the North Atlantic Ocean and therefore exposed to variable water temperatures. Lumpfish is extensively used as cleanerfish in salmon farming in Norway and exposed to a wide temperature range along the north-south axis of the Norwegian coastline. But, if these temperature ranges correspond to the preference temperatures of lumpfish is not known. If lumpfish has adapted to regional temperatures along the Norwegian coast, differences in preference temperature for fish from different regions should be evident. In a selective breeding perspective, different selection lines for preference temperature would then be useful for further development of lumpfish as a cleanerfish. We subjected lumpfish juveniles weighing 154–426g originated from northern (Group North – GN) and southern (Group South – GS) Norway to a temperature preference test, using an electronic shuttle box system. The system allowed the fish to control the water temperature by moving between two chambers, and thereby choosing its preferred temperature in the range from 5 to 16 � C. We started the temperature at 7.8 � 1.37 � C for GN and 7.58 � 1.34 � C for GS, but all the fish except four (two each from GN and GS) chose lower temperatures (5.03–7.6 � C) in the first 18 h and stayed closer to that temperature during the next 30 h. Based on the results, GN and GS lumpfish preferred 6.92 � 1.8 and 6.2 � 1.2, respectively, and there was no significant difference be tween the groups. Neither was there any significant difference in growth rates (SGR) between the two groups. Based on our results, we suggest that lumpfish from any geographical origin along the Norwegian coast can be used anywhere in Norway. It follows that lumpfish from a single selection line could be used at any salmon farm in Norway independent of its location.
1. Introduction The preference temperature often coincides with the ambient tem perature of the natural environment of the fish. Several studies have shown that temperature preference is related to size and age, where smaller fish normally prefer higher temperatures than larger fish. This is, €rnsson et al., for instance, the case for Atlantic cod, Gadus morhua (Bjo 2001; Lafrance et al., 2005) and brown trout, Salmo trutta (Elliot and Allonby, 2013). This is probably an adaptation to their natural envi ronment since younger fish tend to live in shallower and warmer waters than adults (McCauley and Huggins, 1979). Johnson and Kelsch (1998) found a positive relationship between preference temperature and
acclimation temperature in 40 of the 42 temperate fish species they examined. Accordingly, seasonal variation in temperature preference is found in many fish species, including several species from Western Lake Erie (Barans and Tubb, 1973), Atlantic cod (Clark and Green, 1991) and Arctic charr, Salvelinus alpinus (Mortensen et al., 2007). For Atlantic cod the temperature preference is linked to their haemoglobin type, which varies along a north-south axis (Behrens et al., 2012). In contrast to this, Siikavuopio et. (2014) found no difference in temperature preference of three populations of Arctic charr from mainland northern Norway and one from the high arctic Svalbard, even though these populations live under quite different temperature conditions. It is noteworthy that the preference of the charr from Svalbard preferred a temperature (11 � C)
* Corresponding author. Nofima AS, Muninbakken 13, 9291, Tromsø, Norway. E-mail addresses: [email protected] (A. Mortensen), [email protected] (R.B. (Ø.J. Hansen), [email protected] (V. Puvanendran). https://doi.org/10.1016/j.jtherbio.2020.102562 Received 12 September 2019; Received in revised form 24 February 2020; Accepted 24 February 2020 Available online 27 February 2020 0306-4565/© 2020 Elsevier Ltd. All rights reserved.
Johansen), [email protected]
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Journal of Thermal Biology 89 (2020) 102562
which for most of the year is far above what they experience in their natural habitat. Among marine fishes, Atlantic cod is also usually found in areas with much lower temperatures than the optimal temperature for €rnsson et al., 2001). growth (Bjo Lumpfish (Cyclopterus lumpus) is a semi-pelagic fish living in temperate and cold waters at high latitudes on both sides of the North Atlantic Ocean. On the western Atlantic, lumpfish is distributed from Hudson’s Bay and the Labrador coast southward to Cape Cod (USA) and on the eastern Atlantic from Svalbard to south of Portugal, including Iceland and Greenland (Stein, 1986). Lumpfish spends the winter in offshore waters and in spring they move to coastal zones to spawn (Kennedy et al., 2015). During the spawning season, there is a com mercial fishery for lumpfish and the roe is used to produce a caviar substitute (Eriksen et al., 2014). Lumpfish can eat salmon lice (Lepeophtheirus salmonis) from Atlantic salmon (Salmo salar) in cage farms. It was demonstrated for the first time by Willumsen (2001), who deployed wild caught lumpfish together with salmon in cages. In a later study, Imsland et al. (2014) showed that salmon lice infestation was significantly lower in cages with 10–15% of lumpfish equivalent to 10–15% of the number of salmon were stocked compared to cages without lumpfish. Different species of wrasse (Lab ridus spp) were the first “cleanerfish” to be used in commercial salmon farming in Norway, but they have low tolerance to low water temper ature (Sayer and Reader, 1996), and cannot be used in the northern part of Norway, where sea water temperature is below 10 � C most of the year. Lumpfish is more tolerant to low temperatures and can be used along the whole Norwegian coastline. Commercial use of farmed lumpfish as a delousing agent in Norway started around 2010, and now lumpfish is extensively used in all salmon farming countries in the North-Atlantic area and 30 million lumpfish were used in Norway in 2017 (Directorate of Fisheries, 2019). This means that by number, lumpfish is now the second largest aquaculture species in Norway after Atlantic salmon where 330 million salmon transferred to sea in 2017 (Directorate of Fisheries, 2019). Since lump fish in aquaculture is exposed