The thermal response of the brown shrimp Crangon crangon growth from the southern edge of geographic distribution
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Interdisciplinary Center for Marine and Environmental Research, Abel Salazar Institute of Biomedical Sciences, University of Porto, Portugal
INTRODUCTION
The brown shrimp Crangon crangon is both ecologically and commercially important (Campos & van der Veer 2008): it is highly abundant in European estuaries and represents over 31t landed in the North Sea fisheries (ICES 2016). The species wide geographic range extends from Morocco to the White Sea, and reflects its high capability of coping with a large range of environmental conditions, namely of temperature.
The growth of the brown shrimp has been extensively studied both under natural (e.g. Amara & Paul 2003) and controlled conditions, in relation to several factors including food availability (Hufnagl & Temming 2011a), light intensity (Dalley 1980), temperature (Campos et al. 2009a), and using modelling tools (Campos et al. 2009b; Hufnagl & Temming 2011b). Though the growth rate increases with temperature in an expected Gaussian curve, changes in moult time interval are known to be more consistent than the size increment ones in the species growth thermal response (Campos et al. 2009a). Despite the innumerous studies on the growth of the brown shrimp, yet, no information exists on the optimum temperature for growth, and on its sensitivity and tolerance range.
Here we investigate the temperature dependence of the brown shrimp growth for a population near the southern edge of distribution and discuss results in respect to a global change scenario.
MATERIAL AND METHODS
The experiments were run indoors. Ten aquaria were prepared to independently test 10 temperature levels ranging from 5 to 27.5ºC. Shrimps were collected at Minho estuary with a 1m beam trawl 10 days prior the experiment. After one week of acclimation at the prevailing temperature level, 27 shrimps were randomly chosen per level and measured (total length, TL, mm). Mean TL per aquarium did not differ (ANOVA: F = 0.173, p = 0.99) ranging 17-48mm, mean=26.96±4.00mm. During the trials, each shrimp was kept individually placed, separated from the others by perforated plastic cages within the aquarium. Water temperature, salinity (Table 1), light (12:12), food (mussel in excess), moult and death events were controlled daily. All trials took 61 days. In case of death, the shrimp was replaced by another one from the original pool. The survival was estimated as the proportion of live/dead shrimps over the total number of individuals at each temperature level, and used to estimate the lethal temperature for 50% of population (the temperature at which 50% mortality occurs, LT50).
Whenever a shrimp moulted, its TL was measured the following day to determine the moult increment (MI) and the time elapsed was registered (intermoult period, IP).
The growth rate per moult (GR) was calculated by
GR = MI/IP for each two consecutive moult events.
A thermal performance curve (TPC) for GR was used to access the relationship between temperature and physiological performance. The GR data for the range of temperatures between 5 and 27.5 ˚C was fitted to a Gaussian function (Angilletta et al. 2006) which gave us the thermal optimum (the temperature at which performance is maximized) and the performance breadth – the range of temperatures over which physiological performance is at least 69% of the peak (Van der Veer et al. 2006).
The effect of temperature on GR was evaluated by determining the activation energy following Brown et al. (2004) under the Metabolic Theory of Ecology (MTE). The relationship corresponds to a simple linear regression, with data represented through an Arrhenius plot with ln(IM^(-3/4)) against 1/kT:
ln(IM^(-3/4)) = -Ea/kT + ln(i0)
Where I is individual GR (mm.day^(-1)), M is the shrimp wet weight (g), T is the temperature (Kelvin) and k is the Boltzman constant. The Ea is the activation energy (eV) obtained as the (minus signed) slope coefficient of the linear regression, and i0 is a normalization constant independent of body size and temperature, which is given by the intercept coefficient. The range of selected temperatures corresponds to the near-exponential increasing phase of the biological rate as described by Sibly et al. (2012).
The wet weight (WW) was determined with the equation:
Y = 0.019 WW^(1/3) , r^2 = 0.92, n = 5416
obtained through linear regression with field data on individual TL and WW.
Both lethal temperature for 50% of the population and the thermal performance curve for growth rate were performed with RStudio version 1.1.383.
The relationship between survival and temperature was evaluated through a logistic regression model, using the glm (General Linear Model) function. The TPC were drown through nls (Nonlinear Least Squares) function.
RESULTS
A total of 346 shrimps were used in the trials but only 73 gave results useful for the determination of the activation energy for growth. Within the chosen range of temperatures (5 to 20˚C), moults that did not result in growth or for which the growth rate was negative were not considered. Additionally, at the two lower temperatures, moult events were insufficient to determine a growth rate, having only one record at 5 and 7.5˚C.
Survival
Survival was higher at the lower temperature levels (Table 1). The logistic regression suggests a strong association between mortality and temperature, with p-value <0.001 for the two months experiments. The estimated LT50 occurred at 26.62˚C (Figure 1).
