Biotechnology, Biocontrol and Conservation: Potential Approaches—Harnessing RNAi-Based Sex-Differentiation Manipulations in Decapods

  • Amit Savaya-Alkalay
  • Amir SagiEmail author


Invasive species of various taxa, including crustaceans and snails, are harmful to freshwater ecosystems, inflicting a reduction in biodiversity, vast losses for agriculture, alterations in natural ecosystems, and even some human health issues (such as bilharzia). We describe here some destructive invasive species of crustaceans and snails that can be controlled using biotechnological solutions. Specifically, we propose the use of sexually manipulated non-breeding all-male decapod crustacean populations generated through novel techniques that use temporal gene silencing via RNA interference (RNAi), namely, non-genetically modified organisms (non GMO), to control invasive species. The first part of the chapter deals with the control of invasive and destructive freshwater snails using snail-eating freshwater prawns; specifically we propose the use of all-male prawn populations to act as non-invasive and sustainable biocontrol agents. Freshwater prawns have already been shown to act as voracious predators of a few freshwater snail species. Since male prawns grow faster, reach larger size and do not migrate like females, it is likely that they will act as efficient biocontrol agents over snails. The second part of the chapter deals with the proposed control of invasive crustaceans by skewing the sex ratio of the invasive populations by repetitive releases into the invasive populations of neo-females, which bear 100 % male progeny. Since RNAi is becoming widely used and since the commercial use of RNAi-based biotechnologies for the production of neo-females and all-male prawn populations has already been implemented, our proposed solution is readily available for eco-protection applications.


All-male populations Biocontrol Decapod crustaceans Freshwater snails Invasive species RNAi 


  1. Aflalo, E. D., & Sagi, A. (2014). Sustainable aquaculture biotechnology using temporal RNA interference in crustaceans: The case of the insulin-like androgenic gland hormone and prawn monosex culture. In J. N. Govil (Ed.), Animal biotechnology (pp. 319–331). USA: Studium Press LLC.Google Scholar
  2. Aflalo, E. D., Hoang, T. T. T., Nguyen, V. H., Lam, Q., Nguyen, D. M., Trinh, Q. S., et al. (2006). A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture, 256, 468–478. doi: 10.1016/j.aquaculture.2006.01.035.CrossRefGoogle Scholar
  3. Agrawal, N., Dasaradhi, P. V., Mohmmed, A., Malhotra, P., Bhatnagar, R. K., & Mukherjee, S. K. (2003). RNA interference: Biology, mechanism, and applications. Microbiology and Molecular Biology Reviews, 67, 657–685. doi: 10.1128/MMBR.67.4.657-685.2003.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anastacio, P. M., Correia, A. M., & Menino, J. P. (2005a). Processes and patterns of plant destruction by crayfish: Effects of crayfish size and developmental stages of rice. Archiv für Hydrobiologie, 162, 37–51. doi: 10.1127/0003-9136/2005/0162-0037.CrossRefGoogle Scholar
  5. Anastacio, P. M., Correia, A. M., Menino, J. P., & da Silva, L. M. (2005b). Are rice seedlings affected by changes in water quality caused by crayfish? Annales de Limnologie-International Journal of Limnology, 41, 1–6. doi: 10.1051/Limn/2005002.CrossRefGoogle Scholar
