Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Several decapod crustaceans are invaders, but little is known about the biological characteristics that potentiate the success of these decapods in invaded ecosystems. Here, we evaluate and describe some aspects of the reproductive biology and development of Lysmata vittata, an invasive shrimp species in the Atlantic Ocean. In addition, we intend to provide important insights into the biology of invasion by comparing the reproductive traits of this shrimp with some of the predictions about aquatic invasive species. We used experimental and laboratory observations to evaluate the functionality of protandric simultaneous hermaphroditism (PSH), the macro and microscopic development of the ovarian portion of the ovotestes, the reproductive cycle, and the embryonic development of L. vittata. We confirm the functionality of PSH in L. vittata. This shrimp has a rapid reproductive cycle; the ovarian portion of the ovotestes develops (mean ± SD) 6.28 ± 1.61 days after spawning. Embryonic development also occurs over a short time, with a mean (± SD) of 8.37 ± 0.85 days. The larvae hatch without macroscopically visible yolk reserves. Our study provides evidence that the invasive shrimp L. vittata has reproductive and embryonic developmental characteristics (i.e., short generation time and high reproductive capacity) that may be favorable to the establishment of populations during invasive processes. © 2019 Alves et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Registro:

Documento: Artículo
Título:Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean
Autor:Alves, D.F.R.; López Greco, L.S.; de Paiva Barros-Alves, S.; Hirose, G.L.
Filiación:Departamento de Biologia, Universidade Federal de Sergipe–UFS, São Cristóvão, Sergipe, Brazil
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Sergipe–UFS, São Cristóvão, Sergipe, Brazil
Universidad de Buenos Aires, CONICET, Instituto de Biodiversidad y Biología Experimental y Aplicada (IBBEA), Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Laboratorio de Biología de la Reproducción y el Crecimiento de Crustáceos Decápodos, Buenos Aires, Argentina
Laboratório de Ecologia de Ecossistemas Aquáticos, Universidade Federal de Uberlândia–UFU, Uberlândia, Minas Gerais, Brazil
Palabras clave:article; Atlantic Ocean; biology; egg yolk; embryo; embryo development; female; genital system; human; invasive species; larva; male; nonhuman; ovary cycle; ovary development; prediction; shrimp; simultaneous hermaphroditism; spawning
Año:2019
Volumen:14
Número:1
DOI: http://dx.doi.org/10.1371/journal.pone.0210723
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_19326203_v14_n1_p_Alves

Referencias:

  • Hanson, E., Sytsma, M., The potential for mitten crab Eriocheir sinensis H. Milne Edwards, 1853 (Crustacea: Brachyura) invasion of Pacific Northwest and Alaskan Estuaries (2008) Biol Invasions, 10, pp. 603-614. , https://doi.org/10.1007/s10530-007-9156-3
  • Gust, N., Inglis, G.J., Adaptive multi-scale sampling to determine an invasive crab’s habitat usage and range in New Zealand (2006) Biol Invasions, 8, pp. 339-353. , https://doi.org/10.1007/s10530-004-8243-y
  • Mantelatto, F., Luiz-Diaz, L., Extension of the known distribution of Charibdis hellerii (A. Milne-Edwards, 1867) (Decapoda, Portunidae) along the western tropical South Atlantic (1999) Crustaceana, 72, pp. 39-42. , https://doi.org/10.1163/156854099504068
  • Sant’Anna, B.S., Watanabe, T.T., Turra, A., Zara, F.J., Relative abundance and population biology of the non-indigenous crab Charybdis hellerii (Crustacea: Brachyura: Portunidae) in a southwestern Atlantic estuary-bay complex (2012) Aquat Invasions, 7, pp. 347-356. , https://doi.org/org/10.3391/ai.2012.7.3.006
