Skip to main content
SpringerLink
Log in

Physiological seasonality in the symbiont and host of the northern star coral, Astrangia poculata

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

Abstract

Assessing physiological responses that correspond to the normal range of seasonal variation can provide a better understanding of how environmental stressors may impact physiology. Most tropical corals exhibit seasonal variation in their host and symbiont physiology within a narrow range of environmental conditions. In temperate regions and at the northern end of its distribution, Astrangia poculata must adapt to wide ranges in seasonal variability. The species is facultatively symbiotic, and it is unclear if or how symbiotic state and, consequently, host physiology is affected by environmental seasonality. We collected colonies of A. poculata with a visible range of symbiotic states from Fort Wetherill State Park in Jamestown, RI in fall, winter, spring, and summer seasons of 2018–2019. We measured physiological parameters, including symbiotic state [chlorophyll (Chl) a and c2], total lipid content, and stable carbon (δ13C) and nitrogen (δ15N) isotopes of the host and symbiont. Seasonal variation occurred in all physiological parameters we studied. Specifically, Chl a, c2, and lipid content all reached low points in the spring, suggesting a lag, where the consequences of the coldest temperatures in the winter took up to three months to manifest in the tissue. There were seasonal fluctuations in host:symbiont ratios of δ13C, reflecting changing rates of autotrophy relative to heterotrophy during the year. While some autotrophy occurred during the year, isotopic evidence indicated that carbon acquisition in A. poculata was mostly heterotrophic in the winter. Based on δ15N, the symbiont was primarily responsible for nitrogen assimilation, although other sources likely contributed. Both carbon acquisition and nitrogen acquisition were more similar to that of other aposymbiotic coral species, regardless of the symbiotic state of A. poculata. Therefore, it may be more appropriate to view A. poculata as a unique aposymbiotic coral that is capable of symbiosis, rather than the reverse.

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

  • Aichelman HE, Zimmerman RC, Barshis DJ (2019) Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. J Exp Biol 222:

  • Brown BE, Dunne RP, Ambarasari I, Le Tissier MDA, Satapoomin U (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Prog Ser 191:53–69

    Article  Google Scholar 

  • Burmester EM, Breef-Pilz A, Lawrence NF, Kaufman L, Finnerty JR, Rotjan RD (2018) The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals. Ecol Evol 8:10805–10816

    Article  PubMed  PubMed Central  Google Scholar 

  • Burmester EM, Finnerty JR, Kaufman L, Rotjan RD (2017) Temperature and symbiosis affect lesion recovery in experimentally wounded, facultatively symbiotic temperate corals. Mar Ecol Prog Ser 570:87–99

    Article  Google Scholar 

  • Carballo-Bolaños R, Denis V, Huang YY, Keshavmurthy S, Chen CA (2019) Temporal variation and photochemical efficiency of species in symbiodinaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS ONE 14:1–19

    Article  CAS  Google Scholar 

  • Cheng L, Zhu J, Abraham J, Trenberth KE, Fasullo JT, Zhang B, Yu F, Wan L, Chen X, Song X (2019) 2018 Continues Record Global Ocean Warming. Adv Atmos Sci 36:249–252

    Article  Google Scholar 

  • Conti-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, Baker DM (2020) Trophic strategy and bleaching resistance in reef-building corals. Sci Adv 6:

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172

    Article  CAS  Google Scholar 

  • Dimond JL, Kerwin AH, Rotjan R, Sharp K, Stewart FJ, Thornhill DJ (2013) A simple temperature-based model predicts the upper latitudinal limit of the temperate coral Astrangia poculata. Coral Reefs 32:401–409

    Article  Google Scholar 

  • DiRoberts LE (2019) Nitrogen Cycling in the Temperate Northern Star Coral, Astrangia poculata: Distinguishing Autotrophic from Heterotrophic Nutrient Contributions. Boston University

