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Abstract:

The present study was aimed at evaluating the effect of male presence on ovarian maturation in juvenile females and the role of potential chemical, visual and tactile cues emitted by males in that physiological process. A highly gregarious caridean shrimp with sexual dimorphism, Neocaridina davidi, was used as experimental model. We tested the hypothesis that male presence accelerates ovarian maturation, mainly through chemical cues. Two experiments were performed. In Experiment 1, juvenile females were reared with adult males, adult females or alone, allowing full contact among shrimps. In Experiment 2, these treatments were evaluated allowing chemical and visual communication, only visual communication, or only chemical communication among shrimps. In both experiments juvenile females were observed once a week under a stereomicroscope to determine ovarian growth rate. Although male presence was not necessary for ovarian maturation, it clearly accelerated the rate of ovarian growth, particularly in the last maturation phase. This lead to relatively longer mature ovaries with higher lipid content. On the contrary, the presence of adult females delayed ovarian maturation in juvenile females, while females reared alone showed an intermediate ovarian growth. All these results suggest that adult males release certain cues that stimulate ovarian maturation, while adult females release cues that delay this physiological process. Neither visual cues nor chemical cues released at a distance from females were responsible, either alone or in combination, for the observed effects. Ovarian growth was only influenced when shrimps were allowed to interact freely, probably because of the “mounting” behavior of males towards females. Tactile cues and/or potential chemical cues released by males during this behavior may mediate male stimulatory effect on ovarian growth. Altogether, present results partially support our initial hypothesis and contribute to increase the limited amount of information available on the role of intraspecific multimodal communication in non-behavioral reproductive processes in invertebrate species. © 2018 Elsevier GmbH

Registro:

Documento: Artículo
Título:Getting ready for mating: The importance of male touching as an accelerator of ovarian growth in a caridean shrimp
Autor:Tropea, C.; Lavarías, S.M.L.; López Greco, L.S.
Filiación: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, Ciudad Universitaria, Buenos Aires, C1428EGA, Argentina
Instituto de Limnología de La Plata “Dr. Raúl A. Ringuelet” (ILPLA), CCT CONICET La Plata, Universidad Nacional de La Plata (UNLP), La Plata, Argentina
Palabras clave:caridean shrimps; chemical cues; intraspecific communication; ovarian maturation; tactile cues; anatomy and histology; animal; association; Decapoda (Crustacea); female; growth, development and aging; male; ovary; physiology; sexual behavior; sexual maturation; touch; Animals; Cues; Decapoda (Crustacea); Female; Male; Ovary; Sexual Behavior, Animal; Sexual Maturation; Touch
Año:2018
Volumen:130
Página de inicio:57
Página de fin:66
DOI: http://dx.doi.org/10.1016/j.zool.2018.08.003
Título revista:Zoology
Título revista abreviado:Zoology
ISSN:09442006
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09442006_v130_n_p57_Tropea

Referencias:

  • Abbott, D.H., Saltzman, W., Schultz‐Darken, N.J., Smith, T.E., Specific neuroendocrine mechanisms not involving generalized stress mediate social regulation of female reproduction in cooperatively breeding marmoset monkeys (1997) Annals NY Acad. Sci., 807, pp. 219-238
  • Acquistapace, P., Aquiloni, L., Hazlett, B.A., Gherardi, F., Multimodal communication in crayfish: sex recognition during mate search by male Austropotamobius pallipes (2002) Can. J. Zool., 80, pp. 2041-2045
  • Andrés, M., Estévez, A., Simeó, C., Rotllant, G., Annual variation in the biochemical composition of newly hatched larvae of Maja brachydactyla in captivity (2010) Aquaculture, 310, pp. 99-105
