Skip to main content

Advertisement

Log in

Current and future trophic interactions in tropical shallow-reef lagoon habitats

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

Abstract

Calcium carbonate (CaCO3) sediments are the dominant form of CaCO3 on coral reefs accumulating in lagoon and inter-reefal areas. Owing to their mineralogy and a range of physical parameters, tropical CaCO3 sediments are predicted to be more sensitive to dissolution driven by ocean acidification than the skeleton of living reef organisms. How this scales up to impact infaunal organisms, which are an important food source for higher trophic levels, and thereby ecosystem functioning, is not well explored. We combined seasonal field surveys in a shallow-reef lagoon ecosystem on the Great Barrier Reef, Australia, with stable isotope analyses and a tank-based experiment to examine the potential top-down influence of the deposit-feeding sea cucumber, Stichopus herrmanni, on this infaunal community under current and future ocean pH. Densities of surface-sediment meiofauna were lowest in winter and spring, with harpacticoid copepods (38%) and nematodes (27%) the dominant taxa. Stable isotope analyses showed that S. herrmanni had a top-down influence on meiofauna and microphytes with a distinct δ13C and δ15N trophic position that was homogenous across seasons and locations. Tanks that mimicked sandy shallow-reef lagoon habitats were used to examine the effects of ocean acidification (elevated pCO2) on this trophic interaction. We used outdoor control (sediment only) and experimental (sediment plus S. herrmanni) tanks maintained at present-day and near-future pCO2 (+ 570 µatm) for 24 days, which fluctuated with the diel pCO2 cycle. In sediment-only tanks, copepods were > twofold more abundant at elevated pCO2, with no negative effects documented for any meiofauna group. When included in the community, top-down control by S. herrmanni counteracted the positive effects of low pH on meiofaunal abundance. We highlight a novel perspective in coral reef trophodynamics between surface-sediment meiofauna and deposit-feeding sea cucumbers, and posit that community shifts may occur in shallow-reef lagoon habitats in a future ocean with implications for the functioning of coral reefs from the bottom up.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

taken from the a body wall and b tube feet. Note: n = 1 for infaunal groups (see “Methods”)

Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albright R, Caldeira L, Hosfelt J, Kwiatkowski L, Maclaren JK, Mason BM, Nebuchina Y, Ninokawa A, Pongratz J, Ricke KL, Rivlin T, Schneider K, Sesboue M, Shamberger K, Silverman J, Wolfe K, Zhu K, Caldeira K (2016) Reversal of ocean acidification enhances net coral reef calcification. Nature 531:362–365

    Article  CAS  PubMed  Google Scholar 

  • Albright R, Takeshita Y, Koweek DA, Ninokawa A, Wolfe K, Rivlin T, Nebuchina Y, Young J, Caldeira K (2018) Carbon dioxide addition to coral reef waters suppresses net community calcification. Nature 555:516–519

    Article  CAS  PubMed  Google Scholar 

  • Alongi D, Tietjen J (1980) Population growth and trophic interactions among free-living marine nematodes. Marine Benthic Dynamics 151–166

  • Alongi DM (1986) Population structure and trophic composition of the free-living nematodes inhabiting carbonate sands of Davies Reef, Great Barrier Reef, Australia. Aust J Mar Fresh Res 37:609–619

    Article  Google Scholar 

  • Alongi DM (1990) Community dynamics of free-living nematodes in some tropical mangrove and sandflat habitats. B Mar Sci 46:358–373

    Google Scholar 

  • Alsterberg C, Eklof JS, Gamfeldt L, Havenhand JN, Sundback K (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. P Natl Acad Sci USA 110:8603–8608

    Article  CAS  Google Scholar 

  • Andersson AJ, Bates NR, Mackenzie FT (2007) Dissolution of carbonate sediments under rising pCO(2) and ocean acidification: Observations from Devil’s Hole, Bermuda. Aquat Geochem 13:237–264

    Article  CAS  Google Scholar 

  • Andersson AJ, Mackenzie FT (2012) Revisiting four scientific debates in ocean acidification research. Biogeosciences 9:893–905

    Article  CAS  Google Scholar 

  • Arlt G (1995) Composition and seasonal variations in the tropical shallow subtidal meiofauna of a coral reef lagoon near Massawa (Red Sea, Eritrea). Olsen Int S:101–106

  • Bartoń K (2018) MuMIn: Multi-model inference. R Package Version 1(42):1

    Google Scholar 

  • Bickert T (2006) Influence of geochemical processes on stable isotope distribution in marine sediments. In: Schulz HD, Zabel M (eds) Marine Geochemistry. Springer, Berlin, pp 339–369

    Chapter  Google Scholar 

  • Birkeland C (1989) The influence of echinoderms on coral reef communities. In: Jangoux M, Lawrence JM (eds) Echinoderm studies 3. Balkema, Rotterdam, pp 1–79

    Google Scholar 

  • Boucher G, Clavier J (1990) Contribution of benthic biomass to overall metabolism in New Caledonia lagoon sediments. Mar Ecol Prog Ser 271–280

