Abstract
Caging is an active biomonitoring strategy that employs a sentinel species, sometimes a species naturally absent from the studied site, in the surveillance of water bodies to verify whether biota may be at risk. The main advantage of caging is the possibility to standardize several biotic and abiotic parameters. However, little knowledge is available about the effects of confinement on physiology and metabolism of caged organisms. The aim of this study is to characterize confinement and food access restriction effects, induced via caging experiments using a multi-biomarker approach (biometric data, immunity, antioxidant, metabolic detoxication, and digestive enzymes). The study has been undertaken using the same experiment conducted in ecosystem conditions using three-spined stickleback (Gasterosteus aculeatus) during two different periods: one in April, corresponding to breeding season, and the other in October, outside breeding season. Fifteen fish were maintained for 21 days in different conditions (caged or uncaged and with or without food supply). The main result was that confinement stress had little impact on the biological markers of sticklebacks. However, the stressors seemed to increase the negative effects of food restriction on these biomarkers, when sticklebacks needed more energy, that is, during their breeding period. Outside breeding period, most investigated biomarkers were not impacted by caging. This study showed a way to specify the conditions of application and interpretation of biomarkers during active monitoring to ensure an effective, reliable diagnosis of water body quality.
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References
Abolfathi M, Hajimoradloo A, Ghorbani R, Zamani A (2012) Effect of starvation and refeeding on digestive enzyme activities in juvenile roach, Rutilus rutilus caspicus. Comp Biochem Physiol A 161:166–173. https://doi.org/10.1016/j.cbpa.2011.10.020
Ajima MNO, Pandey PK, Kumar K, Poojary N (2017) Assessment of mutagenic, hematological and oxidative stress biomarkers in liver of Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) in response to sublethal verapamil exposure. Drug Chem Toxicol 40:286–294. https://doi.org/10.1080/01480545.2016.1219914
Almeida JR, Gravato C, Guilhermino L (2015) Effects of temperature in juvenile seabass (Dicentrarchus labrax L.) biomarker responses and behaviour: implications for environmental monitoring. Estuar Coasts 38:45–55. https://doi.org/10.1007/s12237-014-9792-7
Babo S, Vasseur P (1992) In vitro effects of thiram on liver antioxidant enzyme activities of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 22:61–68. https://doi.org/10.1016/0166-445X(92)90036-M
Bado-Nilles A, Betoulle S, Geffard A, Porcher JM, Gagnaire B, Sanchez W (2013) Flow cytometry detection of lysosomal presence and lysosomal membrane integrity in the three-spined stickleback (Gasterosteus aculeatus L.) immune cells: applications in environmental aquatic immunotoxicology. Environ Sci Pollut Res Int 20:2692–2704. https://doi.org/10.1007/s11356-012-1410-2
Bado-Nilles A, Techer R, Porcher JM, Geffard A, Gagnaire B, Betoulle S, Sanchez W (2014a) Detection of immunotoxic effects of estrogenic and androgenic endocrine disrupting compounds using splenic immune cells of the female three-spined stickleback, Gasterosteus aculeatus (L.). Environ Toxicol Pharmacol 38:672–683. https://doi.org/10.1016/j.etap.2014.08.002
Bado-Nilles A, Jolly S, Porcher JM, Palluel O, Geffard A, Gagnaire B, Betoulle S, Sanchez W (2014b) Applications in environmental risk assessment of leucocyte apoptosis, necrosis and respiratory burst analysis on the European bullhead, Cottus sp. Environ Pollut 184:9–17. https://doi.org/10.1016/j.envpol.2013.07.049
