Partitioning of Respiratory Energy and Environmental Tolerance in the Copepods Calanipeda Aquaedulcis and Arctodiaptomus Salinus

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Partitioning of Respiratory Energy and Environmental Tolerance in the Copepods Calanipeda Aquaedulcis and Arctodiaptomus Salinus Estuarine, Coastal and Shelf Science 114 (2012) 199e207 Contents lists available at SciVerse ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Partitioning of respiratory energy and environmental tolerance in the copepods Calanipeda aquaedulcis and Arctodiaptomus salinus Leonid Svetlichny*, Antonina Khanaychenko, Elena Hubareva, Larisa Aganesova Institute of Biology of the Southern Seas, Department of Animal Physiology and Biochemistry, Nakhimov Av. 2, Sevastopol 99011, Ukraine article info abstract Article history: Total and basal metabolism was studied in the widely distributed copepod species Calanipeda aquaedulcis Received 21 October 2011 and Arctodiaptomus salinus of both genders in order to estimate respiratory energy partitioning. Specific Accepted 25 July 2012 oxygen consumption was found to double in C. aquaedulcis than in A. salinus, and double in males than in Available online 9 August 2012 females both in terms of total and basal metabolism. Respiration rates in females carrying ovisacs were 1.49 and 1.43 times higher than those in females without ovisacs for C. aquaedulcis and A. salinus, Keywords: respectively. Extra energy expenditures are due to carrying ovisacs and egg respiration. There was no Calanipeda aquaedulcis À1 significant effect of salinity (0.1e40), oxygen concentration (1e8mgO2 l ) or crowding on oxygen Arctodiaptomus salinus fi respiration rate consumption con rming the hypothesis that C. aquaedulcis and A. salinus are the animals with a type of salinity respiratory metabolism independent of salinity and oxygen concentration. At critical oxygen concen- À1 oxygen concentration trations less than 1 mg O2 l respiration rate fell notably by approximately an order of magnitude in crowding both species and in both genders. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction Calanipeda aquaedulcis and Arctodiaptomus salinus are calanoid copepods spawning their eggs into ovisacs that normally remain Calanipeda aquaedulcis Kritschagin 1873, euryhaline Copepoda attached to the female until emergence of nauplii. C. aquaedulcis species, inhabits the coastal lagoons, salt marshes and saline produces only subitaneous eggs and carries them in ovisacs wetlands (mainly transition zones, estuaries) from the Atlantic attached to females until hatching. Thereby, this year-round species coast of Morocco (Ramdani et al., 2001) and Spain (Frisch et al., inhabits only permanent water bodies (Marrone et al., 2006; 2006) across the Mediterranean coastal areas of Europe (Brucet Alfonso and Belmonte, 2011). In contrast, A. salinus produces both et al., 2008; Lucena-Moya et al., 2010; Alfonso and Belmonte, subitaneous and resting eggs and thus are capable of colonizing the 2011), North Africa (Ramdani et al., 2001), North-west Asia temporary reservoirs (Jiménez-Melero et al., 2007). (Ustaoglu, 2004) to the Black and Azov Seas (Siokou-Frangou et al., Semi-permanent estuarine and ephemeral coastal pool ecosys- 2004; Kovalev et al., 2006), Caspian Sea (Garber, 1951) and up to the tems can undergo frequent and rapid temperature, salinity and Aral Sea (Andreev et al., 1992). This species can also penetrate to oxygen regime changes owing to the strong local meteorological inner reservoirs of the Mediterranean basin (Samchyshyna, 2008) influence. Therefore, the organisms living in such ecosystems have where it competes with euryhaline Paleoarctic Copepoda species to develop rapid adaptive reactions to environmental changes in Arctodiaptomus salinus Daday 1885 inhabiting mainly lentic water order to survive at low dissolved oxygen concentration and bodies, from small rock pools (Marrone et al., 2006) to large saline crowding, variable salinity or even total desiccation. lakes (Andreev et al., 1992; Tolomeev et al., 2010). In the Crimean The study of physiological responses of these species to rapid area of the Black Sea C. aquaedulcis was found in Sevastopol Bay changes of environmental parameters can reveal the interspecies (Gubanova et al., 2001) while A. salinus was abundant mainly in salt differences in copepod adaptability. However, the data on the coastal lakes of the Eastern Crimea, Kerch peninsula (Shadrin et al., physiological features of Calanipeda aquaedulcis and Arctodiapto- 2008). mus salinus are noticeably lacking, despite a rather long history of ecological studies of these species. Some ecological aspects of feeding and development of Calani- peda aquaedulcis were studied in their natural habitat in the Caspian * Corresponding author. and Aral Seas (Koudelina,1950; Garber,1951; Kortunova et al.,1972), E-mail address: [email