  • Donovan MK, Adam TC, Shantz AA, Speare KE, Munsterman KS, Rice MM, Schmitt RJ, Holbrook SJ, Burkepile DE (2020) Nitrogen pollution interacts with heat stress to increase coral bleaching across the seascape. Proc Natl Acad Sci U S A 117:5351–5357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrier-Pagès C, Peirano A, Abbate M, Cocito S, Negri A, Rottier C, Riera P, Rodolfo-Metalpa R, Reynauda S (2011) Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol Oceanogr 56:1429–1438

    Article  Google Scholar 

  • Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc London Ser B- Biol Sci 269:1205–1210

  • Fisch J, Drury C, Towle EK, Winter RN, Miller MW (2019) Physiological and reproductive repercussions of consecutive summer bleaching events of the threatened Caribbean coral Orbicella faveolata. Coral Reefs 38:863–876

    Article  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

  • Godinot C, Ferrier-Pagès 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 

  • Goldsmith DB, Pratte ZA, Kellogg CA, Snader SE, Sharp KH (2019) Stability of temperate coral Astrangia poculata microbiome is reflected across different sequencing methodologies. AIMS Microbiol 5:62–76

    Article  PubMed  PubMed Central  Google Scholar 

  • Grace S (2017) Winter Quiescence, Growth Rate, and the Release from Competition in the Temperate Scleractinian Coral Astrangia poculata (Ellis & Solander 1786). Northeast Nat 24:B119–B134

    Article  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Montipora verrucosa and Porites compressa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Grover R, Maguer J-F, Reynaud-Vaganay S, Ferrier-Page C (2002) Uptake of ammonium by the scleractinian coral Stylophora: Effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790

    Article  Google Scholar 

  • Hannides CCS, Popp BN, Landry MR, Graham BS (2009) Quantification of zooplankton trophic position in the north pacific subtropical gyre using stable nitrogen isotopes. Limnol Oceanogr 54:50–61

    Article  CAS  Google Scholar 

  • Hoogenboom M, Beraud E, Ferrier-Pagès C (2010a) Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29:21–29

    Article  Google Scholar 

  • Hoogenboom M, Rodolfo-Metalpa R, Ferrier-Pagès C (2010b) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J Exp Biol 213:2399–2409

    Article  PubMed  Google Scholar 

  • Ingalls AE, Lee C, Druffel ERM (2003) Preservation of organic matter in mound-forming coral skeletons. Geochim Cosmochim Acta 67:2827–2841

    Article  CAS  Google Scholar 

  • Jacques TG, Marshall N, Pilson MEQ (1983) Experimental ecology of the temperate scleractinian coral Astrangia danae II. Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar Biol 76:135–148

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determing chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Article  CAS  Google Scholar 

  • Lanctôt CM, Bednarz VN, Melvin S, Jacob H, Oberhaensli F, Swarzenski PW, Ferrier-Pagès C, Carroll AR, Metian M (2020) Physiological stress response of the scleractinian coral Stylophora pistillata exposed to polyethylene microplastics. Environ Pollut 263

  • Leal MC, Ferrier-Pagès C, Calado R, Brandes JA, Frischer ME, Nejstgaard JC (2014) Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar Ecol Prog Ser 504:171–179

    Article  Google Scholar 

  • Lesser MP (2013) Using energetic budgets to assess the effects of environmental stress on corals: Are we measuring the right things? Coral Reefs 32:25–33

    Article  Google Scholar 

  • Miller MW (1995) Growth of a temperate coral: Effects of temperature, light, depth, and heterotrophy. Mar Ecol Prog Ser 122:217–226

    Article  Google Scholar 

  • Mueller CE, Larsson AI, Veuger B, Middelburg JJ, Van Oevelen D (2014) Opportunistic feeding on various organic food sources by the cold-water coral Lophelia pertusa. Biogeosciences 11:123–133

