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Photoperiod, temperature, and food availability as drivers of the annual reproductive cycle of the sea urchin Echinometra sp. from the Gulf of Aqaba (Red Sea)

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Abstract

In spite of the efforts invested in the search for the environmental factors that regulate discrete breeding periods in marine invertebrates, they remain poorly understood. Here, we present the first account of the annual reproductive cycle of the pantropical sea urchin Echinometra sp. from the Gulf of Aqaba/Eilat (Red Sea) and explore some of the main environmental variables that drive echinoid reproduction. Monthly measurements of gonado-somatic indexes and histological observations of 20 specimens revealed a single seasonal reproductive cycle, with gametogenesis in males and females being highly synchronized. Gametogenesis commenced in June and peak spawning occurred between September and October. Gonado-somatic indexes were significantly correlated with seawater temperatures but not with photoperiod. The latter cycle lagged behind the gonado-somatic cycle by two months, suggesting that the onset of gametogenesis corresponds to shortening day length, while spawning may be driven by warming seawater temperatures. Gonads remained quiescent throughout the winter and spring (January through May) when temperatures were at their lowest. Chlorophyll-a concentrations increased significantly in the months following spawning (October through January). These high concentrations are indicative of high phytoplankton abundance and may reflect the increase in food availability for the developing larvae. Of the external test dimensions, length presented the highest correlation to body weight, indicating length as the best predictor for body size in Echinometra. Neither sexual dimorphism nor size differences between males and females were detected, and the sex ratios were approximately 1:1 in three distant Echinometra populations. Environmentally regulated reproduction, as occurs in sea urchins, might face severe outcomes due to anthropogenic disturbances to the marine environment. Consequently, there is a need to deepen our understanding of the mechanisms that drive and regulate this process in broadcast-spawning species.

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References

  • Alsaffar AH, Lone KP (2000) Reproductive cycles of Diadema setosum and Echinometra mathaei (Echinoidea: Echinodermata) from Kuwait (northern Arabian Gulf). Bull Mar Sci 67:845–856

    Google Scholar 

  • Arakaki Y, Uehara T (1991) Physiological adaptations and reproduction of the four types of Echinometra mathaei (Blainville). In: Yanagisawa T, Yasumasu I, Oguro C, Suzuki N, Motokawa T (eds) Biology of Echinodermata. Balkema, Rotterdam, pp 105–112

    Google Scholar 

  • Aubrecht C, Elvidge CD (2008) Satellite observed nighttime lights as an indicator of human induced stress on coral reefs. Keynote at Darksky 2008: 8th European Symposium for the Protection of the Night Sky, Vienna, Austria

  • Aubrecht C, Elvidge CD, Longcore T, Rich C, Safran J, Strong AE, Eakin CM, Baugh KE, Tuttle BT, Howard AT, Erwin EH (2008) A global inventory of coral reef stressors based on satellite observed nighttime lights. Geocarto Int 23:467–479

    Article  Google Scholar 

  • Bak RPM (1990) Patterns of echinoid bioerosion in two Pacific coral reef lagoons. Mar Ecol Prog Ser 66:267–272

    Article  Google Scholar 

  • Bak RPM (1994) Sea urchin bioerosion on coral reefs: place in the carbonate budget and relevant variables. Coral Reefs 13:99–103

    Article  Google Scholar 

  • Bauer RT (1992) Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebr Reprod Dev 22:193–202

    Article  Google Scholar 

  • Bay-Schmith E, Pearse JS (1987) Effect of fixed daylengths on the photoperiodic regulation of gametogenesis in the sea urchin Strongylocentrotus purpuratus. Invertebr Reprod Dev 11:287–294

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Boolootian RA (1966) Reproductive physiology. Interscience, New York

    Google Scholar 

  • Bronstein O, Loya Y (2013) The Taxonomy and Phylogeny of Echinometra (Camarodonta: Echinometridae) from the Red Sea and Western Indian Ocean. PLoS One 8:e77374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bronstein O, Loya Y (2014) Echinoid community structure and rates of herbivory and bioerosion on exposed and sheltered reefs. J Exp Mar Bio Ecol 456:8–17

    Article  Google Scholar 

  • Byrne M (1990) Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar Biol 104:275–289

    Article  Google Scholar 

  • Carreiro-Silva M, McClanahan TR (2001) Echinoid bioerosion and herbivory on Kenyan coral reefs: the role of protection from fishing. J Exp Mar Bio Ecol 262:133–153