  • Dineen, J., Clark, P., Hines, A., Reed, S., Walton, H., Life history, larval description, and natural history of Charybdis hellerii (Decapoda, Brachyura, Portunidae), an invasive crab in the western Atlantic (2001) J Crustac Biol, 21, pp. 774-805
  • Stasolla, G., Innocenti, G., New records of the invasive crabs Callinectes sapidus Rathbun, 1896 and Percnon gibbesi (H. Milne Edwards, 1853) along the Italian coasts (2014) BioInvasions Rec, 3, pp. 39-43. , https://doi.org/10.3391/bir.2014.3.1.07
  • Garcia, L., Pinya, S., Colomar, V., París, T., Puig, M., Rebassa, M., The first recorded occurrences of the invasive crab Callinectes sapidus Rathbun, 1896 (Crustacea: Decapoda: Portunidae) in coastal lagoons of the Balearic Islands (Spain) (2018) BioInvasion Rec, 7, pp. 191-196. , https://doi.org/10.3391/bir.2018.7.2.12
  • Klotz, W., Miesen, F.W., Hüllen, S., Herder, F., Two Asian fresh water shrimp species found in a thermally polluted stream system in north Rhine-Westphalia, Germany (2013) Aquat Invasions, 8, pp. 333-339. , https://doi.org/10.3391/ai.2013.8.3.09
  • Ricciardi, A., Rasmussen, J.B., Predicting the identity and impact of future biological invaders: A priority for aquatic resource management (1998) Can J Fish Aquat Sci, 55, pp. 1759-1765. , https://doi.org/10.1890/02-0571
  • Marin, I., Korn, O.M., Kornienko, E.S., On the presence of the caridean shrimp Lysmata vittata (Decapoda, Hippolytidae) in the Russian waters of the Sea of Japan (2012) Crustaceana, 85, pp. 123-124. , https://doi.org/10.1163/156854012X623548
  • Marin, I.N., Korn, O.M., Kornienko, E.S., The caridean shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Hippolytidae): A new species for the fauna of Russia (2012) Russ J Mar Biol, 38, pp. 359-363. , https://doi.org/10.1134/S1063074012040062
  • Wang, Y.-R., Sha, Z.-L., Description of two new species of Lysmata Risso, 1816 (Decapoda, Lysmatidae) from the China seas, with remarks on Lysmata vittata (Stimpson 1860) (2018) Zootaxa, 4392, pp. 28-40. , https://doi.org/10.11646/zootaxa.4392.1.2, PMID: 29690415
  • Ahyong, S.T., New species and new records of Caridea (Hippolytidae: Pasiphaeidae) from New Zealand (2010) Zootaxa, 357, pp. 341-357
  • Almeida, A.S., Barros-Alves, S.P., Hirose, G.L., Alves, D.F.R., Reproductive output of the ornamental shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Caridea) in wild populations and under different maturation diets (2018) Invertebr Reprod Dev, , https://doi.org/10.1080/07924259.2018.1509903
  • Soledade, G.O., Baeza, J.A., Boehs, G., Simões, S.M., Santos, P.S., Costa, R.C., A precautionary tale when describing species in a world of invaders: Morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. Vittata (2013) J Crustac Biol, 33, pp. 66-77. , https://doi.org/10.1163/1937240X-00002122
  • Alves, D.F.R., Lima, D.J.M., Hirose, G.L., Martinez, P.A., Dolabella, S.S., Barros-Alves, S.P., Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic (2018) Zootaxa, 4526, pp. 41-55. , https://doi.org/10.11646/zootaxa.4526.1.3, 30486089
  • Fiedler, G., Functional, simultaneous hermaphroditism in female-phase Lysmata amboinensis (Decapoda: Caridea: Hippolytidae) (1998) Pacific Sci, 52, pp. 161-169
  • Bauer, R.T., Newman, W.A., Protandric simultaneous hermaphroditism in the marine shrimp Lysmata cali-fornica (Caridea: Hippolytidae) (2004) J Crustac Biol, 24, pp. 131-139
  • Baeza, J.A., Protandric simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Lysmatidae): Implications for the evolution of hermaphroditism in the genus (2009) Smiths Contr Mar Sci, 38, pp. 95-110
