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Heritability of body weight and resistance to ammonia in the Pacific white shrimp Litopenaeus vannamei juveniles

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Abstract

Ammonia, toxic to aquaculture organisms, represents a potential problem in aquaculture systems, and the situation is exacerbated in closed and intensive shrimp farming operations, expecially for Litopenaeus vannamei. Assessing the potential for the genetic improvement of resistance to ammonia in L. vannamei requires knowledge of the genetic parameters of this trait. The heritability of resistance to ammonia was estimated using two descriptors in the present study: the survival time (ST) and the survival status at half lethal time (SS50) for each individual under high ammonia challenge. The heritability of ST and SS50 were low (0.154 4±0.044 6 and 0.147 5±0.040 0, respectively), but they were both significantly different from zero (P<0.01). Moreover, these two estimates were basically the same and showed no significant differences from each other (P>0.05), suggesting that ST and SS50 could be used as suitable indicators for resistance to ammonia. There were also positive phenotypic and genetic correlation between resistance to ammonia and body weight, which means that resistance to ammonia can be enhanced by the improvement of husbandry practices that increase the body weight. The results from the present study suggest that the selection for higher body weight does not have any negative consequences for resistance to ammonia. In addition to quantitative genetics, tools from molecular genetics can be applied to selective breeding programs to improve the efficiency of selection for traits with low heritability.

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References

  • Alagappan K M, Deivasigamani B, Somasundaram S T, Kumaran S. 2010. Occurrence of Vibrio parahaemolyticus and its specific phages from shrimp ponds in east coast of India. Current Microbiology, 61(4): 235–240.

    Article  Google Scholar 

  • Alcaraz G, Chiappa-Carrara X, Espinoza V, Vanegas C. 1999. Acute toxicity of ammonia and nitrite to white shrimp Penaeus setiferus postlarvae. Journal of the World Aquaculture Society, 30(1): 90–97.

    Article  Google Scholar 

  • Anzenbacher P, Anzenbacherová E. 2001. Cytochromes P450 and metabolism of xenobiotics. Cellular and Molecular Life Sciences, 58(5–6): 737–747.

    Article  Google Scholar 

  • Argue B J, Arce S M, Lotz J M, Moss S M. 2002. Selective breeding of Pacific white shrimp (Litopenaeus vannamei) for growth and resistance to Taura syndrome Virus. Aquaculture, 204(3–4): 447–460.

    Article  Google Scholar 

  • Armstrong D A. 1979. Nitrogen toxicity to crustacea and aspects of its dynamics in culture systems. In: Lewis D, Liang J eds. Proceedings of the 2nd Biennial Crustacean Health Workshop. 2 nd edn. Texas A and M University Sea Grant Publication, Texas. p.329–360.

    Google Scholar 

  • Barajas F J M, Villegas R S, Clark G P, Moreno B L. 2006. Litopenaeus vannamei (Boone) post-larval survival related to age, temperature, pH and ammonium concentration. Aquaculture Research, 37(5): 492–499.

    Article  Google Scholar 

  • Castillo-Juárez H, Casares J C Q, Campos-Montes G, Villela C C, Ortega A M, Montaldo H H. 2007. Heritability for body weight at harvest size in the Pacific white shrimp, Penaeus (Litopenaeus) vannamei, from a multienvironment experiment using univariate and multivariate animal models. Aquaculture, 273(1): 42–49.

    Article  Google Scholar 

  • Charo-Karisa H, Rezk M A, Bovenhuis H, Komen H. 2005. Heritability of cold tolerance in Nile tilapia, Oreochromis niloticus, juveniles. Aquaculture, 249(1–4): 115–123.

    Article  Google Scholar 

  • Chen J C, Chin T C, Lee C K. 1986. Effects of ammonia and nitrite on larval development of the shrimp (Penaeus monodon). In: Maclean J L, Dizon L B, Hosillos L V eds. The First Asian Fisheries Forum. Asian Fisheries Society, Manila, Phillipines. p.657–662.

  • Chen J C, Kou Y Z. 1993. Accumulation of ammonia in the haemolymph of Penaeus monodon exposed to ambient ammonia. Aquaculture, 109(2): 177–185.

