Abstract
Mangrove crabs are ecosystem engineers through their bioturbation activity. On Mayotte Island, the abundance of Neosarmatium africanum decreased in wastewater-impacted areas. Previous analyses showed that global crab metabolism is impacted by wastewater, with a burst in O2 consumption that may be caused by osmo-respiratory trade-offs since gill functioning was impacted. As the hepatopancreas is a key metabolic organ, the purpose of this study was to investigate the physiological effects of wastewater and ammonia-N 5-h exposure on crabs to better understand the potential trade-offs underlying the global metabolic state. Catalase, superoxide dismutase, glutathione S-transferase, total digestive protease, and serine protease (trypsin and chymotrypsin) activities were assessed. Histological analyses were performed to determine structural modifications. No effect of short-term wastewater and ammonia-N exposure was found in antioxidant defenses or digestive enzyme activity. However, histological changes of B-cells indicate an increase in intracellular digestive activity through higher vacuolization processes and tubule dilation in wastewater-exposed crabs.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Ahearn GA, Mandal PK, Mandal A (2004) Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. J Comp Physiol B Biochem Syst Environ Physiol 174. https://doi.org/10.1007/s00360-004-0438-0
Al-Mohanna SY, Nott JA (1989) Functional cytology of the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) during the moult cycle. Mar Biol 101:535–544. https://doi.org/10.1007/BF00541656
Amaral V, Penha-Lopes G, Paula J (2009) Effects of vegetation and sewage load on mangrove crab condition using experimental mesocosms. Estuar Coast Shelf Sci 84:300–304. https://doi.org/10.1016/j.ecss.2009.07.007
Andreetta A, Fusi M, Cameldi I, Cimò F, Carnicelli S, Cannicci S (2014) Mangrove carbon sink. Do burrowing crabs contribute to sediment carbon storage? Evidence from a Kenyan mangrove system. J Sea Res 85:524–533. https://doi.org/10.1016/j.seares.2013.08.010
Barbieri E (2010) Acute toxicity of ammonia in white shrimp (Litopenaeus schmitti) (Burkenroad, 1936, Crustacea) at different salinity levels. Aquaculture 306:329–333. https://doi.org/10.1016/j.aquaculture.2010.06.009
Barbieri E, Doi SA (2011) The effects of different temperature and salinity levels on the acute toxicity of zinc in the Pink Shrimp (Farfantepenaeus paulensis). Mar Freshw Behav Physiol 44:251–263. https://doi.org/10.1080/10236244.2011.617606
Barbieri E, Bondioli ACV, de Melo CB, Henriques MB (2016) Nitrite toxicity to Litopenaeus schmitti (Burkenroad, 1936, Crustacea) at different salinity levels. Aquac Res 47:1260–1268. https://doi.org/10.1111/are.12583
Bautista MN, Lavilla-Pitogo CR, Subosa PF, Begino ET (1994) Aflatoxin B1 contamination of shrimp feeds and its effect on growth and hepatopancreas of pre-adult Penaeus monodon. J Sci Food Agric 65:5–11. https://doi.org/10.1002/jsfa.2740650103
Bermudes M, Ritar AJ (2008) Tolerance for ammonia in early stage spiny lobster (Jasus edwardsii) phyllosoma larvae. J Crustac Biol 28:695–699. https://doi.org/10.1651/08-2994.1
Berti R, Cannicci S, Fabbroni S, Innocenti G (2008) Notes on the structure and the use of Neosarmatium meinerti and Cardisoma carnifex burrows in a kenyan mangrove swamp (decapoda brachyura). Ethol Ecol Evol 20:101–113. https://doi.org/10.1080/08927014.2008.9522531
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
Bright DB, Hogue CL (1972) A synopsis of the burrowing land crabs of the world and list of their arthropod symbionts and burrow associates. Contrib Sci 220:60
Cannicci S, Burrows D, Fratini S, Smith TJ, Offenberg J, Dahdouh-Guebas F (2008) Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquat Bot 89:186–200. https://doi.org/10.1016/j.aquabot.2008.01.009
