SpringerLink
Log in

Responses of growth and hemolymph quality in juvenile Chinese horseshoe crab Tachypleus tridentatus (**phosura) to sublethal tributyltin and cadmium

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Responses of growth endpoints and hemolymph constituents in juvenile Chinese horseshoe crab Tachypleus tridentatus under treatments of 0.01 and 0.1 mg/l tributyltin (TBT) and 0.1 and 1 mg/l cadmium (Cd) were examined in a 12-week experiment. A significant decline in final body weight, final prosomal width, percentage of individuals molted and mean molting time was detected under TBT exposures. While morphological abnormalities of the juveniles between TBT treatments and the control were statistically indistinguishable, significantly higher occurrences of carapace erosion and appendage loss were noted under 0.1 and 1 mg/l Cd exposures. Various hemolymph quality indicators, including hemolymph plasma protein level, amebocyte viability and percentage of granular-spherical state of amebocytes of the juveniles exposed to TBT or Cd were significantly lower than the control. Such a decrease in hemolymph quality suggested deleterious effects of metal contaminant-induced stressors on the health status of the juveniles even at low exposure levels (i.e., 0.01 mg/l TBT and 0.1 mg/l Cd). Changes of hemolymph parameters in juvenile horseshoe crabs were more sensitive than growth performance as well as morphological abnormalities in response to metal stressors, and can be used as an indicator to reflect habitat conditions and contaminant levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahmad AK, Shuhaimi-Othman M (2010) Heavy metal concentrations in sediments and fishes from Lake Chini, Pahang, Malaysia. J Biol Sci 10:93–100

    Article  CAS  Google Scholar 

  • Alzieu C (1998) Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast Manage 40:23–36

    Article  Google Scholar 

  • Bewick V, Cheek L, Ball J (2004) Statistics review 12: survival analysis. Crit Care 8:389–394

    Article  Google Scholar 

  • Blackmore G (1998) An overview of trace metal pollution in the coastal waters of Hong Kong. Sci Total Environ 214:21–48

    Article  CAS  Google Scholar 

  • Boardman GD, Starbuck SM, Hudgins DB, Li X, Kuhn DD (2004) Toxicity of ammonia to three marine fish and three marine invertebrates. Environ Toxicol 19:134–142

    Article  CAS  Google Scholar 

  • Botton ML (2000) Toxicity of cadmium and mercury to horseshoe crab (Limulus polyphemus) embryos and larvae. B Environ Contam Tox 64:37–143

    Article  Google Scholar 

  • Botton ML, Shuster CN Jr (2003) Horseshoe crabs in a food web: who eats whom? In: Shuster CN Jr, Barlow RB, Brockmann HJ (eds) The American horseshoe crab. Harvard Press, Cambridge, pp 133–153

    Google Scholar 

  • Botton ML, Hodge M, Gonzalez TI (1998a) High tolerance to tributyltin in embryos and larvae of the horseshoe crab, Limulus polyphemus. Estuaries 21:340–346

    Article  CAS  Google Scholar 

  • Botton ML, Johnson K, Helleby L (1998b) Effects of copper and zinc on embryos and larvae of the horseshoe crab, Limulus polyphemus. Arch Environ Con Toxicol 35:25–32

    Article  CAS  Google Scholar 

  • Bouchard N, Pelletier É, Fournier M (1999) Effects of butyltin compounds on phagocytic activity of hemocytes from three marine bivalves. Environ Toxicol Chem 18:519–522

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Brouwer M, Bonaventura C, Bonaventura J (1982) Heavy metal ion interactions with Callinectes sapidus hemocyanin: structural and functional changes induced by a variety of heavy metal ions. Biochemistry 21:2529–2538

    Article  CAS  Google Scholar 

  • Brouwer M, Bonaventura C, Bonaventura J (1983) Metal ion interactions with Limulus polyphemus and Callinectes sapidus hemocyanin: stoichiometry and structural and functional consequences of calcium (II), cadmium (II), zinc (II), and mercury (II) binding. Biochemistry 22:4713–4723

    Article  CAS  Google Scholar 

  • Brown RJ, Galloway TS, Lowe D, Browne MA, Dissanayake A, Jones MB, Depledge MH (2004) Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquat Toxicol 66:267–278

    Article  CAS  Google Scholar 

  • Bryan GW, Langston WJ (1992) Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ Pollut 76:89–131

    Article  CAS  Google Scholar 

  • Cao D, Jiang G, Zhou Q, Yang R (2009) Organotin pollution in China: an overview of the current state and potential health risk. J Environ Manag 90:S16–S24

    Article  CAS  Google Scholar 

  • Chang ES (1995) Physiological and biochemical changes during the molt cycle in decapod crustaceans: an overview. J Exp Mar Biol Ecol 193:1–14

