Hostname: page-component-77c89778f8-9q27g Total loading time: 0 Render date: 2024-07-18T10:51:48.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Maximum gonad investment of the sexes of the broadcast-spawning sea cucumber Holothuria (Halodeima) inornata (Echinodermata: Holothuroidea)

Published online by Cambridge University Press:  15 February 2022

Omar Hernando Avila-Poveda Open the ORCID record for Omar Hernando Avila-Poveda [Opens in a new window] ,
Francisco Benítez-Villalobos Open the ORCID record for Francisco Benítez-Villalobos [Opens in a new window] ,
Geoff A. Parker Open the ORCID record for Geoff A. Parker [Opens in a new window] ,
Heleni Cancino-Guzman  and
Everardo Ramos-Ramirez
Omar Hernando Avila-Poveda*
Affiliation:
Facultad de Ciencias del Mar (FACIMAR), Universidad Autónoma de Sinaloa (UAS), Mazatlán, Sinaloa, México Programa de Investigadoras e Investigadores por México, Consejo Nacional de Ciencia y Tecnología (CONACyT), Ciudad de México, México
Francisco Benítez-Villalobos*
Affiliation:
Instituto de Recursos, Universidad del Mar (UMAR), Puerto Angel, Oaxaca, Mexico
Geoff A. Parker
Affiliation:
Department of Evolution, Ecology and Behaviour, University of Liverpool, Liverpool, UK
Heleni Cancino-Guzman
Affiliation:
Instituto de Biociencias, Universidad Autónoma de Chiapas (UNACH), Tapachula, Chiapas, México
Everardo Ramos-Ramirez
Affiliation:
Licenciatura en Biología Marina, Universidad del Mar (UMAR), Puerto Ángel, Oaxaca, México
*
Author for correspondence: Omar Hernando Avila-Poveda, E-mail: oavila@uas.edu.mx, ohavilapo@conacyt.mx; Francisco Benítez-Villalobos, E-mail: fbv@angel.umar.mx
Author for correspondence: Omar Hernando Avila-Poveda, E-mail: oavila@uas.edu.mx, ohavilapo@conacyt.mx; Francisco Benítez-Villalobos, E-mail: fbv@angel.umar.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

An organism's maximum gonad investment (MGI) typically indicates its reproductive season and is often measured by the peak of the gonadosomatic index. Since external sexual dimorphism is often not evident, intrinsic sex differences remain unstudied. We analysed the reproductive seasonality of each sex of the broadcast-spawning sea cucumber Holothuria (Halodeima) inornata in two populations (Caleta de Campos, Michoacán ‘CC’ and Puerto Madero, Chiapas ‘PM’) in the southern coast of the Mexican Pacific by examining: intensity and duration of MGI, frequency of each gonadal developmental stage (GDS) through time, sexual asymmetry in GSI, sexual asymmetry in GDS, and adult sex ratio. We observed a trade-off between the intensity (%) and duration (months) of each sex's MGI: as intensity decreases, duration increases and conversely. The frequency of ripe and spawning stages was consistently higher in females than males. Sexual asymmetry in GSI was slightly female-biased in the PM population, but male-biased in the CC population. Sexual asymmetry in GDS showed a more recurrent sexual equality at PM than at CC. The adult sex ratio of each population did not differ significantly from unity, but showed a near-significant trend for male bias in the CC. Although H. inornata exhibited different MGI responses between males and females and more markedly in CC than in PM, it also showed a synchronized relation between its mass investment (GSI) and physiological investment (GDS), possibly reflecting an optimum reproductive strategy. Lastly, changes in GSI were not underpinned by changes in local temperature, but rather by regional temperature.