  • Aquiloni, L., Gherardi, F., Evidence of female cryptic choice in crayfish (2008) Biol. Let., 4, pp. 163-165
  • Atema, J., Steinbach, M.A., Chemical communication and social behavior of the lobster Homarus americanus and other decapod Crustacea (2007) Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms, pp. 115-146. , J.E. Duffy M. Thiel Oxford University Press New York
  • Bauer, R.T., Sex attraction and recognition in the caridean shrimp Heptacarpus paludicola Holmes (Decapoda: Hippolytidae) (1979) Mar. Freshw. Behav. Phy., 6, pp. 157-174
  • Bauer, R.T., Remarkable Shrimps: Adaptations and Natural History of the Carideans (2004), University of Oklahoma Press Norman; Bennett, N.C., Faulkes, C.G., Spinks, A.C., LH responses to single doses of exogenous GnRH by social Mashona mole-rats: a continuum of socially-induced infertility in the family Bathyergidae (1997) Proc. R. Soc. Lond., 264B, pp. 1001-1006
  • Berry, F.C., Breithaupt, T., To signal or not to signal? Chemical communication by urine-borne signals mirrors sexual conflict in crayfish (2010) BMC Biol., 8, p. 25
  • Bjerkeng, B., Carotenoids in aquaculture: fish and crustaceans (2008) Carotenoids: Natural Functions, 4, pp. 237-254. , G. Britton S. Liaaen-Jensen H. Pfander Birkhauser Verlag AG Basel
  • Borowsky, B., Borowsky, R., The reproductive behaviors of the amphipod crustacean Gammarus palustris (Bousfield) and some insights into the nature of their stimuli (1987) J. Exp. Mar. Biol. Ecol., 107, pp. 131-144
  • Bronson, F.H., Desjardins, C., Circulating concentrations of FSH, LH, oestradiol and progesterone associated with acute male-induced puberty in female mice (1974) Endocrinology, 94, pp. 1658-1661
  • Brooks, P.H., Cole, D.J., The effect of the presence of a boar on the attainment of puberty in gilts (1970) J. Reprod. Fertil., 23, pp. 435-440
  • Bushmann, P.J., Concurrent signals and behavioral plasticity in blue crab (Callinectes sapidus Rathbun) courtship (1999) Biol. Bul., 197, pp. 63-71
  • Caskey, J.L., Bauer, R.T., Behavioral tests for a possible contact sex pheromone in the caridean shrimp Palaemonetes pugio (2005) J. Crust. Biol., 25, pp. 571-576
  • Chak, S.T., Bauer, R.T., Thiel, M., Social behaviour and recognition in decapod shrimps, with emphasis on the Caridea (2015) Social Recognition in Invertebrates, pp. 57-84. , L. Aquiloni E. Tricarico Springer Cham
  • Charron, L., Geffard, O., Chaumot, A., Coulaud, R., Jaffal, A., Gaillet, V., Dedourge-Geffard, O., Geffard, A., Consequences of lower food intake on the digestive enzymes activities, the energy reserves and the reproductive outcome in Gammarus fossarum (2015) PloS One, 10
  • Chatzifotis, S., Papadaki, M., Despoti, S., Roufidou, C., Antonopoulou, E., Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax) (2011) Aquaculture, 316, pp. 53-59
  • Christy, J.H., Salmon, M., Comparative studies of reproductive behavior in mantis shrimps and fiddler crabs (1991) Am. Zool., 31, pp. 329-337
  • Christy, J.H., Backwell, P.R.Y., Schober, U., Interspecific attractiveness of structures built by courting male fiddler crabs: experimental evidence of a sensory trap (2003) Behav. Ecol. Sociobiol., 53, pp. 84-91
  • Chung-Davidson, Y.W., Wang, H., Siefkes, M.J., Bryan, M.B., Wu, H., Johnson, N.S., Li, W., Pheromonal bile acid 3-ketopetromyzonol sulfate primes the neuroendocrine system in sea lamprey (2013) BMC Neurosci., 14, p. 11
  • Correa, C., Thiel, M., Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology (2003) Rev. Chil. Hist. Nat., 76, pp. 187-203
  • Cunningham, E.J.A., Russell, A.F., Egg investment is influenced by male attractiveness in the mallard (2000) Nature, 404, pp. 74-77
  • Di Rienzo, J.A., Guzmán, A.W., Casanoves, F., A multiple-comparisons method based on the distribution of the root node distance of a binary tree (2002) J. Agric. Biol. Envir. S, 7, pp. 129-142