    Article  PubMed  Google Scholar 

  • Dafni J (1986) A biomechanical model for the morphogenesis of regular echinoid tests. Paleobiology 12:143–160

    Google Scholar 

  • Drummond AE (1995) Reproduction of the sea urchins Echinometra mathaei and Diadema savignyi on the South African eastern coast. Mar Freshw Res 46:751–755

    Article  Google Scholar 

  • Dumas P, Kulbicki M, Chifflet S, Fichez R, Ferraris J (2007) Environmental factors influencing urchin spatial distributions on disturbed coral reefs (New Caledonia, South Pacific). J Exp Mar Bio Ecol 344:88–100

    Article  Google Scholar 

  • El-Shenawy M, Farag A, Zaky M (2006) Sanitary and aesthetic quality of Egyptian coastal waters of Aqaba Gulf, Suez Gulf and Red Sea. Egyptian Journal of Aquatic Research 32:220–234

    Google Scholar 

  • Franke HD (1999) Reproduction of the Syllidae (Annelida: Polychaeta). Hydrobiologia 402:39–55

    Article  Google Scholar 

  • Fuji A (1960) Studies on the biology of the sea urchin: I. Superficial and histological gonadal changes in gametogenic process of two sea urchins, Strongylocentrotus nudus and S. intermedius. Bulletin of the faculty of fisheries Hokkaido university 11:1–14

    Google Scholar 

  • Fujisawa H, Shigei M (1990) Correlation of embryonic temperature sensitivity of sea urchins with spawning season. J Exp Mar Bio Ecol 136:123–139

    Article  Google Scholar 

  • Gianguzza P, Badalamenti F, Gianguzza F, Bonaviri C, Riggio S (2009) The operational sex ratio of the sea urchin Paracentrotus lividus populations: the case of the Mediterranean marine protected area of Ustica Island (Tyrrhenian Sea, Italy). Mar Ecol 30:125–132

    Article  Google Scholar 

  • Giese AC (1959) Comparative physiology: Annual reproductive cycles of marine invertebrates. Annu Rev Physiol 21:547–576

    Article  CAS  PubMed  Google Scholar 

  • Giese AC, Pearse JS (1974) Introduction: general principles. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Academic Press, New York, pp 1–49

    Google Scholar 

  • Gonor JJ (1973) Reproductive cycles in oregon populations of the echlnoid, Strongylocentrotvs purpuratus (Stimpson). I. Annual gonad growth and ovarian gametogenic cycles. J Exp Mar Bio Ecol 12:45–64

    Article  Google Scholar 

  • Guillou M, Michel C (1993) Reproduction and growth of Sphaerechinus granularis (Echinodermata: Echinoidea) in southern Brittany. J Mar Biol Assoc U.K. 73:179-192

  • Harrington LH, Walker CW, Lesser MP (2007) Stereological analysis of nutritive phagocytes and gametogenic cells during the annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis. Invertebr Biol 126:202–209

    Article  Google Scholar 

  • Himmelman JH (1975) Phytoplankton as a stimulus for spawning in three marine invertebrates. J Exp Mar Bio Ecol 20:199–214

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2008) Implementing a class of permutation tests: The Coin Package. J Stat Softw 28:1–23

    Google Scholar 

  • James DB, Pearse JS (1969) Echinoderms from the Gulf of Suez and the Northern Red sea. Biological Association of India 11:78–125

    Google Scholar 

  • James PJ, Heath P, Unwin MJ (2007) The effects of season, temperature and initial gonad condition on roe enhancement of the sea urchin Evechinus chloroticus. Aquaculture 270:115–131

    Article  Google Scholar 

  • Johnson MP, Frost NJ, Mosley MWJ, Roberts MF, Hawkins SJ (2003) The area-independent effects of habitat complexity on biodiversity vary between regions. Ecol Lett 6:126–132

    Article  Google Scholar 

  • Jokiel PL, Ito RY, Liu PM (1985) Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis. Mar Biol 88:167–174

    Article  Google Scholar 

  • Kelly MS (2001) Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris. J Exp Mar Bio Ecol 266:67–80

    Article  Google Scholar 

  • Kelso DP (1971) Morphological variation, reproductive periodicity, gamete compatibility and habitat specialization in two species of the sea urchin Echinometra in Hawaii. PhD Thesis, University of Hawaii

  • King CK, Hoegh-Guldberg O, Byrne M (1994) Reproductive cycle of Centrostephanus rodgersii (Echinoidea), with recommendations for the establishment of a sea urchin fishery in New South Wales. Mar Biol 120:95–106

