Skip to main content
SpringerLink
Log in

High levels of inorganic nutrients affect fertilization kinetics, early development and settlement of the scleractinian coral Platygyra acuta

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Dose–response experiments were conducted to investigate the effects of ammonia nitrogen (NH3/NH4 +) and orthophosphate (PO4 3−) on four stages of larval development in Platygyra acuta, including fertilization, embryonic development and the survival, motility, and settlement of planula larvae. Fertilization success was reduced significantly under 200 μM NH3/NH4 + or PO4 3−. These high doses of NH3/NH4 + and PO4 − affected egg viability (or sperm viability and polyspermic block simultaneously) and polyspermic block, respectively. These results provide the first evidence to indicate the mechanisms of how inorganic nutrients might affect coral fertilization processes. For embryonic development, NH3/NH4 + at 25–200 μM caused delay in cell division after 2-h exposure and NH3/NH4 + at 100–200 μM resulted in larval death after 72 h. However, no significant differences were observed in the mobility and survivorship of either planula or competent larvae under different levels of NH3/NH4 + or PO4 3−. There was a significant (~30 %) drop in the settlement of competent larvae under the combined effect of 100 μM NH3/NH4 + and PO4 3−. The effects of elevated nutrients appeared to become more significant only on gametes or larvae undergoing active cellular activities at fertilization, early development, and settlement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Albright R, Mason B (2013) Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLoS One 8:e56468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ang PO, Choi LS, Choi MM, Cornish A, Fung HL, Lee MW, Lin TP, Ma WC, Tam MC, Wong SY (2005) Hong Kong. In: Status of coral reefs of the East Asian Seas Region: 2004. Japan Wildlife Research Centre, Ministry of the Environment, Government of Japan, Japan pp 121–152

  • Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, Saint R, Harrison PL, Miller DJ (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46:671–678

    CAS  PubMed  Google Scholar 

  • Bassim K, Sammarco P (2003) Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigosa). Mar Biol 142:241–252

    CAS  Google Scholar 

  • Birkeland C (1988) Geographic comparisons of coral-reef community processes. Proc 6th Int Coral Reef Symp 1:211–220

  • Chui PY, Ang P (2015) Elevated temperature enhances normal early embryonic development in the coral Platygyra acuta under low salinity conditions. Coral Reefs 34:461–469

    Article  Google Scholar 

  • Chui PY, Wong MC, Liu SH, Lee GW, Chan SW, Lau PL, Leung SM, Ang P (2014) Gametogenesis, embryogenesis, and fertilization ecology of Platygyra acuta in marginal nonreefal coral communities in Hong Kong. J Mar Biol. doi:10.1155/2014/953587

    Google Scholar 

  • Coll J, Bowden B, Meehan G (1994) Chemical aspects of mass spawning in corals. I. Sperm-attractant molecules in the eggs of the scleractinian coral Montipora digitata. Mar Biol 182:177–182

    Article  Google Scholar 

  • Epel D (1978) Mechanisms of activation of sperm and egg during fertilization of sea urchin gametes. Curr Top Dev Biol 12:185–246

    Article  CAS  PubMed  Google Scholar 

  • Ernst S (1997) A century of sea urchin development. Am Zool 259:250–259

    Google Scholar 

  • Franchet C, Goudeau M, Goudeau H (1998) Tributyltin impedes early sperm-egg interactions at the egg coat level in the ascidian Phallusia mammillata but does not prevent sperm-egg fusion in naked. Aquat Toxicol 44:213–222

    Article  Google Scholar 

  • Franke ES, Babcock RC, Styan CA (2002) Sexual conflict and polyspermy under sperm-limited conditions: in situ evidence from field simulations with the free-spawning marine echinoid Evechinus chloroticus. Am Nat 160:485–496

    Article  CAS  PubMed  Google Scholar 

  • Freeman G, Ridgway EB (1993) The role of intracellular calcium and pH during fertilization and egg activation in hydrozoan Phialidum. Dev Biol 156:176–190

