Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology Volume 43, Issue 3 ISSN 1730-413X eISSN 1897- 3191
(0–0) 2014 Received: Accepted:
DOI: 10.2478/s13545-014-0136-9 Original research paper
Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841) from the southern Baltic Sea Joanna Hegele-Drywa *, Monika Normant Department of Experimental Ecology of Marine Organisms, Institute of Oceanography, University of Gdańsk, Al. M. Piłsudskiego 46, 81-378 Gdynia, Poland Key words: Rhithropanopeus harrisii, temperature, food consumption, ammonia excretion, metabolic rate, energy balance, production Abstract Rates of physiological processes and bioenergetics of the Harris mud crab Rhithropanopeus harrisii were determined during a 7-day experiment on adult males (mean wet weight 0.83 ± 0.16 g) exposed to temperatures of 15ºC and 20ºC (S = 7). The results show that the change in temperature by 5ºC caused detectable changes in locomotor activity, food consumption and faeces production and significant (p < 0.05) changes in metabolic rates. Food assimilation efficiency and the ammonia excretion rate did not change significantly (p > 0.05). The energy expended on metabolic processes was similar at both temperatures (15ºC and 20ºC) and amounted to 17.7 ± 6.4% and 16.7 ± 4.3% of the assimilated energy, respectively. Similar values were obtained for net production efficiency K2 (P/A) at 15ºC and 20ºC, i.e. 80.4 ± 22.4% and 82.9 ± 9.7%, respectively. The amount of energy available for production was 2-fold higher at a temperature of 20ºC than at 15ºC and amounted to 103.69 ± 25.61 and 206.40 ± 20.76 J d-1g-1 wet wt, respectively. The results show that from the bioenergetic point of view, higher experimental temperature is more “profitable” for adult R. harrisii specimens because it provides better conditions for the growth and reproduction. *
Corresponding author:
[email protected]
April 04, 2014 June 30, 2014
INTRODUCTION The Harris mud crab Rhithropanopeus harrisii (Gould, 1841) is one of the non-native brachyuran crab species, most widely distributed in the world (Roche & Torchin 2007). Over the past century, most likely due to anthropogenic reasons, R. harrisii has invaded over 20 countries, two oceans, ten seas, and ten fresh water inland reservoirs across four continents, which span over 45 degrees of latitude (Roche & Torchin 2007, Fowler et al. 2013). The most recent introductions include Japan (Iseda et al. 2007), Estonia (Kotta & Ojaveer 2012) and Finland (Fowler et al. 2013) as well as new localities in Lithuania (Bacevičius & Gasiūnaitė 2008) and Poland (Czerniejewski & Rybczyk 2008, Hegele-Drywa & Normant 2014). Due to the high plasticity and resistance to changing environmental factors, the abundance of R. harrisii will probably increase in many of these regions as it has been observed in the Gulf of Gdańsk (Hegele-Drywa & Normant 2014). Despite the fact that R. harrisii is a globally recognized non-native species which continually expands its range, little is known about the physiological functioning of this crab in the inhabited ecosystem. It also refers to specimens from native regions. Osmoregulation is a well studied physiological process in this species, both from native (Smith 1967, Diamond et al. 1989) and nonnative regions (Kinne & Rotthauwe 1952, Normant & Gibowicz 2008). In the literature, there is also some information on the metabolic rate of R. harrisii, however, studies are focused on the species’ responses to environmental stress caused by the herbicide alachlor (Diamond et al. 1989), lack of oxygen (Rychter 1997) or salinity changes (Normant & Gibowicz 2008). Food consumption, feces and ammonia excretion, as well as oxygen uptake are basic physiological processes which are species
Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl
220 | Joanna Hegele-Drywa, Monika Normant
specific and are linking an organism with its environment (Lucas 1993). Unfortunately, none of these processes has been studied to date in the Harris mud crab, with the exception of the metabolic rate. To this end, the aim of our study was to examine (for the first time) the rates of these processes in R. harrisii from the brackish Baltic waters. Since the range of the Harris mud crab occurrence is restricted to the temperate zone, the species is exposed to seasonal changes in the temperature, i.e. the parameter that significantly affects the rates of physiological processes in ectothermic organisms (Hartnoll 1982, Schmidt-Nielsen 1997). Even though eurytrophic organisms are highly tolerant to e.g. temperature, every species has a species-specific thermal optimum which can significantly differ between populations from different locations (Schröer et al. 2009). Moreover, morphological as well as metabolic traits can show indications of phenotypic plasticity caused by differences in metabolic rates among individuals from different populations (Schlichting & Pigliucci 1998, Pigliucci & Preston 2004). The highest abundance of R. harrisii in the Gulf of Gdańsk (the southern Baltic Sea) was recorded at a temperature of 15ºC (Hegele-Drywa & Normant 2014). In terms of thermal tolerance, both the temperature range and the optimal temperature are important for reproduction. It appears that a temperature of around 20°C represents minimum thermal requirements for reproduction, laying eggs and embryonic development of this species (Kujawa 1957, Turoboyski 1973, Christiansen & Costlow 1975, Gonçalves et al. 1995, Forward 2009). This fact might also be confirmed by seasonal migration of R. harrisii to shallower or deeper waters together with changes in the water temperature (Hegele-Drywa & Normant 2014). Based on the above statements, it was also aimed to test whether a small shift in water temperature might be significant for rates of physiological processes in R. harrisii. Additionally, these rates were converted to energy equivalents in order to determine the balanced energy budget and to quantify the scope for growth, which indicates the energy available for individual production, i.e. growth and reproduction (Winberg 1960, Maltby et al. 1990). This parameter is a good indicator of the energy status of an organizm – it has the highest values in most ‘profitable’ conditions (Hulathduwa et al. 2007, Normant et al. 2012). Determination of the relationship between the rates of physiological processes as well as the energy status and