Cannicci S, Bartolini F, Dahdouh-Guebas F, Fratini S, Litulo C, Macia A, Mrabu EJ, Penha-Lopes G, Paula J (2009) Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa. Estuar Coast Shelf Sci 84:305–317. https://doi.org/10.1016/j.ecss.2009.04.021
Capdeville C (2018) Evaluation des capacités de résistance et de résilience de l’écosystème mangrove en réponse à des apports d’eaux usées domestiques prétraitées, PHD Toulouse Université Paul Sabatier
Capdeville C, Abdallah K, Buffan-Dubau E, Lin C, Azemar F, Lambs L, Fromard F, Rols JL, Leflaive J (2018) Limited impact of several years of pretreated wastewater discharge on fauna and vegetation in a mangrove ecosystem. Mar Pollut Bull 129:379–391. https://doi.org/10.1016/j.marpolbul.2018.02.035
Capdeville C, Abdallah K, Walcker R, Rols JL, Fromard F, Leflaive J (2019) Contrasted resistance and resilience of two mangrove forests after exposure to long-term and short-term anthropic disturbances. Mar Environ Res 146:12–23. https://doi.org/10.1016/j.marenvres.2019.03.002
Ceccaldi HJ (1998) A synopsis of the morphology and physiology of the digestive system of some crustacean species studied in France. Rev Fish Sci 6:13–39. https://doi.org/10.1080/10641269891314177
Chapman MG, Tolhurst TJ (2004) The relationship between invertebrate assemblages and bio-dependant properties of sediment in urbanized temperate mangrove forests. J Exp Mar Biol Ecol 304:51–73. https://doi.org/10.1016/j.jembe.2003.11.019
Clough BF, Boto KG, Attiwill PM (1983) Mangroves and sewage: a re-evaluation. Springer, Dordrecht, pp 151–161. https://doi.org/10.1007/978-94-017-0914-9_17
Copeland DE, Fitzjarrell AT (1968) The salt absorbing cells in the gills of the blue crab (Callinectes sapidus rathbun) with notes on modified mitochondria. Z Zellforsch Mikrosk Anat 92:1–22. https://doi.org/10.1007/BF00339398
Correia, A.D., Costa, M.H., Luis, O.J., Livingstone, D.R., 2003. Age-related changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in whole body Gammarus locusta (Crustacea : Amphipoda) 289, 83–101. https://doi.org/10.1016/S0022-0981(03)00040-6
Dall W, Moriarty DJW (1983) Functional aspects of nutrition and digestion. In: Mantel LH (ed) The biology of Crustacea. Vol. 5. Internal anatomy and physiological regulation. Academic Press, New York, pp 215–216 http://hdl.handle.net/102.100.100/286167?index=1
Das S, Tseng LC, Chou C, Wang L, Souissi S, Hwang JS (2019) Effects of cadmium exposure on antioxidant enzymes and histological changes in the mud shrimp Austinogebia edulis (Crustacea: Decapoda). Environ Sci Pollut Res 26:7752–7762. https://doi.org/10.1007/s11356-018-04113-x
De Coen WM, Janssen CR, Giesy JP (2000) Biomarker applications in ecotoxicology: bridging the gap between toxicology and ecology. New Microbiotests Routine Toxic Screen Biomonitoring:13–25. https://doi.org/10.1007/978-1-4615-4289-6_2
De Freitas Rebelo M, Rodriguez EM, Santos EA, Ansaldo M (2000) Histopathological changes in gills of the estuarine crab Chasmagnathus granulata (Crustacea-Decapoda) following acute exposure to ammonia. Comp Biochem Physiol - C Pharmacol Toxicol Endocrinol 125:157–164. https://doi.org/10.1016/S0742-8413(99)00093-6
de Melo MS, dos Santos TPG, Jaramillo M, Nezzi L, Rauh Muller YM, Nazari EM (2019) Histopathological and ultrastructural indices for the assessment of glyphosate-based herbicide cytotoxicity in decapod crustacean hepatopancreas. Aquat Toxicol 210:207–214. https://doi.org/10.1016/j.aquatox.2019.03.007
Dedourge-Geffard O, Charron L, Hofbauer C, Gaillet V, Palais F, Lacaze E, Geffard A, Geffard O (2013) Temporal patterns of digestive enzyme activities and feeding rate in gammarids (Gammarus fossarum) exposed to inland polluted waters. Ecotoxicol Environ Saf 97:139–146. https://doi.org/10.1016/j.ecoenv.2013.07.016
Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvořák J, Hsieh I, Bahgat M, Dissous C, McKerrow JH (2006) A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem 281:39316–39329. https://doi.org/10.1074/jbc.M607128200
