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Coastal versus estuarine nursery grounds: Effect of differential temperature and heat waves on juvenile seabass, Dicentrarchus labrax
Estuarine, Coastal and Shelf Science 109 (2012) 133e137
Contents lists available at SciVerse ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Coastal versus estuarine nursery grounds: Effect of differential temperature and heat waves on juvenile seabass, Dicentrarchus labrax Catarina Vinagre a, *, Luís Narciso b, Henrique N. Cabral a, Maria J. Costa a, Rui Rosa b a b
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Laboratório Marítimo da Guia, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 July 2011 Accepted 23 May 2012 Available online 5 June 2012
This study investigates the biological responses of juvenile fish (Dicentrarchus labrax), that live in both coastal and estuarine nurseries, to differential temperatures and summer heat wave events. More specifically, we compared mortality, growth, condition, metabolic response and thermal sensitivity of 0group juveniles of D. labrax at temperatures that reflect the average summer temperature that they encounter in coastal and estuarine nurseries, and also the temperatures that they endure inside estuaries during heat wave events. The low mortality and peak growth and condition values registered at 24 C suggest that estuarine average summer temperatures are more beneficial for the juveniles than coastal ones. The estuarine water temperature attained during heat waves resulted in higher mortality, arrested growth, lower condition and a steep increase in metabolism, indicating that this species is probably under thermal stress at 28 C. Consequently, future predictions of frequent and prolonged heat waves in Southern Europe are expected to induce negative impacts in the biology and metabolic ecology of 0group seabass juveniles in estuarine nurseries. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: mortality growth condition metabolism thermal sensitivity climate change
1. Introduction Coastal habitats are highly productive areas and are used as nursery grounds by the juveniles of many marine fish species (Costanza et al., 1997). Generally, an area has been called a nursery if juvenile fish occur at higher densities, avoid predation more successfully, or grow faster there than in a different habitat (Haedrich, 1983; Beck et al., 2001). Information on different densities of fish juveniles is abundant in literature, yet direct comparisons of survival and growth among different coastal habitats are rare (Beck et al., 2001). Temperature is considered the most important variable influencing fish growth and one of the key factors that allow high juvenile growth rates in nursery areas (Haedrich, 1983). The higher temperatures registered in nursery areas also increase survival chances because less time is spent at the most vulnerable sizes. One of the most significant differences between coastal and estuarine nurseries is temperature. Juveniles use these areas during summer, when estuarine waters are considerably warmer than coastal waters (Poxton and Allouse, 1982). Various marine fish juveniles use both coastal and estuarine nurseries, yet the effect of
* Corresponding author. E-mail address: [email protected] (C. Vinagre). 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2012.05.029
the differential temperature over the juveniles’ growth and general fitness is generally untested. It is accepted that the higher temperatures attained by the estuarine waters will enable faster growth rates, as growth rate is positively correlated with temperature in ectotherms. Yet, this is only true inside each species optimum thermal interval (Pörtner, 2002). Heat waves are predicted to become more frequent and prolonged (IPCC, 2001), which may lead to estuarine water temperatures above the thermal interval of some fish species, with concomitant negative effects on growth, fitness and survival. As other factors may be at play, such as food availability and salinity, the effect of temperature is better isolated in experimental studies done in captivity, yet such studies are lacking for the 0-group juveniles of most fish species. The European seabass, Dicentrarchus labrax, is a marine species whose juveniles use both coastal and estuarine nurseries. This is a highly valued fish that extends its distribution from North Africa to Norway, including the Mediterranean and the Black Sea (Smith, 1990). Adults migrate to coastal areas during the spawning season, larvae develop in the coast and then migrate to sheltered coastal or estuarine nurseries where they spend their first years of life (Holden and Williams, 1974; Kelley, 1988; Laffaille et al., 2001). Juvenile seabass seems to cease growing at 11e15 C, to grow fast at 22e25 C and their thermal limits to be around 2e3 C and 30e32 C (Barnabé, 1990). The investigation of the effect of temperature on the species 0-group juveniles is particularly