  6. Anastacio, P. M., Parente, V. S., & Correia, A. M. (2005c). Crayfish effects on seeds and seedlings: Identification and quantification of damage. Freshwater Biology, 50, 697–704. doi: 10.1111/j.1365-2427.2005.01343.x.CrossRefGoogle Scholar
  7. Anastacio, P. M., Soares, M., & Correia, A. M. (2005d). Crayfish (Procambarus clarkii) consumption of wet-seeded rice plants (Oryza sativa): Modifications throughout the rice growing period. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen, 29, 849–851.Google Scholar
  8. Barker, G. M. (2002). Molluscs as crop pests. New York: CABI Publishing.CrossRefGoogle Scholar
  9. Basilio, R. (1991). Problems of golden snail infestation in rice farming. In R. S. Pullen (Ed.), Acosta BO. Philippines: ICLARM conference proceedings Central Luzon State University.Google Scholar
  10. Bauer, R. T. (2011). Amphidromy and migrations of freshwater shrimps. II. Delivery of hatching larvae to the sea, return juvenile upstream migration, and human impacts. In A. Asakura (Ed.), New frontiers in crustacean biology (pp. 157–168). Koninklijke Brill NV: Leiden.CrossRefGoogle Scholar
  11. Beisel, J. N. (2001). The elusive model of a biological invasion process: Time to take differences among aquatic and terrestrial ecosystems into account? Ethology Ecology Evolutionary, 13, 193–195. doi: 10.1080/08927014.2001.9522785.CrossRefGoogle Scholar
  12. Burky, A. J. (1974). Growth and biomass production of an amphibious snail, Pomacea urceus (Müller), from the Venezuelan savannah. Journal of Molluscan Studies, 41, 127–143.Google Scholar
  13. Burky, A. J., Pacheco, J., & Pereyra, E. (1972). Temperature, water, and respiratory regimes of an amphibious snail, Pomacea urceus (Müller), from the Venezuelan savannah. The Biological Bulletin, 143, 304–316.CrossRefPubMedGoogle Scholar
  14. Charniaux-Cotton, H. (1954). Discovery in, an amphipod crustacean (Orchestia gammarella) of an endocrine gland responsible for the differentiation of primary and secondary male sex characteristics. Comptes rendus hebdomadaires des séances de l’Académie des sciences, 239, 780–782.PubMedGoogle Scholar
  15. Chung, J. S., Manor, R., & Sagi, A. (2011). Cloning of an insulin-like androgenic gland factor (IAG) from the blue crab, Callinectes sapidus: Implications for eyestalk regulation of IAG expression. General and Comparative Endocrinology, 173, 4–10. doi: 10.1016/j.ygcen.2011.04.017.CrossRefPubMedGoogle Scholar
  16. Clark, E. A., Sterritt, R. M., & Lester, J. N. (1988). The fate of tributyltin in the aquatic environment. Environmental Science and Technology, 22, 600–604. doi: 10.1021/es00171a001.CrossRefGoogle Scholar
  17. Covich, A. P., Palmer, M. A., & Crowl, T. A. (1999). The role of benthic invertebrate species in freshwater ecosystems—Zoobenthic species influence energy flows and nutrient cycling. Bio Science, 49, 119–127. doi: 10.2307/1313537.Google Scholar
  18. Degerman, E., Hammar, J., Nyberg, P., & Svardson, G. (2001). Human impact on the fish diversity in the four largest lakes of Sweden. A Journal of the Human Environment, 30, 522–528.CrossRefGoogle Scholar
  19. Dieguez-Uribeondo, J., & Söderhäll, K. (1993). Procambarus clarkii Girard as a vector for the crayfish plague fungus, Aphanomyces astaci Schikora. Aquaculture Research, 24, 761–765. doi: 10.1111/j.1365-2109.1993.tb00655.x.CrossRefGoogle Scholar
  20. Dumbauld, B. R., Booth, S., Cheney, D., Suhrbier, A., & Beltran, H. (2006). An integrated pest management program for burrowing shrimp control in oyster aquaculture. Aquaculture, 261, 976–992. doi: 10.1016/j.aquaculture.2006.08.030.CrossRefGoogle Scholar