environmental factors leads to a better understanding and explaining the distribution patterns of the studied species. Moreover, it may help to predict the colonization potential of R. harrisii in new environments, which according to international legislative measures and policies may help in the assessment and management of this non-native species (Ojaveer et al. 2014). MATERIALS AND METHODS Collection and maintenance of crabs Animals were collected from the Gulf of Gdańsk (the southern Baltic Sea, Poland) using a bottom dredge deployed from the research vessel Oceanograf 2. The carapace width of R. harrisii adult males (n=15) ranged from 10.7 to 14.1 mm (mean 12.8 ± 0.8 mm) and the wet weight − from 0.49 to 1.04 g (mean 0.83 ± 0.16 g). In the laboratory, animals were put together in a 10-liter tank filled with aerated water of the same temperature and salinity as at the sampling site (T=15°C, S=7), with stones on the bottom and empty shells used as shelters. Crabs were fed with different food, e.g. blue mussel Mytilus edulis trossulus, flesh of flat fish Platichthys flesus and filaments of green algae Enteromorpha sp. R. harrisii was maintained in the laboratory for 2 weeks after which tagged specimens were used in the experiment at T=15°C (S=7). After this experiment, crabs were gradually acclimated (2°C per day) to a higher temperature of 20°C at the constant salinity of 7. They were kept at the appropriate temperature for one week before the second experiment was started. The behavior (locomotor activity, feeding) and mortality were monitored during the whole period of acclimation as well as during the experiment. Experiment sets The experiments were designed based on the methodology applied by Hulathduwa et al. (2007) and the scheme provided by Jakubowska & Normant (2011), except for the starvation period which was shorten to 4 days to avoid an increase in mortality. Because of the low weight of food consumed and faeces produced by a single crab, five specimens of similar size were placed in one 2.5-liter tank for measurements of food consumption and feces production rates. Three experimental tanks for each temperature set were used.
Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl
Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841)| 221
Food consumption rate
Ammonia excretion rate
The food used during the experiments was flesh of flat fish Platichthys flesus of an average (n=15) energy value of 25.8 ± 0.97 J mg-1 dry wt, organic matter content of 92.78 ± 3.01% dry wt and water content of 80.40 ± 6.8% wet wt. The energy value was determined using a bomb microcalorimeter according to Normant et al. (2002), whereas the organic matter content was calculated from the weight loss on incineration in a muffle furnace for 12 h at 450°C (Gnaiger & Bitterlich 1984). The rate of food intake was determined from the weight loss of food given to crabs each day for 7 days. The uneaten leftovers were successively removed from the tanks, after which their wet and dry weights were determined. The feeding rate is given in mg of dry weight per day per gram of wet weight of crab (mg d-1 g-1 wet wt), averaged over the 7-day period of the experiments. The amount of energy acquired with food (C) was calculated on the basis of energy contained in the food consumed.
The rate of ammonia excretion was calculated in crabs (n=15) starved or fed for 7 days based on Koroleff’s (1976) indophenol method. Animals were placed separately from each other for 2 hours in 150 ml beakers filled with aerated water (S = 7, T = 15, 20°C). Three replicate water samples were collected from each beaker (both with crabs and the controls). The results are given in micromoles of ammonium nitrogen per day per gram of wet weight of a crab (μmol NH4-N d-1 g-1 wet wt). Using the equivalent 1 μmol NH4-N = 0.348 J (Elliott & Davison 1975), the energy excreted in the form of ammonia (U) was then calculated.
Faeces production rate During 7 days of the experiment and 2 days after its completion, crab faeces were collected until the alimentary canal was empty in order to calculate the rate of excretion (Choy 1986). Fecal pellets were pipetted onto the previously incinerated (T = 450°C, t = 12 h) GF/C Filter (Whatman 47 mm, 0.45 μm), after which the filter and excreta were dried (T = 55°C, t = 48 h) and again incinerated in a muffle furnace (T = 450°C, t = 12 h) in order to determine the organic matter content (Gnaiger & Bitterlich 1984). The rate of excretion is given in mg of dry weight per day per gram of wet weight of a crab (mg d-1 g-1 wet wt) averaged over 9 days. Food assimilation efficiency Because the mass of excreta from a single crab was insufficient to calculate the energy value in the bomb microcalorimeter, food assimilation efficiency (AE) was calculated using the formula given by Conover (1966): 𝐴𝐸 = (𝐹 − 𝐸) × [(1 − 𝐸) × 𝐹]−1 × 100
where F is the ratio of ash-free dry weight to total dry weight in the food, and E is the ratio of ash-dry weight to total dry weight in faeces. www.oandhs.org
Metabolic rate The energy dissipated in metabolic processes was determined using an isoperibol twin calorimeter of the Calvet type described by Normant et al. (2007). Measurements were made on crabs (n=15) starved or fed for 7 days according to the method given by Normant & Gibowicz (2008). The metabolic rate is expressed in Joules per gram of dry weight per hour (J g-1 wet wt h-1). Individual production The amount of energy assimilated from food (A) was calculated by multiplying the amount of energy consumed as food (C) by the assimilation efficiency (AE). Then the rates of various physiological processes, expressed in energy units − joules per gram of wet weight per day (J g-1 wet wt d-1), were inserted in the energy budget equation given by Winberg (1960) in order to calculate an individual production (P): 𝑃 =𝐴−𝑅−𝑈
Statistical analysis
The Wilcoxon matched pairs test at a confidence level of α = 95% was used to test the significance of differences between the rates of physiological processes at experimental temperatures. The relationship between these processes was calculated by linear regression analysis (y = ax + b) with a coefficient of determination R2 for a significance level p < 0.05.