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important in its southern range where temperatures are higher and more likely to be over its optimum thermal interval. The present work aimed to investigate and compare mortality, growth, condition, metabolic response and thermal sensitivity of 0group juveniles of D. labrax at different temperatures, reflecting the average summer temperature that juveniles of this species encounter in coastal (18 C) and estuarine nurseries (24 C) along the Portuguese coast and also the temperature that they endure inside estuaries during heat wave events (28 C). 2. Materials and methods Juvenile Dicentrarchus labrax (mass range: 4.6 ge7.5 g and total length range: 75 mme86 mm) were obtained from a local hatchery (A. Coelho e Castro, Lda, Póvoa doVarzim, Portugal). Upon arrival at the laboratory they were kept in three indoor re-circulating water systems, each comprising four 70 l tanks, supplied with aerated seawater. The water dissolved O2 level varied between 95% and 100%. There were 5 individuals per tank (3 systems, each with 4 tanks, 5 fish per tank ¼ total of 60 fish). Fish were allowed to acclimate for 3 weeks, at 16 C, the same temperature found in the hatchery upon collection. They were fed twice a day with commercial dry food ad libitum. After 3 weeks, temperature was altered at a rate of 1 C per each 2 h until reaching the experimental temperatures of 18 C, 24 C and 28 C. These temperatures were chosen to reflect: i) the mean western Atlantic coastal water temperature (at w38 N) in summer (18 C) (Locarnini et al., 2006), ii) the mean summer estuarine water temperature (24 C) (Centro de Oceanografia Database 1978e2006, Fig. 1), and iii) the water temperature registered during summer heat waves in Portuguese estuarine nurseries (28 C) (Centro de Oceanografia Database, 1978e2006). Given the size of the fish we worked with, we chose to mimic the month of July at an approximate latitude of 38 N, when fish within the size tested are present at nursery areas. Our team as been studying estuarine juvenile fish in the Tagus estuary since 1978, and thus there are available data on juvenile fish size and water temperature (Cabral and Costa, 2001, Fig. 1). Fish were kept at the experimental temperatures for 60 days and mortality was observed on a daily basis. In order to study individual growth each fish was tagged with an external numbered fine T-bar anchor tag (Hallprint). Fish were measured at the beginning of the experiment and in the last day (to the nearest 0.1 mm). Growth increment was registered and divided by 60 days in order to estimate daily growth rate. At the end of the experiment fish weight (wet weight Wt, measured to the nearest 0.01 g) was measured in order to calculate
the Fulton’s K condition factor, which was directly determined from the morphometric data with the formula
K ¼ 100 Wt=Lt3 where Wt is total wet weight (mg) and Lt total length (mm) (Ricker, 1975). Before the assessment of condition, closed respirometry was carried out individually. Each individual was allowed to deplete the available oxygen in a sealed respirometry chamber (Loligo systems), filled with filtered seawater containing 50 mgl1 streptomycin (Rosa and Seibel, 2008). The O2 levels were recorded continuously with a Clarke-type O2 electrode connected to a Strathkelvin Instruments 929 Oxygen Interface (Rosa and Seibel, 2010). The chamber was submerged in a flow-through container coupled with a water bath (Lauda Ecoline RE 108) that kept experimental temperature stable (0.1 C). Control runs were carried out. Before each experiment fish were allowed to acclimate to the chamber for 2 h. During the experimental runs fish were continuously observed. Feeding was discontinued 24 h before oxygen consumption measurements. All experiments were carried out in shaded day light (15L:09D). The routine metabolic rate (RMR) measured in the resting animal (Randall et al., 1997) was estimated and thermal sensitivity (Q10 value) (Randall et al., 1997) was calculated between 18 C and 24 C, 18 C and 28 C and between 24 C and 28 C, as. ðMR2 =MR1 Þ10=ðt2 t1 Þ in which MR2 and MR1 are the metabolic rates at temperature t1 and t2, respectively. Q10 is a measure of the temperature sensitivity of an enzymatic reaction rate or a physiological process due to an increase by 10 C (Randall et al., 1997). Analyses of variance (ANOVA) were performed to test for the effect of temperature on growth, condition and RMR, followed by Tukey post-hoc tests whenever the null hypothesis was rejected. A significance level of 0.05 was used in all test procedures. 3. Results Mortality was 10% at 18 C, two fish died, one after 22 days and the other after 30 days (Fig. 2). At 24 C no fish died and at 28 C three fish died, after 20 days, 33 days and 41 days respectively, representing 15% of the initial sample (Fig. 2). Temperature significantly affected growth of Dicentrarchus labrax (ANOVA, MS ¼ 0.09, F ¼ 22.17, P ¼ 0.00). Growth was 0.23 mm day1 at 18 C, it increased at to 0.30 mm day1 at 24 C, and it decreased to 0.11 mm day1 at 28 C, to (Fig. 3). Post-hoc tests
25
100 80 % Mortality
Temperature (ºC)
20 15 10 5 0
60 40 20
1
2
3
4
5
6
7
8
9
10
11
12
Month
0 1
5
9 13 17 21 25 29 33 37 41 45 49 53 57 60 Days
Fig. 1. Mean water temperatures (bars stand for standard deviations) in the nursery areas of the Tagus estuary (Portugal), data from 1978, 1979, 1980, 2001, 2002, 2005 and 2006 (Centro de Oceanografia Database).
Fig. 2. Percentage of mortality of D. labrax at 18 C, in black dots, at 24 C, in grey, and at 28 C, in black.
C. Vinagre et al. / Estuarine, Coastal and Shelf Science 109 (2012) 133e137
0.4
18 C and 28 C (p < 0.05), and 24 C and 28 C (p < 0.05). Thermal sensitivity was high for the temperature interval between 24 C and 28 C, reaching a value >3. However, it was low for the other temperature intervals (Fig. 4).
