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Acrosome Reaction of Sperm in the Mud Crab Scylla serrata as a Sensitive Toxicity Test for Metal Exposures

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Abstract

In order to test the sensitivity of the sperm cell of the mud crab Scylla serrata to heavy metals, the toxic effects of Ag+, Cd2+, Cu2+, and Zn2+ on the acrosome reaction (AR) were studied by artificially inducing the AR of sperm exposed to heavy metals, counting the AR rates by light microscopy, and observing structural changes in sperm by transmission electron microscopy. The AR in S. serrata occurs at two stages. The first stage (ARI) is the eversion of the subacrosomal material. The second stage (ARII) is the ejection of the acrosomal filament. The results showed the EC50 values of the AR based on (ARI + ARII)% for Ag+, Cd2+, Cu2+, and Zn2+ were 10.02, 2.14, 13.69, and 2.21 μg/L, and the EC50 values based on ARII % of Ag+, Cd2+, Cu2+, and Zn2+ were 1.96, 0.20, 1.46, and 0.34 μg/L. The order of toxicity is Cd2+ > Zn2+ > Cu2+ > Ag+ based on the percentage of reacted sperm at the second stage. Sperm cells exposed to heavy metals showed an increased rate of swelling, shape irregularities, and the acrosomal filament of some sperm cells was, crooked, ruptured, and even dissolved. The AR of the sperm cell from S. serrata is more sensitive to the tested heavy metals compared to sea urchin sperm cell toxicity tests.

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References

  • Alfaro J, Muñoz N, Vargas M, Komen J (2003) Induction of sperm activation in open and closed thelycum penaeoid shrimps. Aquaculture 216:371–381

    Article  Google Scholar 

  • Alfaro J, Ulate K, Vargas M (2007) Sperm maturation and capacitation in the open thelycum shrimp Litopenaeus (Crustacea: Decapoda: Penaeoidea). Aquaculture 270:436–442

    Article  Google Scholar 

  • Anderson BS, Middaugh DP, Hunt JW, Turpen SL (1991) Copper toxicity to sperm, embryos and larvae of topsmelt Atherinops affinis, with notes on induced spawning. Mar Environ Res 31:17–35. doi:10.1016/0141-1136(91)90003-Q

    Article  CAS  Google Scholar 

  • Au DWT, Chiang MWL, Wu RSS (2000) Effects of cadmium and phenol on motility and ultrastructure of sea urchin and mussel spermatozoa. Arch Environ Contam Toxicol 38:455–463. doi:10.1007/s002449910060

    Article  CAS  Google Scholar 

  • Bhavanishankar S, Subramoniam T (1997) Cryopreservation of spermatozoa of edible mud crab Scylla serrata (Forskal). J Exp Zool 277:326–336. doi:10.1002/(SICI)1097-010X(19970301)277:4<326::AID-JEZ6>3.0.CO;2-R

    Article  CAS  Google Scholar 

  • Burgess RM, Schweitzer KA, McKinney RA, Phelps DK (1993) Contaminated marine sediments, water column and interstitial toxic effects. Environ Toxicol Chem 12:127–138. doi:10.1897/1552-8618(1993)12[127:CMSWCA]2.0.CO;2

    Article  CAS  Google Scholar 

  • Castagna A, Sinatra F, Scalia M, Capodicasa V (1981) Observations of the effect of zinc on the gametes and various development phases of Arbacia lixula. Mar Biol 64:285–289

    CAS  Google Scholar 

  • Chapman GA (1995) Sea urchin sperm cell test. In: Rand GM (ed) Fundamentals of aquatic toxicology effects: environmental fate and risk assessment, 2nd edn. Taylor & Francis, Philadelphia, pp 189–205

    Google Scholar 

  • Clark WH, Griffin FJ (1988) The morphology and physiology of the acrosome reaction in the sperm of the decapod, Sicyonia ingentis. Dev Growth Differ 30:451–462

