Galaxea, Journal of Coral Reef Studies 14: 97-103（2012）

Original paper

Temperature-growth performance curves for a coral reef fish, Acanthochromis polyacanthus

Salvador ZARCO-PERELLÓ*, Morgan PRATCHETT, and Vetea LIAO

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia

* Corresponding author: S. Zarco-Perelló E-mail: [email protected]

Communicated by Saki Harii (Ecology Editor)

Abstract This paper presents the first temperature-growth performance curves for a coral reef fish. Thermal tolerance Introduction and growth for the juvenile spiny damselfish Acantho­ chromis polyacanthus were measured at a range of tem­ Seawater temperature is highly variable and has an peratures from 15℃ to 38℃. A. polyacanthus juveniles important influence on the biology of marine organisms showed a critical thermal minimum at 15.5℃±0.1 and a (Wood and McDonald 1997). Extreme variations in critical thermal maximum at 38℃±0.12. Maximal growth temperature (up to 10℃) are regularly experienced, af­ (based on changes in length) occurred at 28-31℃, whereas fecting seasonal patterns of reproduction and growth weight gain was maximised at 28℃, which cor­responds (Yasue and Takasuka 2009); juvenile fishes of many closely with the annual mean temperature cur­rently ex­ species exhibit maximal growth during summer (Conover perienced by these fishes in their natural en­vironment. At 1992) and some species only reproduce during narrow temperatures ＞31℃ the growth rate de­creas­ed mark­edly time intervals when temperatures are favourable (Hilder in length and weight up to 34℃, where fishes had neg­ and Pankhurst 2003). Seasonality in reproduction will ligible growth and died within 8-15 days. Sustained in­ determine the temperatures and the growth rate experi­ creases in ambient temperature (due to climate change) enced by young fishes (Cargnelli and Gross 1996). In are expected to have significant adverse effects on these turn, growth rate during the early life-stage has im­portant fishes. However, any effects of increasing temperature consequences in survivorship and population dy­namics may also be offset by changing the timing of reproduction; (Campana 1996). In many cases larger larvae and juvenile by breeding in early spring or late summer, these fishes fish have greater chance to evade predation (Sogard 1997) may still be able to exploit narrow windows of thermal and survive lower temperatures in winter (Hurst 2007). optima, whereas fishes breeding in the height of summer The marked influence of temperature on the performance will expose offspring to potentially lethal tem­pera­tures at of fishes has long been known, but now has increased critical stages during their development. importance and is attracting considerable new research attention due to expected changes in local tem­perature Keywords Global warming, Thermal tolerance, Behav­ regimes as a consequence of climate change (Pankhurst iour, Growth, Damselfish and Munday 2011). Seasonal mean and ex­treme tempera­ tures are expected to keep increasing in the future (Sterl et 98 Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus al. 2008; Alexander and Arblaster 2009). This will make acanthus presents a main breeding season from October winter temperatures less harmful but extreme summer to February (Robertson 1973). Eggs are laid in caves and temperatures may be detrimental and may lead to marked after hatching juveniles remain within the parental care of changes in species’ survival, reproductive potential and/ adults for about 1.5 months (Kavanagh 2000). Their growth or spatial distributions (Clusella-Trullas et al. 2011). rate has shown a positive correlation with the number of The construction of temperature-performance curves juveniles in the brood (Thresher 1983) and given their is fundamental to assess the likely effects of climate lack of pelagic larval stage, the populations are genetically change on ectotherms (e.g., fishes and lizards) (Huey and subdivided (Bay et al. 2006) and may be adapted to Stevenson 1979; Angert et al. 2011). Most temperature- perform optimally at local environmental temperatures. performance curves reveal a hump-shaped relationship, whereby performance (e.g., growth) is maximised at some intermediate level of temperature and declines as tem­ Materials and methods perature is increased or decreased (Angilletta 2006). To understand the capacity and vulnerability of these organ­ Thermal tolerance isms to future changes in temperature regimes, it is im­ To test the thermal tolerance we calculated the critical portant to establish the critical minimum and maximum thermal minimum (Ctmin) and maximum (Ctmax) temperature that organisms can withstand, the thermal (Beitinger et al. 2000). We used juvenile fishes from the optima, and