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Effects of thermal stress and nitrate enrichment on the larval performance of two Caribbean reef corals

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Abstract

The effects of multiple stressors on the early life stages of reef-building corals are poorly understood. Elevated temperature is the main physiological driver of mass coral bleaching events, but increasing evidence suggests that other stressors, including elevated dissolved inorganic nitrogen (DIN), may exacerbate the negative effects of thermal stress. To test this hypothesis, we investigated the performance of larvae of Orbicella faveolata and Porites astreoides, two important Caribbean reef coral species with contrasting reproductive and algal transmission modes, under increased temperature and/or elevated DIN. We used a fluorescence-based microplate respirometer to measure the oxygen consumption of coral larvae from both species, and also assessed the effects of these stressors on P. astreoides larval settlement and mortality. Overall, we found that (1) larvae increased their respiration in response to different factors (O. faveolata in response to elevated temperature and P. astreoides in response to elevated nitrate) and (2) P. astreoides larvae showed a significant increase in settlement as a result of elevated nitrate, but higher mortality under elevated temperature. This study shows how microplate respirometry can be successfully used to assess changes in respiration of coral larvae, and our findings suggest that the effects of thermal stress and nitrate enrichment in coral larvae may be species specific and are neither additive nor synergistic for O. faveolata or P. astreoides. These findings may have important consequences for the recruitment and community reassembly of corals to nutrient-polluted reefs that have been impacted by climate change.

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References

  • Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement andpost-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–490

    Article  Google Scholar 

  • Baird AH, Gilmour JP, Kamiki TM, Nonaka M, Pratchet MS, Yamamoto HH, Yamasaki H (2006) Temperature tolerance of symbiotic and non-symbiotic coral larvae. Proc 10th Int Coral Reef Symp 1:38–42

  • 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

    Article  CAS  Google Scholar 

  • Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O (2015) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R Soc Open Sci 2:140297

    Article  PubMed  PubMed Central  Google Scholar 

  • Brainard RE, Birkeland C, Eakin CM, McElhany P, Miller MW, Patterson M, Piniak GA (2011) Status review report of 82 candidate coral species petitioned under the U.S. Endangered Species Act. NOAA Technical Memorandum NOAA-TM-NMFS-PIFSC-27, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Pacific Islands Fisheries Science Center, Honolulu, HI

  • Chornesky EA, Peters EC (1987) Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Biol Bull 172:161–177

    Article  Google Scholar 

  • Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian–algal symbiosis. Mar Ecol Prog Ser 222:85–96

    Article  Google Scholar 

  • Cumbo VR, Fan TY, Edmunds PJ (2013a) Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2. J Exp Mar Bio Ecol 439:100–107

    Article  Google Scholar 

  • Cumbo VR, Edmunds PJ, Wall CB, Fan T-Y (2013b) Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release. Mar Biol 160:2903–2917

    Article  CAS  Google Scholar 

  • Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262

    Article  Google Scholar 

  • D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93

    Article  Google Scholar 

  • D’Elia CF, Wiebe WJ (1990) Biogeochemical nutrient cycles in coral-reef ecosystems. In: Dubinsky Z (ed) Ecosystems of the world: 25. Coral reefs. Elsevier, Amsterdam, pp 89–107

    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, Ross CLM, Didden C (2011) High, but localized recruitment of Montastraea annularis complex in St. John, United States Virgin Islands. Coral Reefs 30:123–130

    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 of the reef coral Porites astreoides. Invertebr Biol 124:185–193

    Article  Google Scholar 

  • Erwin PM, Song B, Szmant AM (2008) Settlement behavior of Acropora palmata planulae: effects of biofilm and crustose coralline algal cover. Proc 11th Int Coral Reef Symp 2:1225–1229

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo J, Baird AH, Harii S, Connolly SR (2014) Increased local retention of reef coral larvae as a result of ocean warming. Nat Clim Chang 4:498–502

    Article  Google Scholar 

  • Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O, Ferrari R, Gonzalez P, Gore S, Guppy R, McCartney MA, McCoy C, Mendes J, Srinivasan A, Steiner S, Vermeij MJ, Weil E, Mumby PJ (2012) Connectivity of caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol Ecol 21:1143–1157

    Article  PubMed  Google Scholar 

  • Green DH, Edmunds PJ, Carpenter RC (2008) Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Mar Ecol Prog Ser 359:1–10