to a wide temperature range, we need to know about their physiological reactions to different temperatures to secure acceptable welfare and performance. Studies have indicated that the temperature for maximum growth rate decreases with the size of the lumpfish. Given the long longitudinal costal area of Norway, it is possible that the temperature preference of lumpfish in southern and northern Nor �nsdo �ttir way to have different temperature preference/requirement. Jo et al. (2018) showed that no population differences exist among lump fish along the Atlantic region in Norway. However, Imsland et al. (2016) suggested possible differences in lice eating ability among different families of lumpfish. Thus, the preference temperature of lumpfish is important to know in relation to optimizing the rearing conditions of larval/juvenile lumpfish along the long Norwegian coast and to select the breeding core for selective breeding to see if they can be used all over Norway independent of its origin (one selective line can cover the whole country) or if different selective lines are needed for different areas. The experiment was carried out in accordance to the national rules and regulations at the site of the experiments and all efforts were undertaken to minimize stress and suffering of the animals. The experimental pro tocol and use of a sufficient number of lumpfish was approved by Nor wegian Animal Research Authority (Forsøksdyrutvalget), which issued the permission to carry out the experiment (Permit number is FOTS ID 8399). Thus, the main aim of the present study was to find out if the preferred temperature of juvenile lumpfish originating from southern and northern Norway vary. We will also evaluate, firstly, if the prefer ence temperature has been used as the optimal temperature for juvenile lumpfish rearing in culture condition, and secondly, if different selective breeding lines are needed for southern and northern Norway based on their preferred temperature.
2. Materials and methods 2.1. Fish and rearing Fish rearing was performed at Nofima’s Centre for Marine Aqua culture (CMA) in Tromsø from May 2015 to November 2015. The lumpfish used in the experiment originated from two locations in Nor way; Flekkefjord in the south (58.2972� N, 6.66� E; GS ¼ Group South) and Tromsø in the north (69� 460 N, 19� 020 E; GN ¼ Group North). Fertilized eggs from wild broodfish from these two locations were brought to the CMA and hatched in May 2015 and were raised according to the standard protocol of the CMA (10 � C water temperature, 32 ppt salinity, O2-saturation above 80%, continuous light, fed to satiation by pellets, Amber Neptun®, Skretting AS, Norway). The juveniles were kept familywise in 190 L circular tanks from hatching until PIT tagging (November 30), when 15 fish from GS and 15 from GN (each fish from different family) were anaesthetized (FINQUEL, 0.07 g L 1) and tagged intramuscularly with Sokymat® pit-tags (Cyntag, Inc., KY, USA). At tagging, body weights of the fish used in the preference test were 36.8 � 8.9 g (SD) and 37.3 � 13.6 (SD) g for GN and GS, respectively and were not significantly different (p > 0.927). Four extra fish per group were tagged to account for any fish mortality in between tagging and start of the temperature preference test (May 2016). To ensure identical con ditions after tagging, all fish were kept together in a 190 L grow out tank until they were used for the preference temperature measurements. During this period, they were given feed in excess and kept at continuous light and ambient water temperature (varied between 6.5 and 9 � C in the tanks), except from November 30 to December 10, when the tempera ture was 10 � C. Eleven fish from each of the groups were used for the temperature preference test, which took place from March 7th to May 9th, 2016. When temperature preference test started, the body weight of juvenile lumpfish ranged from 156 to 318 g in GN and from 154 to 426 g in GS (Fig. 1), with mean weights of 222 g and 280 g, respectively, and were not significantly different (p > 0.063). Specific growth rates of indi vidual fish (SGR, % day 1) from tagging (30 November 2015) to tem perature preference measurements (07 March - May 09, 2016) were calculated as: SGR ¼ 100 (ln W1 – ln W0)/t, where W0 (g) is the body weight by tagging, W1 (g) is the body weight by measurement and t is the number of days between tagging and temperature preference measurement. 2.2. Temperature preference test The measurements were made by using an electronic shuttle-box system from Loligo Inc., Denmark. A sketch of the system including water supply is shown in Fig. 2. The system allowed the fish to control the water temperature, and thereby control its own body temperature, by moving between two chambers (Neill et al., 1972). The two chambers were connected by a channel through which fish could move freely. The position of the fish was monitored continuously by means of a video-system (uEye camera, IDS Imaging Development Systems, Ger many) and the water temperature in the chambers was regulated auto matically such that there was always a constant temperature difference of 1 � C between the two chambers. We continually added small amount new water to the buffer tanks for the whole time to compensate for leakage and evaporation during the 48 h experiment of each fish. We measured the O2 in the tank, but it did not change during the 48 h and above 90% throughout the study period. A new fish was always placed in the ‘hot’ water chamber. The temperatures of both chambers were changed in a dynamic manner dependent upon the position of the fish. When the fish was in the warmest chamber the temperature of both chambers was made to increase at a rate of 1 � C h 1, and when the fish moved to the chamber with lowest temperature, the temperatures of both chambers started to decrease at the same rate. Most fish rapidly learn to control their body temperature by moving between the 2
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Journal of Thermal Biology 89 (2020) 102562
Fig. 1. Body weight (g) of individual juvenile lumpfish from GN and GS used in the temperature preference experiment.