  • Díaz, E.R., Thiel, M., Chemical and visual communication during mate searching in rock shrimp (2004) Biol. Bul., 206, pp. 134-143
  • Drickamer, L.C., Delay of sexual maturation in female house mice by exposure to grouped females or urine from grouped females (1977) J. Reprod. Fertil., 51, pp. 77-81
  • Endler, A., Liebig, J., Schmitt, T., Parker, J.E., Jones, G.R., Schreier, P., Hölldobler, B., Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect (2004) Proc. Natl. Acad. Sci. USA, 101, pp. 2945-2950
  • Fingerman, M., The endocrine mechanisms of crustaceans (1987) J. Crust. Biol., 7, pp. 1-24
  • Folch, J., Lees, M., Sloane Stanley, G.H., A simple method for the isolation and purification of total lipids from animal tissues (1957) J. Biol. Chem., 226, pp. 497-509
  • George, S.B., Lawrence, J.M., Lawrence, A.L., Smiley, J., Plank, L., Carotenoids in the adult diet enhance egg and juvenile production in the sea urchin Lytechinus variegatus (2001) Aquaculture, 199, pp. 353-369
  • Gil, D., Graves, J., Hazon, N., Wells, A., Male attractiveness and differential testosterone investment in zebra finch (1999) Science, 286, pp. 126-128
  • Gwynne, D.T., Sexual competition among females: What causes courtship-role reversal? (1991) Trends Ecol. Evol., 6, pp. 118-121
  • Hardege, J.D., Jennings, A., Hayden, D., Müller, C.T., Pascoe, D., Bentley, M.G., Clare, A.S., Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas (2002) Mar. Ecol. Prog. Ser., 244, pp. 179-189
  • Hazlett, B.A., Rittschof, D., Variation in rate of growth in the crayfish Orconectes virilis (1985) J. Crust. Biol., 5, pp. 341-346
  • Herring, P.J., Depth distribution of the carotenoid pigments and lipids of some oceanic animals. 2. Decapod crustaceans (1973) J. Mar. Biol. Assoc. UK, 53, pp. 539-562
  • Holman, L., Jørgensen, C.G., Nielsen, J., d'Ettorre, P., Identification of an ant queen pheromone regulating worker sterility (2010) Proc. R. Soc. London, 277B, pp. 3793-3800
  • Huertas, M., Almeida, O.G., Canário, A.V., Hubbard, P.C., Tilapia male urinary pheromone stimulates female reproductive axis (2014) Gen. Comp. Endocr., 196, pp. 106-111
  • Hughes, M., The function of concurrent signals: visual and chemical communication in snapping shrimp (1996) Anim. Behav., 52, pp. 247-257
  • Izard, M.K., Pheromones and reproduction in domestic animals (1983) Pheromones and Reproduction in Mammals., pp. 253-285. , J.G. Vandenbergh Academic Press New York
  • Izquierdo, M.S., Fernández-Palacios, H., Tacon, A.G.J., Effect of broodstock nutrition on reproductive performance of fish (2001) Aquaculture, 197, pp. 25-42
  • Johnston, T.A., Wiegand, M.D., Leggett, W.C., Pronyk, R.J., Dyal, S.D., Watchorn, K.E., Kollar, S., Casselman, J.M., Hatching success of walleye embryos in relation to maternal and ova characteristics (2007) Ecol. Freshw. Fish, 16, pp. 295-306
  • Kamio, M., Matsunaga, S., Fusetani, N., Copulation pheromone in the crab Telmessus cheiragonus (Brachyura: Decapoda) (2002) Mar. Ecol. Prog. Ser., 234, pp. 183-190
  • Karplus, I., Barki, A., Social control of growth in the redclaw crayfish, Cherax quadricarinatus: testing the sensory modalities involved (2004) Aquaculture, 242, pp. 321-333
  • Karplus, I., Malecha, S.R., Sagi, A., The biology and management of size variation (2000) Freshwater Prawn Culture: the Farming of Macrobrachium rosenbergii, pp. 259-289. , M.V. New W.C. Valenti Blackwell Science Ltd London
  • Kolm, N., Females produce larger eggs for large males in a paternal mouthbrooding fish (2001) Proc. R. Soc. B, 268, pp. 2229-2234
  • Kotiaho, J.S., Simmons, L.W., Hunt, J., Tomkins, J.L., Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetle Ontophagus taurus (2003) Am. Nat., 161, pp. 852-859
  • Kraus, C., Heistermann, M., Kappeler, P.M., Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? (1999) Physiol. Behav., 66, pp. 855-861
  • Latruffe, C., McGregor, P.K., Oliveira, R.F., Visual signaling and sexual selection in male fiddler crabs Uca tangeri (1999) Mar. Ecol. Prog. Ser., 189, pp. 233-240