Dittmann S (1996) Effects of macrobenthic burrows on infaunal communities in tropical tidal flats. Mar Ecol Prog Ser 134:119–130. https://doi.org/10.3354/meps134119
Fusi M, Babbini S, Giomi F, Fratini S, Daniele FD, Christopher D, Mcquaid D, Porri F, Cannicci S (2017) Thermal sensitivity of the crab Neosarmatium africanum in tropical and temperate mangroves on the east coast of Africa. Hydrobiologia. 803:251–263. https://doi.org/10.1007/s10750-017-3151-1
García-Carreño FL, Hernández-Cortés MP, Haard NF (1994) Enzymes with peptidase and proteinase activity from the digestive systems of a freshwater and a marine decapod. J Agric Food Chem 42:1456–1461. https://doi.org/10.1021/jf00043a013
Garçon DP, Masui DC, Mantelatto FLM, McNamara JC, Furriel RPM, Leone FA (2007) K+ and NH4+ modulate gill (Na+, K+)-ATPase activity in the blue crab, Callinectes ornatus: fine tuning of ammonia excretion. Comp Biochem Physiol - A Mol Integr Physiol 147:145–155. https://doi.org/10.1016/j.cbpa.2006.12.020
Gibson R, Barker PL (1979) The decapod hepatopancreas. Oceanogr Mar Biol Annu Rev 17:285–346
Giddins RL, Lucas JS, Neilson MJ, Richards GN (1986) Feeding ecology of the mangrove crab Neosarmatium smithi (Crustacea: Decapoda: Sesarmidae). Mar Ecol Prog Ser 33:147e155
Gillikin DP, de Grave S, Tack JF (2003) The occurrence of the semi-terrestrial shrimp Merguia oligodon (De Man, 1888) in Neosarmatium smithi H. Milne Edwards, 1853 burrows in Kenyan mangroves. Crustaceana 74:505–507. https://doi.org/10.1163/156854001750243081
Gross WJ, Lasiewski RC, Dennis M, Rudy P (1966) Salt and water balance in selected crabs of Madagascar. Comp Biochem Physiol 17:641–660. https://doi.org/10.1016/0010-406X(66)90594-9
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Harada Y, Lee SY (2016) Foraging behavior of the mangrove sesarmid crab Neosarmatium trispinosum enhances food intake and nutrient retention in a low-quality food environment. Estuar Coast Shelf Sci 174:41–48. https://doi.org/10.1016/j.ecss.2016.03.017
Hastings A, Higgins K (1994) Persistence of transients in spatially structured ecological models. Science 263:1133–1136. https://doi.org/10.1126/science.263.5150.1133
Haywood GP (1983) Ammonia toxicity in teleost fishes: a review. Canadian Technical Report of Fisheries and Aquatic Sciences
Herteman M (2010) Evaluation des capacités bioremédiatrices d’une mangrove impactée par des eaux usées domestiques. Application au site pilote de Malamani, Mayotte. PHD Toulouse Université Paul Sabatier
Hoffmann AA, Hercus MJ (2000) Environmental stress as an evolutionary force. Bioscience 50:217–226
Hogarth PJ (2015) The biology of mangroves and seagrasses, 3rd edn. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198716549.001.0001
Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1665–1679
Jeanson M, Dolique F, Anthony EJ, Aubry A (2019) Decadal-scale dynamics and morphological evolution of mangroves and beaches in a reef-lagoon complex, Mayotte Island. J Coast Res 88:195–208. https://doi.org/10.2112/SI88-015.1
Kristensen E (2008) Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. J Sea Res 59:30–43. https://doi.org/10.1016/j.seares.2007.05.004
Laue M, Kiefer G, Leis B, Pütz N, Mestres P (2005) Use of environmental scanning electron microscopy to study a resin block face. Microsc Anal 19:17–19
Lee SY (1997) Potential trophic importance of the faecal material of the mangrove sesarmine crab Sesarma messa. Mar Ecol Prog Ser 159:275–284. https://doi.org/10.3354/meps159275
Lee SY (2008) Mangrove macrobenthos: assemblages, services, and linkages. J Sea Res 59:16–29. https://doi.org/10.1016/j.seares.2007.05.002
Lehnert SA, Johnson SE (2002) Expression of hemocyanin and digestive enzyme messenger RNAs in the hepatopancreas of the black tiger shrimp Penaeus monodon. Comp Biochem Physiol B Biochem Mol Biol 133:163–171. https://doi.org/10.1016/S1096-4959(02)00123-9
Lemarié G, Dosdat A, Covès D, Dutto G, Gasset E, Person-Le Ruyet J (2004) Effect of chronic ammonia exposure on growth of European seabass (Dicentrarchus labrax) juveniles. Aquaculture 229:479–491. https://doi.org/10.1016/S0044-8486(03)00392-2