    Article  Google Scholar 

  • Chen J C, Lin C Y. 1991a. Lethal effects of ammonia on Penaeus chinensis Osbeck juveniles at different salinity levels. Journal of Experimental Marine Biology and Ecology, 156(1): 138–148.

    Google Scholar 

  • Chen J C, Lin C Y. 1991b. Lethal doses of ammonia on Penaeus chinensis larvae. Bulletin of the Institute of Zoology, Academia Sinica, 30(4): 289–298.

    Google Scholar 

  • Chen J C, Lin C Y. 1992a. Effect of ammonia on growth of Penaeus penicillatus juveniles. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 101(3): 443–447.

    Article  Google Scholar 

  • Chen J C, Lin C Y. 1992b. Effects of ammonia on growth and molting of Penaeus monodon juveniles. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 101(3): 449–452.

    Article  Google Scholar 

  • Chen J C, Liu P C, Lei S C. 1990a. Toxicities of ammonia and nitrite to Penaeus monodon adolescents. Aquaculture, 89(2): 127–137.

    Article  Google Scholar 

  • Chen J C, Liu P C, Lin Y T, Lee C K. 1988. Super intensive culture of red-tailed shrimp Penaeus penicillatus. Journal of the World Aquaculture Society, 19(3): 127–131.

    Article  Google Scholar 

  • Chen J C, Ting Y Y, Lin J N, Lin M N. 1990b. Lethal effects of ammonia and nitrite on Penaeus chinensis juveniles. Marine Biology, 107(3): 427–431.

    Article  Google Scholar 

  • Chin T S, Chen J C. 1987. Acute toxicity of ammonia to larvae of the tiger prawn, Penaeus monodon. Aquaculture, 66(3–4): 247–253.

    Article  Google Scholar 

  • Cock J, Gitterle T, Salazar M, Rye M. 2009. Breeding for disease resistance of Penaeid shrimps. Aquaculture, 286(1–2): 1–11.

    Article  Google Scholar 

  • Colt J E, Armstrong D A. 1981. Nitrogen toxicity to crustaceans, fish and molluscs. In: Allen L J, Kinney E C eds. Proceedings of the Bio-Engineering Symposium for Fish Culture. Fish Culture Section, American Fisheries Society. Northeast Society of Conservation Engineers, Bethesda, MD. p.34–47.

    Google Scholar 

  • Coyle P, Philcox J C, Carey L C, Rofe A M. 2002. Metallothionein: the multipurpose protein. Cellular and Molecular Life Sciences, 59(4): 627–647.

    Article  Google Scholar 

  • Cuzon G, Lawrence A, Gaxiola G, Rosas C, Guillaume J. 2004. Nutrition of Litopenaeus vannamei reared in tanks or in ponds. Aquaculture, 235(1–4): 513–551.

    Article  Google Scholar 

  • Foss A, Vollen T, Øiestad V. 2003. Growth and oxygen consumption in normal and O2 supersaturated water, and interactive effects of O2 saturation and ammonia on growth in spotted wolffish (Anarhichas minor Olafsen). Aquaculture, 224(1–4): 105–116.

    Article  Google Scholar 

  • Frías-Espericueta M G, Harfush-Melendez M, Osuna-López J I, Páez-Osuna F. 1999. Acute toxicity of ammonia to juvenile Shrimp Penaeus vannamei Boone. Bulletin of Environmental Contamination and Toxicology, 62(5): 646–652.

    Article  Google Scholar 

  • Funge-Smith S, Briggs M. 2005. The introduction of Penaeus vannamei and P. stylirostris into the Asia-Pacific region. In: Bartley D M, Bhujel R C, Funge-Smith S, Olin P G, Phillips M J eds. International Mechanisms for the Control and Responsible use of Alien Species in Aquatic Ecosystems, Report of an Ad Hoc Expert Consultation. Food and Agriculture Organization of the United Nations (FAO), Rome. p.149–167.

  • Gilmour A R, Gogel B J, Cullis B R, Thompson R. 2009. ASReml User Guide Release 3.0. VSN International Ltd, Hemel Hempstead.