0.3
4. Discussion
0.2
The low mortality and peak growth and condition values registered at 24 C indicate that the average summer temperatures registered in estuarine nursery areas are more beneficial for the species 0-group juveniles than coastal average summer temperatures (18 C). The estuarine water temperature attained during heat waves (28 C) resulted in higher mortality, arrested growth, lower condition and a steep increase in metabolism, indicating that this species is probably under some degree of thermal stress at 28 C and that more frequent and prolonged heat waves will not be favourable for its 0-group juveniles. The fact that the fish used here were from a fish farm may be a limitation, in that they may be adapted to an artificial environment where the selective pressures are different than those found in the field. However, working with fish from a fish farm allowed us to work with individuals with a known and acclimated thermal history. If we had used wild animals we would not know how much time they and previous generations had spent in coastal and estuarine nurseries and their exposure to different thermal conditions, which might have interfered with the experiment. Growth rates estimated in the present study were lower than field estimates by Cabral and Costa (2001) and Vinagre et al. (2009), 0.65 mm day1 and 0.56 mm day1, based on monthly size distributions and otolith microstructure, respectively. However, these previous estimations involve a considerable degree of uncertainty due to the techniques employed. Condition estimates were very similar to the average condition determined for the species 0-group juveniles in Portuguese estuaries, also based on the Fulton’s K, which was 0.88 (Vasconcelos et al., 2009). It should be noted that, although, a decrease in growth rate and an increase in metabolism was registered at 28 C, the condition of those fish was very similar to that observed at the other experimental temperatures and registered in wild fish (Vasconcelos et al., 2009). This suggests that the degree of thermal stress endured by these fish is not severe. Although Dicentrarchus labrax is a highly valued species, there are no reported similar experimental studies on 0-group juveniles, thus preventing us from making comparisons and testing the soundness of our experimental approach. There is, however, research on adult metabolism (mean weight 629 g) which can
Growth rate (mm.day -1)
0.5
0.1 0 15
20
25
30
T(ºC)
b
1.10
Fulton's K
1.00 0.90 0.80 0.70 0.60 0.50 15
20
25
30
T (ºC)
RMR (µmol O 2.g-1.h -1)
C
25 20 15 10 5 0 15
20
25
30
T (ºC) Fig. 3. Growth rates (a), condition (b) and standard metabolic rate (mmol O2 g1 h1) (c) of D. labrax at 18 C, 24 C and 28 C.
showed that growth was significantly different between 18 C and 28 C (p < 0.05) and 24 C and 28 C (p < 0.05). The condition of Dicentrarchus labrax was also significantly affected by temperature (ANOVA, MS ¼ 0.00, F ¼ 6.14, P ¼ 0.04). Fulton’s K was 0.99 at 18 C, 1.00 at 24 C, and 0.89 at 28 C (Fig. 3). Post-hoc tests showed that condition was significantly different between 18 C and 28 C, and 24 C and 28 C (p < 0.05). Temperature significantly affected the metabolism of this species. RMR was 11.01 mmol O2 g1 h1 at 18 C, 11.53 mmol O2 g1 h1 at 24 C and it increased steeply at 28 C to 19.10 mmol O2 g1 h1 (Fig. 3, ANOVA, MS ¼ 61.52, F ¼ 13.88, P ¼ 0.00). Post-hoc tests showed that metabolism was significantly different between
Thermal sensitivity (Q10)
a
135
4 3 2 1 0 18-24
18-28
24-28
Temperature interval (ºC) Fig. 4. Thermal sensitivity of D. labrax estimated between 18 C and 24 C, 18 C, and 28 C, 24 C and 28 C.
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indicate the thermal optimum of this species (Claireaux and Lagardère, 1999). Our results agree with Claireaux and Lagardère (1999), who observed that between 20 C and 25 C the metabolism of Dicentrarchus labrax became less susceptible to temperature fluctuations, concluding that this thermal interval encompasses the thermal preferendum of this species, permiting complete thermal compensation in metabolism (Precht et al., 1955). These authors also observed that as temperature reached 25 C only small changes in fish metabolic capacity were observed which is indicative of homeostasis. The low thermal sensitivity values estimated by Claireaux and Lagardère (1999) in the intervals of 15 Ce20 C and 20 Ce25 C, 1.88 and 1.08, respectively, are similar to the values estimated for 0-group juveniles between 18 C and 24 C, in the present work. However, these authors did not test temperatures above 25 C and thus did not report on thermal stress in the upper thermal range of this species. Vinagre et al. (2012) using the same experimental temperatures as used here, concluded that at 24 C oxidative stress was at its lowest, indicating that this temperature is within the D. labrax thermal optimum. Person-Le Ruyet et al. (2004) tested the effect of temperature on growth and metabolism of 20-month-old (82 g) Dicentrarchus labrax on an interval from 13 to 29 C. Similarly, to the present work, these authors observed an arrest in growth at 29 C and concluded that 26 C is the temperature for maximal growth for this age-group. It was also concluded that growth is markedly depressed in cooler waters, 65% lower at 13 C than at 26 C, and that this reduction in growth rate results primarily from a decrease in food intake. An increase of 8% in metabolic rate from 25 C to 29 C was also reported and related to maintenance costs due to thermal stress. The metabolic rate steep increase at 28 C, observed in the present work, revealed that Dicentrarchus labrax metabolism accelerates at this temperature, which is indicative of a decline in physiological efficiency. Thermal sensitivity was also higher between 24 C and 28 C than at the other thermal intervals, reaching values >3. Thermal sensitivity values between 2 and 3 are considered usual, yet higher values have been seen in fishes exposed to temperatures outside their normal temperature range (Johnston et al., 