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001
Li E, Chen L, Zeng C, Yu N, Xiong Z, Chen X, Qin JG (2008) Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture 274:80–86. https://doi.org/10.1016/j.aquaculture.2007.11.001
Liu Y, Sui YP, Wang JX, Zhao XF (2009) Characterization of the trypsin-like protease (Ha-TLP2) constitutively expressed in the integument of the cotton bollworm, Helicoverpa armigera. Arch Insect Biochem Physiol 72:74–87. https://doi.org/10.1002/arch.20324
Livingstone DR, Lips F, Martinez PG, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Biol 112:265–276. https://doi.org/10.1007/BF00702471
Macnae W, Kalk M (1962) The ecology of the mangrove swamps at Inhaca Island, Mocambique. J Ecol 50:19. https://doi.org/10.2307/2257188
Martínez-Alarcón D, Saborowski R, Rojo-Arreola L, García-Carreño F (2018) Is digestive cathepsin D the rule in decapod crustaceans? Comp Biochem Physiol Part - B Biochem Mol Biol 215:31–38. https://doi.org/10.1016/j.cbpb.2017.09.006
Martoja R, Martoja-Pierson M (1967) Initiation aux techniques de l’histologie animale. Eds Masson cie, Paris, p 343
McCord JM, Fridovich I (1969) An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
Micheli F, Gherardi F, Vannini M (1991) Feeding and burrowing ecology of two East African mangrove crabs. Mar Biol 111:247–254. https://doi.org/10.1007/BF01319706
Munkittrick KR, McCarty LS (1995) An integrated approach to aquatic ecosystem health: top-down, bottom-up or middle-out? J Aquat Ecosyst Health 4:77–90. https://doi.org/10.1007/BF00044791
Neufeld GJ, Holliday CW, Pritchard JB (1980) Salinity adaption of gill Na, K-ATPase in the blue crab, Callinectes sapidus. J Exp Zool 211:215–224. https://doi.org/10.1002/jez.1402110210
Nobbs M, Blamires SJ (2017) Fiddler crab spatial distributions are influenced by physiological stressors independent of sympatric interactions. J Exp Mar Biol Ecol 491:19–26. https://doi.org/10.1016/j.jembe.2017.03.007
Nott JA, Corner EDS, Marvin LJ, O’Hara SCM (1985) Cyclical contributions of the digestive epithelium to faecal pellet formation by the copepod Calanus helgolandicus. Mar Biol 89:271–279. https://doi.org/10.1007/BF00393661
Nunez-Nogueira G, Mouneyrac C, Amiard JC, Rainbow PS (2006) Subcellular distribution of zinc and cadmium in the hepatopancreas and gills of the decapod crustacean Penaeus indicus. Mar Biol 150:197–211. https://doi.org/10.1007/s00227-006-0350-0
Ortega P, Santos RA, Lacouth P, Rozas EE, Custódio MR, Zanotto FP (2014) Cytochemical characterization of gill and hepatopancreatic cells of the crab Ucides cordatus (Crustacea, Brachyura) validated by cell metal transport. Iheringia Série Zoologia 104(3):347–354. https://doi.org/10.1590/1678-476620141043347354
Ouyang X, Guo F (2016) Paradigms of mangroves in treatment of anthropogenic wastewater pollution. Sci Total Environ 544:971–979. https://doi.org/10.1016/j.scitotenv.2015.12.013
Ouyang X, Guo F (2018) Intuitionistic fuzzy analytical hierarchical processes for selecting the paradigms of mangroves in municipal wastewater treatment. Chemosphere 197:634–642. https://doi.org/10.1016/j.chemosphere.2017.12.102
Ragionieri L, Fratini S, Schubart CD (2012) Revision of the Neosarmatium meinerti species complex (Decapoda: Brachyura: Sesarmidae), with descriptions of three pseudocryptic Indo–West Pacific species. Raffles Bull Zool 60:71–87
Raunkjær K, Hvitved-Jacobsen T, Nielsen PH (1994) Measurement of pools of protein, carbohydrate and lipid in domestic wastewater. Water Res 28:251–262. https://doi.org/10.1016/0043-1354(94)90261-5
Ravndal KT, Opsahl E, Bagi A, Kommedal R (2018) Wastewater characterisation by combining size fractionation, chemical composition and biodegradability. Water Res 131:151–160. https://doi.org/10.1016/j.watres.2017.12.034