    Google Scholar 

  • Gitterle T, Rye M, Salte R, Cock J, Johansen H, Lozano C, Suárez J A, Gjerde B. 2005a. Genetic (co)variation in harvest body weight and survival in Penaeus ( Litopenaeus ) vannamei under standard commercial conditions. Aquaculture, 243(1–4): 83–92.

    Article  Google Scholar 

  • Gitterle T, Salte R, Gjerde B, Cock J, Johansen H, Salazar M, Lozano C, Rye M. 2005b. Genetic (co)variation in resistance to White Spot Syndrome Virus (WSSV) and harvest weight in Penaeus (Litopenaeus) vannamei. Aquaculture, 246(1–4): 139–149.

    Article  Google Scholar 

  • Gjedrem T. 2005. Selection and Breeding Programs in Aquaculture. Springer, The Netherlands.

    Book  Google Scholar 

  • Goyard E, Patrois J, Reignon J M, Vanaa V, Dufour R, Bédier E. 1999. IFREMER’s shrimp genetics program. Global Aquaculture Advocate, 2(6): 26–28.

    Google Scholar 

  • He Y Y, Li J, Liu P, Huang F Y, Wang Q Y. 2008. Comparison of the resistance to pH value and ammonia in Chinese shrimp (Fenner o penaeus Chinensis) families. Periodical of Ocean University of China, 38(5): 761–765. (in Chinese with English abstract)

    Google Scholar 

  • Heath A G. 1995. Osmotic and ionic regulation. In: Heath A G. ed. Water Pollution and Fish Physiology. CRC Press, Boca Raton, FL, USA. p.141–170.

    Google Scholar 

  • Ibarra A M, Famula T R, Arcos F G. 2009. Heritability of vitellogenin in hemolymph, a pre-spawning selectable trait in Penaeus (Litopenaeus) vannamei, has a large genetic correlation with ovary maturity measured as oocytes mean diameter. Aquaculture, 297(1–4): 64–69.

    Article  Google Scholar 

  • Ibarra A M, Pérez-Rostro C I, Ramírez J L, Ortega-Estrada E. 2007. Genetics of the resistance to hypoxia in postlarvae and juveniles of the Pacific white shrimp Penaeus (Litopenaeus ) vannamei (Boone 1931). Aquaculture Research, 38(8): 838–846.

    Article  Google Scholar 

  • Johnson E L. 1985. Ambient water quality for ammonia-1984. EPA 440/5-85-001. Environmental Protection Agency, Duluth, Minnesota, USA.

    Google Scholar 

  • Junkunlo K, Prachumwat A, Tangprasittipap A, Senapin S, Borwornpinyo S, Flegel T W, Sritunyalucksana K. 2012. Anovel lectin domain-containing protein (LvCTLD) associated with response of the whiteleg shrimp Penaeus (Litopenaeus) vannamei to yellow head virus (YHV). Developmental & Comparative Immunology, 37(3–4): 334–341.

    Article  Google Scholar 

  • Kir M, Kumlu M, Eroldogan O T. 2004. Effects of temperature on acute toxicity of ammonia to Penaeus semisulcatus juveniles. Aquaculture, 241(1–4): 479–489.

    Article  Google Scholar 

  • Kong J, Luo K, Luan S, Wang Q Y, Zhang Q W, Zhang T S, Meng X H, Wang W J, Ruan X H. 2012. The new variety of Fenneropenaeus chinensis “Huanghai No.2”. Journal of Fisheries of China, 36(12): 1854–1862. (in Chinese with English abstract)

    Article  Google Scholar 

  • Krishna G, Gopikrishna G, Gopal C, Jahageerdar S, Ravichandran P, Kannappan S, Pillai S M, Paulpandi S, Kiran R P, Saraswati R, Venugopal G, Kumar D, Gitterle T, Lozano C, Rye M, Hayes B. 2011. Genetic parameters for growth and survival in Penaeus monodon cultured in India. Aquaculture, 318(1–2): 74–78.

    Article  Google Scholar 

  • Lewis Jr W M, Morris D P. 1986. Toxicity of nitrite to fish: a review. Transactions of the American Fisheries Society, 115(2): 183–195.