Keywords

Gonad expendituregonadosomatic indexmarine invertebrates of Mexican tropical Pacificreproductive season
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 102 , Issue 1-2 , March 2022 , pp. 99 - 111
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abadia-Chanona, QY, Avila-Poveda, OH, Arellano-Martinez, M, Ceballos-Vazquez, BP, Benítez-Villalobos, F, Parker, GA, Rodriguez-Dominguez, G and Garcia-Ibañez, S (2018) Reproductive traits and relative gonad expenditure of the sexes of the free-spawning Chiton articulatus (Mollusca: Polyplacophora). Invertebrate Reproduction and Development 62, 268–289.CrossRefGoogle Scholar
Avila-Poveda, OH, Abadia-Chanona, QY, Alvarez-Garcia, IL and Arellano-Martinez, M (2021) Plasticity in reproductive traits of an intertidal rocky shore chiton (Mollusca: Polyplacophora) under pre-ENSO and ENSO events. Journal of Molluscan Studies 87, eyaa033.CrossRefGoogle Scholar
Benítez-Villalobos, F, Avila-Poveda, OH and Gutierrez-Mendez, IS (2013) Reproductive biology of Holothuria fuscocinerea (Echinodermata: Holothuroidea) from Oaxaca, Mexico. Sexuality and Early Development in Aquatic Organisms 1, 13–24. [Incorporated into Aquatic Biology].CrossRefGoogle Scholar
Benítez-Villalobos, F, Avila-Poveda, OH, Diaz-Martinez, JP and Bravo-Ruiz, AR (2015) Gonad development stages and reproductive traits of Diadema mexicanum (Echinodermata: Echinoidea) from Oaxaca, Mexico. Invertebrate Reproduction and Development 59, 237–249.CrossRefGoogle Scholar
Brewin, PE, Lamare, MD, Keogh, JA and Mladenov, PV (2000) Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitat in New Zealand. Marine Biology 137, 543–557.CrossRefGoogle Scholar
Chao, SM, Chen, CP and Alexander, PS (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Marine Biology 122, 289–295.CrossRefGoogle Scholar
Charnov, EL (1982) The Theory of Sex Allocation. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Crean, AJ and Marshall, DJ (2008) Gamete plasticity in a broadcast spawning marine invertebrate. Proceedings of the National Academy of Sciences USA 105, 13508–13513.CrossRefGoogle Scholar
Crespi-Abril, AC and Rubilar, T (2018) Ética e invertebrados: análisis de los casos de los cefalópodos y equinodermos. Revista Latinoamericana de Estudios Crticos Animales 5, 212–232. [In Spanish].Google Scholar
Eckelbarger, KJ and Hodgson, AN (2021) Invertebrate oogenesis – a review and synthesis: comparative ovarian morphology, accessory cell function and the origins of yolk precursors. Invertebrate Reproduction and Development 65, 71–140.CrossRefGoogle Scholar
Emlen, ST and Oring, LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science (New York, N.Y.) 197, 215–223.CrossRefGoogle ScholarPubMed
Engstrom, NA (1980) Reproductive cycles of Holothuria (Halodeima) floridana, H. (H.) mexicana and their hybrids (Echinodermata: Holothuroidea) in southern Florida, U.S.A. International Journal of Invertebrate Reproduction 2, 237–244.CrossRefGoogle Scholar
Evans, JP and Lymbery, RA (2020) Sexual selection after gamete release in broadcast spawning invertebrates. Philosophical Transactions of the Royal Society B 375, e20200069.Google ScholarPubMed
Flores, A, Wiff, R, Ahumada, M, Queirolo, D and Apablaza, P (2021) Coping with El Nino: phenotypic flexibility of reproductive traits in red squat lobster determines recruitment success. ICES Journal of Marine Science 78, 3709–3723.CrossRefGoogle Scholar
Gianasi, BL, Hamel, JF and Mercier, A (2019) Triggers of spawning and oocyte maturation in the commercial sea cucumber Cucumaria frondosa. Aquaculture 498, 50–60.CrossRefGoogle Scholar
Giese, AC (1959) Comparative physiology: annual reproductive cycles of marine invertebrates. Annual Review of Physiology 21, 547–576.CrossRefGoogle ScholarPubMed