    Article  Google Scholar 

  • Clark WH Jr, Yudin AI, Griffin FJ, Shigekawa K (1984) The control of gamete activation and fertilization in the marine penaeidae, Sicyonia ingentis. In: Engels W, Clark WH Jr, Fischer A, Olive PJW, Went DF (eds) Advances in invertebrate reproduction, vol 3. Elsevier Science, New York, pp 459–472

    Google Scholar 

  • Clarke GN, de Liu Y, Baker HW (2006) Recovery of human sperm motility and ability to interact with the human zona pellucida after more than 28 years of storage in liquid nitrogen. Fertil Steril 86:721–722. doi:10.1016/j.fertnstert.2006.01.050

    Article  Google Scholar 

  • Damiens G, Mouneyrac C, Quiniou F, His E, Gnassia-Barelli M, Roméo M (2006) Metal bioaccumulation and metallothionein concentrations in larvae of Crassostrea gigas. Environ Pollut 140:492–499. doi:10.1016/j.envpol.2005.08.006

    Article  CAS  Google Scholar 

  • Darszon A, Labarca P, Nishigaki T, Espinosa F (1999) Ion channels in sperm physiology. Physiol Rev 79:481–510

    CAS  Google Scholar 

  • Dinnel PA (1995) Evolution and present status of the sea urchin sperm test. Russ J Mar Biol 21:344–350

    Google Scholar 

  • Dinnel PA, Link JM, Stober OJ, Letourneau MW, Roberts WE (1989) Comparative sensitivity of sea urchin sperm bioassays to metals and pesticides. Arch Environ Contam Toxicol 18:748–755. doi:10.1007/BF01225012

    Article  CAS  Google Scholar 

  • Diwan AD, Joseph W (2000) Cryopreservation of spermatophores of the marine shrimp Penaeus indicus. J Aquac Trop 15:35–43

    Google Scholar 

  • do Nascimento JA, Seppala M, Perdigão A, Espejo-Arce X, Munuce MJ, Hautala L, Koistinen R, Andrade L, Bahamondes L (2007) In vivo assessment of the human sperm acrosome reaction and the expression of glycodelin-A in human endometrium after levonorgestrel-emergency contraceptive pill administration. Hum Reprod 22:2190–2195. doi:10.1093/humrep/dem119

    Article  CAS  Google Scholar 

  • Fickel J, Wagener A, Ludwig A (2007) Semen cryopreservation and the conservation of endangered species. Eur J Wildl Res 53:81–89. doi:10.1007/s10344-007-0089-z

    Article  Google Scholar 

  • Ghirardini AV, Novelli AA, Losso C, Ghetti PF (2005) Sperm cell and embryo toxicology tests using the sea urchin paracentrotus lividus (LmK). In: Ostrander GK (ed) Techniques in aquatic toxicology. CRC Press, Washington DC, pp 147–168

    Google Scholar 

  • González-Martínez MT, Galindo BE, de De La Torre L, Zapato O, Rodrigues E, Florman HM, Darszon A (2001) A sustained increase in intracellular Ca2+ is required for the acrosome reaction in sea urchin sperm. Dev Biol 236:220–229. doi:10.1006/dbio.2001.0323

    Article  Google Scholar 

  • Griffin FJ, Clark WH Jr (1990) Induction of acrosome filament formation in the sperm of Sicyonia ingentis. Exp Zool 254:296–304

    Article  CAS  Google Scholar 

  • Hill BJ (1994) Offshore spawning by the portunid crab Scylla serrata (Crustacea: Decapoda). Mar Biol 120:379–384. doi:10.1007/BF00680211

    Article  Google Scholar 

  • Kobayashi N (1980) Comparative sensitivity of various developmental stages of sea urchins to some chemicals. Mar Biol 58:163–171

    Article  CAS  Google Scholar 

  • Larrain A, Riveros A, Silva J, Bay-Schmith E (1999) Toxicity of metals and pesticides using the sperm cell bioassay with the sea urchin Arbacia spatuligera. Bull Environ Contam Toxicol 62:749–757. doi:10.1007/s001289900936