  • Bozec YM, Gascuel D, Kulbicki M (2004) Trophic model of lagoonal communities in a large open atoll (Uvea, Loyalty islands, New Caledonia). Aquat Living Resour 17:151–162

    Article  Google Scholar 

  • Cai L, Fu S, Yang J, Zhou X (2012) Distribution of meiofaunal abundance in relation to environmental factors in Beibu Gulf, South China Sea. Acta Oceanol Sin 31:92–103

    Article  Google Scholar 

  • Chambers JM, Hastie T (1992) Statistical Models in S. Wadsworth & Brooks/Cole Advanced Books & Software

  • Chou W-C, Liu P-J, Chen Y-H, Huang W-J (2020) Contrasting changes in diel variations of net community calcification support that carbonate dissolution can be more sensitive to ocean acidification than coral calcification. Frontiers in Marine Science 7:3

    Article  Google Scholar 

  • Cigliano M, Gambi M, Rodolfo-Metalpa R, Patti F, Hall-Spencer J (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502

    Article  Google Scholar 

  • Collard M, Eeckhaut I, Dehairs F, Dubois P (2014) Acid-base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva. Environ Sci Pollut R 21:13602–13614

    Article  CAS  Google Scholar 

  • Conand C, Polidoro BA, Mercier A, Gamboa R, Hamel J-F, Purcell SW (2014) The IUCN Red List assessment of aspidochirotid sea cucumbers and its implications. SPC Bêche-de-mer Bulletin 34:3–7

    Google Scholar 

  • Couch CA (1989) Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuar Coast Shelf Sci 28:433–441

    Article  Google Scholar 

  • Coull BC (1990) Are members of the meiofauna food for higher trophic levels? T Am Microsc Soc 233–246

  • Coull BC (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327–343

    Article  Google Scholar 

  • Coull BC, Greenwood JG, Fielder DR, Coull BA (1995) Subtropical Australian juvenile fish eat meiofauna: experiments with winter whiting Sillago maculata and observations on other species. Mar Ecol Prog Ser 125:13–19

    Article  Google Scholar 

  • Crossland CJ, Hatcher BG, Smith SV (1991) Role of coral reefs in global ocean production. Coral Reefs 10:55–64

    Article  Google Scholar 

  • Cyronak T, Andersson AJ, Langdon C, Albright R, Bates NR, Caldeira K, Carlton R, Corredor JE, Dunbar RB, Enochs I, Erez J, Eyre BD, Gattuso JP, Gledhill D, Kayanne H, Kline DI, Koweek DA, Lantz C, Lazar B, Manzello D, McMahon A, Melendez M, Page HN, Santos IR, Schulz KG, Shaw E, Silverman J, Suzuki A, Teneva L, Watanabe A, Yamamoto S (2018) Taking the metabolic pulse of the world’s coral reefs. PLoS ONE 13:e0190872

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cyronak T, Eyre BD (2016) The synergistic effects of ocean acidification and organic metabolism on calcium carbonate (CaCO3) dissolution in coral reef sediments. Mar Chem 183:1–12

    Article  CAS  Google Scholar 

  • Cyronak T, Santos IR, Eyre BD (2013) Permeable coral reef sediment dissolution driven by elevated pCO(2) and pore water advection. Geophys Res Lett 40:4876–4881

    Article  CAS  Google Scholar 

  • Danovaro R, Scopa M, Gambi C, Fraschetti S (2007) Trophic importance of subtidal metazoan meiofauna: evidence from in situ exclusion experiments on soft and rocky substrates. Mar Biol 152:339–350

    Article  Google Scholar 

  • Dashfield SL, Somerfield PJ, Widdicombe S, Austen MC, Nimmo M (2008) Impacts of ocean acidification and burrowing urchins on within-sediment pH profiles and subtidal nematode communities. J Exp Mar Biol Ecol 365:46–52

    Article  CAS  Google Scholar 

  • DeCarlo TM, Cohen AL, Wong GTF, Shiah FK, Lentz SJ, Davis KA, Shamberger KEF, Lohmann P (2017) Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification. J Geophys Res-Oceans 122:745–761

    Article  CAS  Google Scholar 

  • Dove SG, Kline DI, Pantos O, Angly FE, Tyson GW, Hoegh-Guldberg O (2013) Future reef decalcification under a business-as-usual CO2 emission scenario. P Natl Acad Sci USA 110:15342–15347

    Article  CAS  Google Scholar 

  • Ellis MJ, Coull BC (1989) Fish predation on meiobenthos: field experiments with juvenile spot Leiostomus xanthurus Lacepede. J Exp Mar Biol Ecol 130:19–32

    Article  Google Scholar 

  • Eriksson H, Byrne M (2015) The sea cucumber fishery in Australia’s Great Barrier Reef Marine Park follows global patterns of serial exploitation. Fish Fish 16:329–341