chambers in 24 h or less (Reynolds and Casterlin, 1979), but to ensure that the fish was not harmed by too high or too low temperatures the temperature of the chambers was only allowed to vary between 5 � C and 16 � C. For more technical details, see Stol et al. (2013) and Siikavuopio et al. (2014). Water temperature in the tank the fish occupied was recorded every second. Temperature preference measurements were made alternately with fish from GN and GS. Each fish was kept in the shuttle-box for 48 h without food. After recordings, the fish were weighed and returned to the grow out tank, and the shuttle-box was cleaned, water replaced and made ready for the next fish. 2.3. Data collection, calculations and statistics Median occupation temperatures for all fish were calculated for every 6 h from the start of the experiment to the end. In total, an indi vidual fish was monitored for 48 h. Median temperatures, but not the average temperature, were used since medians are not biased even if the fish occupy the highest or lowest temperatures was set by us for a short period. The normality of all data sets was tested with the Shapiro–Wilk W statistic and all data were normally distributed. Statistical differences between the two fish groups in preferred temperature and body weights were tested with Student’s t-test. Correlations amongst preference temperature and initial weight, growth rate and body weight at measuring date were tested with linear regression. A probability level of less than 0.05 was considered significant. 3. Results Among the eleven lumpfish juveniles from each region we used in our study, behaviour of each fish was different which, resulted in higher variations in the preferred temperatures (Fig. 3). While most fish chose lower temperatures compared to the initial temperature at the start, fish 1 and 2 from GN chose higher temperatures. Except for one fish each from GN and GS, all fish learnt to use the shuttle box in the first 18 h by moving between the two boxes. The trend of preferred temperatures for the juvenile lumpfish from GN and GS are shown in Fig. 4. The points in the figure show the mean of the median occupied temperatures in the 6-h intervals from start to the
Fig. 2. Sketch of the shuttle box system showing the components.
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Fig. 3. Variation in behaviour of lumpfish juveniles among selected fish from GN and GS.
Fig. 4. Temperature preference of lumpfish juveniles during the 48-hrs measurement. Values are mean � SE.
temperature preference calculations. We used the temperature regis trations from 18 to 48 h to calculate the temperature preference of the individual fish. Based on these assumptions, the preferred temperatures (final thermal preferendum) for lumpfish juveniles are 6.92 � 1.18 (SD) and 6.2 � 1.17 (SD) for GN and GS, respectively. Despite a difference of 0.72 � C in the mean preference temperature between GN and GS, the values were not significantly different (p > 0.213). There was no significant difference in SGR between the two groups from tagging to start of the temperature preference test (1.37 � 0.225 and 1.43 � 0.13% d 1 for GN and GS, respectively; p > 0.47). Since there was no difference in temperature preference between the groups,
end of registration (�SD), for the groups. Except for four fish, all the fish selected temperatures lower than the average start temperatures (7.81 � C (GN) or 7.58 � C (GS); the temperatures of their hold tanks when the registration started) in the first 18-h period. From period 18 h onwards the selected temperature of the two groups seemed to have reached a plateau. This was especially evident in the GS. Based on the curves (Fig. 4) and the behaviour of different fish species in this type of shuttle-box (Reynolds and Casterlin, 1979), we categorized 0–18 h as the learning period because in this period the lumpfish learned to regulate their body temperatures by moving back and forth between the two chambers and this was not used in 4
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the data from both groups were merged for further correlation analyses. These showed that there was no significant correlation between tem perature preference and body weight at measuring date (r ¼ 0.3, p > 0.175), or between temperature preference and SGR (r ¼ 0.333, p > 0.129).
locusts (Brown and Griffin, 2005; Ward et al., 2010; Coggan et al., 2011). However, fish may also increase their preference temperature when deprived of food, as shown for brown trout, Salmo trutta (Elliot and Allonby, 2013). These different reactions to food deprivation are not necessarily in conflict, but both can be part of a “growth maximizing strategy”. If food is more available in areas with higher temperatures, it may be advantageous to seek food in these areas instead of moving to areas with lower temperatures in order to save energy (Jobling, 1997). Currently, the only reason for producing lumpfish in aquaculture is to use them as “cleanerfish” in salmon sea cages to eat salmon lice. Lice eating ability is therefore the most interesting trait to improve by se lective breeding. Imsland et al. (2016) found family differences in lice grazing in lumpfish and suggested that lice grazing could be an inher itable trait which can be improved by selective breeding. This brings up an important question; that is if we need more than one selection line to account for different populations or subpopulations that can have different environmental requirements such as the temperature. Results from the present study indicate that preference temperature of lumpfish in Norway is independent of geographic origin. Neither did we find any difference in growth rate between the groups of lumpfish used in this study. Genetic analyses have shown that there is only one population of �nsdo �ttir et al., 2018). Taken together, these lumpfish in Norway, (Jo findings support the view that lumpfish can be used as “cleanerfish” anywhere in Norway independent of their geographical origin, and that one selection line can cover the whole country in a selective breeding program. The present results reveal that lumpfish above 150 g prefer low temperatures which are typical for the offshore habitats where fish of this size spend the winter. Lumpfish used as “cleanerfish” are deprived of the possibility to choose their own habitat and may be forced to stay at temperatures substantially above their temperature preference (Hvas et al., 2018). If that has any impact on their welfare and disease resis tance is an open question which has still not been addressed.