    Article  CAS  Google Scholar 

  • Chen JT (1994) Study on the environmental protection countermeasures of Pearl River coast zones. In: Wong CK, Chu KH, Chan QC, Ma XL (eds) Environmental research in Pearl River and Coastal Area. Guangdong Higher Education Press, Guangzhou, pp 153–161

    Google Scholar 

  • Chen CP, Yeh HY, Lin PF (2004) Conservation of the horseshoe crab at Kinmen, Taiwan: strategies and practices. Biodivers Conserv 13:1889–1904

    Article  Google Scholar 

  • Cheng W, Chen JC (2000) Effects of pH, temperature and salinity on immune parameters of the freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immun 10:387–391

    Article  CAS  Google Scholar 

  • Cheung KC, Poon BHT, Lan CY, Wong MH (2003) Assessment of metal and nutrient concentrations in river water and sediment collected from the cities in the Pearl River Delta, South China. Chemosphere 52:1431–1440

    Article  CAS  Google Scholar 

  • Coates CJ, Kelly SM, Nairn J (2011) Possible role of phosphatidylserine–hemocyanin interaction in the innate immune response of Limulus polyphemus. Dev Comp Immunol 35:155–163

    Article  CAS  Google Scholar 

  • Coates CJ, Bradford EL, Krome CA, Nairn J (2012) Effect of temperature on biochemical and cellular properties of captive Limulus polyphemus. Aquaculture 334:30–38

    Article  Google Scholar 

  • Decker H, Hellmann N, Jaenicke E, Lieb B, Meissner U, Markl J (2007) Recent progress in hemocyanin research. Integr Comp Biol 47:631–644

    Article  CAS  Google Scholar 

  • Delaporte M, Soudant P, Lambert C, Moal J, Pouvreau S, Samain JF (2006) Impact of food availability on energy storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254:571–582

    Article  Google Scholar 

  • Dyrynda EA (1998) Shell disease in the common shrimp Crangon crangon: variations within an enclosed estuarine system. Mar Biol 132:445–452

    Article  Google Scholar 

  • Enright MJ, Scott EE, Chang KM (2005) Regional powerhouse: the greater Pearl River Delta and the rise of China. Ann Assoc Am Geog 96:845–847

    Google Scholar 

  • Fingerman M, Devi M, Reddy PS, Katyayani R (1996) Impact of heavy metal exposure on the nervous system and endocrine-mediated processes in crustaceans. Zool Stud 35:1–8

    CAS  Google Scholar 

  • Fu J, Mai B, Sheng G et al (2003a) Persistent organic pollutants in environment of the Pearl River Delta, China: an overview. Chemosphere 52:1411–1422

    Article  CAS  Google Scholar 

  • Fu J, Mai B, Sheng G et al (2003b) Persistent organic pollutants in environment of the Pearl River Delta, China: an overview. Chemosphere 52:1411–1422

    Article  CAS  Google Scholar 

  • Fukue M, Sato Y (2003) Influence of contaminated sediments on Japanese horseshoe crab. 2nd International symposium on contaminated sediments: characterization, evaluation, mitigation/restoration, management strategy performance, Quebec City, Canada

  • Hégaret H, Wikfors GH, Soudant P (2003) Flow cytometric analysis of haemocytes from eastern oysters, Crassostrea virginica, subjected to a sudden temperature elevation: II. Haemocyte functions: aggregation, viability, phagocytosis, and respiratory burst. J Exp Mar Biol Ecol 293:249–265

    Article  Google Scholar 

  • Hong S (2011) Feeding habits. In: Hong S (ed) Biology of Horseshoe Crabs, Tachypleus tridentatus. **amen University Press, China, pp 79–81

    Google Scholar 

  • Hu M, Wang Y, Tsang ST, Cheung SG, Shin PKS (2010) Effect of prolonged starvation on body weight and blood-chemistry in two horseshoe crab species: Tachypleus tridentatus and Carcinoscorpius rotundicauda (Chelicerata: **phosura). J Exp Mar Biol Ecol 395:112–119

    Article  CAS  Google Scholar 

  • Hurton LV, Berkson JM, Smith SA (2005) Selection of a standard culture medium for primary culture of Limulus polyphemus amebocytes. In Vitro Cell Dev–An 41:325–329

    Article  Google Scholar 

  • Itow T (1993) Crisis in the Seto Inland Sea: the decimation of the horseshoe crab. EMECS Newslett 3:10–11

    Google Scholar 

  • Itow T, Igarashi T, Botton ML, Loveland RE (1998a) Heavy metals inhibit limb regeneration in horseshoe crab larvae. Arch Environ Con Toxicol 35:457–463