  21. Dyck, V. A., Hendrichs, J., & Robinson, A. S. (2005). Sterile insect technique. Netherland: Springer.CrossRefGoogle Scholar
  22. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., & Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806–811. doi: 10.1038/35888.CrossRefPubMedGoogle Scholar
  23. Gherardi, F. (2000). Are non-indigenous species “ecological malignancies”? Ethology Ecology Evolutionary, 12, 323–325. doi: 10.1080/08927014.2000.9522805.CrossRefGoogle Scholar
  24. Gherardi, F. (2006). Crayfish invading Europe: The case study of Procambarus clarkii. Marine and Freshwater Behaviour and Physiology, 39, 175–191. doi: 10.1080/10236240600869702.CrossRefGoogle Scholar
  25. Gherardi, F., Raddi, A., Barbaresi, S., & Salvi, G. (2000). Life history patterns of the red swamp crayfish, Procambarus clarkii, in an irrigation ditch in Tuscany, Italy. In F. R. Schram (Ed.), von Vaupel Klein JC (pp. 99–108). Rotterdam: Crustacean Issues. A.A. Balkema.Google Scholar
  26. Gowans, A., Armstrong, J., & Priede, I. (1999). Movements of adult Atlantic salmon in relation to a hydroelectric dam and fish ladder. Journal of Fish Biology, 54, 713–726. doi: 10.1111/j.1095-8649.1999.tb02028.x.CrossRefGoogle Scholar
  27. Guan, R. Z., & Wiles, P. R. (1997). Ecological impact of introduced crayfish on benthic fishes in a British lowland river. Conservation Biology, 11, 641–647. doi: 10.1046/j.1523-1739.1997.96073.x.CrossRefGoogle Scholar
  28. Hirai, Y. (1988). Apple snail in Japan. Japan Agricultural Research Quarterly, 22, 161–165.Google Scholar
  29. Hobbs, H. H., Jass, J. P., & Huner, J. V. (1989). A review of global crayfish introductions with particular emphasis on 2 North-American species (Decapoda, Cambaridae). Crustaceana, 56, 299–316. doi: 10.1163/156854089x00275.CrossRefGoogle Scholar
  30. Hoch, M. (2001). Organotin compounds in the environment—an overview. Applied Geochemistry, 16, 719–743. doi: 10.1016/S0883-2927(00)00067-6.CrossRefGoogle Scholar
  31. Hofkin, B. V., Koech, D. K., Ouma, J., & Loker, E. S. (1991a). The North American crayfish Procambarus clarkii and the biologica control of schistosome-transmitting snails in Kenya: Laboratory and field investigations. Biological Control, 1, 183–187. doi: 10.1016/1049-9644(91)90065-8.CrossRefGoogle Scholar
  32. Hofkin, B. V., Mkoji, G. M., Koech, D. K., & Loker, E. S. (1991b). Control of schistosome-transmitting snails in Kenya by the North-American crayfish Procambarus clarkii. The American Journal of Tropical Medicine and Hygiene, 45, 339–344.PubMedGoogle Scholar
  33. Hofkin, B. V., Hofinger, D. M., Koech, D. K., & Loker, E. S. (1992). Predation of Biomphalaria and nontarget Mollusks by the Crayfish Procambarus clarkii—implications for the biological-control of Schistosomiasis. Annals of Tropical Medicine and Parasitology, 86, 663–670.PubMedGoogle Scholar
  34. Horgan, F. G., Stuart, A. M., & Kudavidanage, E. P. (2014). Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecologica-International Journal Of Ecology, 54, 90–100. doi: 10.1016/j.actao.2012.10.002.CrossRefGoogle Scholar
  35. Huner, J. (2002). Procambarus. In D. M. Holdich (Ed.), Biology of freshwater crayfish. Oxford: Blackwell Science.Google Scholar
  36. Ibrahim, A., Khalil, M., & Mobarak, F. (1995). On the feeding behavior of the exotic crayfish Procambarus clarkii in Egypt and its prospects in the biocontrol of local vector snails. Journal Union Arabian Biology Cairo, 4, 321–340.Google Scholar