4. Discussion The results of this study revealed no difference in preference tem perature or growth rate between lumpfish from Flekkefjord (GS) and �nsdo �ttir et al. (2018), who Tromsø (GN). Our results are in line with Jo indicated that there is only one population of lumpfish along the Nor wegian coast. These results also confirm that lumpfish of the size used in this study prefers low temperatures which might match the tempera tures they experience in the wild during winter, when they stay in deeper water further away from the coast (Kennedy et al., 2015). There were 2-3-fold differences in weight within the groups (156–318 g in GN and from 154 to 426 g in GS). Lumpfish juveniles used in this experiment were from different families within each group. So, the differences in weight within GN and GS were because of family differences in growth and such differences exist between families in many fish species (Xu et al., 2013). Further, geographical differences in distribution can also lead to growth differences as it was seen between GS and GN groups (Nicieza et al., 1994). Lumpfish is a fast-growing fish at this early juvenile stage (Nytrø et al., 2014). The experiment was conducted for 10 weeks and some fish tested during the first weeks were smaller compared to fish tested at later stages. Together, all these factors resulted in the variation in body weight of the fish during the experiment. Nytrø et al. (2014) found that optimal temperature for growth of juvenile lumpfish varied significantly with the fish size, being approxi mately 16 � C for fish between 11 and 40 g, and declining to 8.9 � C for fish between 120 and 200 g. Between the temperature interval of 4–13 � C, growth rate was independent of temperature for fish larger than 160 g. The two groups of lumpfish used in our study had mean weights of 222 g (GN) and 280 g (GS), and might have had an optimal growth temperature close to 8.9 � C or slightly below. If that is true, the tem perature preferences measured by us were 2.0/2.7 � C (GN/GS, respec tively) lower than that of the temperature required for optimal growth rate. Normally, this would mean that the fish are selecting a temperature which would result in a lower growth rate. But this is not necessarily the case for lumpfish because lumpfish of the size used in our experiment has a growth rate independent of temperature in the temperature in terval from 6 to 12 � C (Nytrø et al., 2014). In the present study, we also found that preference temperature was not correlated to growth rate. Thus, lumpfish can select temperature lower than the temperature needed for the optimal growth temperature without compromising growth rate (Nytrø et al., 2014). The reason that lumpfish selects a temperature towards the lower end of the optimal temperature range for growth is probably because it is energetically advantageous. Larsson (2005) found that Arctic charr, Salvelinus alpinus, selected temperatures significantly lower than that required for optimal growth, while brown trout, Salmo trutta, selected temperatures for optimal growth. Larsson suggested that the reason why Arctic charr selected temperatures lower than the optimal growth tem perature is that this species is optimizing food conversion efficiency, which is higher at lower temperatures. When choosing between fast growth and efficient food conversion, Arctic charr prioritizes efficiency. In contrast, lumpfish can choose a low temperature without losing the advantage of faster growth. Still, our values for preference temperatures may have been influenced by the fact that the measurements were made on lumpfish without access to food. To seek lower temperatures in cases of food shortage as a strategy for energy conservation is found in several fish species (Mac, 1985; Despatie et al., 2001; Ward et al., 2010). A similar relationship between temperature preference and nutritional status is also found in several ectothermic animals such as lizards and
5. Conclusion The results from the present study indicate that the temperature preference and growth rate of lumpfish from different parts of Norway are independent of their geographic origin. This suggests that the same lumpfish can be used as “cleanerfish” anywhere in Norway because no significant differences in temperature preference were found in our study. With respect to selective breeding, there is no need for different selection lines to account for different temperatures along the Norwe gian coast. CRediT authorship contribution statement Atle Mortensen: Conceptualization, Methodology, Writing - review & editing. Richard B. Johansen: Methodology, Formal analysis, Writing - review & editing. Øyvind J. Hansen: Formal analysis, Writing - review & editing. Velmurugu Puvanendran: Conceptualization, Methodology, Writing - original draft, Formal analysis, Writing - review & editing. Acknowledgements We thank Thor Arne Hangstad (Akvaplan-niva) and Andreas Lind holm (Norsk Oppdrettsservice AS) for providing the lumpfish eggs and the staff at the CMA for their help during the juvenile rearing and in setting up the shuttle box system. This work has been supported by funding from the Ministry of Trade, Industry and Fisheries of Norway and Nofima. There is no conflict of interest in relation to this study.