    Article  CAS  Google Scholar 

  • Itow T, Loveland RE, Botton ML (1998b) Developmental abnormalities in horseshoe crab embryos caused by exposure to heavy metals. Arch Environ Con Toxicol 35:33–40

    Article  CAS  Google Scholar 

  • Iwanaga S, Kawabata SI, Muta T (1998) New types of clotting factors and defense molecules found in horseshoe crab hemolymph: their structures and functions. J Biochem 123:1–15

    Article  CAS  Google Scholar 

  • Kannan K, Yasunaga Y, Iwata H, Ichihashi H, Tanabe S, Tatsukawa R (1995) Concentrations of heavy metals, organochlorines, and organotins in horseshoe crab, Tachypleus tridentatus, from Japanese coastal waters. Arch Environ Con Toxicol 28:40–47

    Article  CAS  Google Scholar 

  • Ko MMC, Bradley GC, Neller AH, Broom MJ (1995) Tributyltin contamination of marine sediments of Hong Kong. Mar Pollut Bull 31:249–253

    Article  CAS  Google Scholar 

  • Kwan BKY, Chan AK, Cheung SG, Shin PKS (2014) Hemolymph quality as indicator of health status in juvenile Chinese horseshoe crab Tachypleus tridentatus (**phosura) under laboratory culture. J Exp Mar Biol Ecol 457:135–142

    Article  Google Scholar 

  • Kwok KWH, Leung KMY (2005) Toxicity of antifouling biocides to the intertidal harpacticoid copepod Tigriopus japonicus (Crustacea, Copepoda): effects of temperature and salinity. Mar Pollut Bull 51:830–837

    Article  CAS  Google Scholar 

  • Lau MMM (1991) Tributyltin antifoulings: a threat to the Hong Kong marine environment. Arch Environ Con Toxicol 20:299–304

    Article  CAS  Google Scholar 

  • Lau MC, Chan KM, Leung KMY, Luan TG, Yang MS, Qiu JW (2007) Acute and chronic toxicities of tributyltin to various life stages of the marine polychaete Hydroides elegans. Chemosphere 69:135–144

    Article  CAS  Google Scholar 

  • Laughlin R, French W, Guard HE (1983) Acute and sublethal toxicity of tributyltin oxide (TBTO) and its putative environmental product, tributyltin sulfide (TBTS) to zoeal mud crabs, Rhithropanopeus harrisii. Water Air Soil Poll 20:69–79

    Article  CAS  Google Scholar 

  • Le Moullac G, Haffner P (2000) Environmental factors affecting immune responses in Crustacea. Aquaculture 191:121–131

    Article  Google Scholar 

  • Le Moullac G, Soyez C, Saulnier D, Ansquer D, Avarre JC, Levy P (1998) Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish Shellfish Immun 8:621–629

    Article  Google Scholar 

  • Li X, Wai OW, Li YS, Coles BJ, Ramsey MH, Thornton I (2000) Heavy metal distribution in sediment profiles of the Pearl River estuary, South China. Appl Geochem 15:567–581

    Article  CAS  Google Scholar 

  • Li Q, Wu Z, Chu B, Zhang N, Cai S, Fang J (2007) Heavy metals in coastal wetland sediments of the Pearl River Estuary, China. Environ Pollut 149:158–164

    Article  CAS  Google Scholar 

  • Liao Y, Hong S, Li X (2001) A survey on the horseshoe crabs in the north of South China Sea. Acta Zool Sin 47:108–111 (Chinese with English abstract)

    Google Scholar 

  • Lignot JH, Pannier F, Trilles JP, Charmantier G (1998) Effects of tributyltin oxide on survival and osmoregulation of the shrimp Penaeus japonicus (crustacea, decapoda). Aquat Toxicol 41:277–299

    Article  CAS  Google Scholar 

  • Malley DF, Chang PSS (1985) Effects of aluminum and acid on calcium uptake by the crayfish Orconectes virilis. Arch Environ Con Toxicol 14:739–747

    Article  CAS  Google Scholar 

  • Merck Millipore (2014) Overview: Physicochemical information of tributyltin chloride. http://www.emdmillipore.com/INTL/en/product/Tributyltin-chloride,MDA_CHEM-808390. Accessed 02 Aug 2014

  • Nagabhushanam R, Reddy PS, Saro**i R (1990) Tributyltin oxide induced alterations in exuvial weight and calcium content of the prawn, Caridina rajadhari. Proc Anim Sci 99:397–400

    Article  Google Scholar 

  • Niu H, Deng W, Wu Q, Chen X (2009) Potential toxic risk of heavy metals from sediment of the Pearl River in South China. J Environ Sci 21:1053–1058