Baeverfjord G, Krogdahl A (1996) Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 19:375–387. https://doi.org/10.1046/j.1365-2761.1996.d01-92.x
Besse JP, Coquery M, Lopes C, Chaumot A, Budzinski H, Labadie P, Geffard O (2013) Caged Gammarus fossarum (Crustacea) as a robust tool for the characterization of bioavailable contamination levels in continental waters: towards the determination of threshold values. Water Res 47:650–660. https://doi.org/10.1016/j.watres.2012.10.024
Biswas SK, Rahman I (2009) Environmental toxicity, redox signaling and lung inflammation: the role of glutathione. Mol Asp Med 30:60–76. https://doi.org/10.1016/j.mam.2008.07.001
Blom S, Andersson T, Förlin L (2000) Effects of food deprivation and handling stress on head kidney 17alpha-hydroxyprogesterone 21-hydroxylase activity, plasma cortisol and the activities of liver detoxification enzymes in rainbow trout. Aquat Toxicol 48:265–274. https://doi.org/10.1016/S0166-445X(99)00031-4
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cappello T, Maisano M, D’Agata A, Natalotto A, Mauceri A, Fasulo S (2013) Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). Mar Environ Res 91:52–60. https://doi.org/10.1016/j.marenvres.2012.12.010
Chilmonczyk S, Monge D (1999) Flow cytometry as a tool for assessment of the fish cellular immune response to pathogens. Fish Shellfish Immunol 9:319–333. https://doi.org/10.1006/fsim.1998.0188
Conti ME, Cecchetti G (2001) Biological monitoring: lichens as bioindicators of air pollution assessment — a review. Environ Pollut 114:471–492. https://doi.org/10.1016/S0269-7491(00)00224-4
Debnath D, Pal AK, Sahu NP, Yengkokpam S, Baruah K, Choudhury D, Venkateshwarlu G (2007) Digestive enzymes and metabolic profile of Labeo rohita fingerlings fed diets with different crude protein levels. Comp Biochem Physiol B 146:107–114. https://doi.org/10.1016/j.cbpb.2006.09.008
Dey S, Samanta P, Pal S, Mukherjee AK, Kole D, Ghosh AR (2016) Integrative assessment of biomarker responses in teleostean fishes exposed to glyphosate-based herbicide (Excel Mera 71). Emerg Contami 2:191–203. https://doi.org/10.1016/j.emcon.2016.12.002
Ellman GL, Courtney KD, Andres jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Flammarion P, Devaux A, Nehls S, Migeon B, Noury P, Garric J (2002) Multibiomarker responses in fish from the Moselle River (France). Ecotoxicol Environ Saf 51:145–153. https://doi.org/10.1006/eesa.2001.2134
Fulton TW (1902) Rate of growth of sea fishes. Neill & Company, Edinburgh
Furné M, Garcia-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2009) Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquac Nutr 15:587–595. https://doi.org/10.1111/j.1365-2095.2008.00626.x
Gagnaire B, Thomas-Guyon H, Renault T (2004) In vitro effects of cadmium and mercury on Pacific oyster, Crassostrea gigas (Thunberg), haemocytes. Fish Shellfish Immunol 16:501–512. https://doi.org/10.1016/j.fsi.2003.08.007
Galloway TS, Brown RJ, Browne MA, Dissanayake A, Lowe D, Jones MB, Depledge MH (2004) A multibiomarker approach to environmental assessment. Environ Sci Technol 38:1723–1731. https://doi.org/10.1021/es030570
García-Carreño FL, Haard NF (1993) Characterization of proteinase classes in langostilla (Pleuroncodes planipes) and crayfish (Pacifastacus astacus) extracts. J Food Biochem 17:97–113. https://doi.org/10.1111/j.1745-4514.1993.tb00864.x
Geffard O, Ferrari B, Chaumot A, Montuelle B (2010) Les expérimentations in situ : principes et perspectives. Sci Eaux Territoires 1:20–25. https://doi.org/10.14758/SET-REVUE.2010.1.05