rates of change in performance at temperatures fish rearing facilities at James Cook University. All higher and lower than the thermal optima. Temperature- juvenile fishes were offspring of four breeding pairs that Growth performance curves have been calculated exten­ belonged to the second generation of A. polyacanthus sively for temperate fishes with high economic importance, reared in captivity. The breeding pairs were maintained in such as salmonids (Koskela et al. 1997; Jonsson et al. 70 L tanks with constant flow of aerated seawater at 28℃ 2001; Larsson and Berglund 2006; Forseth et al. 2009; (±1℃), similar to their original habitat on Orpheus Island Elliott and Elliott 2010), but there are relatively few in the central GBR. Twenty-four juveniles were selected studies that have attempted to construct temperature- randomly between 2 and 3 weeks after hatching and were performance curves for coral reef fishes (Munday et al. transported to individual 7.5 L tanks. Juveniles were 2008a) and none of these have comprised the complete main­tained at 28℃ for seven days and were fed twice a thermal window for growth, lacking either the right (Ellis day with dry pellets (INVE NRD 2/4 Aquaculture Nutri­ et al. 1997), or the left tail of the curve (Munday et al. tion). After that, twelve juveniles were exposed to a grad­ 2008b), precluding the ability to make more accurate ual increase in temperature (0.26℃/ min±0.07) and projections about the survivorship of coral reef fishes. twelve to a decrease in temperature (0.23℃/ min±0.10), The purpose of this study was to construct a com­ to the point at which fishes lost equilibrium or experienced prehensive temperature-performance curve for a coral muscular spasms (end-point) (Mora and Ospina 2001). reef fish. Our study first identified the overall thermal Temperature was measured continuously during this pro­ tolerance and then tested for changes in the growth of cess using calibrated digital thermometers. The Ctmin and juvenile spiny damselfish, Acanthochromis polyacanthus Ctmax were determined as the arithmetic mean of the Bleeker 1855, at a range of temperatures from current temperatures at which fishes reached the end-point. The mean winter (22℃) to future extreme summer tempera­ average weight of the fishes was 625±36 mg (min＝414 tures (34℃). A. polyacanthus is a common damselfish mg; max＝1185 mg; n＝24) and their average body length (Pomacentridae) of the Indo-pacific coral reefs. Dam­ was 1.3 cm±0.05 cm (min＝1 cm; max＝1.8 cm; n＝24). selfishes are important elements in the reef community given their high abundance and territorial behaviour that Growth Performance impact on coral, fishes and algae (Hoey and Bellwood Temperature performance curves (based on both change 2010). In the southern Great Barrier Reef (GBR) A. poly­ in length and weight) were constructed for A. polyacanthus Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus 99 based on the results from two independent experiments. Growth was calculated as the daily increment of standard length (Ls) and wet weight (Ww) of juvenile A. polyacanthus maintained for eight weeks at a determined temperature. The first experiment used juvenile fishes obtained from the fish rearing facilities at James Cook University (JCU), as in the thermal tolerance experiment. Juvenile fishes were randomly selected and distributed to five thermal treatments three weeks after hatching, each treatment had three replicates consisting in tanks of 35 L, and each tank contained two fishes. Temperature was set at 28℃ for two days and subsequently was reduced or increased by 2℃ per day to the respective temperature of each treatment: 22℃ (21.90±0.20℃), 25℃ (24.90±0.17℃), 28℃ (28.00 ±0.20℃), 31℃ (31.10±0.18℃) and 34℃ (34.20±0.19 ℃) (Fig. 1). The second experiment used juvenile fishes obtained from the Reef HQ aquarium in Townsville, Aus­ tralia where they are held in similar thermal conditions as their original habitat in the central GBR (28-29℃). These juvenile fishes came from three breeding pairs that be­ Fig. 1 Growth performance of A. polyacanthus juveniles longed to the 10th generation of A. polyacanthus reared in at different temperatures. Increments in standard length are captivity. The juvenile fish were transported from the presented in the lower chart and increments in wet weight in ReefHQ aquarium to JCU three to four weeks after hatch­ the upper chart. The letters above the bars (mean±SE) in­ ing and were randomly distributed into five temperature dicate statistically similar means (Tukey’s post hoc, α＝ 0.05) treatments: 25℃ (24.90±0.17℃), 28℃ (28.00±0.20℃), 31℃ (31.04±0.17℃), 32.5℃ (32.40±0.16℃) and 34℃ (34.20±0.10℃), each with three replicates (tanks of 35 and salinity was maintained at 35‰. Fishes were starved

