Las Bacterias en el Inicio de la Alimentación Exógena en Larvas de Camarones Peneidos: Efectos de la Calidad del Agua, Tasas de Ingestión y Rutas de Colonización del Tracto Digestivo
Resumen
En este estudio se presentan resultados de la sobrevivencia y desarrollo de Litopenaeus
vannamei desde Nauplio5 hasta Zoea2 provenientes de 5 tratamientos de calidad de agua
donde la comunidad bacteriana inicial fue manipulada: 1) agua de mar recientemente
filtrada a través de 1 μm; 2) agua de mar esterilizada con un autoclave; 3) agua de mar de
un sistema de recirculación sin carga orgánica; 4) agua de mar de un sistema de
recirculación con carga orgánica; y 5) agua de mar filtrada con una mezcla de un probiótico
comercial. Los resultados de este experimento mostraron que la manipulación de la
comunidad bacteriana del agua donde las larvas se alimentan por primera vez influye en su
sobrevivencia y capacidad para mudar a los estadios larvales posteriores. Utilizar agua
completamente estéril da resultados similares a aquellos donde se utilizó agua de mar con
sólidos suspendidos reducidos y con una comunidad bacteriana normal. El agua de un
sistema de recirculación sin carga orgánica es preferible a aquella con gran carga orgánica
(organismos vivos + alimento). Cepas de probióticos comerciales deben usarse con
precaución dado que potencialmente conllevan un incremento rápido de la concentración
total de amonio. Estos resultados confirman que la colonización inicial del intestino por
bacterias tiene un impacto directo sobre la sobrevivencia, crecimiento y desarrollo larvario.
Entonces se realizaron observaciones para evaluar la capacidad de las larvas para la
filtración e ingestión de bacterias, comparándola con las tasas de filtración de microalgas.
Una vez que la ingestión de bacterias quedó demostrada, se procedió a estudiar el tiempo de
la primera colonización del intestino y la ruta de entrada de las bacterias. Los resultados de
la observación de cortes histológicos, observación mediante microscopía electrónica de
barrido y las observaciones in vivo de bacterias vivas marcadas sugieren que la
colonización bacteriana comienza desde el estadio de Nauplio5, ya que estas larvas ya
presentan un poro anal y movimientos de antiperistálsis que les permiten la colonización
del tracto digestivo por parte de bacterias presentes en la columna de agua.
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Alabi, A. O., Yudiati, E., Jones, D.A., 1997. Bacterial Levels in Penaeid Larval Cultures. Manila: Asian
Fisheries Society.
Alcaraz, M., Paffenhofer, G. A., Strickler, J. R., 1980. Catching the algae: afirst account of visual
observations on filter-feeding calanoids. American Society of Limnology and Oceanography Special
Symposium 3, 241-248.
Alsina, M., Blanch, A. R., 1994. A set of keys for biochemical identification of environmental Vibrio species.
Journal of Applied Bacteriology 76, 79-85.
Alvarez, R. J., 1983. Frequency and distribution of bacterial flora of penaeid shrimp. Caribbean Journal of
Science 19, 43-48.
Anderson, I. G., Shamsudin, M. N., Nash, G., 1989. A preliminary study on the aerobic heterotrophic
bacterial flora in giant freshwater prawn, Macrobrachium rosenbergii, hatcheries in Malasya.
Aquaculture 81, 213-223.
Atlas, R. M., Busdosh, M., Krichecsky, E. J., Kaneko, T., 1982. Bacterial populations associated with the
Arctic amphipod Boeckosimus affinis. Canadian Journal of Microbiology 28, 92-99.
Austin, B., Baudet, E., Stobie, M., 1992. Inhibition of bacterial fish pathogens by Tetraselmis suecica.
Journal of Fish Disease 15, 55-61.
Austin, B., Day, J. G., 1990. Inhibition of prawn pathogenic Vibrio spp. By a commercial spray-dried
preparation of Tetraselmis suecica. Aquaculture 90, 389-392.