  37. Jiang, X. H., & Qiu, G. F. (2013). Female-only sex-linked amplified fragment length polymorphism markers support ZW/ZZ sex determination in the giant freshwater prawn Macrobrachium rosenbergii. Animal Genetics, 44, 782–785. doi: 10.1111/Age.12067.CrossRefPubMedGoogle Scholar
  38. Katakura, Y. (1989). Endocrine and genetic-control of sex-differentiation in the malacostracan crustacea. Invertebrate Reproduction & Development, 16, 177–182. doi: 10.1080/07924259.1989.9672075.CrossRefGoogle Scholar
  39. Kolar, C. S., & Lodge, D. M. (2001). Progress in invasion biology: Predicting invaders. Trends in Ecology & Evolution, 16, 199–204. doi: 10.1016/S0169-5347(01)02101-2.CrossRefGoogle Scholar
  40. Kwong, K.-L., Chan, R. K., & Qiu, J.-W. (2009). The potential of the invasive snail Pomacea canaliculata as a predator of various life-stages of five species of freshwater snails. Malacologia, 51, 343–356. doi: 10.4002/040.051.0208.CrossRefGoogle Scholar
  41. Laughlin, R. B., Jr., & Lindén, O. (1985). Fate and effects of organotin compounds (pp. 88–94). North America: Ambio.Google Scholar
  42. Lee, P. G., Rodrick, G. E., Sodeman, W. A., Jr., & Blake, N. J. (1982). The giant Malaysian prawn, Macrobrachium rosenbergii, a potental predator for controlling the spread of schistosome vector snails in fish ponds. Aquaculture, 28, 293–301. doi: 10.1016/0044-8486(82)90071-0.CrossRefGoogle Scholar
  43. Lezer, Y., Aflalo, E. D., Manor, R., Sharabi, O., Abilevich, L. K., & Sagi, A. (2015). On the safety of RNAi usage in aquaculture: the case of all-male prawn stocks generated through manipulation of the insulin-like androgenic gland hormone. Aquaculture, 435, 157–166. doi: 10.1016/j.aquaculture.2014.09.040.CrossRefGoogle Scholar
  44. Lindqvist, O. V., & Huner, J. V. (1999). Life history characteristics of crayfish: What makes some of them good colonizers? Crayfish European Alien Species, 11, 23–30.Google Scholar
  45. Lodge, D. M., & Lorman, J. G. (1987). Reductions in submersed macrophyte biomass and species richness by the crayfish Orconectes rusticus. Canadian Journal of Fisheries and Aquatic Sciences, 44, 591–597. doi: 10.1139/f87-072.CrossRefGoogle Scholar
  46. Lodge, D. M., Stein, R. A., Brown, K. M., Covich, A. P., Bronmark, C., Garvey, J. E., et al. (1998). Predicting impact of freshwater exotic species on native biodiversity: Challenges in spatial scaling. Australian Journal of Ecology, 23, 53–67. doi: 10.1111/j.1442-9993.1998.tb00705.x.CrossRefGoogle Scholar
  47. Lodge, D. M., Rosenthal, S. K., Mavuti, K. M., Muohi, W., Ochieng, P., Stevens, S. S., et al. (2005). Louisiana crayfish (Procambarus clarkii) (Crustacea: Cambaridae) in Kenyan ponds: Non-target effects of a potential biological control agent for schistosomiasis. African Journal of Aquatic Science, 30, 119–124. doi: 10.2989/16085910509503845.CrossRefGoogle Scholar
  48. López, M. A., Altaba, C. R., Andree, K. B., & López, V. (2010). First invasion of the apple snail pomacea insularum in Europe, The Newsletter of the IUCN/SSC Mollusc Specialist Group. International Union for Conservation of Nature: Species Survival Commission.Google Scholar
  49. Lowe, S., Browne, M., Boudjelas, S., & De Poorter, M. (2000). 100 of the world’s worst invasive alien species: A selection from the global invasive species database. World Conservation Union (IUCN), Auckland: Invasive Species Specialist Group Species Survival Commission.Google Scholar