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Contents lists available at ScienceDirect
Journal of Thermal Biology journal homepage: http://www.elsevier.com/locate/jtherbio
Temperature preference of juvenile lumpfish (Cyclopterus lumpus) originating from the southern and northern parts of Norway Atle Mortensen a, b, Richard B. Johansen b, Øyvind J. Hansen a, b, Velmurugu Puvanendran a, b, * a b
Nofima AS, Muninbakken 13, 9291, Tromsø, Norway Center for Marine Aquaculture, Salarøyvegen 979, 9103, Kvaløya, Norway
A R T I C L E I N F O
A B S T R A C T
Keywords: Temperature preference Lumpfish Growth
Fish are ectothermic animals and have body temperatures close to that of the water they inhabit. They can still control their body temperatures by selecting habitats with temperatures that maximize their growth, feed con version and wellbeing. Lumpfish, Cyclopterus lumpus, is widely distributed in the North Atlantic Ocean and therefore exposed to variable water temperatures. Lumpfish is extensively used as cleanerfish in salmon farming in Norway and exposed to a wide temperature range along the north-south axis of the Norwegian coastline. But, if these temperature ranges correspond to the preference temperatures of lumpfish is not known. If lumpfish has adapted to regional temperatures along the Norwegian coast, differences in preference temperature for fish from different regions should be evident. In a selective breeding perspective, different selection lines for preference temperature would then be useful for further development of lumpfish as a cleanerfish. We subjected lumpfish juveniles weighing 154–426g originated from northern (Group North – GN) and southern (Group South – GS) Norway to a temperature preference test, using an electronic shuttle box system. The system allowed the fish to control the water temperature by moving between two chambers, and thereby choosing its preferred temperature in the range from 5 to 16 � C. We started the temperature at 7.8 � 1.37 � C for GN and 7.58 � 1.34 � C for GS, but all the fish except four (two each from GN and GS) chose lower temperatures (5.03–7.6 � C) in the first 18 h and stayed closer to that temperature during the next 30 h. Based on the results, GN and GS lumpfish preferred 6.92 � 1.8 and 6.2 � 1.2, respectively, and there was no significant difference be tween the groups. Neither was there any significant difference in growth rates (SGR) between the two groups. Based on our results, we suggest that lumpfish from any geographical origin along the Norwegian coast can be used anywhere in Norway. It follows that lumpfish from a single selection line could be used at any salmon farm in Norway independent of its location.
1. Introduction The preference temperature often coincides with the ambient tem perature of the natural environment of the fish. Several studies have shown that temperature preference is related to size and age, where smaller fish normally prefer higher temperatures than larger fish. This is, €rnsson et al., for instance, the case for Atlantic cod, Gadus morhua (Bjo 2001; Lafrance et al., 2005) and brown trout, Salmo trutta (Elliot and Allonby, 2013). This is probably an adaptation to their natural envi ronment since younger fish tend to live in shallower and warmer waters than adults (McCauley and Huggins, 1979). Johnson and Kelsch (1998) found a positive relationship between preference temperature and
acclimation temperature in 40 of the 42 temperate fish species they examined. Accordingly, seasonal variation in temperature preference is found in many fish species, including several species from Western Lake Erie (Barans and Tubb, 1973), Atlantic cod (Clark and Green, 1991) and Arctic charr, Salvelinus alpinus (Mortensen et al., 2007). For Atlantic cod the temperature preference is linked to their haemoglobin type, which varies along a north-south axis (Behrens et al., 2012). In contrast to this, Siikavuopio et. (2014) found no difference in temperature preference of three populations of Arctic charr from mainland northern Norway and one from the high arctic Svalbard, even though these populations live under quite different temperature conditions. It is noteworthy that the preference of the charr from Svalbard preferred a temperature (11 � C)
* Corresponding author. Nofima AS, Muninbakken 13, 9291, Tromsø, Norway. E-mail addresses: [email protected] (A. Mortensen), [email protected] (R.B. (Ø.J. Hansen), [email protected] (V. Puvanendran). https://doi.org/10.1016/j.jtherbio.2020.102562 Received 12 September 2019; Received in revised form 24 February 2020; Accepted 24 February 2020 Available online 27 February 2020 0306-4565/© 2020 Elsevier Ltd. All rights reserved.