    Article  Google Scholar 

  • Muscatine L, D’Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734

    Article  CAS  Google Scholar 

  • Muscatine L, Goiran C, Land L, Jaubert J, Cuif J-P, Allemand D (2005) Stable isotopes (δ13C and δ15N) of organic matrix from coral skeleton. Proc Natl Acad Sci 102:1525–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muscatine L, Kaplan IR (1994) Resource partitioning by reef corals as determined from stable isotope composition II. δ15N of zooxanthellae and animal tissue versus depth. Pacific Sci 48:304–312

    Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. 1. δ13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193

    Article  Google Scholar 

  • Oczkowski A, Schmidt C, Santos E, Miller K, Hanson A, Cobb D, Krumholz J, Pimenta A, Heffner L, Robinson S, Mckinney R, Division AE, Landscape A, Cooperative C, Fish US, Service W, Rd T (2018) How the distribution of anthropogenic nitrogen has changed in Narragansett Bay (RI, USA) following major reductions in nutrient loads. Estuaries and Coasts 41:2260–2276

  • Patrizzi BJ (2010) The distribution and diet of the Scleractinian coral Astrangia poculata in Long Island Sound. Southern Connecticut State University

  • Peters EC, Cairns SD, Pilson MEQ, Wells JW, Jaap WC, Lang JC, Vasleski CE, St Pierre Gollahon L (1988) Nomenclature and biology of Astrangia poculata (=A. danae, =A. astreiformis) (Cnidaria: Anthozoa). Proc Biol Soc Washingt 101:234–250

    Google Scholar 

  • Rodolfo-Metalpa R, Huot Y, Ferrier-Pages C (2008a) Photosynthetic response of the Mediterranean zooxanthellae coral Cladocora caespitosa to the natural range of light and temperature. J Exp Biol 211:1579–1586

    Article  CAS  PubMed  Google Scholar 

  • Rodolfo-Metalpa R, Peirano A, Houlbreque F, Abbate M, Ferrier-Pages C (2008b) Effects of temperature, light and heterotrophy on the growth rate and budding of the temperate coral Cladocera caespitosa. Coral Reefs 27:17–25

    Article  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim Cosmochim Acta 70:2781–2789

    Article  CAS  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • Rotjan RD, Sharp KH, Gauthier AE, Yelton R, Baron Lopez EM, Carilli J, Kagan JC, Urban-Rich J (2019) Patterns, dynamics and consequences of microplastic ingestion by the temperate coral, Astrangia poculata. Proc R Soc B Biol Sci 286:1–9

    Google Scholar 

  • Sale TL, Hunter CL, Hong C, Moran AL (2019) Morphology, lipid composition, and reproduction in growth anomalies of the reef-building coral Porites evermanni and Porites lobata. Coral Reefs 38:881–893

    Article  Google Scholar 

  • Schiller C (1993) Ecology of the Symbiotic Coral Cladocora caespitosa (L.) Faviidae, Scleractinia in the Bay of Piran (Adriatic Sea): I. Distribution and Biometry. Mar Ecol 14:205–219

    Article  Google Scholar 

  • Sharp KH, Pratte ZA, Kerwin AH, Rotjan RD, Stewart FJ (2017) Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata. Microbiome 5:120

    Article  PubMed  PubMed Central  Google Scholar 

  • Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904

    Google Scholar 

  • Szmant-Froelich A (1981) Coral nutrition: Comparison of the fate of 14C from ingested labeled brine shrimp and from the uptake of NaH14CO3 by its zooxanthellae. J Exp Mar Bio Ecol 55:133–144

    Article  CAS  Google Scholar 

  • Szmant-Froelich A, Pilson MEQ (1980) The effects of feeding frequently and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae Milne Edwards & Haime 1849. J Exp Mar Bio Ecol 48:85–97

    Article  CAS  Google Scholar 

  • Szmant-Froelich A, Yevich P, Pilson MEQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae. Biol Bull 158:257–269