Reid DG, Abelló P, Kaiser MJ, Warman CG (1997) Carapace colour, inter-moult duration and the behavioural and physiological ecology of the shore crab Carcinus maenas. Estuar Coast Shelf Sci 44:203–211. https://doi.org/10.1006/ecss.1996.0212
Ren Q, Pan L, Zhao Q, Si L (2015) Ammonia and urea excretion in the swimming crab Portunus trituberculatus exposed to elevated ambient ammonia-N. Comp Biochem Physiol -Part A Mol Integr Physiol 187:48–54. https://doi.org/10.1016/j.cbpa.2015.04.013
Rezende EL, Castañeda LE, Santos M, Fox C (2014) Tolerance landscapes in thermal ecology. Functional Ecology 28:799–809
Rodrigues ET, Pardal MÂ (2014) The crab Carcinus maenas as a suitable experimental model in ecotoxicology. 70:158–182. https://doi.org/10.1016/j.envint.2014.05.018
Romano N, Zeng C (2013) Toxic effects of ammonia, nitrite, and nitrate to decapod crustaceans: a review on factors influencing their toxicity, physiological consequences, and coping mechanisms. Rev Fish Sci 21:1–21. https://doi.org/10.1080/10641262.2012.753404
Rosas C, Bolongaro-Crevenna A, Sanchez A, Gaxiola G, Soto L, Escobar E (1995) Role of digestive gland in the energetic metabolism of Penaeus setiferus. Biol Bull 189:168–174. https://doi.org/10.2307/1542467
Saborowski R, Buchholz F (1999) A laboratory study on digestive processes in the Antarctic krill, Euphausia superba, with special regard to chitinolytic enzymes. Polar Biol 21:295–304. https://doi.org/10.1007/s003000050365
Sainz JC, García-Carreño FL, Córdova-Murueta JH, Cruz-Hernández P (2005) Whiteleg shrimp (Litopenaeus vannamei, Boone, 1931) isotrypsins: their genotype and modulation. J Exp Mar Biol Ecol 326:105–113. https://doi.org/10.1016/j.jembe.2005.05.021
Santos DB, Barbieri E, Bondioli ACV, De Melo CB (2014) Effects of lead in white shrimp (Litopenaeus schmitti) metabolism regarding salinity. Mundo da Saude 38:16–23. https://doi.org/10.15343/0104-7809.20143801016023
Seebaugh DR, L’Amoreaux WJ, Wallace WG (2011) Digestive toxicity in grass shrimp collected along an impact gradient. Aquat Toxicol 105:609–617. https://doi.org/10.1016/j.aquatox.2011.08.015
Sherman E (2015) Can sea urchins beat the heat? Sea urchins, thermal tolerance and climate change. PeerJ 3:e1006. https://doi.org/10.7717/peerj.1006
Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295. https://doi.org/10.1113/expphysiol.1997.sp004024
Sreeram MP, Menon NR (2005) Histopathological changes in the hepatopancreas of the penaeid shrimp Metapenaeus dobsoni exposed to petroleum hydrocarbons. J Mar Biol Assoc India 47:160–168
Tam NFY, Wong YS (1995) Mangrove soils as sinks for wastewater-borne pollutants. Hydrobiologia 295:231–241. https://doi.org/10.1007/BF00029130
Tam NFY, Wong YS (1996) Retention of wastewater-borne nitrogen and phosphorus in mangrove soils. Environ Technol (United Kingdom) 17:851–859. https://doi.org/10.1080/09593331708616453
Theuerkauff D (2018) http://www.theses.fr. Effets des rejets d’eaux usées domestiques sur la physiologie et l’écologie des crabes de mangrove, Sesarmidae et Ocypodidae, PHD Université de Montpellier, Mayotte
Theuerkauff D, Rivera-Ingraham GA, Mercky Y, Lejeune M, Lignot JH, Sucré E (2018a) Effects of domestic effluent discharges on mangrove crab physiology: integrated energetic, osmoregulatory and redox balances of a key engineer species. Aquat Toxicol 196:90–103. https://doi.org/10.1016/j.aquatox.2018.01.003
Theuerkauff D, Rivera-Ingraham GA, Roques JAC, Bertini M, Lejeune M, Farcy E, Lignot J (2018b) Salinity variation in a mangrove ecosystem : a physiological investigation to assess potential consequences of salinity disturbances on mangrove crabs. Zool Stud 57:1–16. https://doi.org/10.6620/ZS.2018.57-36
Theuerkauff D, Rivera-Ingraham GA, Lambert S, Mercky Y, Lejeune M, Lignot JH, Sucré E (2020) Wastewater bioremediation by mangrove ecosystems impacts crab ecophysiology: In-situ caging experiment. Aquat Toxicol 218. https://doi.org/10.1016/j.aquatox.2019.105358
