Skip to main content

Advertisement

SpringerLink
Log in

Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

To evaluate the effects of temperature and pCO2 on coral larvae, brooded larvae of Pocillopora damicornis from Nanwan Bay, Taiwan (21°56.179′N, 120°44.85′E), were exposed to ambient (419–470 μatm) and high (604–742 μatm) pCO2 at ~25 and ~29 °C in two experiments conducted in March 2010 and March 2012. Larvae were sampled from four consecutive lunar days (LD) synchronized with spawning following the new moon, incubated in treatments for 24 h, and measured for respiration, maximum photochemical efficiency of PSII (F v/F m), and mortality. The most striking outcome was a strong effect of time (i.e., LD) on larvae performance: respiration was affected by an LD × temperature interaction in 2010 and 2012, as well as an LD × pCO2 × temperature interaction in 2012; F v/F m was affected by LD in 2010 (but not 2012); and mortality was affected by an LD × pCO2 interaction in 2010, and an LD × temperature interaction in 2012. There were no main effects of pCO2 in 2010, but in 2012, high pCO2 depressed metabolic rate and reduced mortality. Therefore, differences in larval performance depended on day of release and resulted in varying susceptibility to future predicted environmental conditions. These results underscore the importance of considering larval brood variation across days when designing experiments. Subtle differences in experimental outcomes between years suggest that transgenerational plasticity in combination with unique histories of exposure to physical conditions can modulate the response of brooded coral larvae to climate change and ocean acidification.

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

Similar content being viewed by others

References

  • Agostini S, Suzuki Y, Higuchi T, Casereto BE, Yoshinaga K, Nakano Y, Fujimura H (2012) Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31:147–156

    Article  Google Scholar 

  • Agrawal AA, LaForsch C, Tollrian R (1999) Transgenerational induction of defenses in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol. doi:10.1155/2011/473615

    Google Scholar 

  • Albright R, Langdon C (2011) Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob Change Biol 17:2478–2487

    Article  Google Scholar 

  • Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–900

    Article  Google Scholar 

  • Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci USA 107:20400–20404

    Article  CAS  Google Scholar 

  • Anlauf H, D’Croz L, O’Dea A (2011) A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J Exp Mar Biol Ecol 397:13–20

    Article  Google Scholar 

  • Baird AH, Gilmour JP, Kamiki TM, Nonaka M, Pratchett MS, Yamamoto H, Yamasaki H (2006) Temperature tolerance of symbiotic and non-symbiotic coral larvae. Proceedings of the 10th international coral reef symposium, pp 38–42

  • 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  Google Scholar 

  • Bassim KM, Sammarco PW (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 

  • Bassim KM, Sammarco PW, Snell TL (2002) Effects of temperature on success of (self and non-self) fertilization and embryogenesis in Diploria strigosa (Cnidaria, Scleractinia). Mar Biol 140:479–488

    Article  Google Scholar 

  • Bhagooli R, Hidaka M (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J Exp Mar Biol Ecol 291:181–197

    Article  Google Scholar 

  • Black KP (1993) The relative importance of local retention and inter-reef dispersal of neutrally buoyant material on coral reefs. Coral Reefs 12:43–53

    Google Scholar 

  • Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Annu Rev 49:1–42

    Google Scholar 

  • Chua MC, Leggat B, Moya A, Baird AH (in press) Near-future reductions in pH will have no consistent ecological effects on the early life history stages of reef corals. Mar Ecol Prog Ser. doi:10.3354/meps10318

  • Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophys Geosyst 10:Q07005. doi:10.1029/2009GC002411

    Article  Google Scholar 

  • Cowan RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • Cumbo VR, Fan TY, Edmunds PJ (2012a) Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2. J Exp Mar Biol Ecol 439:100–107

    Article  Google Scholar 

  • Cumbo VR, Fan TY, Edmunds PJ (2012b) Physiological development of brooded larvae from two pocilloporid corals in Taiwan. Mar Biol. doi:10.1007/s00227-012-2046-y

    Google Scholar 

  • de Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2011) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs 30:321–328

    Article  Google Scholar 

  • Detlef PV, Edmonds J, Kainuma M, Riahi K, Thomason A, Hibbard K, Hurtt GC, Kram T, Krey V, Lamarque J-F, Masui T, Meinshausen M, Nakicenovic N, Smith SJ, Rose SK (2011) The representative concentration pathways: an overview. Clim Change 109:5–31

    Article  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (eds) (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, p 191

  • Dufault AM, Cumbo VR, Fan TY, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on calcification and survival of coral recruits. Proc R Soc Lond B. doi:10.1098/rspb.2011.2545

    Google Scholar 

  • Edmunds PJ, Davies PS (1988) Post-illumination stimulation of the respiration rate in the coral Porites porites. Coral Reefs 7:7–9

    Article  Google Scholar 

  • Edmunds PJ, Gates RD, Gleason DF (2001) The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar Biol 139:981–989

    Article  Google Scholar 

  • Edmunds PJ, Gates RD, Leggat W, Hoegh-Guldberg O, Allen-Requa L (2005) The effect of temperature on the size and population density of dinoflagellates in larvae on the reef coral Porites astreoides. Invert Biol 124:185–193