protected] (L. Svetlichny). Sicilian inland water (Marrone et al., 2006). Brucet et al. (2008) 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2012.07.023 200 L. Svetlichny et al. / Estuarine, Coastal and Shelf Science 114 (2012) 199e207 studied feeding of different stages of C. aquaedulcis in the Mediter- studied in separate experiments. Prior to the experiments, about 50 ranean salt marshes. The effect of temperature on stage duration individuals of females or males of each species were placed in and stage-specific mortality of Arctodiaptomus salinus was exam- 100-ml beakers containing 0.45 mm FSW. The copepods were ined by Jiménez-Melero et al. (2007) and salinity tolerance of this allowed to empty guts as they were deprived of food for approxi- species was studied by Rokneddine and Chentoufi (2004). Lapesa mately 2 h prior the experiment. After this procedure only data et al. (2004) described feeding behavior of A. salinus from the from actively swimming copepods, both at the beginning and end coastal ponds of Spain. Tolomeev et al. (2010) compared adaptive of each incubation period were selected. À1 À1 changes of feeding spectra and chemical composition of A. salinus Respiration rate (R, mgO2 ind h ) of copepods was deter- from the salt lakes of South Siberia with different physico-chemical mined using sealed chamber method with experimental and conditions. Parra et al. (2005) carried out the experiments with control syringes of 2.0 ml as the respirometers. 5e10 females or populations of A. salinus to study the negative effect of pesticides males of Calanipeda aquaedulcis and 3e6 females or males of Arc- generated by intensive olive tree cultivation on aquatic ecosystem. todiaptomus salinus per 1 ml were gently transferred by a pipette Our aim was to study under laboratory conditions the effect of into filled with filtered seawater experimental syringe supplied by À salinity (0.1e40), dissolved oxygen concentration (0.2e8.0 mg l 1), protective sieve disc (mesh size 200 mm) at the confluent outlet. À crowding (2e27 ind ml 1), gender and fecundity status (egg- In order to obtain identical oxygen, salinity and seston content, carrying and non-egg-carrying females) on the respiration rate of we connected the control and experimental syringes with a plastic Calanipeda aquaedulcis and Arctodiaptomus salinus. Metabolic tube and pumped the water through it back and forth several times. patterns as the indicators of the type of acclimation response Then the syringes were separated, closed by the stoppers and (regulation or conformality) to changes in salinity and dissolved placed to the dark chamber at 20 Æ 0.5 C. Incubation periods oxygen concentration were analyzed. Fecundity status was amounted to about 2e3 h. During the incubation the total oxygen considered in order to estimate the cost of egg-carrying strategy. consumed was never more than 20% of the initial value. There were Crowding was considered in the methodological aspect in order to 10 replicates for each experiment. correct oxygen consumption measurements. In order to investigate basal metabolism, the copepods in our experiments were narcotized until complete immobilization 2. Materials and methods (not more than 2 min) with 1: 5000 MS-222 Sandoz according to common experimental practice (Gill, 1987; Knutsen et al., 2001; 2.1. Laboratory experiments Van Duren et al., 2003). Just after immobilization, double number of narcotized cope- Calanipeda aquaedulcis and Arctodiaptomus salinus used in pods (in comparison with the number of intact actively swimming laboratory experiments were initially collected from the salt lakes individuals used in the experiments on total metabolism) was located near the sea coast of Kerch peninsula (Crimea) in 2007. transferred to the experimental syringes filled by the FSW with Copepods of these species were cultivated successfully during three times lower concentration of MS-222 enough for the cope- 2007e2011 in semi-continuous monospecific batch cultures in the pods to be immobile during 3 h exposure. During the incubation Department of Mariculture of the Institute of Biology of the the syringes with narcotized animals were rotated every 10 min to Southern Seas (IBSS, Sevastopol, Ukraine) through numerous avoid the development of O2 gradients within the respirometer. generations and were used as models for various ecological and After incubation, the individuals were gently transferred to the physiological investigations. The experiments were conducted on fresh seawater free of MS-222 where they rapidly recovered full specimens of C. aquaedulcis and A. salinus separated from contin- activity within 10e20 min. Only the results of the experiments in uous cultures and maintained before the experiments in the filtered which the copepods did not awaken during incubation but Black Sea water (FSW) of salinity
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