    Article  CAS  PubMed  Google Scholar 

  • Godinot C, Ferrier-Pagés C, Grover R (2009) Control of phosphate uptake by zooxanthellae and host cells in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 54:1627–1633

    Article  Google Scholar 

  • Grasso LC, Negri AP, Fôret S, Saint R, Hayward DC, Miller DJ, Ball EE (2011) The biology of coral metamorphosis: molecular responses of larvae to inducers of settlement and metamorphosis. Dev Biol 353:411–419

    Article  CAS  PubMed  Google Scholar 

  • Harrison PL, Ward S (2001) Elevated levels of nitrogen and phosphorus reduce fertilisation success of gametes from scleractinian reef corals. Mar Biol 139:1057–1068

    Article  Google Scholar 

  • Hédouin L, Gates RD (2013) Assessing fertilization success of the coral Montipora capitata under copper exposure: does the night of spawning matter? Mar Pollut Bull 66:221–224

    Article  PubMed  Google Scholar 

  • Hollows C, Johnston E, Marshall D (2007) Copper reduces fertilisation success and exacerbates Allee effects in the field. Mar Ecol Prog Ser 333:51–60

    Article  CAS  Google Scholar 

  • Holmes RM, Aminot A, Kérouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808

    Article  CAS  Google Scholar 

  • Humphrey C, Weber M, Lott C, Cooper T, Fabricius K (2008) Effects of suspended sediments, dissolved inorganic nutrients and salinity on fertilisation and embryo development in the coral Acropora millepora (Ehrenberg, 1834). Coral Reefs 27:837–850

    Article  Google Scholar 

  • Jaffe LA, Gould M (1985) Polyspermy-preventing mechanisms. In: Metz C (ed) Biology Of fertilization 3: The fertilization response of the egg. Elsevier, New York, pp 223–250

    Chapter  Google Scholar 

  • Kuntz N, Kline D, Sandin S, Rohwer F (2005) Pathologies and mortality rates caused by organic carbon and nutrient stressors in three Caribbean coral species. Mar Ecol Prog Ser 294:173–180

    Article  CAS  Google Scholar 

  • Kwok CK, Ang PO (2013) Inhibition of larval swimming activity of the coral (Platygyra acuta) by interactive thermal and chemical stresses. Mar Pollut Bull 74:264–273

    Article  CAS  PubMed  Google Scholar 

  • Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution (NY) 58:308–323

    Article  Google Scholar 

  • Marshall DJ (2006) Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners. Mar Pollut Bull 52:734–738

    Article  CAS  PubMed  Google Scholar 

  • Millar RB, Anderson MJ (2003) The kinetics of monospermic and polyspermic fertilization in free-spawning marine invertebrates. J Theor Biol 224:79–85

    Article  PubMed  Google Scholar 

  • Morita M, Nishikawa A, Nakajima A, Iguchi A, Sakai K, Takemura A, Okuno M (2006) Eggs regulate sperm flagellar motility initiation, chemotaxis and inhibition in the coral Acropora digitifera, A. gemmifera and A. tenuis. J Exp Biol 209:4574–4579

    Article  CAS  PubMed  Google Scholar 

  • Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2010) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107

    Article  CAS  PubMed  Google Scholar 

  • Muller-Parker G, Cook C, D’Elia C (1994) Elemental composition of the coral Pocillopora damicornis exposed to elevated seawater ammonium. Pac Sci 48:234–246

    CAS  Google Scholar 

  • Murphy J, Riley J (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Negri A, Heyward A (2000) Inhibition of fertilization and larval metamorphosis of the coral Acropora millepora (Ehrenberg, 1834) by petroleum products. Mar Pollut Bull 41:420–427

    Article  CAS  Google Scholar 

  • Negri AP, Marshall PA, Heyward AJ (2007) Differing effects of thermal stress on coral fertilization and early embryogenesis in four Indo Pacific species. Coral Reefs 26:759–763