Bell, W. H., Lang, J. M., 1974b. Selective stimulation of marine bacteria by algal extracellular products.
Limnology and Oceanography 19, 833-839.
Bell, W. H., Lang, J. M., 1974a. Selective stimulation of marine bacteria by algal extracellular products.
Limnology and Oceanography 19, 833-839.
Bell, W. H., Mitchell, R., 1972. Chemostatic and growth responses of marine bacteria to algal extracellular
products. Biologicall Bulletin 143, 265-277.
Boyd, C. M., 1976. Selection of particle sizes by filter-feeding copepods: A plea for reason. Limnology and
Oceanography 21, 175-180.
Brock, J. A., Lightner, D. V., 1990. Diseases of Crustacea. Diseases caused by microrganisms. In: Diseases of
Marine Animals, pp. 296-422. New York, John Wiley & Sons.
Brock, T. D., Clyne, J., 1984. Significance of algal excretory products for growth of epilimnetic bacteria.
Applied and Environmental Microbiology 47, 731-734.
Cahill, M. M., 1990. Bacterial flora of fishes: a review. Microbial Ecology 19, 21-41.
Cahu, C. L., Zambombino-Infante, J. L., 1994. Early weaning of sea bass (Dicentrarchus labrax) larvae with
a compund diet: effect on digestive enzymes. Comparative Biochemistry and Physiology 109A, 213-
Chen, J. C., Chin, T. S., Lee, C. K., Effects of ammonia and nitrite on larval development of the shrimp
Penaeus monodon. Maclean, J. L., Dizon, L. B., and Hosillos, L. V. 657-662. 1986. Malina,
Philippines, Asian Fisheries Society. The first Asian Fisheries Forum.
Chen, J. C., Lin, C. Y., 1991. Lethal doses of ammonia on Penaeus chinensis larvae. Bull. Inst. Zool. Acad.
Sin 30, 289-297.
Chen, J. C., Tu, C. C., 1990. Acute toxicity of nitrite to larval Penaeus japonicus. J. Fish. Soc. Taiwan 17,
-287.
Chen, J. C., Tu, C. C., Yang, W. S., 1989. Acute toxicity of ammonia to larval Penaeus japonicus. Journal of
the Fisheries Society of Taiwan 16, 17-26.
Cheng, S. Y., Chen, J. C., 1994. Lethal concentration of nitrite on Penaeus chinensis larvae. Zoological
Studies 33, 228-231.
Christopher, F. M., Vanderzant, C., Parker, J. D., Conte, F. S., 1978. Microbial flora of pond reared shrimp
(Penaeus stylirostris, Penaeus vannamei and Penaeus setiferus). J. Fd. Prot. 41, 20-23.
Cole, J. J., 1982. Interaction between bacteria and algae in aquatic ecosystems. Annual Review on Ecological
Systems 13, 291-314.
Colorni, A., 1985. A study on the bacterial flora of giant prawn, Macrobrachium rosenbergii, larvae fed with
Artemia nauplii. Aquaculture 49, 1-10.
Dabrowski, K., Glogowski, J., 1977. Studies on the role of exogenous proteolytic enzymes in digestion
processes in fish. Hydrobiologia 54, 129-134.
Dempsey, A. C., Kitting, C. L., 1987. Characteristics of bacteria isolated from penaeid shrimp. Crustaceana
, 90-94.
Dempsey, A. C., Kitting, C. L., Rosson, R., A., 1989. Bacterial variability among individual penaeid shrimp
digestive tracts. Crustaceana 56, 267-278.
Douillet, P. A., Langdon, C. J., 1993. Effect of marine bacteria on the culture ofaxenic oyster Crassostrea
gigas. Biological Bulletin 184, 36-51.
Douillet, P. A., Langdon, C. J., 1994. Use of a probiotic for the culture of larvae of the Pacific oyster
(Crassostrea gigas Thunberg). Aquaculture 119, 25-40.
Duff, D. C. B., Bruce, D.L., Anita, N. J., 1966. The antibacterial activity of marine planktonic algae.