L) and each replicate containing­ five juveniles. Tempera­ 24 hrs before the measurements of the Ls and Ww done at ture was set at 28℃ for two days and subsequently was the beginning and at the end of the experiments. The reduced or increased 2℃ per day to the respective tem­ length of the fishes was measured with a vernier caliper perature of each treatment. There was no variation in the while being held with a hand-net. The weight was intial size of fishes among all treatments or experiments measured with an electronic balance by putting the fish in

(one-way ANOVA; Experiment 1: Ls, F4, 20＝0.766, p＝ a beaker filled with water from the tank of the fish. The

0.560, Ww, F4,19＝0.489, p＝0.744; Experiment 2: Ls, F4,70, procedures were done with appropriate care in order not p＝0.071, Ww, F4, 70, p＝0.069). to disturb severely or cause any damage to the fishes. The

During the course of both experiments, temperature Ls and Ww of fishes that died along the experiment were was monitored daily every hour from 7 am to 12 am using measured and included in the analysis only when the fish calibrated digital thermometers; fish were fed twice a day didn’t present physical damage. (morning and afternoon) to satiation with dry pellets Differences in growth performance among thermal (INVE NRD 2/4 Aquaculture Nutrition). Fish behaviour treatments­ were tested twice with one-way ANOVA fol­ was monitored daily before, during and after feeding lowed by Tukey’s post hoc comparisons. Analyses were throughout the experiments. The water in the tanks was conducted with and without data from extreme tempera­ constantly circulating to maintain good levels of oxy­gen­ ture treatments­ (22℃ and 34℃) to test whether these ation; photoperiod was set up as 12 hrs light: 12 hrs dark treatments­ had a disproportionate influence on statistical 100 Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus

Fig. 2 Acanthochromis polyacanthus juveniles performing aquatic surface respiration in the thermal treatment of 34°C.

pat­terns (Fig. 1). The number of individuals from each varied significantly with temperature (Ls: F5, 39＝27.28, treatment included in the statistical analysis were as p＝0.001; Ww: F5, 26＝17.38, p＝0.001), with growth rates follows: 22℃: 6 individuals (only first experiment), 25℃: showing the expected humped shaped relationship over 20 individuals, 28℃: 20 individuals, 31℃: 20 individuals, the range of temperatures tested. Fishes at 22℃ and 34℃ 32.5℃: 15 individuals (only second experiment) and exhibited significantly slower growth rates compared to 34℃: 19 indi­viduals for length and 16 individuals for the other intermediate (25-32.5℃) temperature treatments weight (some individuals were discarded from the analysis (Fig. 1). Growth rates were fairly similar from 25℃ to because they presented physical damage) 32.5℃, but overall maximum growth (both for Ls and Ww) was recorded at 28-31℃. Fishes at 32.5℃ presented a

growth rate (Ww) significantly lower than fishes at 28℃ by Results anal­ysing the data without the extreme temperature treatments (p＝0.04) (Fig. 1). Ctmin and Ctmax were very consistent among indi­ Aside from strong physiological responses, temperature viduals, indicating fairly clear temperature thresholds. A. also had a marked effect on the behaviour of juvenile A. polyacanthus juveniles presented a Ctmin at 15.5℃±0.1 polyacanthus. Food intake (based on visual assessment of and a Ctmax at 38℃±0.12. However, prolonged exposure the amount of material remaining) increased with rising to temperatures of 34℃ and 22℃ (during the growth ex­ temperature, and was highest at 31℃ and 32.5℃. Never­ periments) still caused high levels of mortality in these theless, at extreme temperatures (22℃ and 34℃) fishes fishes. During growth experiments, all fishes subject to reduced greatly their food intake in comparison with the 34℃ died within 8-15 days, while half of the fishes ex­ other thermal treatments. Fishes in the extreme tempera­ posed to 22℃ died within 13 days. No mortality was tures also displayed differences with the other treatments recorded in any other temperature treatments. regarding boldness. Fishes at 34℃ were trying to hide Despite sourcing fishes from distinct populations, there most of the time by staying closer to the walls and corners was no difference in growth rates recorded between ex­ of the aquarium and these were observed per­forming periments (two-way ANOVA; Length: F3, 39＝0.99, p＝ surface respiration during the day (Fig. 2), while at night