    Article  Google Scholar 

  • Harii S, Kayanne H, Takigaw H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141:39–46

    Article  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 

  • Hartmann AC, Marhaver KL, Chamberland VF, Sandin SA, Vermeij MJA (2013) Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species. Ecology 94:1966–1976

    Article  PubMed  Google Scholar 

  • Holstein DM, Paris CB, Mumby PJ (2014) Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Mar Ecol Prog Ser 499:1–18

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Humanes A, Noonan SH, Willis BL, Fabricius KE, Negri AP (2016) Cumulative effects of nutrient enrichment and elevated temperature compromise the early life history stages of the coral Acropora tenuis. PloS One 11:e0161616

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones R, Ricardo GF, Negri AP (2015) Effects of sediments on the reproductive cycle of corals. Mar Pollut Bull 100:13–33

    Article  CAS  PubMed  Google Scholar 

  • Kuffner IB, Lidz BH, Hudson JH, Anderson JS (2015) A century of ocean warming on Florida keys coral reefs: historic in situ observations. Estuar Coasts 38:1085–1096

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models. R package version 2.0-29. http://CRAN.R-project.org/package=lmerTest

  • Lam EKY, Chui APY, Kwok CK, Ip AHP, Chan SW, Leung HN, Yeung LC, Ang PO (2015) High levels of inorganic nutrients affect fertilization kinetics, early development and settlement of the scleractinian coral Platygyra acuta. Coral Reefs 34:837–848

    Article  Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09S07

  • Manzello DP, Berkelmans R, Hendee JC (2007) Coral bleaching indices and thresholds for the Florida Reef Tract, Bahamas, and St. Croix, US Virgin Islands. Mar Pollut Bull 54:1923–1931

    Article  CAS  PubMed  Google Scholar 

  • McGuire MP (1998) Timing of larval release by Porites astreoides in the northern Florida Keys. Coral Reefs 17:369–375

    Article  Google Scholar 

  • Miller MW (2014) Post-settlement survivorship in two Caribbean broadcasting corals. Coral Reefs 33:1041–1046

    Article  Google Scholar 

  • Negri AP, Hoogenboom MO (2011) Water contamination reduces the tolerance of coral larvae to thermal stress. PLoS One 6:e19703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negri AP, Harford AJ, Parry DL, van Dam RA (2011) Effects of alumina refinery wastewater and signature metal constituents at the upper thermal tolerance of: 2. The early life stages of the coral Acropora tenuis. Mar Pollut Bull 62:474–482

    Article  CAS  PubMed  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 

  • 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 U S A 104:1266–1271

    Article  PubMed  PubMed Central  Google Scholar 

  • Olsen K, Ritson-Williams R, Ochrietor JD, Paul VJ, Ross C (2013) Detecting hyperthermal stress in larvae of the hermatypic coral Porites astreoides: the suitability of using biomarkers of oxidative stress versus heat-shock protein transcriptional expression. Mar Biol 160:2609–2618

    Article  CAS  Google Scholar 

  • Pasparakis C, Mager EM, Stieglitz JD, Benetti D, Grosell M (2016) Effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval mahi-mahi (Coryphaena hippurus). Aquat Toxicol 181:113–123

    Article  CAS  PubMed  Google Scholar 

  • Polato NR, Voolstra CR, Schnetzer J, DeSalvo MK, Randall CJ, Szmant AM, Medina M, Baums IB (2010) Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS One 5:e1122

    Article  Google Scholar 

  • Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Putnam HM, Mayfield AB, Fan TY, Chen CS, Gates RD (2013) The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2. Mar Biol 160:2157–2173

    Article  CAS  Google Scholar 

  • Randall CJ, Szmant AM (2009a) Elevated temperature affects development, survivorship, and settlement of the elkhorn coral, Acropora palmata (Lamarck 1816). Biol Bull 217:269–282

    Article  PubMed  Google Scholar 

  • Randall CJ, Szmant AM (2009b) 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 

  • Renegar DA, Riegl BM (2005) Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. Mar Ecol Prog Ser 293:69–76

    Article  Google Scholar 

  • Rivest EB, Hofmann GE (2014) Responses of the metabolism of the larvae of Pocillopora damicornis to ocean acidification and warming. PLoS One 9:e96172