Canadian Journal of Microbiology 12, 877-884.
Felgenhauer, B. E., 1987. Techniques for preparing crustaceans for scanning electron microscopy. Journal of
Crustacean Biology 7, 71-76.
Fisher, W. S., 1977. epibiotic microbial infestations of cultured crustaceans. Proceedings of the World
Mariculture Society 8, 673-684.
Fisher, W. S., 1988a. Microbial epibionts of Dungeness crabs. In: Disease Diagnosis and Control of North
America Marine Aquaculture (Ed. by C.J.Sindermann & D.V.Lightner), pp. 222-225. New York,
Elsevier.
Fisher, W. S., 1988b. Microbial epibionts of lobsters. In: Disease Diagnosis and Control of North America
Marine Aquaculture (Ed. by C.J.Sindermann & D.V.Lightner), pp. 243-246. New York, Elsevier.
Fukami, K., Nishijima, T., Murata, H., Doi, S., Hata, Y., 1991. Distribution of bacteria influential on the
development and the decay of Gymnodinium nagasakiense red tide and their effects on algal growth.
Bulletin of the Japanese Society of Scientific Fisheries - Nippon Suisan Gakkaishi 57, 2321-2326.
García-Ortega, A., Verreth, J., Segner, H., 2000. Post-prandial protease activity in the digestive tract of
African catfish Clarias gariepinus larvae fed decapsulated cysts of Artemia. Fish Physiology and
Biochemistry 22, 237-244.
Garriques, D., Arevalo, G., 1995. An Evaluation of the Production and Use of a Live Bacterial Isolate to
Manipulate the Microbial Flora in the Commercial Production of Penaeus Vannamei Postlarvae in
Ecuador. Baton Rouge, Lousiana, USA: World Aquaculture Society.
Gherna, L., 1994. Culture preservation. In: Methods for General and Molecular Microbiology (Ed. by
P.Gerhardt, R.G.E.Murray, W.A.Wood & N.R.Krieg) Washington, American Society for
Microbiology.
Gomez-Gil, B., Roque, A., Turnbull, J. F., 2000. The use and selection of probiotic bacteria for use in the
culture of larval aquatic organisms. Aquaculture 19, 259-270.
Gomez-Gil, B., Roque, A., Velasco, G., 2002. Culture of Vibrio alginolyticus C7b, a potential probiotic
bacterium, with the microalga Chaetoceros muelleri. Aquaculture 211, 43-48.
Gomez-Gil, B., Tron-Mayen, L., Roque, A., Turnbull, J. F., Inglis, V., Guerra-Flores, A. L., 1998. Species of
Vibrio isolated from hepatopancreas, haemolymph and digestive tract of a population of healthy
juvenile Penaeus vannamei. Aquaculture 163, 1-9.
Grahame, J., 1983. Adaptive aspects of feeding mechanisms. In: Environmental Adaptations (Ed. by
J.Venberg & U.Venberg), pp. 65-107. Academic Press Inc.
Gram, L., Nys, R., Maximilien, R., Givskov, M., Steinberg, P.D., Kjelleberg, S. 1996. Inhibitory effects of
secondary metabolites from the red alga Delisea Pulchra on swarming motility of Proteus mirabilis.
Applied and Environmental Microbiology 62, 4284-4287.
Guillard, R. R. L., Hellebust, J. A., 1971. Growth and the production of extracellulat substances by two strains
of Phaeocystis pouchettii. Journal of Phycology 7, 330-338.
Hameed, A. S. S., 1993. A study of the aerobic heterotrophic bacterial-flora of hatchery-reared eggs, larvae
and post-larvae of Penaeus indicus. Aquaculture 117, 195-204.
Haugland, R. P., 2001. Handbook of Fluorescent Probes and Research Chemicals. 8th edition edn. Eugene,
Oregon: Molecular Probes.
Hood, M. A., Meyers, S. P., Colmer, A. R., 1971. Bacteria of the digestive tract of the white shrimp, Penaeus
setiferus. Bacteriological Proceedings 71, G-147.