  50. Lv, S., Zhang, Y., Liu, H.-X., Hu, L., Yang, K., Steinmann, P., et al. (2009). Invasive snails and an emerging infectious disease: Results from the first national survey on Angiostrongylus cantonensis in China. PLoS Neglected Tropical Diseases, 3, e368. doi: 10.1371/journal.pntd.0000368.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Manor, R., Aflalo, E. D., Segall, C., Weil, S., Azulay, D., Ventura, T., et al. (2004). Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebrate Reproduction & Development, 45, 151–159. doi: 10.1080/07924259.2004.9652584.CrossRefGoogle Scholar
  52. Manor, R., Weil, S., Oren, S., Glazer, L., Aflalo, E. D., Ventura, T., et al. (2007). Insulin and gender: An insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. General and Comparative Endocrinology, 150, 326–336. doi: 10.1016/j.ygcen.2006.09.006.CrossRefPubMedGoogle Scholar
  53. Mareddy, V. R., Rosen, O., Thaggard, H. B., Manor, R., Kuballa, A. V., Aflalo, E. D., et al. (2011). Isolation and characterization of the complete cDNA sequence encoding a putative insulin-like peptide from the androgenic gland of Penaeus monodon. Aquaculture, 318, 364–370. doi: 10.1016/j.aquaculture.2011.05.027.CrossRefGoogle Scholar
  54. Mkoji, G. M., Hofkin, B. V., Kuris, A. M., Stewart-Oaten, A., Mungai, B. N., Kihara, J. H., et al. (1999). Impact of the crayfish Procambarus clarkii on Schistosoma haematobium transmission in Kenya. The American Journal of Tropical Medicine and Hygiene, 61, 751–759.PubMedGoogle Scholar
  55. Mochida, O. (1991). Spread of freshwater Pomacea snails (Pilidae, Mollusca) from Argentina to Asia. (51–62). Guam: MicronesicaGoogle Scholar
  56. Moyle, P. B., & Light, T. (1996). Biological invasions of fresh water: Empirical rules and assembly theory. Biological Conservation, 78, 149–161. doi: 10.1016/0006-3207(96)00024-9.CrossRefGoogle Scholar
  57. Nagamine, C., Knight, A. W., Maggenti, A., & Paxman, G. (1980). Effects of androgenic gland ablation on male primary and secondary sexual characteristics in the Malaysian prawn, Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae), with first evidence of induced feminization in a nonhermaphroditic decapod. General and Comparative Endocrinology, 41, 423–441. doi: 10.1016/0016-6480(80)90048-9.CrossRefPubMedGoogle Scholar
  58. Nair, C. M., Salin, K. R., Raju, M. S., & Sebastian, M. (2006). Economic analysis of monosex culture of giant freshwater prawn (Macrobrachium rosenbergii De Man): A case study. Aquaculture Research, 37, 949–954. doi: 10.1111/j.1365-2109.2006.01521.x.CrossRefGoogle Scholar
  59. Naylor, R. (1996). Invasions in agriculture: Assessing the cost of the golden apple snail in Asia. A Journal of the Human Environment, 25, 443–448.Google Scholar
  60. Nyström, P. (1999). Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. Crustacean issues, 11, 63–86.Google Scholar
  61. Nyström, P., Br Önmark, C., & Graneli, W. (1996). Patterns in benthic food webs: A role for omnivorous crayfish? Freshwater Biology, 36, 631–646.CrossRefGoogle Scholar
  62. Oluoch, A. (1990). Breeding biology of the Louisiana red swamp crayfish Procambarus clarkii Girard in Lake Naivasha, Kenya. Hydrobiologia, 208, 85–92.CrossRefGoogle Scholar
  63. Paglianti, A., & Gherardi, F. (2004). Combined effects of temperature and diet on growth and survival of young-of-year crayfish: A comparison between indigenous and invasive species. Journal of Crustacean Biology, 24, 140–148. doi: 10.1651/C-2374.CrossRefGoogle Scholar