Gerhardt A (2000) Biomonitoring of polluted water: reviews on actual topics. Trans Tech, United-States
German DP, Horn MH, Gawlicka A (2004) Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol Biochem Zool 77:789–804. https://doi.org/10.1086/422228
Girao PM, Pereira da Silva EM, de Melo MP (2012) Dietary lycopene supplementation on Nile Tilapia (Oreochromis niloticus) juveniles submitted to confinement: effects on cortisol level and antioxidant response: dietary lycopene supplementation on Nile Tilapia. Aquac Res 43:789–798. https://doi.org/10.1111/j.1365-2109.2011.02890.x
Grosell M, Hansen HJ, Rosenkilde P (1998) Cu uptake, metabolism and elimination in fed and starved European eels (Anguilla anguilla) during adaptation to water-borne cu exposure. Comp Biochem Physiol C 120:295–305. https://doi.org/10.1016/S0742-8413(98)10009-9
Guderley H, Lapointe D, Bedard M, Dutil JD (2003) Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A 135:347–356. https://doi.org/10.1016/S1095-6433(03)00089-8
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Hani YMI, Marchand A, Turies C, Kerambrun E, Palluel O, Bado-Nilles A, Beaudouin R, Porcher JM, Geffard A, Dedourge-Geffard O (2018) Digestive enzymes and gut morphometric parameters of threespine stickleback (Gasterosteus aculeatus): influence of body size and temperature. PLoS One 13:e0194932. https://doi.org/10.1371/journal.pone.0194932
Henry M, Fountoulaki E (2014) Optimal dietary protein/lipid ratio for improved immune status of a newly cultivated Mediterranean fish species, the shi drum Umbrina cirrosa, L. Fish Shellfish Immunol 37:215–219. https://doi.org/10.1016/j.fsi.2014.02.005
Htun-Han M (1978) The reproductive biology of the dab Limanda limanda (L.) in the North Sea: seasonal changes in the ovary. J Fish Biol 13:351–359. https://doi.org/10.1111/j.1095-8649.1978.tb03445.x
Infante JZ, Cahu CL (1994) Influence of diet on pepsin and some pancreatic enzymes in sea bass (Dicentrarchus labrax) larvae. Comp Biochem Physiol A 109:209–212. https://doi.org/10.1016/0300-9629(94)90122-8
Javed M, Ahmad MI, Usmani N, Ahmad M (2017) Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water. Sci Rep 7:1675. https://doi.org/10.1038/s41598-017-01749-6
Junge W, Wortmann W, Wilke B, Waldenström J, Kurrle-Weittenhiller A, Finke J, Klein G (2001) Development and evaluation of assays for the determination of total and pancreatic amylase at 37 degrees C according to the principle recommended by the IFCC. Clin Biochem 34:607–615. https://doi.org/10.1016/S0009-9120(01)00278-8
Kenari AA, Naderi M (2016) Effects of enriched artemia by fish and soybean oils supplemented with vitamin E on growth performance, lipid peroxidation, lipase activity and fatty acid composition of Persian sturgeon (Acipenser persicus) larvae. Aquac Nutr 22:382–391. https://doi.org/10.1111/anu.12260
Kumar S, Tembre M (1998) Digestive system. In: Kumar S, Tembre M (eds) Anatomy and physiology of fishes. Vikas Pub. Housse Pvt, New Delhi, pp 56–76
Lacaze E, Devaux A, Mons R, Bony S, Garric J, Geffard A, Geffard O (2011) DNA damage in caged Gammarus fossarum amphipods: a tool for freshwater genotoxicity assessment. Environ Pollut 159:1682–1691. https://doi.org/10.1016/j.envpol.2011.02.038
Lall SP (2000) Nutrition and health of fish. In: Cruz -Suárez LE, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R (eds) Avances en Nutrición Acuícola V. Memorias del V Simposium Internacional de Nutrición Acuícola, Mexico, 19–22