Huq, A., Huq, S. A., Grimes, D. J., O'Brien, M., Chu, K. H., Capuzzo, J. M., Colwell, R. R., 1986.
Colonization of the gut of the blue crab (Callinectes sapidus) by Vibrio cholerae. Applied and
Environmental Microbiology 52, 586-588.
Huq, A., Small, E. B., West, P. A. H. M. I., Rahman, R., Colwell, R. R., 1983. Ecological relationships
between Vibrio cholerae and planktonic crustacean copepods. Applied and Environmental
Microbiology 45, 275-283.
Intriago, P., 1993. Bacteria as food for Artemia. Aquaculture 113, 115-127.
Johansson, O., Wedborg, M., 1980. The ammonia-ammonium equilibrium in seawater at temperatures
between 5 and 25oC. Journal of Solution Chemistry 9, 37-44.
Jones, D. A., 1998. Crustacean larval microparticulate diets. Reviews in Fisheries and Science 6, 41-54.
Jones, D. A., Walton, M., Bridson, P., 2000. The use of recirculated seawater as a pretreatment for the larval
culture of Fenneropenaeus indicus on microencapsulated feeds. Vanroose, S., Titeca, E., Aspeslagh,
L., Joncheere, H., Flos, R., and Creswell, L. AQUA 2000, Responsible Aquaculture in the New
Millennium. 28, 318. 2000. Belgium, European Aquaculture Society. European Aquaculture Society,
Special Publication. 6-2-2000.
Jones, D. A., Yule, A. B., Holland, D. L., 1997. Larval nutrition. In: Crustacean Nutrition. Advances in World
Aquaculture (Ed. by L.R.D'Abramo, D.E.Conclin & D.M.Akiyama) World Aquaculture Society.
Juarez, L. M., 1997. The Zoea-II Syndrome: A Recently Recognized Problem in Shrimp Hatcheries.
Tegucigalpa, Honduras.: Asociacion Nacional de Acuicultores de Honduras and the Latin American
chapter of the World Aquaculture Society.
Kellam, S.J., Walker, J. M., 1989. Antibacterial activity from marine microalgae in laboratory culture. British
Phycology Journal 24, 191-194.
Khoo, K. H., Culberson, C.H., Bates, R. G., 1977. Thermodynamics of the dissociation of ammonium ion in
seawater from 5-40oC. Journal of Solution Chemistry 6, 281-290.
Koehl, M. A., Strickler, J. R., 1981. Copepod feeding currents: food capture at low Reynolds number.
Limnology and Oceanography 26, 1062-1073.
Kogure, K., Simidu, U., Taga, N., 1979. Effect of Skeletonema costatum (Grev.) Cleve on the growth of
marine bacteria. Journal of Experimental Marine Biology and Ecology 36, 201-215.
Kurokawa, T., Shiraishi, M., Suzuki, T., 1998. Quantification of exogenous protease derived from
zooplankton in the intestine of Japanese sardine (Sardinops melanotictus) larvae. Aquaculture 161,
-499.
Lauff, M., Hofer, R., 1984. Proteolytic enzymes in fish development and the importance of dietary enzymes.
Aquaculture 37, 335-346.
Lovett, D. L., Felder, D. L., 1989. Ontogeny of gut morphology in the white shrimp Penaeus setiferus
(Decapoda: Penaeidae). Journal of Morphology 201, 253-272.
Lovett, D. L., Felder, D. L., 1990. Ontogeny of kynematics in the gut of the white shrimp Penaeus setiferus
(Decapoda: Penaeidae). Journal of Crustacean Biology 10, 53-68.
Moss, S. M., LeaMaster, B. R., Sweeney, J. N. Effects of water source on gut microflora in juvenile white
shrimp Penaeus vannamei. WAS Meeting. 263. 1996. WAS Book of Abstracts.
Naviner, M., Berge, J. P., Durand, P., Le Bris, H., 1999. Antibacterial activity of the marine diatom
Skeletonema costatum against aquacultural pathogens. Aquaculture 174, 15-24.