222 | Joanna Hegele-Drywa, Monika Normant
RESULTS At a temperature of 15°C, the rate of food consumption varied strongly between crabs from three experimental tanks, from 1.85 to 7.14 mg d-1 g-1 wet wt. The increase in temperature affected the mean food consumption rate of R. harrisii, which increased from 4.31 ± 2.66 mg d-1 g-1 wet wt at 15°C to 10.99 ± 0.91 mg d-1 g-1 wet wt at 20°C (Fig. 1A). Similarly at higher temperature, the faeces production rate by R. harrisii increased 2.4-fold compared to a mean value of 0.66 ± 0.12 mg d-1 g-1 wet wt at 15°C (Fig. 1B). Unfortunately, due to a low number of data (n=3) it was impossible to determine the significance level of differences between food consumption and faeces excretion at two experimental temperatures. Food assimilation efficiency reached very high values, which were very similar at both experimental temperatures of 15°C and 20°C, 94.21 ± 1.51% and 95.67 ± 0.45%, respectively. The temperature rise from 15°C to 20°C had no significant effect (p>0.05) on the rate of ammonia excretion by R. harrisii. The fed animals excreted significantly (p<0.05) more ammonia than the starved ones, on average 1.46 ±
0.34 and 2.74 ± 1.84 times more at 15°C and 20°C, respectively (Fig. 2 A,B). The mean metabolic rate of R. harrisii at 15°C was 13.08 ± 7.50 J d-1 g-1 wet wt (Table 1). It increased significantly (p<0.05), i.e. to 34.08 ± 11.85 J d-1 g-1 wet wt at 20°C (Fig. 3). It was observed that animals were more active and started to molt at higher experimental temperature. The metabolic rate of fed individuals was on average 3.32 ± 2.29 times higher at 15°C and 1.42 ± 0.46 times higher at 20°C compared to starved specimens. The difference in the metabolic rate between starved and fed crabs was statistically significant (p<0.05) at both temperatures. The range for growth was positive at both experimental temperatures (Fig. 4). Values of the net production efficiency K2 (P/A) were 80.9 ± 22.4% and 82.9 ± 9.7% at a temperature of 15°C and 20°C, respectively. The energy expended on metabolic processes was similar at both temperatures of 15°C and 20°C, and amounted to 17.7 ± 6.4% and 16.7 ± 4.3% of the assimilated energy, respectively. The amount of energy lost in the conversion of nitrogen compounds in relation to energy assimilated with food at both salinities was small, not exceeding 2%.
Fig. 1. Rates (mean ± SD) of food consumption (A) and faeces production (B) in R. harrisii adult males at 15°C and 20°C
Fig. 2. Rates (mean ± SD) of ammonia excretion for R. harrisii adult males at 15°C (A) and (B) at 20°C. Mean values marked with different letters are significantly different (p<0.05) Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl
Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841)| 223
DISCUSSION
Fig. 3. Metabolic rate (mean ± SD) of R. harrisii adult males at 15°C and 20°C. Mean values marked with different letters are significantly different (p<0.05) Table 1 -1 -1
Effect of temperature on bioenergetics (J d g wet wt) of R. harrisii averaged over 7 days Energy allocation Ingested (C) Assimilated (A) Metabolic rate (MR) Unfed Fed Excreted (U) Unfed Fed Production (P)
Temperature 15°C 20°C 133.45 ± 27.69 262.57 ± 21.63 127.67 ± 26.49 247.34 ± 20.42 13.08 ± 7.50a 30.16 ± 9 .43a
34.08 ± 11.84b 46.77 ± 12.60b
2.03 ± 0.55a 2.69 ± 0.50a 103.69 ± 25.61
1.84 ± 0.76a 3.82 ± 1.56a 206.40 ± 20.76
Mean values ± SD. Mean values marked with different letters are significantly different (p < 0.05)
Non-native organisms need to optimize their physiological processes in the new environment to achieve invasion success. An animal requires food which provides energy necessary to sustain the metabolic processes as well as the growth and reproduction (Schimdt-Nielsen 1997). The daily portion of energy consumed by an organism is mostly species specific, but it may also be affected by many different factors, both biotic and abiotic ones. Daily food intake in the studied R. harrisii amounted to 2% of the crab body weight. This value was similar to the one recorded in omnivorous crabs, like e.g. Chinese mitten crab Eriocheir sinensis, Tanner crab Chionoectes bairdi or Cancer polyodon (Wolf & Cerda 1992, Paul et al. 1994, Normant et al. 2012). Moreover, being an omnivorous organism, the mud crab has easy access to a variety of food resources and probably does not manifest feeding behavior specific to organisms feeding sporadically. Furthermore, small daily food intake should not be surprising in the case of a small crab whose metabolic activity is lower compared to other crustacean species (Wallace 1973, Radford et al. 2004). Usually in terrestrial and sea crabs, 3 or 4% of the food intake weight is excreted in the form of feces (Lee 1997, Normant et al. 2012). However, it may be much more, even 25% like e.g. in the freshwater crab Barytelphusa cunicularis (Corte Rosaria & Martin 2010). Such a wide spectrum of values might be dependent on varying external and internal conditions affecting
Fig. 4. Mean (± SD) rates of energy losses (R+U) and energy available for production (P) in relation to energy assimilated (A) from food by R. harrisii at different temperatures www.oandhs.org
224 | Joanna Hegele-Drywa, Monika Normant