    Google Scholar 

  • Lawrence JM, Lane JM (1982) The utilization of nutrients by post-metamorpgic echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam, pp 331–371

  • Lawrence JM, Sammarco PW (1982) Effect of feeding on the environment: Echinoidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema Press, Rotterdam, A. A, pp 499–519

    Google Scholar 

  • Lessios HA (1981) Reproduction periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. J Exp Mar Bio Ecol 50:47–61

    Article  Google Scholar 

  • Lewis JB, Storey GS (1984) Differences in morphology and life history traits of the echinoid Echinometra lucunter from different habitats. Mar Ecol Prog Ser 15:207–211

    Article  Google Scholar 

  • Lipani C, Vitturi R, Sconzo G, Barbata G (1996) Karyotype analysis of the sea urchin Paracentrotus lividus (Echinodermata): evidence for a heteromorphic chromosome sex mechanism. Mar Biol 127:67–72

    Article  Google Scholar 

  • Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198

    Article  Google Scholar 

  • Loya Y (2004) The coral reefs of Eilat — past, present and future: three decades of coral community structure studies. In: Rosenberg E, Loya Y (eds) Coral Health and Disease. Springer, Berlin Heidelberg, pp 1–34

    Chapter  Google Scholar 

  • McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400

    Article  CAS  PubMed  Google Scholar 

  • McClanahan TR (1988a) Coexistence in a sea urchin guild and its implications to coral reef diversity and degradation. Oecologia 77:210–218

    Article  Google Scholar 

  • McClanahan TR (1988b) Seasonality in East Africa’s coastal waters. Mar Ecol Prog Ser 44:191–199

    Article  Google Scholar 

  • McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362–370

    Article  Google Scholar 

  • McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea urchin Echinometra mathaei (de Blainville). J Exp Mar Bio Ecol 147:121–146

    Article  Google Scholar 

  • McClanahan TR, Muthiga NA (2001) The ecology of Echinometra. In: Lawrence JM (ed) Developments in aquaculture and fisheries science. Elsevier, Amsterdam, pp 225–243

    Google Scholar 

  • McClanahan TR, Muthiga NA (2013) Echinometra. In: Lawrence JM (ed) Sea urchins: biology and ecology. Elsevier, Amsterdam, pp 337–353

    Chapter  Google Scholar 

  • McClintock JB, Watts SA (1990) The effects of photoperiod on gametogenesis in the tropical sea urchin Eucidaris tribuloides (Lamarck) (Echinodermata: Echinoidea). J Exp Mar Biol Ecol 139:175–184

    Article  Google Scholar 

  • Mercier A, Hamel JF (2009) Endogenous and exogenous control of gametogenesis and spawning in echinoderms. In: Annie M, Jean-Francois H (eds) Advances in Marine Biology. Elsevier, Amsterdam, p 302

    Google Scholar 

  • Mokady O, Lazar B, Loya Y (1996) Echinoid bioerosion as a major structuring force of Red Sea coral reefs. Biol Bull 190:367–372

    Article  Google Scholar 

  • Monismith SG, Genin A (2004) Tides and sea level in the Gulf of Aqaba (Eilat). J Geophys Res 109:C04015

    Google Scholar 

  • Muthiga NA, Jaccarini V (2005) Effects of seasonality and population density on the reproduction of the Indo-Pacific echinoid Echinometra mathaei in Kenyan coral reef lagoons. Mar Biol 146:445–453

    Article  Google Scholar 

  • Orton JH (1920) Sea-temperature, breeding and distribution in marine animals. J Mar Biol Assoc U.K. 12:339–366

  • Packard GC, Boardman TJ (1988) The misuse of ratios, indices, and percentages in ecophysiological research. Physiol Zool 61:1–9

    Google Scholar 

  • Palumbi SR, Metz EC (1991) Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol 8:227–239

    CAS  PubMed  Google Scholar 

  • Pearse JS (1968) Patterns of reproductive periodicities in four species of indo-pacific echinoderms. Proc Indian Natl Sci Acad B Biol Sci 67:247–279

    Google Scholar 

  • Pearse JS (1969a) Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. I. The echinoids Prionocidaris baculosa (Lamarck) and Lovenia elongata (Gray). Bull Mar Sci 19:323–350

    Google Scholar 

  • Pearse JS (1969b) Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. II. The echinoid Echinometra mathaei (de Blanville). Bull Mar Sci 19:580–613

    Google Scholar 

  • Pearse JS (1970) Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. III. The echinoid Diadema setosum (Leske). Bull Mar Sci 20:697–720