0.407, weight: F2, 23＝2, p＝0.168), thus, data was pooled they were motionless at the bottom. Fishes at 22℃ were for all subsequent analyses. The growth rate of fishes less active and displayed slower swimming reaction times Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus 101 than fishes at higher temperatures, as suggested by careful because the extreme temperature may have severely observations of the tanks. Fishes from 25℃ to 32.5℃ did reduced their aerobic scope and thus these results may be not present clear differences in boldness. evidence supporting the OCLT. The annual mean temperature of the GBR is expected to increase between 1 and 3℃ by the end of the century Discussion (Lough 2007), taking maximum summertime temperatures up to 34℃. Given their tolerance of different temperatures The optimal temperature for maximising growth per­ (which is probably even higher in adult fishes), global formance of juvenile A. polyacanthus (28-31℃) corre­ warming does not pose a direct cause of mortality to A. sponds well with current summertime temperatures in the polyacanthus but will be detrimental for the growth of central section of the Great Barrier Reef, where parental juvenile fishes. The future reproductive success of A. fishes were originally caught. Ambient temperatures at polyacanthus in the central Great Barrier Reef will largely Orpheus Island, central Great Barrier Reef, range from depend upon their capacity for acclimation and/or ad­ 〜21℃ to 〜31℃, with an annual mean temperature of aptation. One potential adaptation is to change the timing 28.5℃ (Munday et al. 2008b). This suggests that these of reproduction to take advantage of cooler temperatures fishes are well adapted to local temperature regimes. before or after summer. A. polyacanthus in the southern Similarly, reproductive performance of A. polyacanthus GBR have been reported to breed from October to from the same source populations has been shown to be February (Robertson 1973). Low temperatures during the greatest at 28.5℃ (Donelson et al. 2010). However, at winter months tend to limit breeding by suppressing the temperatures ＞31℃ there was a significant decline in the production of gonadal steroids and causing high mortality growth of A. polyacanthus, which is expected to translate of eggs (Hilder and Pankhurst 2003). However, as tem­ into lower survivorship, following the bigger-is-better peratures continue to increase, it is possible that fishes hypothesis (Sogard 1997). This suggests that unless these may begin spawning much earlier in the year (Shoji et al. fishes can adapt to changing environmental conditions, 2011), especially if reproduction is initated when tem­ projected increases in ocean temperatures (Lough 2007) perature exceeds a specific level (Hilder and Pankhurst will have significant adverse effects. 2003). If so, juvenile fishes may experience several months Marked declines in growth rates of fishes at temperatures of normal growth before being subject to extreme summer above their normal summer maxima is generally attributed temperatures. to increased energy requirements for maintenance com­ Establishing temperature-performance curves is the bined with declines in energy attainment due to failures in first step towards assessing the vulnerability of marine the circulatory and respiratory systems (hypothesis of fishes to projected temperature increases, but further oxygen and capacity limited tolerance: OCLT) (Pörtner significant research is required to establish the application and Peck 2010). It has been shown that A. polyacanthus of current experimental findings to field situations. Im­ juveniles from Lizard Island reduce their aerobic scope portantly, the growth rates of our study were obtained when exposed to temperatures above 29℃ (Nilsson et al. under conditions of unlimited food; however this is not 2009; Gardiner et al. 2010), correlating well with our always the case in nature and this may impact on the results in growth and other studies of reproduction growth rates of fishes (Booth and Alquezar 2002). Limited (Donelson et al. 2010). In our study the performance supply of food may have a big impact the growth rates and became critical at 34℃, where fishes started to perform survival of juvenile fish A. polyacanthus at higher tem­ surface respiration, had markedly reduced food intake peratures, where there is an increased demand (Munday et and ultimately died after prolonged exposure. Surface al. 2008b). It is also possible that sensitivity of these fishes respiration is a behaviour that fishes adopt in order to cope to temperature occurs at other stages in their life-history with hypoxic stress (Gee and Gee 1991). Juvenile fishes (e.g. at fertilization, or during adulthood), so ongoing might have been attempting to increase their oxygenation studies are required to firmly establish the vulnerability of 102 Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus

A. polyacanthus, and many other marine fishes, to global Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic climate change. predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am Nat 177: 738-751 Acknowledgements Conover D (1992) Seasonality and the scheduling of life history at different latitudes. J Fish Biol 41: 161-178 Donelson J, Munday P, McCormick M, Pankhurst N, Pankhurst Thanks to the National Council of Science and Tech­ P (2010) Effects of elevated water temperature and food nology of Mexico (CONACYT) for sponsoring the post­ availability on the reproductive performance of a coral reef graduate studies of Salvador Zarco-Perello at James Cook fish. Mar Ecol Prog Ser 401: 233-243 University. Thanks to the Reef HQ Aquarium for the Elliott JM, Elliott JA (2010) Temperature requirements of At­ supply of A. polyacanthus juvenile fishes and thanks to lantic salmon Salmo salar, brown trout Salmo trutta and Jennifer Donelson and Carlos Alvarez-Roa for their tech­ Arctic charr Salvelinus alpinus: predicting the effects of nical help with the experiments. The present research pro­ climate change. J Fish Biol 77: 1793-1817 ject was approved by the ethics committee of James Cook Ellis SC, Watanabe WO, Ellis EP (1997) Temperature effects on University (A-1351). feed utilization and growth of postsettlement stage Nassau grouper. Trans Am Fish Soc 126: 309-315 Forseth T, Larsson S, Jensen AJ, Jonsson B, Näslund I, Berglund References I (2009) Thermal growth performance of juvenile brown trout Salmo trutta: no support for thermal adaptation hy­ potheses. J Fish Biol 74: 133-149 Alexander LV, Arblaster JM (2009) Assessing trends in observed Gardiner NM, Munday PL, Nilsson GE (2010) Counter-gradient and modelled climate extremes over Australia in relation to variation in respiratory performance of coral reef fishes at future projections. Int J Climatol 29: 417-435 elevated temperatures. Plos One 5: e13299 Angilletta MJ (2006) Estimating and comparing thermal per­ Gee JH, Gee PA (1991) Reactions of gobioid fishes to hypoxia: formance­ curves. J Therm Biol 31: 541-545 buoyancy control and aquatic surface respiration. Copeia Angert AL, Sheth SN, Paul JR (2011) Incorporating population- 1: 17-28 level variation in thermal performance into predictions of Hilder M, Pankhurst N (2003) Evidence that temperature change geographic range shifts. Integ Comp Biol 51: 733-750 cues reproductive development in the spiny damselfish, Bay L, Crozier R, Caley M (2006) The relationship between Acanthochromis polyacanthus. Environ Biol Fish 66: 187- population genetic structure and pelagic larval duration in 196 coral reef fishes on the Great Barrier Reef. Mar Biol 149: Hoey AS, Bellwood DR (2010) Damselfish territories as a refuge 1247-1256 for macroalgae on coral reefs. Coral Reefs 29: 107-118 Beitinger TL, Bennett WA, McCauley RW (2000) Temperature Huey RB, Stevenson R (1979) Integrating thermal physiology tolerance of North American freshwater fishes exposed to and ecology of ectotherms: a discussion of approaches. dynamic changes in temperature. Environ Biol Fish 58: Am Zool 19: 357 237-275 Hurst T (2007) Causes and consequences of winter mortality in Booth D, Alquezar R (2002) Food supplementation increases fishes. J Fish Biol 71: 315-345 larval growth, condition and survival of Acanthochromis Jonsson B, Forseth T, Jensen AJ, Næsje TF (2001) Thermal polyacanthus. J Fish Biol 60: 1126-1133 Performance of Juvenile Atlantic Salmon, Salmo salar L. Campana SE (1996) Year-class strength and growth rate in Funct Ecol 15: 701-711 young Atlantic cod Gadus morhua. Mar Ecol Prog Ser Kavanagh KD (2000) Larval brooding in the marine damselfish 135: 21-26 Acanthochromis polyacanthus (Pomacentridae) is corre­ Cargnelli LM, Gross MR (1996) The temporal dimension in fish lated with highly divergent morphology, ontogeny and recruitment: birth date, body size, and size-dependent sur­ life-history traits. Bull Mar Sci 66: 321-337 vival in a sunfish (bluegill: Lepomis macrochirus). Can J Koskela J, Pirhonen J, Jobling M (1997) Feed intake, growth Fish Aquat Sci 53: 360-367 rate and body composition of juvenile Baltic salmon ex­ Zarco-Perelló et al.: Temperature-growth performance curves for a coral reef fish,Acanthochromis polyacanthus 103