  • Baeza, J.A., Fuentes, M.S., Exploring phylogenetic informativeness and nuclear copies of mitochondrial DNA (Numts) in three commonly used mitochondrial genes: Mitochondrial phylogeny of peppermint, cleaner, and semi-terrestrial shrimps (Caridea: Lysmata, Exhippolysmata, and Merguia) (2013) Zool J Linn Soc, 168, pp. 699-722. , https://doi.org/10.1111/zoj.12044
  • Baeza, J.A., Molecular phylogeny of broken-back shrimps (genus Lysmata and allies): A test of the “Tom-linson-Ghiselin” hypothesis explaining the evolution of hermaphroditism (2013) Mol Phylogenet Evol, 69, pp. 46-62. , https://doi.org/10.1016/j.ympev.2013.05.013, PMID: 23727055
  • Bauer, R.T., Holt, G.T., Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): An undescribed sexual system in the decapod Crustacea (1998) Mar Biol, 132, pp. 223-235
  • Hayes, K.R., Barry, S.C., Are there any consistent predictors of invasion success? (2008) Biol Invasions, 10, pp. 483-506. , https://doi.org/10.1007/s10530-007-9146-5
  • Bazin, É., Mathé-Hubert, H., Facon, B., Carlier, J., Ravigné, V., The effect of mating system on invasiveness: Some genetic load may be advantageous when invading new environments (2014) Biol Invasions, 16, pp. 875-886. , https://doi.org/10.1007/s10530-013-0544-6
  • Lardies, M.A., Bozinovic, F., Genetic variation for plasticity in physiological and life-history traits among populations of an invasive species, the terrestrial isopod Porcellio laevis (2008) Evol Ecol Res, 10, pp. 747-762
  • Lenz, M., Ahmed, Y., Canning-Clode, J., Díaz, E., Eichhorn, S., Fabritzek, A.G., Heat challenges can enhance population tolerance to thermal stress in mussels: A potential mechanism by which ship transport can increase species invasiveness (2018) Biol Invasions, 20, pp. 3107-3122. , https://doi.org/10.1007/s10530-018-1762-8
  • Negri, M., Schubart, C.D., Mantelatto, F.L., Tracing the introduction history of the invasive swimming crab Charybdis hellerii (A. Milne-Edwards, 1867) in the Western Atlantic: Evidences of high genetic diversity and multiple introductions (2018) Biol Invasions, pp. 1-28. , https://doi.org/10.1007/s10530-018-1660-0
  • Calado, R., Vitorino, A., Dionísio, G., Dinis, M.T., A recirculated maturation system for marine ornamental decapods (2007) Aquaculture, 263, pp. 68-74. , https://doi.org/10.1016/j.aquaculture.2006.10.013
  • Bauer, R.T., Same sexual system but variable sociobiology: Evolution of protandric simultaneous hermaphroditism in Lysmata shrimps (2006) Integr Comp Biol, 46, pp. 430-438. , https://doi.org/10.1093/icb/icj036, PMID: 21672755
  • Baeza, J.A., Male mating opportunities affect sex allocation in a protrandric-simultaneous hermaphroditic shrimp (2007) Behav Ecol Sociobiol, pp. 365-370. , https://doi.org/10.1007/s00265-006-0265-2
  • Keunecke, K.A., Demarques, R.S., Vianna, M., Verani, J.R., D’Incao, F., Ovarian development stages of Callinectes danae and Callinectes ornatus (Brachyura, Portunidae) (2009) Crustaceana, 82, pp. 753-761. , https://doi.org/10.1163/156854009X423175
  • Gregati, R.A., Fransozo, V., López-Greco, L.S., Negreiros-Fransozo, M.L., Reproductive cycle and ovarian development of the marine ornamental shrimp Stenopus hispidus in captivity (2010) Aquaculture, 306, pp. 185-190. , https://doi.org/10.1016/j.aquaculture.2010.05.009
  • López Greco, L.S., Vazquez, F., Rodríguez, E.M., Morphology of the Male reproductive system and sper-matophore formation in the freshwater “red claw” crayfish Cherax quadricarinatus (Von Martens, 1898) (Decapoda, Parastacidae) (2007) Acta Zool, 88, pp. 223-229. , https://doi.org/10.1111/j.1463-6395.2007.00269.x
  • Tropea, C., López Greco, L.S., Effect of long-term injection of dopamine on the ovarian growth of Cherax quadricarinatus juvenile females (Parastacidae, Decapoda) (2012) Acta Zool, 94, pp. 462-470. , https://doi.org/10.1111/j.1463-6395.2012.00575.x