  64. Pain, T. (1960). Pomacea (Ampullariidae) of the Amazon river system. Journal of Conchology, 24, 421–432.Google Scholar
  65. Perera, G. (1996). Apple snails in the aquarium: Ampullariids-their identification, care, and breeding. USA: TFH Publications.Google Scholar
  66. Prashad, B. (1925). Anatomy of the common Indian apple-snail. Zoological Survey of India: Pila globosa.Google Scholar
  67. Qi, Y., & Hannon, G. J. (2005). Uncovering RNAi mechanisms in plants: Biochemistry enters the foray. Federation of European Biochemical Societies letters, 579, 5899–5903. doi: 10.1016/j.febslet.2005.08.035.CrossRefPubMedGoogle Scholar
  68. Roberts, J. K., & Kuris, A. M. (1990). Predation and control of laboratory populations of the snail Biomphalaria glabrata by the freshwater prawn Macrobrachium rosenbergii. Annals of Tropical Medicine and Parasitology, 84, 401–412.PubMedGoogle Scholar
  69. Roll, U., Dayan, T., Simberloff, D., & Mienis, H. K. (2009). Non-indigenous land and freshwater gastropods in Israel. Biological Invasions, 11, 1963–1972. doi: 10.1007/s10530-008-9373-4.CrossRefGoogle Scholar
  70. Sagi, A., & Cohen, D. (1990). Growth, maturation and progeny of sex-reversed Macrobrachium rosenbergii males. World Aquaculture, 21, 87–90.Google Scholar
  71. Sagi, A., Ra’anan, Z., Cohen, D., & Wax, Y. (1986). Production of Macrobrachium rosenbergii in monosex populations: Yield characteristics under intensive monoculture conditions in cages. Aquaculture, 51, 265–275.CrossRefGoogle Scholar
  72. Sagi, A., Snir, E., & Khalaila, I. (1997). Sexual differentiation in decapod crustaceans: Role of the androgenic gland. Invertebrate Reproduction & Development, 31, 55–61. doi: 10.1080/07924259.1997.9672563.CrossRefGoogle Scholar
  73. Sagi, A., Manor, R., & Ventura, T. (2013). Gene silencing in crustaceans: From basic research to biotechnologies. Genes, 4, 620–645. doi: 10.3390/genes4040620.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., et al. (2000). Biodiversity—global biodiversity scenarios for the year 2100. Science, 287, 1770–1774. doi: 10.1126/science.287.5459.1770.CrossRefPubMedGoogle Scholar
  75. Savaya-Alkalay, A., Rosen, O., Sokolow, S. H., Faye, Y. P., Faye, D. S., Aflalo, E. D., et al. (2014). The prawn Macrobrachium vollenhovenii in the Senegal River Basin: towards sustainable restocking of all-male populations for biological control of schistosomiasis. PLoS Neglected Tropical Diseases, 8, e3060. doi: 10.1371/journal.pntd.0003060.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Silva-Oliveira, G. C., Ready, J. S., Iketani, G., Bastos, S., Gomes, G., Sampaio, I., et al. (2011). The invasive status of Macrobrachium rosenbergii (De Man, 1879) in Northern Brazil, with an estimation of areas at risk globally. Aquatic Invasions, 6, 319–328. doi: 10.3391/ai.2011.6.3.08.CrossRefGoogle Scholar
  77. Sokolow, S. H., Lafferty, K. D., & Kuris, A. M. (2013). Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): Implications for control of schistosomiasis. Acta Tropica, 132C, 64–67. doi: 10.1016/j.actatropica.2013.12.013.Google Scholar
  78. Sokolow, S. H., Huttinger, E., Jouanard, N., Hsieh, M. H., Lafferty, K. D., Kuris, A. M., et al. (2015). Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host. Proceedings of the National Academy of Sciences, 112, 9650–9655.CrossRefGoogle Scholar
  79. Southgate, V. R. (1997). Schistosomiasis in the Senegal River Basin: Before and after the construction of the dams at Diama, Senegal and Manantali, Mali and future prospects. Journal of Helminthology, 71, 125–132.CrossRefPubMedGoogle Scholar