    Article  Google Scholar 

  • Lin H P, Thuet P, Trilles J P, Mounet-Guillaume R, Charmantier G. 1993. Effects of ammonia on survival and osmoregulation of various development stages of the shrimp Penaeus japonicus. Marine Biology, 117(4): 591–598.

    Article  Google Scholar 

  • Lin Y C, Chen J C. 2001. Acute toxicity of ammonia on Litopenaeus vannamei Boone juveniles at different salinity levels. Journal of Experimental Marine Biology and Ecology, 259(1): 109–119.

    Article  Google Scholar 

  • Liu B S, Zhang T S, Kong J, Wang Q Y, Luan S, Cao B X. 2011. Estimation of genetic parameters for growth and upper thermal tolerance traits in turbot Scophthalmus maximus. Journal of Fisheries of China, 35(11): 1601–1606. (in Chinese with English abstract)

    Google Scholar 

  • Losordo T M. 1991. Engineering considerations in closed recirculating systems. In: Giovannini P ed. Aquaculture Systems Engineering: Proceedings of the World aquaculture Society and the American Society of Agricultural Engineers, WAS 22nd Annual Meeting American Society of Agricultural, SanJuan, PuertoRico. p.58–69.

    Google Scholar 

  • Luan S, Yang G L, Wang J Y, Luo K, Zhang Y F, Gao Q, Hu H L, Kong J. 2012. Genetic parameters and response to selection for harvest body weight of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture, 362–363: 88–96.

    Article  Google Scholar 

  • Lynch M, Kuramitsu H. 2000. Expression and role of superoxide dismutases (SOD) in pathogenic bacteria. Microbes and Infection, 2(10): 1245–1255.

    Article  Google Scholar 

  • Magallón-Barajas F, Villegas S R, Clark G P, Mosqueda G J, Moreno L B. 2006. Daily variation in short-term static toxicity of unionized ammonia in Litopenaeus vannamei (Boone) postlarvae. Aquaculture Research, 37(14): 1406–1412.

    Article  Google Scholar 

  • Moore S S, Whan V, Davis G P, Byrne K, Hetzel D J S, Preston N. 1999. The development and application of genetic markers for the Kuruma prawn Penaeus japonicus. Aquaculture, 173(1–4): 19–32.

    Article  Google Scholar 

  • Nguyen N H, Khaw H L, Ponzoni R W, Hamzah A, Kamaruzzaman N. 2007. Can sexual dimorphism and body shape be altered in Nile tilapia (Oreochromis niloticus) by genetic means? Aquaculture, 272(S1): S38–S46.

    Article  Google Scholar 

  • Noor-Hamid S, Fortes R D, Parado-Estepa F. 1994. Effect of pH and ammonia on survival and growth of the early larval stages of Penaeus monodon Fabricius. Aquaculture, 125(1–2): 67–72.

    Article  Google Scholar 

  • Pante M J R, Gjerde B, McMillan I, Misztal I. 2002. Estimation of additive and dominance genetic variances for body weight at harvest in rainbow trout, Oncorhynchus mykiss. Aquaculture, 204(3–4): 383–392.

    Article  Google Scholar 

  • Parsell D A, Lindquist S. 1993. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annual Review of Genetics, 27: 437–496.

    Article  Google Scholar 

  • Peaydee P, Klinbunga S, Menasveta P, Jiravanichpaisal P, Puanglarp N. 2014. An involvement of aquaporin in heat acclimation and cross-tolerance against ammonia stress in black tiger shrimp, Penaeus monodon. Aquaculture International, 22(4): 1361–1375.

    Article  Google Scholar 

  • Pérez-Rostro C I, Ibarra A M. 2003a. Heritabilities and genetic correlations of size traits at harvest size in sexually dimorphic Pacific white shrimp (Litopenaeus vannamei) grown in two environments. Aquaculture Research, 34(12): 1079–1085.

    Article  Google Scholar 

  • Pérez-Rostro C I, Ibarra A M. 2003b. Quantitative genetic parameter estimates for size and growth rate traits in Pacific white shrimp, Penaeus vannamei (Boone 1931) when reared indoors. Aquaculture Research, 34(7): 543–553.