    Article  Google Scholar 

  • Edmunds PJ, Cumbo VR, Fan TY (2011) Effects of temperature on the respiration of brooded larvae from tropical reef corals. J Exp Biol 214:2783–2790

    Article  Google Scholar 

  • Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032

    Article  Google Scholar 

  • Fan TY, Li JJ, Ie SX, Fang LS (2002) Lunar periodicity of larval release by pocilloporid corals in southern Taiwan. Zool Stud 41:288–294

    Google Scholar 

  • Fan TY, Lin KH, Kuo FW, Soong K, Liu LL, Fang LS (2006) Diel patterns of larval release by five brooding scleractinian corals. Mar Ecol Prog Ser 321:133–142

    Article  Google Scholar 

  • Fangue NA, O’Donnell MJ, Sewell MA, Matson PG, MacPherson AC, Hoffman GE (2010) A laboratory-based, experimental system for the study of ocean acidification effects on marine invertebrate larvae. Limnol Oceanogr Methods 8:441–452

    Article  CAS  Google Scholar 

  • Gaither MR, Rowan R (2010) Zooxanthellar symbiosis in planula larvae of the coral Pocillopora damicornis. J Exp Mar Biol Ecol 386:45–53

    Article  Google Scholar 

  • Garcia HE, Gordon LI (1992) Solubility in seawater: better fitting solutions. Limnol Oceanogr 37:1307–1312

    Article  CAS  Google Scholar 

  • Gleason DF, Hofmann DK (2011) Coral larvae: from gametes to recruits. J Exp Mar Biol Ecol 408:42–57

    Article  Google Scholar 

  • Gleason DF, Edmunds PJ, Gates RD (2006) Ultraviolet radiation effects on the behavior and recruitment of larvae from the reef coral Porites astreoides. Mar Biol 148:503–512

    Article  Google Scholar 

  • Gleason DF, Danilowicz BS, Nolan CJ (2009) Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals. Coral Reefs 28:549–554

    Article  Google Scholar 

  • Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 46:265–282

    Article  Google Scholar 

  • Hadfield MG (2000) Why and how marine-invertebrate larvae metamorphose so fast. Cell Dev Biol 11:437–443

    Article  CAS  Google Scholar 

  • Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750

    Article  CAS  Google Scholar 

  • Harland AD, Davies PS (1995) Symbiont photosynthesis increases both respiration and photosynthesis in the symbiotic sea anemone Anemonia viridis. Mar Biol 123:715–722

    Article  Google Scholar 

  • Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 59–85

    Chapter  Google Scholar 

  • Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world, vol 25., Coral reefsElsevier, Amsterdam, pp 133–207

    Google Scholar 

  • Herndl GJ, Velimirov B (1985) Bacteria in the coelenterons of Anthozoa: control of coelenteric bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93:115–130

    Article  Google Scholar 

  • Heyward AJ, Negri AP (2010) Plasticity of larval pre-competency in response to temperature: observations on multiple broadcast spawning coral species. Coral Reefs 29:631–636

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Fresh Res 50:839–866

    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, Muthuga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  Google Scholar 

  • Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Evol Syst 41:127–147

    Article  Google Scholar 

  • IPCC (2007) Climate change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri RK, Reisinger A (eds)]. IPCC, Geneva, Switzerland, 104 pp

  • Isomura N, Nishihara M (2001) Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs 20:309–315

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • Kleypas JA, Buddemeier RW, Archer D, Gattuso JP, Langdon C, Opdyke BN (1999) Goechemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  CAS  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • Lee HJ, Chao SY, Fan KL, Kuo TY (1999) Tide-induced eddies and upwelling in a semi-enclosed basin: Nan Wan. Estuar Coast Shelf Sci 49:775–787

    Article  Google Scholar 

  • Levitan DR (1996) Predicting optimal and unique egg sizes in free-spawning marine invertebrates. Am Nat 148:174–188

    Article  Google Scholar 

  • Markey KL, Baird AH, Humphrey C, Negri AP (2007) Insecticides and fungicide affect multiple coral life stages. Mar Ecol Prog Ser 330:127–137

    Article  CAS  Google Scholar 

  • Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Dev 9:355–367

    Article  Google Scholar 

  • Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418–427

    Article  Google Scholar 

  • Marshall DJ, Keough MJ (2003) Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size. Mar Ecol Prog Ser 255:145–153

    Article  Google Scholar 

  • Marubini F, Ferrier-Pagès C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27:491–499

    Article  Google Scholar 

  • Mason B, Beard M, Miller MW (2011) Coral larvae settle at a higher frequency on red surfaces. Coral Reefs. doi:10.1007/s00338-011-0739-1

    Google Scholar 

  • Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2009) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107

    Article  Google Scholar 

  • Moya A, Huisman L, Ball EE, Hayward DC, Grasso LC, Chua CM, Woo HN, Gattuso JP, Foret S, Miller DJ (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol Ecol 21:2440–2454

    Article  CAS  Google Scholar 

  • Mundy CN, Babcock RC (1998) Role of light intensity and spectral quality in coral settlement: implications for depth-dependent settlement? Mar Ecol Prog Ser 223:235–255