  80. Southgate, V., Tchuem Tchuente, L. A., Sene, M., De Clercq, D., Theron, A., Jourdane, J., et al. (2001). Studies on the biology of schistosomiasis with emphasis on the Senegal river basin. Memórias do Instituto Oswaldo Cruz, 96(Suppl), 75–78. doi: 10.1590/S0074-02762001000900010.CrossRefPubMedGoogle Scholar
  81. Souty-Grosset, C. (2006). Atlas of crayfish in Europe. The Netherlands: Backhuys Publishers.Google Scholar
  82. Sow, S., de Vlas, S. J., Engels, D., & Gryseels, B. (2002). Water-related disease patterns before and after the construction of the Diama dam in northern Senegal. Annals of Tropical Medicine and Parasitology, 96, 575–586. doi: 10.1179/000349802125001636.CrossRefPubMedGoogle Scholar
  83. Taketomi, Y., Murata, M., & Miyawaki, M. (1990). Androgenic gland and secondary sexual characters in the crayfish Procambarus clarkii. Journal of Crustacean Biology, 10, 492–497.CrossRefGoogle Scholar
  84. Touir, A. (1977). New data concerning sexual endocrinology of hermaphroditic and gonochoristic crustacea decapoda natantia. 2. Maintenance of gonia and evolution of gametogenesis invivo and invitro. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie D, 284, 2515–2518.Google Scholar
  85. Vázquez-Islas, G., Garza-Torres, R., Guerrero-Tortolero, D. A., & Campos-Ramos, R. (2014). Histology of the androgenic gland and expression of the insulin-like androgenic gland hormone precursor gene in the genital organ of Pacific white shrimp Litopenaeus vannamei. Journal of Crustacean Biology, 34, 293–299. doi: 10.1163/1937240X-00002232.CrossRefGoogle Scholar
  86. Ventura, T., & Sagi, A. (2012). The insulin-like androgenic gland hormone in crustaceans: From a single gene silencing to a wide array of sexual manipulation-based biotechnologies. Biotechnology Advances, 30, 1543–1550. doi: 10.1016/j.biotechadv.2012.04.008.CrossRefPubMedGoogle Scholar
  87. Ventura, T., Manor, R., Aflalo, E. D., Weil, S., Raviv, S., Glazer, L., et al. (2009). Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology, 150, 1278–1286. doi: 10.1210/en.2008-0906.CrossRefPubMedGoogle Scholar
  88. Ventura, T., Manor, R., Aflalo, E. D., Weil, S., Rosen, O., & Sagi, A. (2012). Timing sexual differentiation: Full functional sex reversal achieved through silencing of a single insulin-like gene in the prawn. Macrobrachium rosenbergii. Biology of Reproduction, 86, 6. doi: 10.1095/biolreprod.111.097261.Google Scholar
  89. Vitousek, P. M., DAntonio, C. M., Loope, L. L., & Westbrooks, R. (1996). Biological invasions as global environmental change. American Science, 84, 468–478.Google Scholar
  90. WHO. (2013a). Schistosomiasis—facts sheet. World health organization. Publ. Internet. Accessed Dec 30, 2015
  91. WHO. (2013b). Schistosomiasis: Progress report 2001–2011, Strategic Plan 2012–2020.Google Scholar
  92. Yusa, Y., Sugiura, N., & Wada, T. (2006). Predatory potential of freshwater animals on an invasive agricultural pest, the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae), in southern Japan. Biological Invasions, 8, 137–147. doi: 10.1007/s10530-004-1790-4.CrossRefGoogle Scholar

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© Springer International Publishing AG 2016

Authors and Affiliations

  1. 1.Department of Life SciencesNational Institute for Biotechnology in the Negev, Ben-Gurion UniversityBeer-ShevaIsrael

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