the physiology of a given organism including e.g. environmental conditions, the type of food or the molting stage. Despite the fact that feces excreted by the Harris mud crab represented on average 15% of the consumed food, the calculated food assimilation efficiency had very high values exceeding 90%. Although assimilation efficiency might be high in carnivores, Willmer et al. (2000) stated that such high values of AE are rather unusual in invertebrates. On the other hand, equally high AE values (as in the present studies) were also recorded in other crustaceans, like Munida gregaria and E. sinensis (Romero et al. 2006, Jakubowska & Normant 2011). R. harrisii was fed with highly organic, and thus potentially efficiently digestible, flat fish tissue. According to Pirestani et al. (2009) and Peng et al. (2013), fish flesh usually contains from 18 to even 24% of crude proteins, which could explain a significant increase in the ammonia excretion rate in fed crabs as compared to starved ones. R. harrisii belongs to ammonotelic organisms which excrete mainly soluble ammonia as a deamination product and only small proportion of other nitrogenous wastes like urea or free amino acids (Regnault 1987, Chen & Kou 1996, Weihrauch et al. 2009). According to Lucas (1993), Radford et al. (2004) and Rosas et al. (2007), an increase in the metabolic rate is observed when ingested materials are biochemically processed and then transformed into new molecules, used in further physiological and biochemical traits. Digestion of highly energetic food items, consisting mainly of proteins and lipids, is a complex process. Moreover, assimilation and storage of nutrients, deamination of amino acids, synthesis of excretory products and synthesis of lipids and proteins associated with the growth, requires a lot of energy (Robertson et al. 2001, Whitely et al. 2001). Usually, the metabolic rate in fed organisms is 2 or 3 times higher compared to the starved ones and depends mostly on the type and the amount of consumed food (Radford et al. 2004, Normant et al. 2012). This might also explain the 3.3-fold increase in the metabolic rate of fed R. harrisii compared to the starved specimens. The increase in the temperature by 5°C caused an increase in all physiological rates studied in R. harrisii, except the ammonia excretion rate in starved specimens. It is a little bit surprising, because according to the literature, the rate of ammonia excretion in many crustaceans increases with the temperature (Regnault 1987, Chen & Chia 1996, Crear & Forteath 2002). In general, the temperature
rise leads to an increase in locomotor activity and thereby to overall metabolic activity (Wallace 1973, Wyban et al. 1995). Whereas it seems that in the present study, an increase in the temperature might not be sufficient to affect the ammonia excretion rate in the starved crabs or may indicate that rates of excretion have adjusted to the temperature changes. In both temperatures, however, an increase in ammonia excretion was observed after feeding. It is unusual that a temperature increase by 5°C causes such a high increase in the metabolic rate as it was recorded in R. harrisii. In the present study, crabs became more active and started to molt at higher experimental temperature. Exposure to 20°C caused a 2.6-fold increase in the metabolic rate of starved R. harrisii compared to 15°C. According to Klekowski & Opaliński (1993) and Schmidt-Nielsen (1997), a 2fold increase in the metabolic rate should occur after an increase in temperature by 10°C. Moreover, in natural environment an increase in temperature stimulates migration to warmer waters for reproduction, which itself is an energetically costly activity. Furthermore, both crab males and females expend energy for finding a partner and then copulation. Females expend even more energy taking care of the spawned eggs. Thus, in warmer waters where more energy for the overall physiology is required, individuals must compensate this excessive energy loss by increasing the food intake. With a 2.5 fold increase in the consumption rate and 2.4 fold growth in faeces production observed at 20°C compared to 15°C, the assimilation efficiency remained almost equal. Although it is commonly known that the temperature can significantly affect food intake in crabs (e.g. Kondzela & Shirley 1993), there is only limited information in the literature on the effect of this factor on AE. According to Klekowski & Fischer (1993) and Schmidt-Nielsen (1997), this environmental parameter is, besides the availability of food, the most significant exogenous factor affecting the amount of absorbed food, contributing to a change in enzymatic activity. Nevertheless, as it was mentioned before, high values of AE and the fact that there were no differences in this parameter between the two studied temperatures might also be related to the type of food provided (McCue 2006). A less pronounced increase in the metabolic rate observed after feeding in specimens held at 20°C might be related to physico-chemical conditions of enzyme-catalyzed reactions which are sensitive to temperature (Hochachka 1991, Hutchison & Dupré 1992, Sébert et al. 1995).
Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl
Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841)| 225
According to Vega-Villasante et al. (1993) in pacific brown shrimp or other crustaceans thermal optimum for digestive enzymes like amylases, is noticed at higher temperatures. Thus it might be concluded that the digestion in R. harrisii requires higher energy expenditure at 15°C than at 20°C. In the Harris mud crab from the Gulf of Gdańsk R/A (metabolic rate/assimilation) and P/A (net production efficiency) ratios amounted to 0.1:1.0 and 0.8:1.0, respectively. Identical observations were made by Jakubowska & Normant (2011) and Normant et al. (2012) for the Chinese mitten crab. Moreover, similar values of R/A and P/A ratios were obtained for the lesser blue crab Callinectes similis (Guerin & Stickle 1992) and the white shrimp Litopenaeus setiferus (Sãnchez et al. 2002), i.e. 0.2:1.0 and 0.8:1.0, and 0.2:1.0 and 0.7:1.0, respectively. Therefore, a lot of energy can be used for the growth and reproduction. Moreover, such low energy expenditures and large supplies of energy available for production seem to be one of the advantages allowing R. harrisii to be a successful invader. Nevertheless, our observations should be interpreted with caution due to laboratory conditions and highlyenergetic food served. In addition, handling of food items by crabs in nature and in the laboratory could vary greatly, the digestion of food by starved crabs could differ from the digestive process in nature, and less energetic food available in the environment might affect the amount of energy available for production. Our studies showed that even a change by 5°C in water temperature can affect the amount of energy available for individual production in R. harrisii. At both experimental temperatures, the amount of energy assimilated from food significantly exceeded the energy expenditures, so the amount of energy available for individual production was positively high, exceeding 82% of the assimilated energy. The temperatures used in this experiment are within the range of thermal tolerance of R. harrisii (Kujawa 1957) and are not extreme, so they were not expected to cause drastic changes in the rates of physiological processes. It seems, however, that although the rates of physiological processes at a temperature of 20°C were higher, this temperature seems to be energetically more “profitable” for R. harrisii since the production was on average 2 times higher compared to 15°C. The latest reports on the occurrence of the Harris mud crab in higher latitudes of the northern hemisphere, i.e. Finland coastal waters (Fowler et al. 2013), might deny the recent www.oandhs.org
successful range expansion from the physiological and bioenergetic perspectives. Nevertheless, eurytrophic species like R.harrisii may undoubtedly compensate this disadvantage by generating a large number of adaptations, e.g. at physiological and biochemical levels. Furthermore, according to literature the largest amounts of energy for the growth and reproduction are available in environmental conditions to which organisms are adapted (Guerin & Stickle 1992, Sãnchez et al. 2002, Normant & Lamprecht 2006, Hulathduwa et al. 2007). It might be concluded that the Harris mud crab changes its behavior and the rates of physiological processes due to a slight shift in water temperature. Higher water temperature causes a detectable increase in locomotor activity and the molting rate, food consumption and the metabolic rate, which seems to be associated with both the growth and the reproduction. Moreover, due to very high rates of individual production we assumed that the analyzed thermal range is favorable to R. harrisii with the thermal optimum at a temperature around 20°C. The above conclusion, however, should be still confirmed by similar studies at a broader temperature range. It should also be emphasized that the first studies on the effect of temperature on physiological processes in R. harrisii have already been conducted and they undoubtedly helped to understand the