    Article  CAS  Google Scholar 

  • Nolan MW, Smith SA (2009) Clinical evaluation, common diseases, and veterinary care of the horseshoe crab, Limulus polyphemus. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and conservation of Horseshoe Crabs. Springer, New York, pp 479–499

    Chapter  Google Scholar 

  • Pipe RK, Coles JA (1995) Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immun 5:581–595

    Article  Google Scholar 

  • Rodríguez J, Le Moullac G (2000) State of the art of immunological tools and health control of penaeid shrimp. Aquaculture 191:109–119

    Article  Google Scholar 

  • Rodríguez MP, Medesani DA, Rodríguez EM (2003) Inhibition of molting by cadmium in the crab Chasmagnathus granulata (Decapoda Brachyura). Aquat Toxicol 64:155–164

    Article  Google Scholar 

  • Rudkin DM, Young GA (2009) Horsehsoe crabs – An ancient ancestry revealed. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and conservation of Horseshoe Crabs. Springer, New York, pp 25–44

    Chapter  Google Scholar 

  • Sánchez A, Pascual C, Sánchez A, Vargas-Albores F, Le Moullac G, Rosas C (2001) Hemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of acclimation. Aquaculture 198:13–28

    Article  Google Scholar 

  • Sauvé S, Brousseau P, Pellerin J, Morin Y, Senecal L, Goudreau P, Fournier M (2002) Phagocytic activity of marine and freshwater bivalves: in vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquat Toxicol 58:189–200

    Article  Google Scholar 

  • Shin PKS, Li H, Cheung SG (2009) Horseshoe crabs in Hong Kong: current population status and human exploitation. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and conservation of Horseshoe Crabs. Springer, New York, pp 347–360

    Chapter  Google Scholar 

  • Smith VJ, Swindlehurst RJ, Johnston PA, Vethaak AD (1995) Disturbance of host defence capability in the common shrimp, Crangon crangon, by exposure to harbour dredge spoils. Aquat Toxicol 32:43–58

    Article  CAS  Google Scholar 

  • Spicer JI, Weber RE (1991) Respiratory impairment in crustaceans and molluscs due to exposure to heavy metals. Comp Biochem Phys C 100:339–342

    Article  CAS  Google Scholar 

  • Sullivan B, Bonaventura J, Bonaventura C (1974) Functional differences in the multiple hemocyanins of the horseshoe crab, Limulus polyphemus L. Proc Natl Acad Sci 71:2558–2562

    Article  CAS  Google Scholar 

  • Tessier A, Campbell P (1988) Partitioning of trace metals in sediments. In: Kramer JR, Allen HE (eds) Metal speciation: theory, analysis and application. Lewis Publishers, New York, pp 183–199

    Google Scholar 

  • Thermo Scientific (2010) Calculations: published extinction coefficient. In: Protein A280 Thermo Scientific NanoDrop Spectrophometers, Thermo Fisher Scientific Inc., Wilmington, USA, pp 14

  • Wilson AP (1986) Cytotoxicity and viability assays. In: Freshney RI (ed) Animal cell culture. IRL Press, Oxford, pp 192–193

    Google Scholar 

  • Wu JP, Chen HC (2005) Effects of cadmium and zinc on the growth, food consumption, and nutritional conditions of the white shrimp, Litopenaeus vannamei (Boone). B Environ Contam Toxicol 74:234–241

    Article  CAS  Google Scholar 

  • Zhang D, Zhang X, Tian L, Ye F, Huang X, Zeng Y, Fan M (2013) Seasonal and spatial dynamics of trace elements in water and sediment from Pearl River Estuary, South China. Environ Earth Sci 68:1053–1063

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work described in this paper was funded by the Ocean Park Conservation Foundation, Hong Kong (Project No. OT03). Thanks are given to Virginia K.Y. Un and K.C. Siu for their assistance in the laboratory work.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biology and Chemistry, City University of Hong Kong, Hong Kong, China

    Billy K. Y. Kwan, Alice K. Y. Chan, Siu Gin Cheung & Paul K. S. Shin

  2. State Key Laboratory in Marine Pollution, City University of Hong Kong, Hong Kong, China

    Siu Gin Cheung & Paul K. S. Shin

Authors
  1. Billy K. Y. Kwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice K. Y. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siu Gin Cheung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul K. S. Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul K. S. Shin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwan, B.K.Y., Chan, A.K.Y., Cheung, S.G. et al. Responses of growth and hemolymph quality in juvenile Chinese horseshoe crab Tachypleus tridentatus (**phosura) to sublethal tributyltin and cadmium. Ecotoxicology 24, 1880–1895 (2015). https://doi.org/10.1007/s10646-015-1524-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-015-1524-7

Keywords

Search

Navigation