Guzman, HM, Guevara, CA and Hernandez, IC (2003) Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama. Marine Biology 142, 271–279.CrossRefGoogle Scholar
Harrington, LH, Walker, CW and Lesser, MP (2007) Stereological analysis of nutritive phagocytes and gametogenic cells during the annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis. Invertebrate Biology 126, 202–209.CrossRefGoogle Scholar
Hernandez, E, Vázquez, OA, Torruco, A and Rahman, MS (2020) Reproductive cycle and gonadal development of the Atlantic sea urchin Arbacia punctulata in the Gulf of Mexico: changes in nutritive phagocytes in relation to gametogenesis. Marine Biology Research 16, 177–194.CrossRefGoogle Scholar
Humason, GL (1962) Animal Tissue Techniques. San Francisco, CA: WH Freeman & Co.CrossRefGoogle Scholar
Kalachev, AV and Yurchenko, OV (2017) Microautophagy in nutritive phagocytes of sea urchins. Protoplasma 254, 609–614.CrossRefGoogle ScholarPubMed
Karlen, Y, McNair, A, Perseguers, S, Mazza, C and Mermod, N (2007) Statistical significance of quantitative PCR. BMC Bioinformatics 8, e131.CrossRefGoogle ScholarPubMed
Leite-Castro, LV, Souza-Junior, J, Salmito-Vanderley, CSB, Ferreira-Nunes, J, Hamel, JF and Mercier, A (2016) Reproductive biology of the sea cucumber Holothuria grisea in Brazil: importance of social and environmental factors in breeding coordination. Marine Biology 163, e67.CrossRefGoogle Scholar
Levitan, DR (2005) The distribution of male and female reproductive success in a broadcast spawning marine invertebrate. Integrative and Comparative Biology 45, 848–855.CrossRefGoogle Scholar
Levitan, DR (2010) Sexual selection in external fertilisers. In Westneat, DF and Fox, CW (eds), Evolutionary Behavioral Ecology. Oxford: Oxford University Press, pp. 365–378.Google Scholar
Lima-Bueno, M, Garcia-Tavares, YA, Di-Domenico, M and Borges, M (2015) Gametogenesis and weight change of body organs of the sea cucumber Holothuria (Halodeima) grisea (Aspidochirotida: Holothuriidae) in southern Brazil. Revista de Biologia Tropical 63 (Suppl. 2), 285–296.Google Scholar
Lincoln, RJ and Sheals, JG (1979) Invertebrate Animals: Collection and Preservation. London: British Museum and Cambridge University Press.CrossRefGoogle Scholar
Machado, I, Moura, P, Pereira, F, Vasconcelos, P and Gaspar, MB (2019) Reproductive cycle of the commercially harvested sea urchin (Paracentrotus lividus) along the western coast of Portugal. Invertebrate Biology 138, 40–54.CrossRefGoogle Scholar
Magalhaes-de-Souza, ME, Leite, LV, Ribeiro-Pinheiro, RR, Sousa-Junior, J, Ferreira-Nunes, J and Salmito-Vanderley, CSB (2014) Variação do indice gonadal de pepino do mar (Holothuria grisea) no litoral cearense. Acta Veterinaria Brasilica 8 (Suppl. 2), 229–230. [In Portuguese].Google Scholar
Manríquez, PH, Guiñez, R, Olivares, A, Clarke, M and Castilla, JC (2018) Effects of inter-annual temperature variability, including ENSO and post-ENSO events, on reproductive traits in the tunicate Pyura praeputialis. Marine Biology Research 14, 462–477.CrossRefGoogle Scholar
Marquet, N, Conand, C, Power, DM, Canario, AVM and Gonzalez-Wangüemert, M (2017) Sea cucumbers, Holothuria arguinensis and H. mammata, from the southern Iberian Peninsula: variation in reproductive activity between populations from different habitats. Fisheries Research 191, 120–130.CrossRefGoogle Scholar
Maynard Smith, J (1982) Evolution and the Theory of Games. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
McCune, B, Grace, JB and Urban, DL (2002) Analysis of Ecological Communities. Gleneden Beach, OR: MjM Sofware Design.Google Scholar
Mercier, A and Hamel, JF (2009) Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Advances in Marine Biology 55, 1–302.CrossRefGoogle ScholarPubMed