1991), which confirms that D. labrax southern European populations are not adapted to spend prolonged periods at this high temperature. Madeira et al. (2012) determined that the critical thermal maximum of D. labrax juveniles is 33.3 C. Studies with other marine fish species indicate that the borders of the thermal tolerance window are characterized by the onset of internal systemic hypoxia despite fully oxygenated waters, resulting in anaerobic metabolism that cannot be sustained for long periods (Pörtner, 2002). Currently, heat waves have a duration of 1e2 weeks, and this species can certainly cope with that, yet a longterm experiment such as this reveals that the temperatures reached during heat waves are not favourable for this species over longer periods. This is important from a climate change perspective, since an increase in duration and frequency of such elevated temperatures is to be expected in the near future (IPCC, 2001). The ecological consequences of climate change will, however, depend on the rate of adaptation of species to their changing environment. It is likely that this species has the ability to adapt to higher temperatures, since it also occurs in North Africa. Gene flow from lower latitude populations may be crucial for the adaptation of southern European populations to increased temperatures, with genotypes that are tolerant to higher temperatures gradually becoming prevalent in European populations due to natural selection (Helmuth et al., 2005; Visser, 2008). Knowledge of the relative value of each habitat may be crucial for prioritizing management and/or conservation actions that affect
fish nurseries for this and other species (Johnston et al., 2002; Vinagre et al., 2006, 2008). Reliable information based on field and experimental studies will allow funding institutions to better target their conservation efforts and make better regulatory decisions for fisheries management, habitat restoration and climate change impacts mitigation. However, predicting the impact of climate change on a particular species is a complex task and requires input from several subjects including ecology, eco-physiology, molecular ecology, genetics and evolution. It is a multi-disciplinary endeavour and deals with a high level of uncertainty given the many interacting variables. We consider that studies such has the one presented here, are necessary first-steps unravelling the complexity behind some of the climate change effects that may be just around the corner.
Acknowledgements Authors would like to thank everyone involved in the maintenance of the experimental tanks. This study had the support of the Portuguese Fundação para a Ciência e a Tecnologia (FCT) through the grant SFRH/BPD/34934/2007 awarded to C. Vinagre.
References Barnabé, G., 1990. Rearing bass and gilthead bream. In: Barnabé, G. (Ed.), Aquaculture. Ellis Horwood, NY, pp. 647e686. Beck, M.W., Heck, K.L., Able, K.W., Childers, D.L., Eggleston, D.B., Gillanders, B.M., Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F., Weinstein, M.R., 2001. The identification, conservation and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633e641. Cabral, H.N., Costa, M.J., 2001. Abundance, feeding ecology and growth of 0-group sea bass, Dicentrarchus labrax, within the nursery areas of the Tagus estuary. Journal of the Marine Biological Association of the UK 81, 679e682. Claireaux, G., Lagardère, J.-P., 1999. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. Journal of Sea Research 42, 157e168. Costanza, R., Arge, R., de Groot, R., Farberk, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O’Neill, R.V., Paruelo, J., Raskin, R.G., Suttonkk, P., van den Bel, M., 1997. The value of the world’s ecosystem services and natural capital. Nature 387, 253e260. Haedrich, R.L., 1983. Estuarine fishes. In: Ketchum, B. (Ed.), Ecosystems of the World 26. Estuarine and Enclosed Seas. Elsevier, Amsterdam, pp. 183e207. Helmuth, B., Kingsolver, J.G., Carrington, E., 2005. Biophysics, physiological ecology and climate change: does mechanism matter? Annual Reviews in Physiology 67, 177e201. Holden, M.J., Williams, T., 1974. The biology, movements and populations dynamics of bass, Dicentrarchus labrax, in English waters. Journal of the Marine Biological Association of the UK 54, 91e107. IPCC, 2001. Third assessment report of the working group I. In: Houghton, J.T., et al. (Eds.), The Science of Climate Change. Cambridge University Press, Cambridge, p. 785. Johnston, I.A., Clarke, A., Ward, P., 1991. Temperature and metabolic rate in sedentary fish from the Antartic, North-Sea and Indo-West Pacific. Ocean Marine Biology 109, 191e195. Johnston, R.J., Grigalunas, T.A., Opaluch, J.J., Mazzotta, M., Diamantedes, J., 2002. Valuing estuarine resource services using economic and ecological models: the Peconic estuary system study. Coastal Management 30, 47e65. Kelley, D.F., 1988. The importance of estuaries for sea bass, Dicentrarchus labrax (L.). Journal of Fish Biology 33, 25e33. Laffaille, P., Lefeuvre, J.-C., Schricke, M.-T., Feunteun, E., 2001. Feeding ecology of 0group sea bass, Dicentrarchus labrax, in salt marshes of Mont Saint Michel Bay (France). Estuaries and Coasts 24, 116e125. Locarnini, R.A., Mishonov, A.V., Antonov, J.I., Boyer, T.P., Garcia, H.E., 2006. World Ocean Atlas 2005. In: Levitus, S. (Ed.), Temperature. NOAA Atlas NESDIS 61, vol. 1. U.S. Government Printing Office, Washington, D.C, p. 182. Madeira, D., Narciso, L., Cabral, H., Vinagre, C., 2012. Thermal tolerance and potential climate change impact in marine and estuarine organisms. Journal of Sea Research 70, 32e41. Precht, H., Christophersen, J., Hensel, J., 1955. Temperatur und Leben. Springer, Berlin. Person-Le Ruyet, J., Mahé, K., Bayon, N., Delliou, H., 2004. Effects on growth and metabolism in a Mediterranean population of European sea bass, Dicentrarchus labrax. Aquaculture 237, 269e280. Pörtner, H.O., 2002. Climate change and temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals. Comparative Biochemistry and Physiology A 132, 739e761.