Nogami, K., Maeda, M., 1992. Bacteria as biocontrol agents for rearing larvae of the crab Portunus
trituberculatus. Canadian Journal of Fisheries and Aquatic Sciences 49, 2373-2376.
Nys, R., Steinberg, P. D., Willemsen, P., Dworjanyn, S. A., Gabelish, C. L., King, R. J., 1995. Broad
spectrum effects of secondary metabolites from the red alga Delisea pulchra in antifouling assays.
Biofouling 8, 259-271.
Pantoja, C. R., Lightner, D. V., Redman, R. M., 1997. Morphological pathology of the zoea-II syndrome of
penaeid shrimp. Alston, D. E., Green, B. W., and Clifford, H. C. IV symposium on aquaculture in
Central America: focusing on shrimp and tilapia. 184-186. 1997. Latin American chapter of the
World Aquaculture Society and the Asociacion Nacional de Acuicultores de Honduras and.
Parsons, T. R., Maita, Y., Lalli, C. M., 1984. A Mannual of Chemical and Biological Methods for Seawater
Analysis. Pergamon Press.
Peterson, B. J., Hobbie, J. E., Haney, J. F., 1978. Daphnia grazing on natural bacteria. Limnology and
Oceanography 23, 1039-1043.
Price, H. J., Paffenhofer, G. A., Strickler, J. R., 1983. Modes of cell capture in calanoid copepods. Limnology
and Oceanography 28, 116-123.
Reichelt, J. L., Borowitzka, M. A., 1984. Antimicrobial activity from marine algae: Results of a large-scale
screening programme. Hydrobiologia 116/117, 158-168.
Riquelme, C., Araya, R., Escribano, R., 2000. selective incorporation of bacteria by Argopecten purpuratus
larvae: implications for the use of probiotics in culturing systems of the chilean scallop. Aquaculture
, 25-36.
Riquelme, C., Araya, R., Vergara, N., Rojas,A., Guaita, M., Candia, M., 1997. Potential probiotic strains in
the culture of the Chilean scallop Argopecten purpuratus (Lamarck, 1819). Aquaculture 154, 17-26.
Riquelme, C., Haayashida, G., Araya, R., Uchida, A., Satomi, M., Ishida, Y., 1996. Isolation of a native
bacterial strain from the scallop Argopecten purpuratus with inhibitory effects against pathogenic
Vibrios. Journal of Shellfish Research 15, 369.
Riquelme, C., Jorquera, M. A., Rojas, A. I., Avendano, R .E., Reyes, N., 2001. Addition of inhibitorproducing
bacteria to mass cultures of Argopecten purpuratus larvae (Lamarck, 1819). Aquaculture
, 111-119.
Roque, A., Molina-Aja, A., Bolan-Mejia, C., Gomez-Gil, B., 2001. In vitro susceptibilities of Vibrio isolates
isolated from penaeid shrimps in Northwestern Mexico to 15 antibiotics. International Journal of
Antimicrobial Agents 15, 383-387.
Salvesen, I., Skjermo, J., Vadstein, O., 1999. Growth of turbot (Scophthalmus maximus L.) during first
feeding in relation to the proportion of r/K-strategists in the bacterial community of the rearing water.
Aquaculture 175, 337-350.
Sieburth, J. M., 1960. Acrylic acid, an "antibiotic" principle in Phaeocystis bloom in antarctic waters. Science
, 676-677.
Singh, B. I., 1986. Studies on the Bacteria Associated With Penaeus Indicus in a Culture System. Ph.D.
Cochim University of Science and Technology.
Skjermo, J., Salvesen, I., Oie, G., Olsen, Y., Vadstein, O., 1997. Microbially matured water: a technique for
selection of a non-opportunistic bacterial flora in water that may improve performance of marine
larvae. Aquaculture International 5, 13-28.
Skjermo,J., Vadstein, O., 1993. The effect of microalgae on skin and gut bacterial flora of halibut larvae. In:
Fish Farm Technology (Ed. by H.Reinertsen, L.A.Dahle, L.B.Jorgensen & K.Tvinnereim), pp. 61-
Rotterdam, Balkema.