functioning and the successful invasion of this crab into new regions. ACKNOWLEDGMENTS This research was funded by the Polish National Science Centre, grant No. 3016/B/P01/2011/40. REFERENCE Bacevičius, E. & Gasiūnaitė Z.R. (2008). Two crab speciesChinese mitten crab (Eriocheir sinensis Milne-Edwards) and mud crab (Rhithropanopeus harrisii Gould ssp. Tridentatus Maitland) in the Lithuanian coastal waters, Baltic Sea. Trans. Wat. Bull. 2: 63–68. DOI: 10.1285/i1825229Xv2n2p63 Chen, J.C. & Chia P.G. (1996). Oxygen Uptake and Nitrogen Excretion of Juvenile Scylla serrata at Different Temperature and Salinity Levels. J. Crust. Biol. 16 (3): 437-442. DOI: 10.1163/193724096X00441 Chen, J.C. & Kou T. (1996). Effects of temperature on oxygen consumption and nitrogenous excretion of juvenile Macrobrachium rosenbergii. Aquaculture. 145 (1-4): 295-303. DOI: 10.1016/S0044-8486(96)01348-8
226 | Joanna Hegele-Drywa, Monika Normant Choy, S.C. (1986). Natural diet and feeding habits of the crabs Liocarcinus puber and L. holsatus (Decapoda, Brachyura, Portunidae). Mar. Ecol. Prog. Ser. 31: 87–99 Christiansen, M.E. & Costlow J.D.Jr. (1975). The effect of salinity and cyclic temperature on larval develop of the mud crab Rhithropanopeus harrisii (Brachyura: Xantidae) reared in the laboratory. Mar. Biol. 32: 215–221. DOI: 10.1007/BF00399201 Conover, R.J. (1966). Assimilation of organic matter by zooplankton. Limnol. Oceanog. 11: 338–290. DOI: 10.4319/lo.1966.11.3.0338 Corte Rosaria, J. & Martin E.R. (2010). Behavioral Changes in Freshwater Crab Barytelphusa cunicularis after Exposure to Low Frequency Electromagnetic Fields. World J. Fish. Mar. Sci. 2 (6): 487-494 Crear, B.J. & Forteath G.N.R. (2002). Feeding has the largest effect on the ammonia excretion rate of the southern rock lobster, Jasus edwardsii, and the western rock lobster, Panulirus cygus. Aquac. Eng. 26: 239–250. DOI:10.1016/S01448609(02)00033-X Czerniejewski, P. & Rybczyk A. (2008). Body weight, morphometry, and diet of the mud crab Rhithropanopeus harrisii tridentatus (Maitland, 1874) in the Odra Estuary, Poland. Crustaceana. 81 (11): 1289–1299. DOI: 10.1163/156854008X369483 Diamond, D.W., Scott L.K., Forward R.B.Jr. & Kirby-Smith W. (1989). Respiration and osmoregulation of the estuarine crab Rhithropanopeus harrisii (Gould): effect of the herbicide, alachlor. Comp. Biochem. Physiol. 93A: 313-318. DOI: 0.1016/0300-9629(89)90043-1 Elliott, J.M. & Davison W. (1975). Energy equivalents of oxygen consumption in animal energetic. Oecologia. 19:195–201 Forward, R.B.Jr. (2009). Larval Biology of the Crab Rhithropanopeus harrisii (Gould): A Synthesis. Biol. Bull. 216 (3): 243-256 Fowler, A.E., Forsström T., von Numers M. & Vesakoski O. (2013). The North American mud crab Rhithropanopeus harrisii (Gould, 1841) in newly colonized Northern Baltic Sea: distribution and ecology. Aquat. Inv. 8 (1): 89-96. DOI: 0.3391/ai.2013.8.1.10. Gnaiger, E. & Bitterlich G. (1984). Proximate biochemical composition and caloric content calculate from elemental CHN analysis: a stoichiometric concept. Oecologia. 62: 289– 298. Gonçalves, F., Ribeiro R. & Soares M.V.M. (1995). Rhithropanopeus harrisii (Gould), an American crab in the Estuary of the Mondego River. J. Crust. Biol. 15 (4): 756-762. DOI: 10.2307/1548824. Guerin, J.L. & Stickle W.B. (1992). Effects of salinity gradients on the tolerance and bioenergetics of juvenile blue crabs (Callinectes sapidus) from waters of different environmental salinities. Mar. Biol. 114 (3): 391-396. DOI: 10.1007/BF00350029 Hartnoll, R.G. (1982). Growth in the Biology of Crustacea. In D.E. Bliss (Eds.), Embryology, Morphology and Genetics 2 (pp 116-196). Academic Press. Hegele-Drywa, J. & Normant M. (2014). Non–native crab Rhithropanopeus harrisii (Gould, 1984) – a new component of the benthic communities in the Gulf of Gdańsk (southern Baltic Sea). Oceanologia. 56 (1): 125-139. DOI: 10.5697/oc.561.125 Hochachka, P.W. (1991). Temperature: the ectothermy option. In P.W. Hochachka & T.P. Mommsen (Eds.), Biochemistry and molecular ecology of fishes (pp 313-322). Amsterdam, Elsevier.