    Article  CAS  Google Scholar 

  • Leung-Trujillo JR, Lawrence AL (1987) Observations on the decline in sperm quality of Penaeus setiferus under laboratory conditions. Aquaculture (Amsterdam) 65:363–370

    Google Scholar 

  • Lera S, Macchia S, Pellegrini D (2006) Standardizing the methodology of sperm cell test with Paracentrotus lididus. Environ Monit Assess 122:101–109. doi:10.1007/s10661-005-9167-4

    Article  CAS  Google Scholar 

  • Liévano A, Vega-Saenzdemiera AEC, Darszon A (1990) Ca2+ channels from the sea urchin sperm plasma membrane. J Gen Physiol 95:273–296. doi:10.1085/jgp.95.2.273

    Article  Google Scholar 

  • Lindsay LL, Clark WH Jr (1992) Preloading of micromolar intracellular Ca2+ during capacitation of Sicyonia ingentis sperm and the role of the pH decrease during the acrosome reaction. J Exp Zool 262:219–229. doi:10.1002/jez.1402620212

    Article  CAS  Google Scholar 

  • Novelli AA, Losso D, Ghetti PF, Ghirardini AV (2003) Toxicity of heavy metals using sperm cell and embryo toxicity bioassays with Paracentrotus lividus (ehchinodermata: echinoidea): comparisons with exposure concentrations in the lagoon of Venice, Italy. Environ Toxicol Chem 22:1295–1301. doi:10.1897/1551-5028(2003)022<1295:TOHMUS>2.0.CO;2

    Article  CAS  Google Scholar 

  • Phavale DM (1990) Environmental variables and heavy metal toxicity in crabs. Bull Mar Sci 46:244–245

    Google Scholar 

  • Pillai MC, Blethrow H, Higasih RM, Vines CA, Cherr GN (1997) Inhibition of the sea urchin sperm acrosome reaction by a lignin-derived macromolecule. Aquat Toxicol 37:139–156. doi:10.1016/S0166-445X(96)00821-1

    Article  CAS  Google Scholar 

  • Pongtippatee P, Vanichviriyakit R, Chavadej J, Plodpai P, Pratoomchart B, Sobhon P, Withyachumnarnkul B (2007) Acrosome reaction in the sperm of the black tiger shrimp Penaeus monodon (Decapoda, Penaeidae). Aquac Res 38:1635–1644

    Article  Google Scholar 

  • Rainbow PS, Dallinger R (1993) Metal uptake, regulation and excretion in freshwater invertebrates. In: Rainbow PS, Dallinger R (eds) Ecotoxicology of metal in invertebrates. Lewis Publishers, Chelsea, pp 119–131

    Google Scholar 

  • Ringwood AH (1992) Comparative sensitivity of gametes and early development stages of a sea urchin species (Echinometra mathaei) and a bivalve species (Isognomon californicum) during metal exposures. Arch Environ Contam Toxicol 22:288–295. doi:10.1007/BF00212088

    Article  CAS  Google Scholar 

  • Rogers JB, Yanagimachi R (1976) Competitive effect of magnesium on the calcium-dependent acrosome reaction in guinea pig spermatozoa. Biol Reprod 15:614–619. doi:10.1095/biolreprod15.5.614

    Article  CAS  Google Scholar 

  • Sanders BM, Jenkins KD, Sunda WG, Costlow JD (1983) Free cupric ion activity in seawater: effects on metallothionein and growth in crab larvae. Science 222:53–55. doi:10.1126/science.222.4619.53

    Article  CAS  Google Scholar 

  • Schuel H, Goldstein E, Mechoulam R, Zimmerman AM, Zimmerman S (1994) Anandamide (arachidonylethanolamide), a brain cannabinoid receptor agonist, reduces sperm fertilizing capacity in sea urchins by inhibiting the acrosome reaction. Proc Natl Acad Sci USA 91:7678–7682. doi:10.1073/pnas.91.16.7678

    Article  CAS  Google Scholar 

  • Shigekawa K, Clark WHJ (1986) Spermiogenesis in the marine shrimp Sicyonia ingentis. Dev Growth Differ 28:95–112