Johansen), [email protected]
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Journal of Thermal Biology 89 (2020) 102562
which for most of the year is far above what they experience in their natural habitat. Among marine fishes, Atlantic cod is also usually found in areas with much lower temperatures than the optimal temperature for €rnsson et al., 2001). growth (Bjo Lumpfish (Cyclopterus lumpus) is a semi-pelagic fish living in temperate and cold waters at high latitudes on both sides of the North Atlantic Ocean. On the western Atlantic, lumpfish is distributed from Hudson’s Bay and the Labrador coast southward to Cape Cod (USA) and on the eastern Atlantic from Svalbard to south of Portugal, including Iceland and Greenland (Stein, 1986). Lumpfish spends the winter in offshore waters and in spring they move to coastal zones to spawn (Kennedy et al., 2015). During the spawning season, there is a com mercial fishery for lumpfish and the roe is used to produce a caviar substitute (Eriksen et al., 2014). Lumpfish can eat salmon lice (Lepeophtheirus salmonis) from Atlantic salmon (Salmo salar) in cage farms. It was demonstrated for the first time by Willumsen (2001), who deployed wild caught lumpfish together with salmon in cages. In a later study, Imsland et al. (2014) showed that salmon lice infestation was significantly lower in cages with 10–15% of lumpfish equivalent to 10–15% of the number of salmon were stocked compared to cages without lumpfish. Different species of wrasse (Lab ridus spp) were the first “cleanerfish” to be used in commercial salmon farming in Norway, but they have low tolerance to low water temper ature (Sayer and Reader, 1996), and cannot be used in the northern part of Norway, where sea water temperature is below 10 � C most of the year. Lumpfish is more tolerant to low temperatures and can be used along the whole Norwegian coastline. Commercial use of farmed lumpfish as a delousing agent in Norway started around 2010, and now lumpfish is extensively used in all salmon farming countries in the North-Atlantic area and 30 million lumpfish were used in Norway in 2017 (Directorate of Fisheries, 2019). This means that by number, lumpfish is now the second largest aquaculture species in Norway after Atlantic salmon where 330 million salmon transferred to sea in 2017 (Directorate of Fisheries, 2019). Since lump fish in aquaculture is exposed to a wide temperature range, we need to know about their physiological reactions to different temperatures to secure acceptable welfare and performance. Studies have indicated that the temperature for maximum growth rate decreases with the size of the lumpfish. Given the long longitudinal costal area of Norway, it is possible that the temperature preference of lumpfish in southern and northern Nor �nsdo �ttir way to have different temperature preference/requirement. Jo et al. (2018) showed that no population differences exist among lump fish along the Atlantic region in Norway. However, Imsland et al. (2016) suggested possible differences in lice eating ability among different families of lumpfish. Thus, the preference temperature of lumpfish is important to know in relation to optimizing the rearing conditions of larval/juvenile lumpfish along the long Norwegian coast and to select the breeding core for selective breeding to see if they can be used all over Norway independent of its origin (one selective line can cover the whole country) or if different selective lines are needed for different areas. The experiment was carried out in accordance to the national rules and regulations at the site of the experiments and all efforts were undertaken to minimize stress and suffering of the animals. The experimental pro tocol and use of a sufficient number of lumpfish was approved by Nor wegian Animal Research Authority (Forsøksdyrutvalget), which issued the permission to carry out the experiment (Permit number is FOTS ID 8399). Thus, the main aim of the present study was to find out if the preferred temperature of juvenile lumpfish originating from southern and northern Norway vary. We will also evaluate, firstly, if the prefer ence temperature has been used as the optimal temperature for juvenile lumpfish rearing in culture condition, and secondly, if different selective breeding lines are needed for southern and northern Norway based on their preferred temperature.
2. Materials and methods 2.1. Fish and rearing Fish rearing was performed at Nofima’s Centre for Marine Aqua culture (CMA) in Tromsø from May 2015 to November 2015. The lumpfish used in the experiment originated from two locations in Nor way; Flekkefjord in the south (58.2972� N, 6.66� E; GS ¼ Group South) and Tromsø in the north (69� 460 N, 19� 020 E; GN ¼ Group North). Fertilized eggs from wild broodfish from these two locations were brought to the CMA and hatched in May 2015 and were raised according to the standard protocol of the CMA (10 � C water temperature, 32 ppt salinity, O2-saturation above 80%, continuous light, fed to satiation by pellets, Amber Neptun®, Skretting AS, Norway). The juveniles were kept familywise in 190 L circular tanks from hatching until PIT tagging (November 30), when 15 fish from GS and 15 from GN (each fish from different family) were anaesthetized (FINQUEL, 0.07 g L 1) and tagged intramuscularly with Sokymat® pit-tags (Cyntag, Inc., KY, USA). At tagging, body weights of the fish used in the preference test were 36.8 � 8.9 g (SD) and 37.3 � 13.6 (SD) g for GN and GS, respectively and were not significantly different (p > 0.927). Four extra fish per group were tagged to account for any fish mortality in between tagging and start of the temperature preference test (May 2016). To ensure identical con ditions after tagging, all fish were kept together in a 190 L grow out tank until they were used for the preference temperature measurements. During this period, they were given feed in excess and kept at continuous light and ambient water temperature (varied between 6.5 and 9 � C in the tanks), except from November 30 to December 10, when the tempera ture was 10 � C. Eleven fish from each of the groups were used for the temperature preference test, which took place from March 7th to May 9th, 2016. When temperature preference test started, the body weight of juvenile lumpfish ranged from 156 to 318 g in GN and from 154 to 426 g in GS (Fig. 1), with mean weights of 222 g and 280 g, respectively, and were not significantly different (p > 0.063). Specific growth rates of indi vidual fish (SGR, % day 1) from tagging (30 November 2015) to tem perature preference measurements (07 March - May 09, 2016) were calculated as: SGR ¼ 100 (ln W1 – ln W0)/t, where W0 (g) is the body weight by tagging, W1 (g) is the body weight by measurement and t is the number of days between tagging and temperature preference measurement. 2.2. Temperature preference test The measurements were made by using an electronic shuttle-box system from Loligo Inc., Denmark. A sketch of the system including water supply is shown in Fig. 2. The system allowed the fish to control the water temperature, and thereby control its own body temperature, by moving between two chambers (Neill et al., 1972). The two chambers were connected by a channel through which fish could move freely. The position of the fish was monitored continuously by means of a video-system (uEye camera, IDS Imaging Development Systems, Ger many) and the water temperature in the chambers was regulated auto matically such that there was always a constant temperature difference of 1 � C between the two chambers. We continually added small amount new water to the buffer tanks for the whole time to compensate for leakage and evaporation during the 48 h experiment of each fish. We measured the O2 in the tank, but it did not change during the 48 h and above 90% throughout the study period. A new fish was always placed in the ‘hot’ water chamber. The temperatures of both chambers were changed in a dynamic manner dependent upon the position of the fish. When the fish was in the warmest chamber the temperature of both chambers was made to increase at a rate of 1 � C h 1, and when the fish moved to the chamber with lowest temperature, the temperatures of both chambers started to decrease at the same rate. Most fish rapidly learn to control their body temperature by moving between the 2
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Fig. 1. Body weight (g) of individual juvenile lumpfish from GN and GS used in the temperature preference experiment.