C. Vinagre et al. / Estuarine, Coastal and Shelf Science 109 (2012) 133e137 Poxton, M.G., Allouse, S.B., 1982. Water quality criteria for marine fisheries. Aquacultural Engineering 1, 153e191. Randall, D., Burggren, W., French, K., 1997. Eckert Animal Physiology: Mechanisms and Adaptations. Freeman W.H. and Company, USA, p. 727. Ricker, W.E., 1975. Computation and interpretation of biological statistics of fish populations. Bulletin of the Fisheries Research Board of Canada 191, 1e382. Rosa, R., Seibel, B.A., 2008. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proceedings of the National Academy of Sciences of the USA 105, 20776e20780. Rosa, R., Seibel, B.A., 2010. Metabolic physiology of the Humboldt squid, Dosidicus gigas: implications for vertical migration in a pronounced oxygen minimum zone. Progresses in Oceanography 86, 72e80. Smith, C.L., 1990. Moronidae. In: Quero, J.C., Hureau, J.C., Karrer, C., Post, A., Saldanha, L. (Eds.), 1990. Check-list of the Fishes of the Eastern Tropical Atlantic (CLOFETA), vol. 2. UNESCO, Paris, pp. 692e694. Vasconcelos, R.P., Reis-Santos, P., Fonseca, V., Ruano, M., Tanner, S., Costa, M.J., Cabral, H.N., 2009. Juvenile fish condition in estuarine nurseries along the Portuguese coast. Estuarine, Coastal and Shelf Science 82, 128e138.
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Vinagre, C., Fonseca, V., Cabral, H., Costa, M.J., 2006. Habitat suitability index models for the juvenile soles, Solea solea and Solea senegalensis: defining variables for management. Fisheries Research 82, 140e149. Vinagre, C., Fonseca, V., Maia, A., Amara, R., Cabral, H.N., 2008. Habitat specific growth rates and condition indices for the sympatric soles populations of Solea solea (Linnaeus, 1758) and S. senegalensis Kaup 1858, in the Tagus estuary, Portugal, based on otolith daily increments and RNA: DNA ratio. Journal of Applied Ichthyology 24, 163e169. Vinagre, C., Ferreira, T., Matos, L., Costa, M.J., Cabral, H.N., 2009. Latitudinal gradients in growth and spawning of sea bass, Dicentrarchus labrax (L.) and their relationship with temperature and photoperiod. Estuarine, Coastal and Shelf Science 81, 375e380. Vinagre, C., Madeira, D., Narciso, L., Cabral, H., Diniz, M., 2012. Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecological Indicators 23, 274e279. Visser, M.E., 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B275, 649e659.
Contents lists available at SciVerse ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Coastal versus estuarine nursery grounds: Effect of differential temperature and heat waves on juvenile seabass, Dicentrarchus labrax Catarina Vinagre a, *, Luís Narciso b, Henrique N. Cabral a, Maria J. Costa a, Rui Rosa b a b
Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Laboratório Marítimo da Guia, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 July 2011 Accepted 23 May 2012 Available online 5 June 2012
This study investigates the biological responses of juvenile fish (Dicentrarchus labrax), that live in both coastal and estuarine nurseries, to differential temperatures and summer heat wave events. More specifically, we compared mortality, growth, condition, metabolic response and thermal sensitivity of 0group juveniles of D. labrax at temperatures that reflect the average summer temperature that they encounter in coastal and estuarine nurseries, and also the temperatures that they endure inside estuaries during heat wave events. The low mortality and peak growth and condition values registered at 24 C suggest that estuarine average summer temperatures are more beneficial for the juveniles than coastal ones. The estuarine water temperature attained during heat waves resulted in higher mortality, arrested growth, lower condition and a steep increase in metabolism, indicating that this species is probably under thermal stress at 28 C. Consequently, future predictions of frequent and prolonged heat waves in Southern Europe are expected to induce negative impacts in the biology and metabolic ecology of 0group seabass juveniles in estuarine nurseries. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: mortality growth condition metabolism thermal sensitivity climate change
1. Introduction Coastal habitats are highly productive areas and are used as nursery grounds by the juveniles of many marine fish species (Costanza et al., 1997). Generally, an area has been called a nursery if juvenile fish occur at higher densities, avoid predation more successfully, or grow faster there than in a different habitat (Haedrich, 1983; Beck et al., 2001). Information on different densities of fish juveniles is abundant in literature, yet direct comparisons of survival and growth among different coastal habitats are rare (Beck et al., 2001). Temperature is considered the most important variable influencing fish growth and one of the key factors that allow high juvenile growth rates in nursery areas (Haedrich, 1983). The higher temperatures registered in nursery areas also increase survival chances because less time is spent at the most vulnerable sizes. One of the most significant differences between coastal and estuarine nurseries is temperature. Juveniles use these areas during summer, when estuarine waters are considerably warmer than coastal waters (Poxton and Allouse, 1982). Various marine fish juveniles use both coastal and estuarine nurseries, yet the effect of