Hulathduwa, Y.D., Stickle W.B. & Brown K.M. (2007). The effect of salinity on survival, bioenergetics and predation risk in the mud crabs Panopeus simpsoni and Eurypanopeus depressus. Mar. Biol. 152: 363–370. Hutchison, V.H. & Dupré R.K. (1992). Thermoreulation. In M.E. Feder &W.W. Burggren (Eds.), Environmental physiology of the amphipods (pp 206-249). University of Chicago Press. Iseda, M., Otani M. & Kimura T. (2007). First record of an introduced crab Rhithropanopeus harrisii (Crusteacea: Brachyura: Panopeidae) in Japan. JPN. J. Benthol. 62: 39–44. Jakubowska M. & Normant M. (2011). Effect of temperature on the physiology and bioenergetics of adults of the Chinese mitten crab Eriocheir sinensis: considerations for a species invading cooler waters. Mar. Freshwater. Behav. Physiol. 44 (3): 171–183. DOI:10.1080/10236244.2011.598283 Kinne, O. & Rotthauwe H.W. (1952). Biologische Beobachtungen und Untersuchungen über die Blutkonzentration an Heteropanope tridentatus Maitland (Decapoda). Kieler Meeresforsch. 8: 212–217 (in German). Klekowski, R.Z. & Fischer Z. (1993). Bioenergetyka ekologiczna zwierząt zmiennocieplnych. Warszawa, PAN (in Polish). Klekowski, R.Z. & Opaliński K.W. (1993). Metabolizm energetyczny. In R.Z.Klekowski & Z. Fisher (Eds.), Bioenergetyka ekologiczna zwierząt zmiennocieplnych (pp 35-82). Polska Akademia Nauk, Wydział II Nauk Biologicznych. Kondzela, C.M. & Shirley T.C. (1993). Survival, feeding, and growth of juvenile Dungeness crabs from southeastern Alaska reared at different temperatures. J. Crust. Biol. 13: 25– 35 Koroleff, F. (1976). Determination of nutrients. In K. Grasshoff, K. Kremling & M. Ehrhardt (Eds.), Methods of seawater analysis (pp 159–229). New York, Weinheim. Kotta, J. & Ojaveer H. (2012). Rapid establishment of the alien crab Rhithropanopeus harrisii (Gould) in the Gulf of Riga. Est. J. Ecol. 61 (4): 293-298. DOI: 10.3176/eco.2012.4.04 Kujawa, S. (1957). Biology and culture of the crab Rhithropanopeus harrisii (Gould) subsp. tridentatus (Maitland) from Vistula Lagoon. Wszechświat. 2: 57–59 Lee, S.Y. (1997). Potential trophic importance of the faecal material of the mangrove sesarmine crab Sesarma messa. Mar. Ecol. Prog. Ser. 159: 275-284 Lucas, A. (1993). Bioénergétique Des Animaux Aquatiques. Paris, Masson (in French). Maltby, L., Naylor C. & Calow P. (1990). Effect of stress on a freshwater benthic detritivore: Scope for growth in . Ecotox. Environ. Safety. 9 (3): 285-291. DOI: 10.1016/01476513(90)90030-9 McCue, M.D. (2006). Specific dynamic action: A century of investigation. Comp. Biochem. Physiol. 144 A: 381–394. DOI: 10.1016/j.cbpa.2006.03.011 Normant, M., Chrobak M. & Szaniawska A. (2002). Energy value and chemical composition (CHN) of the Chinese mitten crab Eriocheir sinensis (Decapoda: Grapsidae) from the Baltic Sea. Therm. Acta. 394: 233–237. DOI: 10.1016/S00406031(02)00259-9 Normant, M. & Gibowicz M. (2008). Salinity induced changes in haemolymph osmolality and total metabolic rate of the mud crab Rhithropanopeus harrisii Gould, 1841 from Baltic coastal waters. J. Exp. Mar. Biol. Ecol. 355 (2): 145–152. DOI: 10.1016/j.jembe.2007.12.014 Normant, M., Dziekoński M., Drzazgowski J. & Lamprecht I. (2007). Metabolic investigations of aquatic organisms with a
Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl
Effect of temperature on physiology and bioenergetics of adult Harris mud crab Rhithropanopeus harrisii (Gould, 1841)| 227 new twin heat conduction calorimeter. Therm. Acta. 458 (1-2): 101-106. DOI: 10.1016/j.tca.2007.01.025 Normant, M., Król M. & Jakubowska M. (2012). Effect of salinity on the physiology and bioenergetics of adult Chinese mitten crabs Eriocheir sinensis. J. Exp. Mar. Biol. Ecol. (416417): 215-220. DOI:10.1016/j.jembe.2012.01.001 Normant, M. & Lamprecht I. (2006). Does scope for growth change as a result of salinity stress in the amphipod Gammarus oceanicus? J. Exp. Mar. Biol. Ecol. 334 (1): 158-163. DOI: 10.1016/j.jembe.2006.01.022 Ojaveer, H., Galil B.S., Minchin D., Olenin S., Amorim A. et al. (2014). Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar. Pol. (44):160-165. DOI: 10.1016/j.marpol.2013.08.019. Paul, J.M., Paul A.J. & Kimker A. (1994). Compensatory feeding capacity of 2 Brachyuran crabs, Tanner and Dungeness, after starvation periods like those encountered in pots. Alaska Fish. Res. Bul. 1 (2): 184-187 Peng, S., Chen C., Shi Z. & Wang L. (2013). Amino Acid and Fatty Acid Composition of the Muscle Tissue of Yellowfin Tuna (Thunnus Albacares) and Bigeye Tuna (Thunnus Obesus). Journal of Food and Nutrition Research. 