Le Guernic A, Sanchez W, Bado-Nilles A, Palluel O, Turies C, Chadili E, Cavalié I, Delahaut L, Adam-Guillermin C, Porcher JM, Geffard A, Betoulle S, Gagnaire B (2016a) In situ effects of metal contamination from former uranium mining sites on the health of the three-spined stickleback (Gasterosteus aculeatus,L). Ecotoxicol 25:1234–1259. https://doi.org/10.1007/s10646-016-1677-z
Le Guernic A, Sanchez W, Palluel O, Bado-Nilles A, Turies C, Chadili E, Cavalié I, Adam-Guillermin C, Porcher JM, Geffard A, Betoulle S, Gagnaire B (2016b) In situ experiments to assess effects of constraints linked to caging on ecotoxicity biomarkers of the three-spined stickleback (Gasterosteus aculeatus L.). Fish Physiol Biochem 42:643–657. https://doi.org/10.1007/s10695-015-0166-2
Leloutre C, Péry ARR, Porcher JM, Beaudouin R (2016) A bioenergetics model of the entire life cycle of the three-spined stickleback, Gasterosteus aculeatus. Ecol Freshw Fish 27:116–127. https://doi.org/10.1111/eff.12329
Liao K, Meng R, Ran Z, Cheng G, Wang Y, Xu J, Xu S, Yan X (2017) Short-term starvation in silver pomfret (Pampus argenteus): molecular effects on lipid mobilization and utilization. Aquac Res 48:4874–4885. https://doi.org/10.1111/are.13307
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Morales AE, Perez-Jimenez A, Hidalgo MC, Abellan E, Cardenete G (2004) Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C 139:153–161. https://doi.org/10.1016/j.cca.2004.10.008
Morrow MD, Higgs D, Kennedy CJ (2004) The effects of diet composition and ration on biotransformation enzymes and stress parameters in rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol C 137:143–154. https://doi.org/10.1016/j.cca.2004.01.001
Nwani CD, Somdare PO, Ogueji EO, Nwani JC, Ukonze JA, Nwadinigwe AO (2017) Genotoxicity assessment and oxidative stress responses in freshwater African catfish Clarias gariepinus exposed to fenthion formulations. Drug Chem Toxicol 40:273–280. https://doi.org/10.1080/01480545.2016.1209772
OECD (2000) Fish, juvenile growth test. In: Eleventh addendum to the OECD guidelines for testing of chemicals. OECD publishing, Paris. https://doi.org/10.1787/9789264070202-en
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3
Oikari A (2006) Caging techniques for field exposures of fish to chemical contaminants. Aquat Toxicol 78:370–381. https://doi.org/10.1016/j.aquatox.2006.03.010
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Panteghini MMD, Bais R (2008) Enzymes. In: Tietz Fundamentals of Clinical Chemistry, Saunders ELSEVIER 6 ed. Burtis Carl A Ashwood Edward R and Bruns David E, pp 317–36
Paoletti F, Aldinucci D, Mocali A, Caparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541. https://doi.org/10.1016/0003-2697(86)90026-6
Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 145:191–199. https://doi.org/10.1016/S0009-2797(03)00002-4
Peakall DB, Walker CH (1994) The role of biomarkers in environmental assessment (3). Vertebrates Ecotoxicol 3:173–179. https://doi.org/10.1007/BF00117082
Peixoto MJ, Salas-Leiton E, Brito F, Pereira LF, Svendsen JC, Baptista T, Pereira R, Abreu H, Reis PA, Gonçalves JFM, Otavio R, de Almeida Ozorio RO (2017) Effects of dietary Gracilaria sp and Alaria sp supplementation on growth performance, metabolic rates and health in meagre (Argyrosomus regius) subjected to pathogen infection. J Appl Phycol 29:433–447. https://doi.org/10.1007/s10811-016-0917-1
Péres A, Infante JZ, Cahu CL (1998) Dietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 19:145–152
Pottinger TG, Carrick TR, Yeomans WE (2002) The three-spined stickleback as an environmental sentinel: effects of stressors on whole-body physiological indices. J Fish Biol 61:207–229. https://doi.org/10.1111/j.1095-8649.2002.tb01747.x