* Corresponding author. E-mail address: [email protected] (C. Vinagre). 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2012.05.029
the differential temperature over the juveniles’ growth and general fitness is generally untested. It is accepted that the higher temperatures attained by the estuarine waters will enable faster growth rates, as growth rate is positively correlated with temperature in ectotherms. Yet, this is only true inside each species optimum thermal interval (Pörtner, 2002). Heat waves are predicted to become more frequent and prolonged (IPCC, 2001), which may lead to estuarine water temperatures above the thermal interval of some fish species, with concomitant negative effects on growth, fitness and survival. As other factors may be at play, such as food availability and salinity, the effect of temperature is better isolated in experimental studies done in captivity, yet such studies are lacking for the 0-group juveniles of most fish species. The European seabass, Dicentrarchus labrax, is a marine species whose juveniles use both coastal and estuarine nurseries. This is a highly valued fish that extends its distribution from North Africa to Norway, including the Mediterranean and the Black Sea (Smith, 1990). Adults migrate to coastal areas during the spawning season, larvae develop in the coast and then migrate to sheltered coastal or estuarine nurseries where they spend their first years of life (Holden and Williams, 1974; Kelley, 1988; Laffaille et al., 2001). Juvenile seabass seems to cease growing at 11e15 C, to grow fast at 22e25 C and their thermal limits to be around 2e3 C and 30e32 C (Barnabé, 1990). The investigation of the effect of temperature on the species 0-group juveniles is particularly
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important in its southern range where temperatures are higher and more likely to be over its optimum thermal interval. The present work aimed to investigate and compare mortality, growth, condition, metabolic response and thermal sensitivity of 0group juveniles of D. labrax at different temperatures, reflecting the average summer temperature that juveniles of this species encounter in coastal (18 C) and estuarine nurseries (24 C) along the Portuguese coast and also the temperature that they endure inside estuaries during heat wave events (28 C). 2. Materials and methods Juvenile Dicentrarchus labrax (mass range: 4.6 ge7.5 g and total length range: 75 mme86 mm) were obtained from a local hatchery (A. Coelho e Castro, Lda, Póvoa doVarzim, Portugal). Upon arrival at the laboratory they were kept in three indoor re-circulating water systems, each comprising four 70 l tanks, supplied with aerated seawater. The water dissolved O2 level varied between 95% and 100%. There were 5 individuals per tank (3 systems, each with 4 tanks, 5 fish per tank ¼ total of 60 fish). Fish were allowed to acclimate for 3 weeks, at 16 C, the same temperature found in the hatchery upon collection. They were fed twice a day with commercial dry food ad libitum. After 3 weeks, temperature was altered at a rate of 1 C per each 2 h until reaching the experimental temperatures of 18 C, 24 C and 28 C. These temperatures were chosen to reflect: i) the mean western Atlantic coastal water temperature (at w38 N) in summer (18 C) (Locarnini et al., 2006), ii) the mean summer estuarine water temperature (24 C) (Centro de Oceanografia Database 1978e2006, Fig. 1), and iii) the water temperature registered during summer heat waves in Portuguese estuarine nurseries (28 C) (Centro de Oceanografia Database, 1978e2006). Given the size of the fish we worked with, we chose to mimic the month of July at an approximate latitude of 38 N, when fish within the size tested are present at nursery areas. Our team as been studying estuarine juvenile fish in the Tagus estuary since 1978, and thus there are available data on juvenile fish size and water temperature (Cabral and Costa, 2001, Fig. 1). Fish were kept at the experimental temperatures for 60 days and mortality was observed on a daily basis. In order to study individual growth each fish was tagged with an external numbered fine T-bar anchor tag (Hallprint). Fish were measured at the beginning of the experiment and in the last day (to the nearest 0.1 mm). Growth increment was registered and divided by 60 days in order to estimate daily growth rate. At the end of the experiment fish weight (wet weight Wt, measured to the nearest 0.01 g) was measured in order to calculate
the Fulton’s K condition factor, which was directly determined from the morphometric data with the formula