    Google Scholar 

  • Nakamura M, Ohki S, Suzuki A, Sakai K (2011) Coral larvae under ocean acidification: survival, metabolism and metamorphosis. PLoS ONE 6:e14521

    Article  CAS  Google Scholar 

  • Nakamura M, Morita M, Kurihara H, Mitarai S (2012) Expression of hsp70, hsp90 and hsf1 in the reef coral Acropora digitifera under prospective acidified conditions over the next several decades. Biol Open 1:75–81

    Article  CAS  Google Scholar 

  • Negri AP, Smity LD, Webster NS, Heyward AJ (2002) Understanding ship-grounding impacts on a coral reef: potential effects of anti-foulant paint contamination on coral recruitment. Mar Pollut Bull 44:111–117

    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 

  • Nozawa Y, Okubo N (2011) Survival dynamics of reef coral larvae with special consideration of larval size and the genus Acropora. Biol Bull 220:15–22

    Google Scholar 

  • O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Natl Acad Sci USA 104:1266–1271

    Article  Google Scholar 

  • Orr JC (2011) Recent and future changes in ocean carbonate chemistry. In: Gattuso J-P, Hansonn L (eds) Ocean acidification. Oxford University Press, Oxford, pp 41–66

  • Permata WD, Kinzie RA, Hidakal M (2000) Histological studies on the origin of planulae of the coral Pocillopora damicornis. Mar Ecol Prog Ser 200:191–200

    Article  Google Scholar 

  • Pierrot D, Lewis E, Wallace DWR (2006) MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee

  • Putnam HM, Edmunds PJ, Fan TY (2008) Effects of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biol Bull 215:135–142

    Article  Google Scholar 

  • Putnam HM, Edmunds PJ, Fan TY (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invert Biol 129:199–209

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Raimondi PT, Morse ANC (2000) The consequence of complex larval behavior in a coral. Ecology 81:3193–3211

    Article  Google Scholar 

  • Randall CJ, Szmant AM (2009) Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28:537–545

    Article  Google Scholar 

  • Rivest E, Hofmann G (2012) Metabolic plasticity in coral larvae under ocean acidification and warming. Proceedings of the 12th international coral reef symposium (abstracts) 158

  • Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:1501–5114

    Article  Google Scholar 

  • Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The ocean sink for anthropogenic CO2. Science 305:367–371

    Article  CAS  Google Scholar 

  • Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  CAS  Google Scholar 

  • Salinas S, Munch SB (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163

    Article  Google Scholar 

  • Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:L05606

    Article  Google Scholar 

  • Stambler N (2011) Zooxanthellae: the yellow symbionts inside animals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 87–106

    Chapter  Google Scholar 

  • Stoddart JA, Black R (1985) Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Mar Ecol Prog Ser 23:153–164

    Article  Google Scholar 

  • Strathmann RR (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annu Rev Ecol Syst 16:339–361

    Article  Google Scholar 

  • Suwa R, Nakamur M, Morita M, Shimada K, Iguchi A, Sakai K, Suzuki A (2010) Effects of acidified seawater on early life stages of scleractinian corals (Genus Acropora). Fish Sci 76:93–99

    Article  CAS  Google Scholar 

  • Webster NS, Uthicke S, Botte ES, Flores F, Negri A (2012) Ocean acidification reduces induction of coral settlement by crustose coralline algae. Glob Change Biol. doi:10.1111/gcb.12008

    Google Scholar 

  • Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112

    Article  CAS  Google Scholar 

  • Yeoh S-R, Dai C-F (2010) The reproduction of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157:351–359

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

Download references

Acknowledgments

This research was funded through the US National Science Foundation (BIO-OCE 08-44785) and contributes to the collaboration supported under the Memorandum of Understanding between California State University, Northridge, USA and National Dong Hwa University, Hualien, Taiwan. We thank A. Dufault, H.M. Putnam, S. Zamudio, A. Mayfield, P.J. Liu, Y.H Chen and O. Chan for field and laboratory assistance. Comments from four anonymous reviewers and H. Pörtner improved an earlier draft of this paper. This is contribution number 194 of the CSUN Marine Biology Program.

Author information

Authors and Affiliations

  1. Department of Biology, California State University, 18111 Nordhoff Street, Northridge, CA, 91330-8303, USA

    Vivian R. Cumbo, Peter J. Edmunds & Christopher B. Wall

  2. National Museum of Marine Biology and Aquarium, Pingtung, Taiwan, ROC

    Tung-Yung Fan

  3. Institute of Marine Biodiversity and Evolution, National Dong Hwa University, Hualien, Taiwan, ROC

    Tung-Yung Fan

Authors
  1. Vivian R. Cumbo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter J. Edmunds
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher B. Wall
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tung-Yung Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vivian R. Cumbo.

Additional information

Communicated by U. Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 87 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cumbo, V.R., Edmunds, P.J., Wall, C.B. et al. Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release. Mar Biol 160, 2903–2917 (2013). https://doi.org/10.1007/s00227-013-2280-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2280-y

Keywords

Search

Navigation