Quabius ES, Nolan DT, Segner H, Wendelaar Bonga SE (2001) Confinement stress and starvation modulate the induction of EROD activity after dietary exposure to PCB 126 in the Mozambique tilapia (Oreochromis mossambicus). Fish Physiol Biochem 25:109–119. https://doi.org/10.1023/A:1020590726262
Reimer G (1982) The influence of diet on the digestive enzymes of the Amazon fish Matrincha, Brycon cf. melanopterus. J Fish Biol 21:637–642. https://doi.org/10.1111/j.1095-8649.1982.tb02867.x
Sanchez W, Palluel O, Meunier L, Coquery M, Porcher JM, Aït-Aïssa S (2005) Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183. https://doi.org/10.1016/j.etap.2004.07.003
Sanchez W, Aït-Aïssa S, Palluel O, Ditche JM, Porcher JM (2007) Preliminary investigation of multi-biomarker responses in three-spined stickleback (Gasterosteus aculeatus L.) sampled in contaminated streams. Ecotoxicol 16:279–287. https://doi.org/10.1007/s10646-006-0131-z
Sanchez W, Katsiadaki I, Piccini B, Ditche JM, Porcher JM (2008a) Biomarker responses in wild three-spined stickleback (Gasterosteus aculeatus L.) as a useful tool for freshwater biomonitoring: a multiparametric approach. Environ Int 34:490–498. https://doi.org/10.1016/j.envint.2007.11.003
Sanchez W, Piccini B, Porcher JM (2008b) Effect of prochloraz fungicide on biotransformation enzymes and oxidative stress parameters in three-spined stickleback (Gasterosteus aculeatus L.). J Environ Sci Health B 43:65–70. https://doi.org/10.1080/03601230701735151
Sanz A, Furne M, Trenzado CE, de Haro C, Sanchez-Muros MJ (2012) Study of the oxidative state, as a marker of welfare, on Gilthead Sea bream, Sparus aurata, subjected to handling stress. J World Aquacult Soc 43:707–715. https://doi.org/10.1111/j.1749-7345.2012.00602.x
Sesay DF, Habte-Tsion HM, Zhou Q, Ren M, Xie J, Liu B, Chen R, Pan L (2016) Effects of dietary folic acid on the growth, digestive enzyme activity, immune response and antioxidant enzyme activity of blunt snout bream (Megalobrama amblycephala) fingerling. Aquacutlure 452:142–150. https://doi.org/10.1016/j.aquaculture.2015.10.026
Shiu YL, Lin HL, Chi CC, Yeh SP, Liu CH (2016) Effects of hirami lemon, Citrus depressa Hayata, leaf meal in diets on the immune response and disease resistance of juvenile barramundi, Lates calcarifer (bloch), against Aeromonas hydrophila. Fish Shellfish Immunol 55:332–338. https://doi.org/10.1016/j.fsi.2016.06.001
Silva FCP, Nicoli JR, Zambonino-Infante JL, Le Gall MM, Kaushik S, Gatesoupe FJ (2010) Influence of partial substitution of dietary fish meal on the activity of digestive enzymes in the intestinal brush border membrane of gilthead sea bream, Sparus aurata and goldfish, Carassius auratus. Aquaculture 306:233–237. https://doi.org/10.1016/j.aquaculture.2010.05.018
Slooff W, Van Kreijl CF, Baars AJ (1983) Relative liver weights and xenobiotic-metabolizing enzymes of fish from polluted surface waters in the Netherlands. Aquat Toxicol 4:1–14. https://doi.org/10.1016/0166-445X(83)90057-7
Stancova V, Plhalova L, Blahova J, Zivna D, Bartoskova M, Siroka Z, Marsalek P, Svobodova Z (2017) Effects of the pharmaceutical contaminants ibuprofen, diclofenac, and carbamazepine alone, and in combination, on oxidative stress parameters in early life stages of tench (Tinca tinca). Vet Med 62:90–97. https://doi.org/10.17221/125/2016-VETMED
Stepić S, Hackenberger BK, Hackenberger DK, Velki M, Lončarić Ž (2012) Impact of oxidative stress indicated by thiobarbituric acid reactive substances (TBARS) and protein carbonyl levels (PC) on ethoxyresorufin-O-DEETHYLASE (EROD) induction in common carp (Cyprinus carpio). Water Air Soil Pollut 223:4785–4793. https://doi.org/10.1007/s11270-012-1234-1