Sochard, M. R., Wilson, D. F., Austin, B., Colwell, R. R., 1979. Bacteria associated with the surface and gut
of marine copepods. Applied and Environmental Microbiology 37, 750-759.
Soto-Rodriguez, S. A., Simões, N., Jones, D. A., Roque, A., Gomez-Gil, B. 2002. Assessment of fluorescent
labeled bacteria (FLB) for evaluation of in vivo uptake of bacteria (Vibrio spp.) by crustacean larvae.
Journal of Microbiological Methods in press.
Spotte, S., Adams, G., 1983. Estimation of the allowable upper limit of ammonia in saline waters. Marine
Ecology Progress Series 10, 207-210.
Suzuki, K., Muroga, K., Nogami, K., Maruyama, K., 1990. Bacterial flora of cultured swimming crab
(Portunus trituberculatus) larvae. Fish Pathology 25, 29-36.
Tanasomwang,V., Ruangpan, L., 1995. Bacterial flora of larvae of the black tiger shrimp, Penaeus monodon.
In: Diseases in Asian Aquaculture II (Ed. by M.Shariff, J.R.Arthur & R.P.Subasinghe), pp. 151-162.
Manila, Philipines, Fish Health Section, Asian Fisheries Society.
Tezuka, Y., 1971. Feeding of Daphnia on planktonic bacteria. Japanese Journal of Ecology 21, 127-134.
Vanderzant, C., Nickelson, R., Judkins, P. W., 1971. Microbial flora of pond-reared shrimp Penaeus aztecus.
Applied Microbiology 21, 916-921.
Verschuere, L., Rombaut, G., Sorgeloos, P., Verstraete, W., 2000. Probiotic bacteria as biological control
agents in aquaculture. Microbiology and Molecular Biology Reviews 64, 655-671.
Villegas, D. K., Kanazawa, A., 1979. Relationship between diet composition and growth of the zoeal and
mysis stages of Penaeus japonicus Bate. Fish Res. J. Philipp. 4, 32-40.
Wheaton, F. W., Hochheimer, J. N., Kaiser, G. E., Krones, M. J., Libey, G. S., Easter, C., 1994. Nitrification
filter principles. In: Aquaculture Reuse Systems: Engineering Design and Management (Ed. by
M.B.Timmons & T.M.Losordo), pp. 101-126. Amsterdam, Lausanne, New York, Oxford,
Shannon,Tokyo, Elsevier.
Whitfield, M., 1974. The hydrolysis of ammonium ions in seawater: theoretical study. Journal of the Marine
Biology Association UK 54, 565-580.
Williams, O.B., Rees, H. B., 1952. The bacteriology of Gulf coast shrimp III - The internal flora. Texas
Journal of Science 1, 55-58.
Williams, R. R., Bell, T. A., Lightner, D. V., 1992. Shrimp antimicrobial testing II. Toxicity testing and safety
determination for twelve antimicrobials with penaeid shrimp larvae. Journal of Aquatic Animal
Health 4, 262-270.
Yasuda, K., Kitao, T., 1980. Bacterial flora in the digestive tract of prawns, Penaeus japonicus. Aquaculture
, 229-234.
Yule, A. B., Crisp, D. J., 1983. A study of feeding behaviour in Temora longicornis (Muller) (CRUSTACEA:
COPEPODA). Journal of Experimental Marine Biology and Ecology 71, 271-282.
Zachary, A., Colwell, R. R., 1979. Gut associated microflora of Limnoria tripunctata in marine creosotetreated
wood pilings. Nature (London) 282, 716-717.
Zar, J. H., 1999. Biostatistical Analysis. 4th edn. New Jersey: prentice Hall.
Zilch, R., 1978. Embryologische Untersuchungen an der holoblastischen Ontogenese von Penaeus trisulcatus
Leach (Crustacea, Decapoda). Zoomorphologie 90, 67-100.