    Google Scholar 

  • Pearse JS, Phillips BF (1968) Continuous reproduction in the Indo-Pacific sea urchin Echinometra mathaei at Rottnest Island, Western Australia. Mar Freshw Res 19:161–172

    Article  Google Scholar 

  • Pearse JS, Cameron RA (1991) Echinodermata: Echinoidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, echinoderms and lophophorates. Boxwood Press, Pacific Grove, CA, pp 513–662

    Google Scholar 

  • Pearse JS, Pearse VB, Davis KK (1986) Photoperiodic regulation of gametogenesis and growth in the sea urchin Strongylocentrotus purpuratus. J Exp Zool 237:107–118

    Article  Google Scholar 

  • Pecorino D, Barker MF, Dworjanyn SA, Byrne M, Lamare MD (2014) Impacts of near future sea surface pH and temperature conditions on fertilisation and embryonic development in Centrostephanus rodgersii from northern New Zealand and northern New South Wales, Australia. Mar Biol 161:101–110

    Article  CAS  Google Scholar 

  • Poorbagher H, Lamare MD, Barker MF (2010) Effects of nutrition on somatic growth and reproductive strategy of the sea urchin Pseudechinus huttoni. Mar Biol Res 6:292–301

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from http://www.R-project.org, Vienna, Austria

  • Sadovy Y, Shapiro DY (1987) Criteria for the diagnosis of hermaphroditism. Copeia 1:136–156

    Article  Google Scholar 

  • Sakai K, Yamazato K (1984) Coral recruitment to artificially denuded natural substrates on an Okinawan reef flat. Galaxea 3:57–69

    Google Scholar 

  • Sakairi K, Yamamoto M, Ohtsu K, Yoshida M (1989) Environmental control of gonadal maturation in laboratory-reared sea urchins, Anthocidaris crassispina and Hemicentrotus pulcherrimus. Zool Sci 6:721–730

    Google Scholar 

  • Shpigel M, McBride SC, Marciano S, Lupatsch I (2004) The effect of photoperiod and temperature on the reproduction of European sea urchin Paracentrotus lividus. Aquaculture 232:343–355

    Article  Google Scholar 

  • Uthicke S, Schaffelke B, Byrne M (2009) A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24

    Article  Google Scholar 

  • Vaïtilingon D, Rasolofonirina R, Jangoux M (2005) Reproductive cycle of edible echinoderms from the southwestern Indian Ocean I. Tripneustes gratilla L. (Echinoidea, Echinodermata). Western Indian Ocean Journal of Marine Science 4:47–60

    Google Scholar 

  • Walker CW, Lesser MP (1998) Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. Mar Biol 132:663–676

    Article  Google Scholar 

  • Walker CW, Unuma T, Lesser MP (2007) Gametogenesis and reproduction of sea urchins. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 11–33

    Chapter  Google Scholar 

  • Walker CW, Harrington LM, Lesser MP, Fagerberg WR (2005) Nutritive phagocyte incubation chambers provide a structural and nutritive microenvironment for germ cells of Strongylocentrotus droebachiensis, the green sea urchin. Biol Bull 209:31–48

    Article  PubMed  Google Scholar 

  • Wangensteen OS, Turon X, Casso M, Palacín C (2013) The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod. Mar Biol 160:3157–3168

    Article  Google Scholar 

  • Wheeler B (2010) lmPerm: Permutation tests for linear models Linear model functions using permutation tests

  • Williamson J, Steinberg P (2002) Reproductive cycle of the sea urchin Holopneustes purpurascens (Temnopleuridae: Echinodermata). Mar Biol 140:519–532

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge A. Rankov and J. Larsson for their assistance in the field and laboratory. We are in debt to Dr. I. Brikner for assistance with the histological analysis and for fruitful discussions. We thank the Inter-University Institute (IUI) at Eilat for providing laboratory and logistical support throughout this study. We also thank N. Paz for linguistic editing of the text and M. Chen-Bronstein for graphical assistance. This research was supported by the Israel Science Foundation (ISF) to Y.L.

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  1. Department of Zoology, The George S. Wise Faculty of Life Sciences, Tel-Aviv University, 69978, Tel Aviv, Israel

    Omri Bronstein & Yossi Loya

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  1. Omri Bronstein
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Bronstein, O., Loya, Y. Photoperiod, temperature, and food availability as drivers of the annual reproductive cycle of the sea urchin Echinometra sp. from the Gulf of Aqaba (Red Sea). Coral Reefs 34, 275–289 (2015). https://doi.org/10.1007/s00338-014-1209-3

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