    Article  Google Scholar 

  • Simkiss K, Taylor MG (1989) Metal fluxes across the membranes of aquatic organisms. CRC Crit Rev Aquat Sci 1:173–188

    CAS  Google Scholar 

  • Talbot P, Summers RG, Hylander BL, Keough EM, Fra LE (1976) The role of calcium in the acrosome reaction: an analysis using ionophore A23187. J Exp Zool 198:382–392

    Google Scholar 

  • Vaschenko MA, Zhang ZP, Lam PKS, Wu RSS (1999) Toxic effects of cadmium on fertilizing capability of spermatozoa, dynamics of the first cleavage and pluteus formation in the sea urchin Anthocidaris crassispina (Agassiz). Mar Pollut Bull 38:1097–1104. doi:10.1016/S0025-326X(99)00116-2

    Article  CAS  Google Scholar 

  • Vazquez LC (2003) Effect of sperm cell density of measured toxicity from the sea urchin Tripneustes gratilla fertilization bioassay. Environ Toxicol Chem 22:2191–2194. doi:10.1897/02-614

    Article  CAS  Google Scholar 

  • Wang YL, Zhang ZP, Li SJ (1997) Ultrastructure of spermatogenesis in the crab Scylla serrata. Acta Zool Sin 43:249–254 (in Chinese with English abstract)

    Google Scholar 

  • Wang YL, Zhang ZP, Xie FJ, Li SJ (2001) Acrosome reaction in sperm from mud crab Scylla serrata. Acta Zool Sin 47:310–316 (in Chinese with English abstract)

    Google Scholar 

  • Wassarman PM (1999) Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96:175–183. doi:10.1016/S0092-8674(00)80558-9

    Article  CAS  Google Scholar 

  • Weng WH, Li SJ (1996) Acute toxicity of heavy metals to Scylla serrata (Forskal). Fujian Fish 4:15–19 (in Chinese with English abstract)

    Google Scholar 

  • Young LG, Nelson L (1974) The effects of heavy metal ions on the motility of sea urchin spermatozoa. Biol Bull 147:236–246. doi:10.2307/1540581

    Article  CAS  Google Scholar 

  • Zhao ZY, Kong LH (2000) Present environmental condition of Bohai Bay and protective measures. Hai Yang Huan Jing Ke Xue 13:23–27 (in Chinese with English abstract)

    Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 30571430) and the Innovation Team foundation of Jimei University (2008A001). We thank Prof. Rudolf Wu and Prof. Paul Lam (Department of Biology & Chemistry, City University of Hong Kong, China) for their encouragements for this project. We thank Dr. Nicholas Johnson, Mr. Scot Libants and Mr. Steven Chang (Department of Fisheries & Wildlife, Michigan State University, USA) for critical reading of the manuscript. We thank Prof. Karl E. Havens (Department of Fisheries and Aquatic Sciences, University of Florida, USA) for his positive comments on the manuscript. We are also grateful to several anonymous reviewers for their comments on the article

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  1. Ziping Zhang

    Present address: Department of Chemistry and Biochemistry, Texas State University, San Marcos, TX, 78666, USA

  2. Hua Cheng

    Present address: Department of Biostatistics, School of Public Health, Louisiana State University, New Orleans, LA, 70112, USA

Authors and Affiliations

  1. The Key Laboratory of Science and Technology for Aquaculture and Food Safety, Fisheries College, Jimei University, 361021, Xiamen, China

    Ziping Zhang, Hua Cheng, Yilei Wang, Shuhong Wang & Fangjing Xie

  2. Oceanography Department, Xiamen University, 361005, Xiamen, China

    Shaojin Li

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Correspondence to Yilei Wang.

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Zhang, Z., Cheng, H., Wang, Y. et al. Acrosome Reaction of Sperm in the Mud Crab Scylla serrata as a Sensitive Toxicity Test for Metal Exposures. Arch Environ Contam Toxicol 58, 96–104 (2010). https://doi.org/10.1007/s00244-009-9326-7

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