    Article  Google Scholar 

  • Tambutte S, Tambutte E, Zoccola D, Caminiti N, Lotto S, Moya A, Allemand D, Adkins J (2007) Characterization and role of carbonic anhydrase in the calcification process of the azooxanthellate coral Tubastrea aurea. Mar Biol 151:71–83

    Article  CAS  Google Scholar 

  • Tremblay P, Maguer JF, Grover R, Ferrier-Pagès C (2015) Trophic dynamics of scleractinian corals: Stable isotope evidence. J Exp Biol 218:1223–1234

    PubMed  Google Scholar 

  • Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: Comparison with two other scleractinian species. Mar Ecol Prog Ser 422:165–177

    Article  Google Scholar 

  • Venegas RM, Oliver T, Liu G, Heron SF, Clark SJ, Pomeroy N, Young C, Eakin CM, Brainard RE (2019) The Rarity of Depth Refugia from Coral Bleaching Heat Stress in the Western and Central Pacific Islands. Sci Rep 9:1–12

    Article  CAS  Google Scholar 

  • Viladrich N, Bramanti L, Tsounis G, Chocarro B, Martínez-Quitana A, Ambroso S, Madurell T, Rossi S (2016) Variation in lipid and free fatty acid content during spawning in two temperate octocorals with different reproductive strategies: surface versus internal brooder. Coral Reefs 35:1033–1045

    Article  Google Scholar 

  • Vinagre C, Salgado J, Costa MJ, Cabral HN (2008) Nursery fidelity, food web interactions and primary sources of nutrition of the juveniles of Solea solea and S. senegalensis in the Tagus estuary (Portugal): A stable isotope approach. Estuar Coast Shelf Sci 76:255–264

    Article  Google Scholar 

  • Wainright SC, Fry B (1994) Seasonal variation of the stable isotopic compositions of coastal marine plankton from Woods Hole, Massachusetts and Georges Bank. Estuaries 17:552–560

    Article  Google Scholar 

  • Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastrea. Mar Biol 141:31–38

    Article  CAS  Google Scholar 

  • Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719

    Article  CAS  PubMed  Google Scholar 

  • Wild C, Naumann M, Niggl W, Haas A (2010) Carbohydrate composition of mucus released by scleractinian warm- and cold-water reef corals. Aquat Biol 10:41–45

    Article  Google Scholar 

Download references

Acknowledgements

We thank G. DiPreta and S. Koerner for their assistance in the field; D. Velinsky and M. Gannon for isotopic analyses; and K. Henderson and K. Shakya for comments to an earlier draft of this manuscript. Funding was provided to WT by a graduate assistantship and summer research fellowship from the Graduate College of Liberal Arts and Sciences, Villanova University; and to LJR by the Department of Geography and the Environment, Villanova University. We extend appreciation to K. Sharp, R. Rotjan, S. Grace and the annual Astrangia Workshop hosted by Roger Williams University for fostering creative conversations and collaborations leading to this work.

Author information

Authors and Affiliations

  1. Department of Geography and the Environment, Villanova University, 800 Lancaster Avenue, Villanova, PA, 19085, USA

    Wolfgang Trumbauer & Lisa J. Rodrigues

  2. Department of Biology, Werth Center for Coastal and Marine Studies, Southern Connecticut State University, 501 Crescent Street, New Haven, CT, 06515, USA

    Sean P. Grace

Authors
  1. Wolfgang Trumbauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sean P. Grace
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa J. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa J. Rodrigues.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical approval

No approval of a research ethics committee was required to accomplish the goals of this study because the research was conducted with an unregulated invertebrate species.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Steve Vollmer

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trumbauer, W., Grace, S.P. & Rodrigues, L.J. Physiological seasonality in the symbiont and host of the northern star coral, Astrangia poculata. Coral Reefs 40, 1155–1166 (2021). https://doi.org/10.1007/s00338-021-02119-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-021-02119-5

Keywords

Search

Navigation