  • Ma, W.D., Miao, Z.S., Novotny, M.V., Induction of estrus in grouped female mice (Mus domesticus) by synthetic analogues of preputial gland constituants (1999) Chem. Senses, 24, pp. 289-293
  • Marshall, J., Cronin, T.W., Shashar, N., Land, M., Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication (1999) Curr. Biol., 9, pp. 755-758
  • Martin, G.B., Oldham, C.M., Cognie, Y., Pearce, D.T., The physiological responses of anovulatory ewes to the introduction of rams – a review (1986) Livest. Prod. Sci., 15, pp. 219-247
  • Mathews, L.M., Tests of the mate-guarding hypothesis for social monogamy: male snapping shrimp prefer to associate with high-value females (2003) Behav. Ecol., 14, pp. 63-67
  • Matsuura, K., Himuro, C., Yokoi, T., Yamamoto, Y., Vargo, E.L., Keller, L., Identification of a pheromone regulating caste differentiation in termites (2010) Proc. Natl. Acad. Sci. USA, 107, pp. 12963-12968
  • Murata, K., Wakabayashi, Y., Kitago, M., Ohara, H., Watanabe, H., Tamogami, S., Warita, Y., Okamura, H., Modulation of gonadotrophin‐releasing hormone pulse generator activity by the pheromone in small ruminants (2009) J. Neuroendocrinol., 21, pp. 346-350
  • Nagabhushanam, R., Machale, P.R., Sarojini, R., Pheromonal and hormonal control of reproduction in the freshwater prawn, Macrobrachium kistnensis (1989) Proc. Anim. Sci., 98, pp. 95-98
  • Novotny, M.V., Ma, W.D., Wiesler, D., Zidek, L., Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein (1999) Proc. Royal Soc. London Ser. Biol. Sci., 266, pp. 2017-2022
  • Palacios, E., Racotta, I.S., Marty, Y., Samain, J.F., Lipid composition during embryogenesis and early larval development in shrimp (Penaeus vannamei) (2001) Larvi 2001 Fish and Crustacean Larviculture Symposium, pp. 453-456. , C.I. Hendry G. Van Stappen M. Wille P. Sorgeloos Ghent, Belgium
  • Raethke, N., MacDiarmid, A.B., Montgomery, J.C., The role of olfaction during mating in the southern temperate spiny lobster Jasus edwardsii (2004) Horm. Behav., 46, pp. 311-318
  • Reimers, E., Kjørrefjord, A.G., Stavøstrand, S.M., Compensatory growth and reduced maturation in second sea winter farmed Atlantic salmon following starvation in February and March (1993) J. Fish Biol., 43, pp. 805-810
  • Reyer, H.U., Frei, G., Som, C., Cryptic female choice: frogs reduce their clutches when amplexed by undesired male (1999) Proc. R. Soc. B, 266, pp. 2101-2107
  • Rotllant, G., Simeó, C., Guerao, G., Sastre, M., Cleary, D., Calado, R., Estévez, A., Interannual variability in the biochemical composition of newly hatched larvae of the spider crab Maja brachydactyla (Decapoda, Majidae) (2014) Mar. Ecol., 35, pp. 298-307
  • Rybak, F., Sureau, G., Aubin, T., Functional coupling of acoustic and chemicals signals in the courtship behaviour of the male Drosophila melanogaster (2002) Proc. Royal Soc. London Ser. Biol. Sci., 269, pp. 695-701
  • Saino, N., Ferrari, R.P., Martinelli, R., Romano, M., Rubolini, D., Møller, A.P., Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner (2002) Proc. R. Soc. 269B, pp. 1005-1009
  • Sal Moyano, M.P., Silva, P., Luppi, T., Gavio, M.A., Female mate choice by chemical signals in a semi-terrestrial crab (2014) J. Sea Res., 85, pp. 300-307
  • Salmon, M., Courtship, mating systems, and sexual selection in decapods (1983) Studies in Adaptation: the Behavior of Higher Crustaceans, pp. 143-169. , S. Rebach D.W. Dunham John Wiley & Sons New York
  • Schmidt, M., Mellon, D., Neuronal processing of chemical information in crustaceans (2010) Chemical Communication in Crustaceans, pp. 123-147. , T. Breithaup M. Thiel Springer New York
  • Seibt, U., Wickler, W., The biological significance of the pair‐bond in the shrimp Hymenocera picta (1979) Ethology, 50, pp. 166-179
  • Sganga, D.E., Tropea, C., Valdora, M., Statti, M.F., López-Greco, L.S., Large mothers, but not large fathers, influence offspring number in a caridean shrimp (2018) Can. J. Zool.