posed to different constant temperatures. Aquacult Int 5: acanthus. Z Tierpsychol 32: 319-324 351-360 Shoji J, Toshito S, Mizuno K, Kamimura Y, Hori M, Hirakawa K Larsson S, Berglund I (2006) Thermal performance of juvenile (2011) Possible effects of global warming on fish recruit­ Atlantic salmon (Salmo salar L.) of Baltic Sea origin. J ment: shifts in spawning season and latitudinal distribution Therm Biol 31: 243-246 can alter growth of fish early life stages through changes in Lough J (2007) Climate and climate change on the Great Barrier daylength. ICES J Mar Sci 68: 1165-1169 Reef. In: Johnson JE, Marshall PA (eds) Climate Change Sterl A, Severijns C, Dijkstra H, Hazeleger W, van Oldenborgh and the Great Barrier Reef: a vulnerability assesment. GJ, van den Broeke M, Burgers G, van den Hurk B, van Great Barrier Reef Marine Park Authority, Townsville, pp Leeuwen PJ, van Velthoven P (2008) When can we expect 15-50 extremely high surface temperatures? Geophys Res Lett. Nilsson GE, Crawley N, Lunde IG, Munday PL (2009) Elevated 35: L14703, doi:10.1029/2008GL034071 temperature reduces the respiratory scope of coral reef Sogard SM (1997) Size-selective mortality in the juvenile stage fishes. Glob Change Biol 15: 1405-1412 of teleost fishes: a review. Bull Mar Sci 60: 1129-1157 Mora C, Ospina AF (2001) Tolerance to high temperatures and Thresher R (1983) Habitat effects on reproductive success in the potential impact of sea warming on reef fishes of Gorgona coral reef fish, Acanthochromis polyacanthus (Pomacen­ island (Tropical eastern Pacific). Mar Biol 139: 765-769 tridae). Ecology 64: 1184-1199 Munday P, Jones G, Pratchett M, Williams A (2008a) Climate Wood CM, McDonald DG (1997) Global warming: implications change and the future for coral reef fishes. Fish Fisheries 9: for freshwater and marine fish, Society for Experimental 261-285 Biology Seminar Series 61. Cambridge University Press, Munday P, Kingsford M, O’Callaghan M, Donelson J (2008b) Cambridge Elevated temperature restricts growth potential of the coral Yasue N, Takasuka A (2009) Seasonal variability in growth of reef fish Acanthochromis polyacanthus. Coral Reefs 27: larval Japanese anchovy Engraulis japonicus driven by 927-931 fluctuations in sea temperature in the Kii Channel, Japan. J Pankhurst NW, Munday PL (2011) Effects of climate change on Fish Biol 74: 2250-2268 fish reproduction and early life history stages. Mar Freshw Res 62: 1015-1026 Received: 7 May 2012 Pörtner H, Peck M (2010) Climate change effects on fishes and Accepted: 7 November 2012 fisheries: towards a cause and effect understanding. J Fish Biol 77: 1745-1779 Ⓒ Japanese Coral Reef Society Robertson D (1973) Field observations on the reproductive behaviour of a pomacentrid fish, Acanthochromis poly­