van Oosterom J, Codi King S, Negri A, Humphrey C, Mondon J (2010) Investigation of the mud crab (Scylla serrata) as a potential bio-monitoring species for tropical coastal marine environments of Australia. Mar Pollut Bull 60:283–290. https://doi.org/10.1016/j.marpolbul.2009.09.007
Van Wormhoudt A, Bourreau G, Le Moullac G (1995) Amylase polymorphism in crustacea decapoda: electrophoretic and immunological studies. Biochem Syst Ecol 23:139–149. https://doi.org/10.1016/0305-1978(94)00090-4
Verbost PM, Van Rooij J, Flik G, Lock RAC, Wendelaar Bonga SE (1989) The movement of cadmium through freshwater trout branchial epithelium and its interference with calcium transport. J Exp Biol 145:185–197
Vogt G (1993) Differentiation of B-cells in the hepatopancreas of the prawn Penaeus monodon. Acta Zool 74:51–60. https://doi.org/10.1111/j.1463-6395.1993.tb01220.x
Vogt G (1994) Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology 114:83–101. https://doi.org/10.1007/BF00396642
Vogt G (2019) Functional cytology of the hepatopancreas of decapod crustaceans. J Morphol 280:1405–1444. https://doi.org/10.1002/jmor.21040
Vogt G, Stöcker W, Storch V, Zwilling R (1989) Biosynthesis of Astacus protease, a digestive enzyme from crayfish. Histochemistry 91:373–381. https://doi.org/10.1007/BF00493824
Wang L, Yan B, Liu N, Li Y, Wang Q (2008) Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense. Chemosphere 74:51–56. https://doi.org/10.1016/j.chemosphere.2008.09.025
Warren JH, Underwood AJ (1986) Effects of burrowing crabs on the topography of mangrove swamps in New South Wales. J Exp Mar Biol Ecol 102:223–235. https://doi.org/10.1016/0022-0981(86)90178-4
Weihrauch D, Morris S, Towle DW (2004) Ammonia excretion in aquatic and terrestrial crabs. J Exp Biol 207:4491–4504. https://doi.org/10.1242/jeb.01308
Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G, Moritz C (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLoS Biology 6:e325
Wong YS, Lan CY, Chen GZ, Li SH, Chen XR, Liu ZP, Tam NFY (1995) Effect of wastewater discharge on nutrient contamination of mangrove soils and plants. Hydrobiologia 295:243–254. https://doi.org/10.1007/BF00029131
Wong YS, Tam NFY, Lan CY (1997) Mangrove wetlands as wastewater treatment facility: a field trial. Hydrobiologia 352:49–59. https://doi.org/10.1007/978-94-011-5234-1_6
Zilli L, Schiavone R, Scordella G, Zonno V, Verri T, Storelli C, Vilella S (2003) Changes in cell type composition and enzymatic activities in the hepatopancreas of Marsupenaeus japonicus during the moulting cycle. J Comp Physiol B Biochem Syst Environ Physiol 173:355–363. https://doi.org/10.1007/s00360-003-0348-6
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The authors are thankful to the Syndicat Intercommunal d'Eau et d'Assainissement de Mayotte (SIEAM), and especially to Kissimati Abdallah for her help in the field.
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ES, JHL, and GR contributed to the study conceptualization and design, and supervised the research. Experimental design, material preparation, and data collection were performed by DT. DT and LM performed the assessment of antioxidant enzyme activities. DM performed the assessment of digestive enzymes activities and the pretreatment of the outcome data. ML realized the cut sections and staining of the hepatopancreas tubules. LM analyzed the histological sections and the outcomes of the antioxidant enzymes activities and realized the statistical analyses of the manuscript dataset. The first draft of the manuscript was written by LM, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Mégevand, L., Martínez-Alarcón, D., Theuerkauff, D. et al. The hepatopancreas of the mangrove crab Neosarmatium africanum: a possible key to understanding the effects of wastewater exposure (Mayotte Island, Indian Ocean). Environ Sci Pollut Res 28, 60649–60662 (2021). https://doi.org/10.1007/s11356-021-14892-5
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DOI: https://doi.org/10.1007/s11356-021-14892-5