1(4): 42-45. DOI: 10.12691/jfnr-1-4-2 Pigliucci, M. & Preston K. 2004. The Evolutionary Biology of Complex Phenotypes. Oxford, Oxford University Press. Pirestani, S., Ali Sahari M., Barzegar M. & Seyfabadi S.J. (2009). Chemical compositions and minerals of some commercially important fish species from the South Caspian Sea. International Food Research Journal. 16: 39-44. Radford, C.A., Marsden I.M. & Davison W. (2004). Temporal variation in the specific dynamic action of juvenile New Zealand rock lobsters, Jasus edwardsii. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 139A: 1-9. DOI:10.1016/j.cbpb.2004.02.015 Regnault, M. (1987). Nitrogen excretion in marine and freshwater crustacean. Biol. Rev. 62(1): 1-24. DOI: 10.1111/j.1469-185X.1987.tb00623.x Robertson, R.F., El-Haj A.J., Clarke A. & Taylor E.W. (2001). Effects of temperature on specific dynamic action and protein synthesis rates in the Baltic isopod crustacean, Saduria entomon. J. Exp. Mar. Biol. Ecol. 262 (1): 113-129. DOI: 10.1016/S0022-0981(01)00286-6 Roche, D.G. & Torchin M.E. (2007). Established population of the North American Harris mud crab, Rhithropanopeus harrisii (Gould 1841) (Crustacea: Brachyura: Xanthidae) in the Panama Canal. Aquat. Inv. 2 (3): 155-161. DOI:10.3391/ai.2007.2.3.1 Romero, M.C., Vanella F., Tapella F. & Lovrich G.A. (2006). Assimilation and oxygen uptake associated with two different feeding habits of Munida gregaria (=M. subrugosa) (Crustacea, Decapoda). J. Exp. Mar. Biol. Ecol. 333(1): 40-48. DOI: 10.1016/j.jembe.2005.11.018 Rosas, C., Cuzon G., Pascual C., Gaxiola G. et al. (2007). Energy balance of Octopus maya fed crab or artificial diet. Mar. Biol. 152: 371-381. DOI: 10.1007/s00227-007-0692-2 Rychter, A. (1997). Effect of anoxia on the behaviour, haemolymph lactate and glycogen concentrations in the mud crab Rhithropanopeus harrisii ssp. tridentatus (Maitland) (Crustacea: Decapoda). Oceanologia. 39 (3): 325–335 Sãnchez, A., Pascual C., Sãnchez A., Vargas-Albores F.et al. (2002). Acclimation of Adult Males of Litopenaeus Setiferus Exposed at 27 °C and 31 °C: Bioenergetic Balance. In: E. Esobar-Briones & F. Alvarez (Eds.), Modern approaches to the www.oandhs.org
study of Crustacea (pp 45-52). New York, Kluwer Academic/Plenum Publishers. Schmidt-Nielsen, K. (1997). Fizjologia zwierząt: Adaptacja do środowiska. Warszawa, PWN. Schlichting, C.D. & Pigliucci M. (1998). Phenotypic Evolution: A Reaction Norm Perspective. Sunderland, MA: Sinauer Associates. Schröer, M., Wittmann A.C., Grüner N., Steeger H.U., Bock C., Paul R. & Pörtner H.O. (2009). Oxygen limited thermal tolerance and performance in the lugworm Arenicola marina: a latitudinal comparison. J. Exp. Mar. Biol. Ecol. 372 , 22-30. Sébert, P., Pequeux A., Simon B. & Barthelemy L. (1995). Effects of hydrostatic pressure and temperature on the energy metabolism of the Chinese crab (Eriocheir sinensis) and the yellow eel (Anguilla Anguilla). Comp. Biochem. Physiol. 112(1): 131–136. DOI: 10.1016/0300-9629(95)00079-M Smith, R.I. (1967). Osmotic regulation and adaptive reduction of water permeability in a brackish-water crab, Rhithropanopeus harrisii (Brachyura: Xanthidae). Biological Bulletin. 133: 643-658 Turoboyski, K. (1973). Biology and ecology of the crab Rhithropanopeus harrisii ssp. tridentatus. Mar. Biol. 23 (4): 303– 313. DOI: 10.1007/BF00389338 Vega-Villasante, F., Nolasco H. & Civera R. (1993). The digestive enzymes of the pacific brown shrimp Penaeus californiensis.: I—Properties of amylase activity in the digestive tract. Comp. Biochem .Phisiol. Part B: Comparative Biochemistry. 106 (3): 547550. Wallace, J.C. (1973). Feeding, starvation and metabolic rate in the Shore crab Carcinus maenas. Mar. Biol. 20: 277-281. DOI: 10.1007/BF00354271 Weihrauch, D., Wilkie M.P. & Walsh P.J. (2009). Ammonia and urea transporters in gills of fish and aquatic crustaceans. J. Exp. Biol. 212: 1716-1730. DOI: 10.1242/jeb.036103 Whiteley, N.M., Roberston R.F., Meagor J., El Haj A. J.& Taylor E.W. (2001). Protein synthesis and specific dynamic action in crustaceans: effects of temperature. Compar. Biochem. Pysiol. Mol. Integr. Physiol. 128 (3): 593-604. DOI: 10.1016/S10956433(00)00337-8 Willmer, P., Stone G. & Johnson J. (2000). Environmental physiology of animals. Metabolism and energy. Oxford, Blackwell Science. Winberg, G.G. (1960). Rate of metabolism and food requirements of fishes. Transl. Ser. Fish. Res. Bd. Can. 194-202. Wolff, M. & Cerda G. (1992). Feeding Ecology of the crab Cancer Polyodon in La Herradura Bay, northern Chile. Feeding chronology, food intake, gross growth and ecological efficiency. Mar. Ecol. Prog. Ser. 89: 213-219. DOI: 10.3354/meps089213 Wyban, J., Walsh W.A. & Godin D.M. (1995). Temperature effects on growth, feeding rate and food conversion of the Pacific white shrimp (Penaeus vannamei). Aquaculture. 138: 267279. DOI: 10.1016/0044-8486(95)00032-1