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:5101–5114

    Article  CAS  PubMed  Google Scholar 

  • Ross C, Ritson-Williams R, Olsen K, Paul VJ (2012) Short-term and latent post-settlement effects associated with elevated temperature and oxidative stress on larvae from the coral Porites astreoides. Coral Reefs 32:71–79

    Article  Google Scholar 

  • Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6:21619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinn EA, Reese RS, Reich CD (1994) Fate and pathways of injection-well effluent in the Florida Keys. Open-File Report 94-276, U.S. Geological Survey, Reston, VA, USA

  • Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–53

    Article  Google Scholar 

  • Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25

    Article  Google Scholar 

  • Szmant AM, Miller MW (2006) Settlement preferences and post-settlement mortality of laboratory cultured and settled larvae of the Caribbean hermatypic coral Montastraea faveolata and Acropora palmata in the Florida Keys, USA. Proc 10th Int Coral Reef Symp 1:43–49

  • Villinski JT (2003) Depth-independent reproductive characteristics for the Caribbean reef-building coral Montastraea faveolata. Mar Biol 142:1043–1053

    Article  Google Scholar 

  • Ward S, Harrison PL (1997) The effects of elevated nutrient levels on settlement of coral larvae during the ENCORE experiment, Great Barrier Reef, Australia. Proc 8th Int Coral Reef Symp 1:891–896

  • Ward S, Harrison P (2000) Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment. J Exp Mar Bio Ecol 246:179–221

    Article  CAS  PubMed  Google Scholar 

  • Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164

    Article  CAS  Google Scholar 

  • Woods RM, Baird AH, Mizerek TL, Madin JS (2016) Environmental factors limiting fertilisation and larval success in corals. Coral Reefs 35:1433–1440

    Article  Google Scholar 

  • Wooldridge SA (2009) Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751

    Article  CAS  PubMed  Google Scholar 

  • Wooldridge SA (2013) Differential thermal bleaching susceptibilities amongst coral taxa: re-posing the role of the host. Coral Reefs 33:15–27

    Article  Google Scholar 

  • Wooldridge SA, Done TJ (2009) Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19:1492–1499

    Article  PubMed  Google Scholar 

  • Yashchenko V, Fossen EI, Kielland ON, Einum S (2016) Negative relationships between population density and metabolic rates are not general. J Anim Ecol 85:1070–1077

    Article  PubMed  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 

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Acknowledgements

The authors thank A. Palacio, P. Kushlan and R. Winter for help in the laboratory. Field assistance was provided by the B.E.A.R. team at the NOAA Southeast Fisheries Science Center and J. Fisch, N. Fogarty, M. Rushmore and J. Voss. R. Cunning provided valuable statistical advice. C. Woodley provided a constructive review of the manuscript. O. faveolata gametes were collected under permit FKNMS-2014-047-A1 to M. Miller, and P. astreoides adult coral colonies were collected under research permit FKNMS-2014-096 to N. Fogarty and X. Serrano. Water samples were analyzed by A. Renegar, N. Tuner and/or J. Stocker from NOVA Southeastern Oceanographic Center. This research was supported with funds from MOTE Protect Our Reefs grants (2013–2015) and grants from the NOAA Coral Reef Conservation Program and NSF (OCE-1358699). X. Serrano was supported by a National Research Council Associateship and a Ford Foundation Postdoctoral fellowship.

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Authors and Affiliations

  1. Cooperative Institute of Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL, 33149, USA

    Xaymara M. Serrano

  2. National Oceanic and Atmospheric Administration, Atlantic Oceanographic and Meteorological Laboratory, 4301 Rickenbacker Causeway, Miami, FL, 33149, USA

    Xaymara M. Serrano & James C. Hendee

  3. Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL, 33149, USA

    Brittany A. Jensen, Justine Z. Gapayao, Christina Pasparakis, Martin Grosell & Andrew C. Baker

  4. National Oceanic and Atmospheric Administration, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami, FL, 33149, USA

    Margaret W. Miller

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  1. Xaymara M. Serrano
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  2. Margaret W. Miller
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  3. James C. Hendee
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Correspondence to Xaymara M. Serrano.

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Serrano, X.M., Miller, M.W., Hendee, J.C. et al. Effects of thermal stress and nitrate enrichment on the larval performance of two Caribbean reef corals. Coral Reefs 37, 173–182 (2018). https://doi.org/10.1007/s00338-017-1645-y

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