K ¼ 100 Wt=Lt3 where Wt is total wet weight (mg) and Lt total length (mm) (Ricker, 1975). Before the assessment of condition, closed respirometry was carried out individually. Each individual was allowed to deplete the available oxygen in a sealed respirometry chamber (Loligo systems), filled with filtered seawater containing 50 mgl1 streptomycin (Rosa and Seibel, 2008). The O2 levels were recorded continuously with a Clarke-type O2 electrode connected to a Strathkelvin Instruments 929 Oxygen Interface (Rosa and Seibel, 2010). The chamber was submerged in a flow-through container coupled with a water bath (Lauda Ecoline RE 108) that kept experimental temperature stable (0.1 C). Control runs were carried out. Before each experiment fish were allowed to acclimate to the chamber for 2 h. During the experimental runs fish were continuously observed. Feeding was discontinued 24 h before oxygen consumption measurements. All experiments were carried out in shaded day light (15L:09D). The routine metabolic rate (RMR) measured in the resting animal (Randall et al., 1997) was estimated and thermal sensitivity (Q10 value) (Randall et al., 1997) was calculated between 18 C and 24 C, 18 C and 28 C and between 24 C and 28 C, as. ðMR2 =MR1 Þ10=ðt2 t1 Þ in which MR2 and MR1 are the metabolic rates at temperature t1 and t2, respectively. Q10 is a measure of the temperature sensitivity of an enzymatic reaction rate or a physiological process due to an increase by 10 C (Randall et al., 1997). Analyses of variance (ANOVA) were performed to test for the effect of temperature on growth, condition and RMR, followed by Tukey post-hoc tests whenever the null hypothesis was rejected. A significance level of 0.05 was used in all test procedures. 3. Results Mortality was 10% at 18 C, two fish died, one after 22 days and the other after 30 days (Fig. 2). At 24 C no fish died and at 28 C three fish died, after 20 days, 33 days and 41 days respectively, representing 15% of the initial sample (Fig. 2). Temperature significantly affected growth of Dicentrarchus labrax (ANOVA, MS ¼ 0.09, F ¼ 22.17, P ¼ 0.00). Growth was 0.23 mm day1 at 18 C, it increased at to 0.30 mm day1 at 24 C, and it decreased to 0.11 mm day1 at 28 C, to (Fig. 3). Post-hoc tests
25
100 80 % Mortality
Temperature (ºC)
20 15 10 5 0
60 40 20
1
2
3
4
5
6
7
8
9
10
11
12
Month
0 1
5
9 13 17 21 25 29 33 37 41 45 49 53 57 60 Days
Fig. 1. Mean water temperatures (bars stand for standard deviations) in the nursery areas of the Tagus estuary (Portugal), data from 1978, 1979, 1980, 2001, 2002, 2005 and 2006 (Centro de Oceanografia Database).
Fig. 2. Percentage of mortality of D. labrax at 18 C, in black dots, at 24 C, in grey, and at 28 C, in black.
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0.4
18 C and 28 C (p < 0.05), and 24 C and 28 C (p < 0.05). Thermal sensitivity was high for the temperature interval between 24 C and 28 C, reaching a value >3. However, it was low for the other temperature intervals (Fig. 4).
0.3
4. Discussion
0.2
The low mortality and peak growth and condition values registered at 24 C indicate that the average summer temperatures registered in estuarine nursery areas are more beneficial for the species 0-group juveniles than coastal average summer temperatures (18 C). The estuarine water temperature attained during heat waves (28 C) resulted in higher mortality, arrested growth, lower condition and a steep increase in metabolism, indicating that this species is probably under some degree of thermal stress at 28 C and that more frequent and prolonged heat waves will not be favourable for its 0-group juveniles. The fact that the fish used here were from a fish farm may be a limitation, in that they may be adapted to an artificial environment where the selective pressures are different than those found in the field. However, working with fish from a fish farm allowed us to work with individuals with a known and acclimated thermal history. If we had used wild animals we would not know how much time they and previous generations had spent in coastal and estuarine nurseries and their exposure to different thermal conditions, which might have interfered with the experiment. Growth rates estimated in the present study were lower than field estimates by Cabral and Costa (2001) and Vinagre et al. (2009), 0.65 mm day1 and 0.56 mm day1, based on monthly size distributions and otolith microstructure, respectively. However, these previous estimations involve a considerable degree of uncertainty due to the techniques employed. Condition estimates were very similar to the average condition determined for the species 0-group juveniles in Portuguese estuaries, also based on the Fulton’s K, which was 0.88 (Vasconcelos et al., 2009). It should be noted that, although, a decrease in growth rate and an increase in metabolism was registered at 28 C, the condition of those fish was very similar to that observed at the other experimental temperatures and registered in wild fish (Vasconcelos et al., 2009). This suggests that the degree of thermal stress endured by these fish is not severe. Although Dicentrarchus labrax is a highly valued species, there are no reported similar experimental studies on 0-group juveniles, thus preventing us from making comparisons and testing the soundness of our experimental approach. There is, however, research on adult metabolism (mean weight 629 g) which can
Growth rate (mm.day -1)
0.5
0.1 0 15
20
25
30
T(ºC)
b
1.10
Fulton's K
1.00 0.90 0.80 0.70 0.60 0.50 15
20
25
30
T (ºC)
RMR (µmol O 2.g-1.h -1)
C
25 20 15 10 5 0 15
20
25
30
T (ºC) Fig. 3. Growth rates (a), condition (b) and standard metabolic rate (mmol O2 g1 h1) (c) of D. labrax at 18 C, 24 C and 28 C.