  • Zar, J.H., (2010) Biostatistical Analysis, , 5th ed. New Jersey: Pearson
  • Crawley, M.J., (2013) Statistical Computing–An Introduction to Data Analysis Using S-Plus, , 2nd ed. London: John Wiley and Sons
  • Turner, R.L., Lawrence, J.M., Volume and composition of echinoderm eggs: Implications for the use of egg size in life history models (1979) Reproductive Ecology of Marine Invertebrates, pp. 25-40. , Stancik SE, editor
  • García-Guerrero, M.U., Hendrickx, M.E., Embryology of decapod crustaceans, II: Gross embryonic development of Petrolisthes robsonae Glassell, 1945 and Petrolisthes armatus (Gibbes, 1850) (Decapoda, Anomura, Porcellanidae) (2006) Crustaceana, 78, pp. 1089-1097. , https://doi.org/10.2307/20107582
  • González-Pisani, X., Dellatorre, F.G., López-Greco, L., Embryology of the spider crabs Leurocyclus tuber-culosus (H. Milne-Edwards & Lucas 1842) and Libinia spinosa (H. Milne-Edwards 1834) (Brachyura, Majoidea) (2007) Zootaxa, 3718 (4), pp. 301-316. , https://doi.org/10.11646/zootaxa.3718.4.1
  • Baeza, J.A., Reitz, J., Collin, R., Protandric simultaneous hermaphroditism and sex ratio in Lysmata nayaritensis Wicksten, 2000 (Decapoda: Caridea) (2007) J Nat Hist, 41, pp. 2843-2850. , https://doi.org/10.1080/00222930701770778
  • d’Udekem d’Acoz, C., Lysmata seticaudata (Risso, 1816) and L. Nilita Dohrn & Holthuis, 1950 are protan-drous simultaneous hermaphrodites (Decapoda, Caridea, Hippolytidae) (2003) Crustaceana, 75, pp. 1149-1152
  • Baeza, J.A., Anker, A., Lysmata hochi n. Sp., a new hermaphroditic shrimp from the southwestern Caribbean sea (Caridea: Hippolytidae) (2008) J Crustac Biol, 28, pp. 148-155
  • Bauer, R.T., Remarkable Shrimps—Adaptations and natural history of the carideans (2004) Reproductive Biology
  • Bauer, R.T., Chemical communication in decapod shrimps: The influence of mating and social systems on the relative importance of olfactory and contact pheromones (2011) Chemical Communication in Crustaceans, pp. 277-296. , https://doi.org/10.1007/978-0-387-77101-4, Breithaupt T, editor
  • Bauer, R.T., Martin, J., (1991) Crustacean Sexual Biology, , New York: Columbia University Press
  • Tziouveli, V., Hall, M., Smith, G.G., Evaluation of lipid-enriched Artemia on the reproductive performance of the white-striped cleaner shrimp, Lysmata amboinensis (2012) Aquac Int, 20, pp. 201-211. , https://doi.org/10.1007/s10499-011-9496-y
  • Bauer, R.T., Cost of maleness on brood production in the shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae), a protandric simultaneous hermaphrodite (2005) J Mar Biol Assoc UK, 85, pp. 101-106. , https://doi.org/10.1017/S0025315405010891h
  • García-Guerrero, M., Villarreal, H., Racotta, I.S., Effect of temperature on lipids, proteins, and carbohydrates levels during development from egg extrusion to juvenile stage of Cherax quadricarinatus (Decapoda: Parastacidae) (2003) Comp Biochem Physiol—A Mol Integr Physiol, 135, pp. 147-154. , https://doi.org/10.1016/S1095-6433(02)00354-9, PMID: 12727551
  • Brillon, S., Lambert, Y., Dodson, J., Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions (2005) Mar Biol, 147, pp. 895-911. , https://doi.org/10.1007/s00227-005-1633-6
  • Martins, J., Ribeiro, K., Rangel-Figueiredo, T., Coimbra, J., Reproductive cycle, ovarian development, and vertebrate-type steroids profile in the freshwater prawn Macrobrachium rosembergii (2007) J Crustac Biol, 27, pp. 220-228
  • Silva, G.M.F., Ferreira, P.M.A., von Ledebur, E.I.C.F., Rocha, R.M., Gonadal structure analysis of Macrobrachium amazonicum (Heller, 1862) from a wild population: A new insight into the morphotype characterization (2009) Aquac Res, 40, pp. 798-803. , https://doi.org/10.1111/j.1365-2109.2009.02165.x