chambers in 24 h or less (Reynolds and Casterlin, 1979), but to ensure that the fish was not harmed by too high or too low temperatures the temperature of the chambers was only allowed to vary between 5 � C and 16 � C. For more technical details, see Stol et al. (2013) and Siikavuopio et al. (2014). Water temperature in the tank the fish occupied was recorded every second. Temperature preference measurements were made alternately with fish from GN and GS. Each fish was kept in the shuttle-box for 48 h without food. After recordings, the fish were weighed and returned to the grow out tank, and the shuttle-box was cleaned, water replaced and made ready for the next fish. 2.3. Data collection, calculations and statistics Median occupation temperatures for all fish were calculated for every 6 h from the start of the experiment to the end. In total, an indi vidual fish was monitored for 48 h. Median temperatures, but not the average temperature, were used since medians are not biased even if the fish occupy the highest or lowest temperatures was set by us for a short period. The normality of all data sets was tested with the Shapiro–Wilk W statistic and all data were normally distributed. Statistical differences between the two fish groups in preferred temperature and body weights were tested with Student’s t-test. Correlations amongst preference temperature and initial weight, growth rate and body weight at measuring date were tested with linear regression. A probability level of less than 0.05 was considered significant. 3. Results Among the eleven lumpfish juveniles from each region we used in our study, behaviour of each fish was different which, resulted in higher variations in the preferred temperatures (Fig. 3). While most fish chose lower temperatures compared to the initial temperature at the start, fish 1 and 2 from GN chose higher temperatures. Except for one fish each from GN and GS, all fish learnt to use the shuttle box in the first 18 h by moving between the two boxes. The trend of preferred temperatures for the juvenile lumpfish from GN and GS are shown in Fig. 4. The points in the figure show the mean of the median occupied temperatures in the 6-h intervals from start to the
Fig. 2. Sketch of the shuttle box system showing the components.
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Fig. 3. Variation in behaviour of lumpfish juveniles among selected fish from GN and GS.
Fig. 4. Temperature preference of lumpfish juveniles during the 48-hrs measurement. Values are mean � SE.
temperature preference calculations. We used the temperature regis trations from 18 to 48 h to calculate the temperature preference of the individual fish. Based on these assumptions, the preferred temperatures (final thermal preferendum) for lumpfish juveniles are 6.92 � 1.18 (SD) and 6.2 � 1.17 (SD) for GN and GS, respectively. Despite a difference of 0.72 � C in the mean preference temperature between GN and GS, the values were not significantly different (p > 0.213). There was no significant difference in SGR between the two groups from tagging to start of the temperature preference test (1.37 � 0.225 and 1.43 � 0.13% d 1 for GN and GS, respectively; p > 0.47). Since there was no difference in temperature preference between the groups,
end of registration (�SD), for the groups. Except for four fish, all the fish selected temperatures lower than the average start temperatures (7.81 � C (GN) or 7.58 � C (GS); the temperatures of their hold tanks when the registration started) in the first 18-h period. From period 18 h onwards the selected temperature of the two groups seemed to have reached a plateau. This was especially evident in the GS. Based on the curves (Fig. 4) and the behaviour of different fish species in this type of shuttle-box (Reynolds and Casterlin, 1979), we categorized 0–18 h as the learning period because in this period the lumpfish learned to regulate their body temperatures by moving back and forth between the two chambers and this was not used in 4
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the data from both groups were merged for further correlation analyses. These showed that there was no significant correlation between tem perature preference and body weight at measuring date (r ¼ 0.3, p > 0.175), or between temperature preference and SGR (r ¼ 0.333, p > 0.129).
locusts (Brown and Griffin, 2005; Ward et al., 2010; Coggan et al., 2011). However, fish may also increase their preference temperature when deprived of food, as shown for brown trout, Salmo trutta (Elliot and Allonby, 2013). These different reactions to food deprivation are not necessarily in conflict, but both can be part of a “growth maximizing strategy”. If food is more available in areas with higher temperatures, it may be advantageous to seek food in these areas instead of moving to areas with lower temperatures in order to save energy (Jobling, 1997). Currently, the only reason for producing lumpfish in aquaculture is to use them as “cleanerfish” in salmon sea cages to eat salmon lice. Lice eating ability is therefore the most interesting trait to improve by se lective breeding. Imsland et al. (2016) found family differences in lice grazing in lumpfish and suggested that lice grazing could be an inher itable trait which can be improved by selective breeding. This brings up an important question; that is if we need more than one selection line to account for different populations or subpopulations that can have different environmental requirements such as the temperature. Results from the present study indicate that preference temperature of lumpfish in Norway is independent of geographic origin. Neither did we find any difference in growth rate between the groups of lumpfish used in this study. Genetic analyses have shown that there is only one population of �nsdo �ttir et al., 2018). Taken together, these lumpfish in Norway, (Jo findings support the view that lumpfish can be used as “cleanerfish” anywhere in Norway independent of their geographical origin, and that one selection line can cover the whole country in a selective breeding program. The present results reveal that lumpfish above 150 g prefer low temperatures which are typical for the offshore habitats where fish of this size spend the winter. Lumpfish used as “cleanerfish” are deprived of the possibility to choose their own habitat and may be forced to stay at temperatures substantially above their temperature preference (Hvas et al., 2018). If that has any impact on their welfare and disease resis tance is an open question which has still not been addressed.