showed that growth was significantly different between 18 C and 28 C (p < 0.05) and 24 C and 28 C (p < 0.05). The condition of Dicentrarchus labrax was also significantly affected by temperature (ANOVA, MS ¼ 0.00, F ¼ 6.14, P ¼ 0.04). Fulton’s K was 0.99 at 18 C, 1.00 at 24 C, and 0.89 at 28 C (Fig. 3). Post-hoc tests showed that condition was significantly different between 18 C and 28 C, and 24 C and 28 C (p < 0.05). Temperature significantly affected the metabolism of this species. RMR was 11.01 mmol O2 g1 h1 at 18 C, 11.53 mmol O2 g1 h1 at 24 C and it increased steeply at 28 C to 19.10 mmol O2 g1 h1 (Fig. 3, ANOVA, MS ¼ 61.52, F ¼ 13.88, P ¼ 0.00). Post-hoc tests showed that metabolism was significantly different between
Thermal sensitivity (Q10)
a
135
4 3 2 1 0 18-24
18-28
24-28
Temperature interval (ºC) Fig. 4. Thermal sensitivity of D. labrax estimated between 18 C and 24 C, 18 C, and 28 C, 24 C and 28 C.
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indicate the thermal optimum of this species (Claireaux and Lagardère, 1999). Our results agree with Claireaux and Lagardère (1999), who observed that between 20 C and 25 C the metabolism of Dicentrarchus labrax became less susceptible to temperature fluctuations, concluding that this thermal interval encompasses the thermal preferendum of this species, permiting complete thermal compensation in metabolism (Precht et al., 1955). These authors also observed that as temperature reached 25 C only small changes in fish metabolic capacity were observed which is indicative of homeostasis. The low thermal sensitivity values estimated by Claireaux and Lagardère (1999) in the intervals of 15 Ce20 C and 20 Ce25 C, 1.88 and 1.08, respectively, are similar to the values estimated for 0-group juveniles between 18 C and 24 C, in the present work. However, these authors did not test temperatures above 25 C and thus did not report on thermal stress in the upper thermal range of this species. Vinagre et al. (2012) using the same experimental temperatures as used here, concluded that at 24 C oxidative stress was at its lowest, indicating that this temperature is within the D. labrax thermal optimum. Person-Le Ruyet et al. (2004) tested the effect of temperature on growth and metabolism of 20-month-old (82 g) Dicentrarchus labrax on an interval from 13 to 29 C. Similarly, to the present work, these authors observed an arrest in growth at 29 C and concluded that 26 C is the temperature for maximal growth for this age-group. It was also concluded that growth is markedly depressed in cooler waters, 65% lower at 13 C than at 26 C, and that this reduction in growth rate results primarily from a decrease in food intake. An increase of 8% in metabolic rate from 25 C to 29 C was also reported and related to maintenance costs due to thermal stress. The metabolic rate steep increase at 28 C, observed in the present work, revealed that Dicentrarchus labrax metabolism accelerates at this temperature, which is indicative of a decline in physiological efficiency. Thermal sensitivity was also higher between 24 C and 28 C than at the other thermal intervals, reaching values >3. Thermal sensitivity values between 2 and 3 are considered usual, yet higher values have been seen in fishes exposed to temperatures outside their normal temperature range (Johnston et al., 1991), which confirms that D. labrax southern European populations are not adapted to spend prolonged periods at this high temperature. Madeira et al. (2012) determined that the critical thermal maximum of D. labrax juveniles is 33.3 C. Studies with other marine fish species indicate that the borders of the thermal tolerance window are characterized by the onset of internal systemic hypoxia despite fully oxygenated waters, resulting in anaerobic metabolism that cannot be sustained for long periods (Pörtner, 2002). Currently, heat waves have a duration of 1e2 weeks, and this species can certainly cope with that, yet a longterm experiment such as this reveals that the temperatures reached during heat waves are not favourable for this species over longer periods. This is important from a climate change perspective, since an increase in duration and frequency of such elevated temperatures is to be expected in the near future (IPCC, 2001). The ecological consequences of climate change will, however, depend on the rate of adaptation of species to their changing environment. It is likely that this species has the ability to adapt to higher temperatures, since it also occurs in North Africa. Gene flow from lower latitude populations may be crucial for the adaptation of southern European populations to increased temperatures, with genotypes that are tolerant to higher temperatures gradually becoming prevalent in European populations due to natural selection (Helmuth et al., 2005; Visser, 2008). Knowledge of the relative value of each habitat may be crucial for prioritizing management and/or conservation actions that affect
fish nurseries for this and other species (Johnston et al., 2002; Vinagre et al., 2006, 2008). Reliable information based on field and experimental studies will allow funding institutions to better target their conservation efforts and make better regulatory decisions for fisheries management, habitat restoration and climate change impacts mitigation. However, predicting the impact of climate change on a particular species is a complex task and requires input from several subjects including ecology, eco-physiology, molecular ecology, genetics and evolution. It is a multi-disciplinary endeavour and deals with a high level of uncertainty given the many interacting variables. We consider that studies such has the one presented here, are necessary first-steps unravelling the complexity behind some of the climate change effects that may be just around the corner.
Acknowledgements Authors would like to thank everyone involved in the maintenance of the experimental tanks. This study had the support of the Portuguese Fundação para a Ciência e a Tecnologia (FCT) through the grant SFRH/BPD/34934/2007 awarded to C. Vinagre.
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