    Article  Google Scholar 

  • Nozawa Y, Harrison PL (2007) Effects of elevated temperature on larval settlement and post-settlement survival in scleractinian corals, Acropora solitaryensis and Favites chinensis. Mar Biol 152:1181–1185

    Article  Google Scholar 

  • Reichelt-Brushett AJ, Harrison PL (1999) The effect of copper, zinc and cadmium on fertilization success of the scleractinian coral Goniastrea aspera. Mar Poll Bull 38:182–187

    Article  CAS  Google Scholar 

  • Reichelt-Brushett AJ, Harrison PL (2000) The effect of copper on the settlement success of larvae from the scleractinian coral Acropora tenuis. Mar Poll Bull 41:385–391

    Article  CAS  Google Scholar 

  • Reichelt-Brushett AJ, Harrison PL (2004) Development of a sub-lethal test to determine the effects of copper and lead on scleractinian coral larvae. Arch Environ Contam Toxicol 47:40–55

    Article  CAS  PubMed  Google Scholar 

  • Reichelt-Brushett AJ, Michalek-Wagner K (2005) Effects of copper on the fertilization success of the soft coral Lobophytum compactum. Aquat Toxicol 74:280–284

    Article  CAS  PubMed  Google Scholar 

  • Rothschild L, Swann M (1952) The fertilization reaction in the sea-urchin. The block to polyspermy. J Exp Biol 26:469–483

    Google Scholar 

  • Szmant A (2002) Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries Coast 25:743–766

    Article  CAS  Google Scholar 

  • Tam TW, Ang PO (2008) Repeated physical disturbances and the stability of sub-tropical coral communities in Hong Kong, China. Aquat Conserv 18:1005–1024

    Article  Google Scholar 

  • Tanaka Y, Miyajima T, Koike I (2007) Imbalanced coral growth between organic tissue and carbonate skeleton caused by nutrient enrichment. Limnol Oceanogr 52:1139–1146

    Article  CAS  Google Scholar 

  • Vermeij M, Fogarty N, Miller M (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128

    Article  Google Scholar 

  • Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F, Postle AD, Achterberg EP (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164

    Article  Google Scholar 

  • Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett 38:L04601. doi:10.1029/2010GL046474

    Article  Google Scholar 

  • Yellowlees D, Rees T, Fitt W (1994) Effect of ammonium-supplemented seawater on glutamine synthetase and glutamate dehydrogenase activities in host tissue and zooxanthellae of Pocillopora. Pac Sci 48:291–295

    CAS  Google Scholar 

Download references

Acknowledgments

The study was partly supported by Research Grant Council of Hong Kong General Research Fund No. 460013 and Chinese University of Hong Kong Research Committee Group Research Scheme. We thank YH Yung, KH Chan, and HB Yeung for logistic supports and many other labmates, CW Yeung, SM Leung, TY Ng, YH Leung, HL Tsang, KT Wong, PY Cheung, WL Fong, FK Hui, HT Wong, WY Lau and TC Wong, for helping in the collection and preparation of coral larvae during the spawning trips. Comments and suggestions from five anonymous reviewers are gratefully acknowledged for significantly improving the manuscript.

Author information

Authors and Affiliations

  1. Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong, People’s Republic of China

    E. K. Y. Lam, A. P. Y. Chui, C. K. Kwok, A. H. P. Ip, S. W. Chan, H. N. Leung, L. C. Yeung & P. O. Ang Jr.

Authors
  1. E. K. Y. Lam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. P. Y. Chui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. K. Kwok
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. H. P. Ip
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. W. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. N. Leung
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L. C. Yeung
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. O. Ang Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. O. Ang Jr..

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lam, E.K.Y., Chui, A.P.Y., Kwok, C.K. et al. High levels of inorganic nutrients affect fertilization kinetics, early development and settlement of the scleractinian coral Platygyra acuta . Coral Reefs 34, 837–848 (2015). https://doi.org/10.1007/s00338-015-1317-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-015-1317-8

Keywords

Search

Navigation