4. Discussion The results of this study revealed no difference in preference tem perature or growth rate between lumpfish from Flekkefjord (GS) and �nsdo �ttir et al. (2018), who Tromsø (GN). Our results are in line with Jo indicated that there is only one population of lumpfish along the Nor wegian coast. These results also confirm that lumpfish of the size used in this study prefers low temperatures which might match the tempera tures they experience in the wild during winter, when they stay in deeper water further away from the coast (Kennedy et al., 2015). There were 2-3-fold differences in weight within the groups (156–318 g in GN and from 154 to 426 g in GS). Lumpfish juveniles used in this experiment were from different families within each group. So, the differences in weight within GN and GS were because of family differences in growth and such differences exist between families in many fish species (Xu et al., 2013). Further, geographical differences in distribution can also lead to growth differences as it was seen between GS and GN groups (Nicieza et al., 1994). Lumpfish is a fast-growing fish at this early juvenile stage (Nytrø et al., 2014). The experiment was conducted for 10 weeks and some fish tested during the first weeks were smaller compared to fish tested at later stages. Together, all these factors resulted in the variation in body weight of the fish during the experiment. Nytrø et al. (2014) found that optimal temperature for growth of juvenile lumpfish varied significantly with the fish size, being approxi mately 16 � C for fish between 11 and 40 g, and declining to 8.9 � C for fish between 120 and 200 g. Between the temperature interval of 4–13 � C, growth rate was independent of temperature for fish larger than 160 g. The two groups of lumpfish used in our study had mean weights of 222 g (GN) and 280 g (GS), and might have had an optimal growth temperature close to 8.9 � C or slightly below. If that is true, the tem perature preferences measured by us were 2.0/2.7 � C (GN/GS, respec tively) lower than that of the temperature required for optimal growth rate. Normally, this would mean that the fish are selecting a temperature which would result in a lower growth rate. But this is not necessarily the case for lumpfish because lumpfish of the size used in our experiment has a growth rate independent of temperature in the temperature in terval from 6 to 12 � C (Nytrø et al., 2014). In the present study, we also found that preference temperature was not correlated to growth rate. Thus, lumpfish can select temperature lower than the temperature needed for the optimal growth temperature without compromising growth rate (Nytrø et al., 2014). The reason that lumpfish selects a temperature towards the lower end of the optimal temperature range for growth is probably because it is energetically advantageous. Larsson (2005) found that Arctic charr, Salvelinus alpinus, selected temperatures significantly lower than that required for optimal growth, while brown trout, Salmo trutta, selected temperatures for optimal growth. Larsson suggested that the reason why Arctic charr selected temperatures lower than the optimal growth tem perature is that this species is optimizing food conversion efficiency, which is higher at lower temperatures. When choosing between fast growth and efficient food conversion, Arctic charr prioritizes efficiency. In contrast, lumpfish can choose a low temperature without losing the advantage of faster growth. Still, our values for preference temperatures may have been influenced by the fact that the measurements were made on lumpfish without access to food. To seek lower temperatures in cases of food shortage as a strategy for energy conservation is found in several fish species (Mac, 1985; Despatie et al., 2001; Ward et al., 2010). A similar relationship between temperature preference and nutritional status is also found in several ectothermic animals such as lizards and
5. Conclusion The results from the present study indicate that the temperature preference and growth rate of lumpfish from different parts of Norway are independent of their geographic origin. This suggests that the same lumpfish can be used as “cleanerfish” anywhere in Norway because no significant differences in temperature preference were found in our study. With respect to selective breeding, there is no need for different selection lines to account for different temperatures along the Norwe gian coast. CRediT authorship contribution statement Atle Mortensen: Conceptualization, Methodology, Writing - review & editing. Richard B. Johansen: Methodology, Formal analysis, Writing - review & editing. Øyvind J. Hansen: Formal analysis, Writing - review & editing. Velmurugu Puvanendran: Conceptualization, Methodology, Writing - original draft, Formal analysis, Writing - review & editing. Acknowledgements We thank Thor Arne Hangstad (Akvaplan-niva) and Andreas Lind holm (Norsk Oppdrettsservice AS) for providing the lumpfish eggs and the staff at the CMA for their help during the juvenile rearing and in setting up the shuttle box system. This work has been supported by funding from the Ministry of Trade, Industry and Fisheries of Norway and Nofima. There is no conflict of interest in relation to this study.
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