    Article  Google Scholar 

  • Racotta I S, Hernández-Herrera R. 2000. Metabolic responses of the white shrimp Penaeus vannamei, to ambient ammonia. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 125(4): 437–443.

    Article  Google Scholar 

  • Robertson A, Lerner I M. 1949. The heritability of all-or-none traits: viability of poultry. Genetics, 34(4): 395–411.

    Google Scholar 

  • Rutten M J M, Komen H, Bovenhuis H. 2005. Longitudinal genetic analysis of Nile tilapia (Oreochromis niloticus L.) body weight using a random regression model. Aquaculture, 246(1–4): 101–113.

    Article  Google Scholar 

  • SAS Institute Inc. 2005. SAS/STAT Software: version 9.1.3 (TS1M3) for Microsoft Windows. SAS Institute, Cary, NC, USA.

  • Sun G M, Tang J H, Zhong X M. 2002. Toxicity research of ammonia nitrogen and nitrite nitrogen to Penaeus vannamei. Journal of Aquaculture, (1): 22–24. (in Chinese with English abstract)

    Google Scholar 

  • Wang X Q, Wang Z Y, He X R. 2009. Heritability and tolerance of Larimichthys crocea to environmental factors. Oceanologia et Limnologia Sinica, 40(6): 781–785. (in Chinese with English abstract)

    Google Scholar 

  • Wicks B J, Joensen R, Tang Q, Randall D J. 2002. Swimming and ammonia toxicity in salmonids: the effect of sub lethal ammonia exposure on the swimming performance of coho salmon and the acute toxicity of ammonia in swimming and resting rainbow trout. Aquatic Toxicity, 59(1–2): 55–69.

    Article  Google Scholar 

  • Wright P A. 1995. Nitrogen excretion: three end products, many physiological roles. The Journal of Experimental Biology, 198(Pt2): 273–281.

    Google Scholar 

  • Young-Lai W W, Charmantier-Daures M, Charmantier G. 1991. Effect of ammonia on survival and osmo regulation in different life stages of the lobster Homarus americanus. Marine Biology, 110(2): 293–300.

    Article  Google Scholar 

  • Zhao J H, Lam T J, Guo J Y. 1997. Acute toxicity of ammonia to the early stage-larvae and juveniles of Eriocheir sinensis H. Milne-Edwards, 1853 (Decapoda: grapsidae) reared in the laboratory. Aquaculture Research, 28(7): 517–525.

    Google Scholar 

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Authors and Affiliations

  1. Key Laboratory for Sustainable Utilization of Marine Fisheries Resources, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Wenjia Li  (李文嘉), Xia Lu  (卢霞), Sheng Luan  (栾生), Kun Luo  (罗坤), Juan Sui  (隋娟) & Jie Kong  (孔杰)

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  1. Wenjia Li  (李文嘉)
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  2. Xia Lu  (卢霞)
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  6. Jie Kong  (孔杰)
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Correspondence to Jie Kong  (孔杰).

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Supported by the National High Technology Research and Development Program of China (863 Program) (No. 2012AA10A404), the Qingdao Postdoctoral Science Foundation Funded Project (No. Q51201403), the National Natural Science Foundation of China (Nos. 31302179, 31172402), the 948 Project from the Ministry of Agriculture of China (No. 2015-Z17), the Improved Agricultural Breeds Engineering Project of Shandong Province—the Taishan Scholar Program for seed industry “Multi-Tarits Selective Breeding of New Variety and Its Industrialization”, and the Fundamental Research Funds for the Yellow Sea Fisheries Research Institute Chinese Academy of Fishery Sciences (No. 20603022013011)

LI Wenjia and LU Xia contributed equally to this work.

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Li, W., Lu, X., Luan, S. et al. Heritability of body weight and resistance to ammonia in the Pacific white shrimp Litopenaeus vannamei juveniles. Chin. J. Ocean. Limnol. 34, 1025–1033 (2016). https://doi.org/10.1007/s00343-016-5034-0

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