  • Sheldon, B.C., Differential allocation: tests, mechanisms and implications (2000) Trends Ecol. Evol., 15, pp. 397-402
  • Shih, H.T., Cai, Y., Two new species of the land-locked freshwater shrimps genus, Neocaridina Kubo, 1938 (Decapoda: Caridea: Atyidae), from Taiwan, with notes on speciation on the island (2007) Zool. Stud., 46, p. 680
  • Slessor, K.N., Winston, M.L., Le Conte, Y., Pheromone communication in the honeybee (Apis mellifera L.) (2005) J. Chem. Ecol., 31, pp. 2731-2745
  • Sokal, R.R., Rohlf, F.J., Biometry (1995), W.H. Freeman New York; Takács, S., Mistal, C., Gries, G., Communication ecology of webbing clothes moth: attractiveness and characterization of male-produced sonic aggregation signals (2003) J. Appl. Entomol., 127, pp. 127-133
  • Takayanagi, H., Yamamoto, Y., Takeda, N., Ovary‐stimulating pheromone in the freshwater shrimp, Paratya compressa (1986) J. Exp. Zool., 240A, pp. 397-400
  • Trhlin, M., Rajchard, J., Chemical communication in the honeybee (Apis mellifera L.), a review (2011) Vet. Med., 56, pp. 265-273
  • Tropea, C., López Greco, L.S., Morfología ovárica en el camarón ornamental de desarrollo directo, Neocaridina davidi (Decapoda, Atyidae) (2016) Proc. from IV Congreso Uruguayo de Zoología, Montevideo, Uruguay, , December 4–9th
  • Tropea, C., Stumpf, L., López Greco, L.S., Effect of temperature on biochemical composition, growth and reproduction of the ornamental red cherry shrimp Neocaridina heteropoda heteropoda (Decapoda, Caridea) (2015) PLoS One, 10
  • Uetz, G.W., Roberts, J.A., Multisensory cues and multimodal in spiders: insights from video/audio playback studies (2002) Brain Behav. Evol., 59, pp. 222-230
  • Urzúa, Á., Paschke, K., Gebauer, P., Anger, K., Seasonal and interannual variations in size, biomass and chemical composition of the eggs of North Sea shrimp, Crangon crangon (Decapoda: Caridea) (2012) Mar. Biol., 159, pp. 583-599
  • Vandenbergh, J.G., Puberty acceleration (1999) Encyclopedia of Reproduction, pp. 563-565. , E. Knobil J.D. Neill Academic Press New York
  • Vazquez, N.D., Delevati-Colpo, K., Sganga, D.E., López-Greco, L.S., Density and gender segregation effects in the culture of the caridean ornamental red cherry shrimp Neocaridina davidi Bouvier, 1904 (Caridea: Atyidae) (2017) J. Crust. Biol., 37, pp. 367-373
  • Wanner, K.W., Nichols, A.S., Walden, K.K.O., Brockmann, A., Luetje, C.W., Robertson, H.M., A honeybee odorant receptor for the queen substance 9-oxo-2- decenoic acid (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 14383-14388
  • Weber, S., Traunspurger, W., Influence of the ornamental red cherry shrimp Neocaridina davidi (Bouvier, 1904) on freshwater meiofaunal assemblages (2016) Limnologica, 59, pp. 155-161
  • Wouters, R., Molina, C., Lavens, P., Calderon, J., Lipid composition and vitamin content of wild female Litopenaeus vannamei in different stages of sexual maturation (2001) Aquaculture, 198, pp. 307-323
  • Zhang, D., Lin, J., Mate recognition in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Caridea: Hippolytidae) (2006) Anim. Behav., 71, pp. 1191-1196
  • Zhang, D., Terschak, J.A., Harley, M.A., Lin, J., Hardege, J.D., Simultaneously hermaphroditic shrimp use lipophilic cuticular hydrocarbons as contact sex pheromones (2011) PLoS One, 6

Citas:

---------- APA ----------
Tropea, C., Lavarías, S.M.L. & López Greco, L.S. (2018) . Getting ready for mating: The importance of male touching as an accelerator of ovarian growth in a caridean shrimp. Zoology, 130, 57-66.
http://dx.doi.org/10.1016/j.zool.2018.08.003
---------- CHICAGO ----------
Tropea, C., Lavarías, S.M.L., López Greco, L.S. "Getting ready for mating: The importance of male touching as an accelerator of ovarian growth in a caridean shrimp" . Zoology 130 (2018) : 57-66.
http://dx.doi.org/10.1016/j.zool.2018.08.003
---------- MLA ----------
Tropea, C., Lavarías, S.M.L., López Greco, L.S. "Getting ready for mating: The importance of male touching as an accelerator of ovarian growth in a caridean shrimp" . Zoology, vol. 130, 2018, pp. 57-66.
http://dx.doi.org/10.1016/j.zool.2018.08.003
---------- VANCOUVER ----------
Tropea, C., Lavarías, S.M.L., López Greco, L.S. Getting ready for mating: The importance of male touching as an accelerator of ovarian growth in a caridean shrimp. Zoology. 2018;130:57-66.
http://dx.doi.org/10.1016/j.zool.2018.08.003