Mezali, K, Soualili, DL, Neghli, L and Conand, C (2014) Reproductive cycle of the sea cucumber Holothuria (Platyperona) sanctori (Holothuroidea: Echinodermata) in the southwestern Mediterranean Sea: interpopulation variability. Invertebrate Reproduction and Development 58, 179–189.CrossRefGoogle Scholar
NOAA (2017) Historical El Nino/La Nina episodes (1950–present) – Cold & Warm Episodes by Season. Accessed through: NOAA/National Weather Service Climate Prediction Centre. Available at https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php (Accessed 01 January 2017).Google Scholar
NOAA (2018) NOAA comprehensive large array-data stewardship system (CLASS): search—SST100. Available at https://www.avl.class.noaa.gov/saa/products/search?datatype_family=SST100 (Accessed 06 January 2018).Google Scholar
Oyarzun, PA, Toro, JE, Garces-Vargas, J, Alvarado, C, Guiñez, R, Jaramillo, R, Briones, C and Campos, B (2018) Reproductive patterns of mussel Perumytilus purpuratus (Bivalvia: Mytilidae), along the Chilean coast: effects caused by climate change? Journal of the Marine Biological Association of the United Kingdom 98, 375–385.CrossRefGoogle Scholar
Parker, GA (2014) The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. Cold Spring Harbor Perspectives in Biology 6, a017509.CrossRefGoogle ScholarPubMed
Parker, GA (2020) Conceptual developments in sperm competition: a very brief synopsis. Philosophical Transactions of the Royal Society B 375, e20200061.CrossRefGoogle ScholarPubMed
Parker, GA and Pizzari, T (2015). Sexual selection: the logical imperative. In Hoquet, T (ed.), Current Perspectives on Sexual Selection. History, Philosophy and Theory of the Life Sciences. Dordrecht: Springer Science + Business Media, pp. 119–163.CrossRefGoogle Scholar
Parker, GA, Ramm, SA, Lehtonen, J and Henshaw, JM (2018) The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast-spawning invertebrates. Biological Reviews 93, 693–753.CrossRefGoogle ScholarPubMed
Ramos-Miranda, J, del Rio-Rodriguez, R, Flores-Hernandez, D, Rojas-Gonzalez, RI, Gomez-Solano, M, Cu-Escamilla, AD, Gomez-Criollo, F, Sosa-Lopez, A, Torres-Rojas, YE and Juarez-Camargo, P (2017) Reproductive cycle of the sea cucumber Holothuria floridana in the littorals of Campeche, Mexico. Fisheries Science 83, 699–714.CrossRefGoogle Scholar
Rubilar, T and Crespi-Abril, A (2017) Does echinoderm research deserve an ethical consideration? Revista de Biologia Tropical 65 (Suppl. 1), S11–S22.CrossRefGoogle Scholar
Sokal, RR and Rohlf, FJ (1995) Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edn. New York, NY: WH Freeman and Co.Google Scholar
Stearns, SC (1992) The Evolution of Life Histories. Oxford: Oxford University Press.Google Scholar
Szekely, T, Weissing, FJ and Komdeur, J (2014) Adult sex ratio variation: implications for breeding system evolution. Journal of Evolutionary Biology 27, 1500–1512.CrossRefGoogle ScholarPubMed
Unuma, T and Walker, CW (2009) Relationship between gametogenesis and food quality in sea urchin gonads. In Stickney R, Iwamoto R, Rust M, eds. Aquaculture Technologies for Invertebrates: Proceedings of the Thirty-sixth U.S.-Japan Aquaculture Panel Symposium; 2007 October 29–30; Durham, New Hampshire and Milford, Connecticut, November 2, 2007. NOAA Tech. Memo. NMFSF/SPO-99, pp. 45–54.Google Scholar
Walker, CW, Lesser, MP and Unuma, T (2013) Sea urchin gametogenesis – structural, functional and molecular/ genomic biology. Developments in Aquaculture and Fisheries Science 38, 25–43.CrossRefGoogle Scholar
Wolter, KM (2007) Introduction to Variance Estimation, 2nd edn. Chicago, IL: Springer Science + Business Media.Google Scholar
Yates, F (1934) Contingency tables involving small numbers and the χ2 test. Supplement to the Journal of the Royal Statistical Society 1, 217–235.CrossRefGoogle Scholar
Zar, JH (2010) Biostatistical Analysis, 5th edn. Upper Saddle River, NJ: Prentice-Hall.Google Scholar