  • Triay-Portella, R., Ruiz-Díaz, R., Pajuelo, J.G., González, J.A., Ovarian maturity, egg development, and offspring generation of the deep-water shrimp Plesionika edwardsii (Decapoda, Pandalidae) from three isolated populations in the eastern North Atlantic (2017) Mar Biol Res, 13, pp. 174-187. , https://doi.org/10.1080/17451000.2016.1239018
  • Romero-Carvajal, A., Turnbull, M.W., Baeza, J.A., Embryonic development in the peppermint shrimp, Lysmata boggessi (Caridea: Lysmatidae) (2018) Biol Bull, 234. , https://doi.org/10.1086/698468, PMID: 29949441
  • Klann, M., Scholtz, G., Early embryonic development of the freshwater shrimp Caridina multidentata (Crustacea, Decapoda, Atyidae) (2014) Zoomorphology, 133, pp. 295-306. , https://doi.org/10.1007/s00435-014-0224-9
  • Hertzler, P., Crustacea: Decapoda (Dendrobranchiata) (2015) Evolutionary Developmental Biology of Invertebrates, pp. 63-100. , Wanninger A, editor. Vienna: Springer
  • Fletcher, D.J., Kotter, I., Wunsch, M., Yasir, I., Preliminary observations on the reproductive biology of ornamental cleaner prawns. Stenopus hispidus, Lysmata amboinensis and Lysmata debelius (1995) Int Zoo Yearb, 34, pp. 73-77. , https://doi.org/10.1111/j.1748-1090.1995.tb00661.x
  • Calado, R., Dionísio, G., Dinis, M.T., Starvation resistance of early zoeal stages of marine ornamental shrimps Lysmata spp. (Decapoda: Hippolytidae) from different habitats (2007) J Exp Mar Bio Ecol, 351, pp. 226-233. , https://doi.org/10.1016/j.jembe.2007.06.022
  • Morran, L.T., Schmidt, O.G., Gelarden, I.A., Parrish, R.C., Lively, C.M., Running with the Red Queen: Host-parasite coevolution selects for biparental sex (2011) Science, 333, pp. 216-218. , https://doi.org/10.1126/science.1206360, PMID: 21737739
  • Hiller, A., Lessios, H.A., Phylogeography of Petrolisthes armatus, an invasive species with low dispersal ability (2017) Sci Rep, 7, p. 3359. , https://doi.org/10.1038/s41598-017-03410-8, PMID: 28611408
  • Yang, H.J., Kim, C.H., Zoeal stages of Lysmata vittata (Decapoda: Caridea: Hippolytidae) reared in the laboratory (2010) Korean J Syst Zool, 26, pp. 261-278. , https://doi.org/10.5635/KJSZ.2010.26.3.261
  • Gore, R.H., Petrolisthes armatus (Gibbes, 1850): The development under laboratory conditions of larvae from a Pacific specimen (Decapoda, Porcellanidae) (1972) Crustaceana, 22, pp. 67-83. , https://doi.org/10.1163/156854072X00688
  • Tavares, M., Alien decapod crustaceans in the southwestern Atlantic Ocean (2011) The Wrong Place—Alien Marine Crustaceans: Distribution, Biology and Impacts, 6, pp. 251-268. , https://doi.org/10.1007/978-94-007-0591-3, Galil BS, editor. In Springer Series in Invasion Ecology

Citas:

---------- APA ----------
Alves, D.F.R., López Greco, L.S., de Paiva Barros-Alves, S. & Hirose, G.L. (2019) . Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean. PLoS ONE, 14(1).
http://dx.doi.org/10.1371/journal.pone.0210723
---------- CHICAGO ----------
Alves, D.F.R., López Greco, L.S., de Paiva Barros-Alves, S., Hirose, G.L. "Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean" . PLoS ONE 14, no. 1 (2019).
http://dx.doi.org/10.1371/journal.pone.0210723
---------- MLA ----------
Alves, D.F.R., López Greco, L.S., de Paiva Barros-Alves, S., Hirose, G.L. "Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean" . PLoS ONE, vol. 14, no. 1, 2019.
http://dx.doi.org/10.1371/journal.pone.0210723
---------- VANCOUVER ----------
Alves, D.F.R., López Greco, L.S., de Paiva Barros-Alves, S., Hirose, G.L. Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean. PLoS ONE. 2019;14(1).
http://dx.doi.org/10.1371/journal.pone.0210723