Sturve J, Hultman MT, Wassmur B, Almroth BC (2017) Determining oxidative stress and EROD activity in dab (Limanda limanda) in the north and Baltic Seas. Mar Environ Res 124:46–53. https://doi.org/10.1016/j.marenvres.2016.10.008
Trevisan R, Uliano-Silva M, Franco JL, Posser T, Hoppe R, Farina M, Bainy AC, Dafre AL (2013) Confinement during field studies may jeopardize antioxidant and physiological responses of Nile tilapia to contaminants. Mar Environ Res 91:97–103. https://doi.org/10.1016/j.marenvres.2013.07.005
Turja R, Lehtonen KK, Meierjohann A, Brozinski JM, Vahtera E, Soirinsuo A, Sokolov A, Snoeijs P, Budzinski H, Devier MH, Peluhet L, Paakkonen JP, Viitasalo M, Kronberg L (2015) The mussel caging approach in assessing biological effects of wastewater treatment plant discharges in the Gulf of Finland (Baltic Sea). Mar Pollut Bull 97:135–149. https://doi.org/10.1016/j.marpolbul.2015.06.024
Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Vandeputte C, Guizon I, Genestie-Denis I, Vannier B, Lorenzon G (1994) A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol Toxicol 10:415–421. https://doi.org/10.1007/BF00755791
Vieira CED, Costa PG, Cabrera LC, Primel EG, Fillmann G, Bianchini A, Bueno Dos Reis Martinez C (2017) A comparative approach using biomarkers in feral and caged neotropical fish: implications for biomonitoring freshwater ecosystems in agricultural areas. Sci Total Environ 586:598–609. https://doi.org/10.1016/j.scitotenv.2017.02.026
Viganò L, Arillo A, Bagnasco M, Bennicelli C, Melodia F (1993) Xenobiotic metabolizing enzymes in uninduced and induced rainbow trout (Oncorhynchus mykiss): effects of diets and food deprivation. Comp Biochem Physiol C 104:51–55. https://doi.org/10.1016/0742-8413(93)90110-7
Villarreal F, Falisse E, Morin D, Buckpitt A, Kültz D (2012) Effect of naphthalene and copper nanoparticles on three-spined stickleback (Gasterosteus aculeatus). FASEB J 26(1_supplement):833.13
Wootton RJ (1976) The biology of the sticklebacks. Academic Press, Cambridge
Wootton RJ (1984) A functional biology of sticklebacks. University of California Press, Berkeley
Wootton RJ (1994) Energy allocation in the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University, United-States, pp p114–p140
Yengkokpam S, Debnath D, Pal AK, Sahu NP, Jain KK, Norouzitallab P, Baruah K (2013) Short-term periodic feed deprivation in Labeo rohita fingerlings: effect on the activities of digestive, metabolic and anti-oxidative enzymes. Aquaculture 412–413:186–192. https://doi.org/10.1016/j.aquaculture.2013.07.025
Zeyl JN, Love OP, Higgs DM (2014) Evaluating gonadosomatic index as an estimator of reproductive condition in the invasive round goby, Neogobius melanostomus. J Great Lakes Res 40:164–171. https://doi.org/10.1016/j.jglr.2013.12.004
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The authors are grateful to Ms. Felicity Mc Callum for native English reviewing of this paper.
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This work was financially supported by the ecotoxicology research program of the French Ministry in charge of the environment (P190) and the European Regional Development Fund (ERDF).
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Catteau, A., Le Guernic, A., Marchand, A. et al. Impact of confinement and food access restriction on the three-spined stickleback (Gasterosteus aculeatus, L.) during caging: a multi-biomarker approach. Fish Physiol Biochem 45, 1261–1276 (2019). https://doi.org/10.1007/s10695-019-00670-1
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DOI: https://doi.org/10.1007/s10695-019-00670-1