Growth
The number of moult events, the IP and the MI varied significantly between temperature levels (ANOVA: F=5.481; F=4.719; F=5.778, p<0.0001, respectively). Up to four moult events were observed from 15ºC and over, except at 22.5ºC, while at the two lower temperature levels shrimps moulted only twice. The IP tended to decrease with increasing temperature, stabilizing from 17.5˚C on. In contrast, the MI increased in the lower temperature levels up to aprox. 17.5ºC, decreasing hereafter. Mean GR ranged from 0.05 mm.day^(-1) at 5ºC to 0.23 mm.day^(-1) at 20ºC (Table 1). The TPC for the brown shrimp GR estimated a thermal optimum of 18.84˚C ± 0.88˚C and suggested a species that can tolerate a large amount of temperatures changes, with a performance breadth ranging between 11.83 and 25.85˚C, as depicted in Figure 2(A).
Activation energy
The activation energy obtained for brown shrimp GR within the selected temperature range was 0.51eV (p-value < 0.05) as shown in Figure 2(B).
DISCUSSION
The present study confirmed a general positive trend of the temperature impact on growth of the brown shrimp from Minho estuary, determined the optimum temperature for growth as near 19ºC, and found a large temperature breadth. The positive trend means that the metabolic costs due to increasing temperature are smaller than the increase in energy ingestion and allocation into growth. Food is known to affect the growth of shrimps: living prey favour the size increase, while frozen food, like the one provided in this study, is less beneficial (Hufnagl & Temming 2011a). The initial nutritional condition of the animals was not evaluated. In the North Sea, about one third of the population is food limited but food limitation is not known in the Minho Estuary (Hufnagl et al. 2010). Yet, obtained growth rate values were within the range of previous studies suggesting healthy nutritional condition.
The activation energy, which represents the sensitivity of a given process to changes in temperature, was within the expected range of 0.2-1.2 eV suggested by Gillooly et al. (2001) and close to the average referred by Brown et al (2004), as the typical activation energy observed for most biochemical metabolism reactions. Thus, 0.51 eV can be a sign of high temperature sensitivity and tolerance range confirming previous suggestions (Freitas et al. 2007), though impacts of temperature may have different trends. Countergradient growth compensation has been described in the brown shrimp, whereby northern populations from colder areas grow faster than southern populations (Campos et al. 2009a). Therefore, it is expected that in populations other than the one from Minho Estuary, the thermal optimum can differ, as well as the range of favouring temperatures.
In the North Atlantic, sea surface temperature has been increasing (IPCC 2014), affecting the metabolism of ectotherms (Angilletta 2009; Schulte 2015; Van Donk & De Wilde 1981), with consequences for several biological processes including growth. The population from Minho estuary is close to the southern edge of geographic distribution and hence expected to be close to the upper tolerance limit of temperature. Besides the temperature sensitivity, the growth trajectory in relation to temperature may condition future adaptation to water warming, as it also responds to the prevailing food conditions, which in turn also depend on temperature as well. Mismatch between growth season and periods of food abundance may constrain the population growth, and should be clarified in future assessments of climate change impacts on the species.
List of table and figures captions
Table 1. Experimental conditions of temperature (˚C), salinity (ppm), total number of shrimps, maximum number of moults per shrimp, mean (± standard deviation, sd) growth rate (mm.day^(-1)) and number of deaths.
Figure 1. LT50 curve for the Crangon crangon experiments along two months.
Figure 2. Crangon crangon temperature dependence. (A) Thermal performance curve for growth rate (mm.day^(-1)) fitted to a Gaussian function, showing the thermal optimum and the performance breadth. (B) Arrhenius plot obtained for growth rate (mm.day^(-1)) along with the activation energy (Ea, Ev).
Acknowledgements
The present study was supported by the Strategic Funding UID/Multi/04423/2019.
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Keywords:
temperature,
Climate Change,
Growth,
Moult increment,
Intermoult period
Conference:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.
Presentation Type:
Poster Presentation
Topic:
Global Change, Invasive Species and Conservation
Citation:
Costa
A,
Peperstraete
I,
Arenas
F and
Campos
J
(2019). The thermal response of the brown shrimp Crangon crangon growth from the southern edge of geographic distribution.
Front. Mar. Sci.
Conference Abstract:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) .
doi: 10.3389/conf.fmars.2019.08.00093
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Received:
13 May 2019;
Published Online:
27 Sep 2019.
*
Correspondence:
Mx. Ana Filipa Costa, Interdisciplinary Center for Marine and Environmental Research, Abel Salazar Institute of Biomedical Sciences, University of Porto, Matosinhos, Portugal, ana.costaciimar@ciimar.up.pt