    Article  Google Scholar 

  • Eriksson H, Thorne BV, Byrne M (2013) Population metrics in protected commercial sea cucumber populations (curryfish: Stichopus herrmanni) on One Tree Reef, Great Barrier Reef. Mar Ecol Prog Ser 473:225–234

    Article  Google Scholar 

  • Eyre BD, Andersson AJ, Cyronak T (2014) Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat Clim Change 4:969–976

    Article  CAS  Google Scholar 

  • Furnas MJ, Mitchell AW, Gilmartin M, Revelante N (1990) Phytoplankton biomass and primary production in semi-enclosed reef lagoons of the central Great Barrier Reef, Australia. Coral Reefs 9:1–10

    Article  Google Scholar 

  • Gattuso JP, Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst 29:405–434

    Article  Google Scholar 

  • Gee J (1989) An ecological and economic review of meiofauna as food for fish. Zool J Linn Soc-Lond 96:243–261

    Article  Google Scholar 

  • Gibbons M, Griffiths C (1986) A comparison of macrofaunal and meiofaunal distribution and standing stock across a rocky shore, with an estimate of their productivities. Mar Biol 93:181–188

    Article  Google Scholar 

  • Giere O (2008) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer Science & Business Media

  • Guzman HM, Obando VL, Cortes J (1987) Meiofauna associated with a Pacific coral reef in Costa Rica. Coral Reefs 6:107–112

    Article  Google Scholar 

  • Hale R, Calosi P, McNeill L, Mieszkowska N, Widdicombe S (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674

    Article  Google Scholar 

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  CAS  PubMed  Google Scholar 

  • Hansen JA, Klumpp DW, Alongi DM, Dayton PK, Riddle MJ (1992) Detrital pathways in a coral reef lagoon. 2. Detritus deposition, benthic microbial biomass and production. Mar Biol 113:363–372

    Article  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, van de Leemput IA, Lough JM, Morrison TH, Palumbi SR, van Nes EH, Scheffer M (2017) Coral reefs in the Anthropocene. Nature 546:82–90

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim S, Hussin WMRW, Kassim Z, Joni ZM, Zakaria MZ, Hajisamae S (2006) Seasonal abundance of benthic communities in coral areas of Karah Island, Terengganu, Malaysia. Turk J Fish Aquat Sc 6:129–136

    Google Scholar 

  • Kinsey D (1985) Metabolism, calcification and production: I. System level studies. Proceedings of the 5th International Coral Reef Congress 4:503–542

  • Kolasinski J, Rogers K, Cuet P, Barry B, Frouin P (2011) Sources of particulate organic matter at the ecosystem scale: a stable isotope and trace element study in a tropical coral reef. Mar Ecol Prog Ser 443:77–93

    Article  CAS  Google Scholar 

  • Koweek D, Dunbar RB, Rogers JS, Williams GJ, Price N, Mucciarone D, Teneva L (2015) Environmental and ecological controls of coral community metabolism on Palmyra Atoll. Coral Reefs 34:339–351

    Article  Google Scholar 

  • Kozak ER, Franco-Gordo C, Godínez-Domínguez E, Suárez-Morales E, Ambriz-Arreola I (2020) Seasonal variability of stable isotope values and niche size in tropical calanoid copepods and zooplankton size fractions. Mar Biol 167:37

    Article  CAS  Google Scholar 

  • Kramer MJ, Bellwood O, Bellwood DR (2013) The trophic importance of algal turfs for coral reef fishes: the crustacean link. Coral Reefs 32:575–583

    Article  Google Scholar 

  • Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011) Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc Natl Acad Sci 108:14515–14520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurihara H, Ishimatsu A, Shirayama Y (2007) Effects of elevated seawater CO2 concentration on the meiofauna. Journal of Marine Science and Technology:17–22

  • Lenth R (2019) emmeans: estimated marginal means (least-squares means). R Package Version 1(3):3

    Google Scholar 

  • Logan D, Townsend KA, Townsend K, Tibbetts IR (2008) Meiofauna sediment relations in leeward slope turf algae of Heron Island reef. Hydrobiologia 610:269–276

    Article  Google Scholar 

  • Naumann MS, Mayr C, Struck U, Wild C (2010) Coral mucus stable isotope composition and labeling: experimental evidence for mucus uptake by epizoic acoelomorph worms. Mar Biol 157:2521–2531

    Article  Google Scholar 

  • Noonan SHC, Kluibenschedl A, Fabricius KE (2018) Ocean acidification alters early successional coral reef communities and their rates of community metabolism. Plos One 13

  • Ollivier QR, Hammill E, Booth DJ, Madin EMP, Hinchliffe C, Harborne AR, Lovelock CE, Macreadie PI, Atwood TB (2018) Benthic meiofaunal community response to the cascading effects of herbivory within an algal halo system of the Great Barrier Reef. PLoS ONE 13:e0193932

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Piot A, Nozais C, Archambault P (2014) Meiofauna affect the macrobenthic biodiversity–ecosystem functioning relationship. Oikos 123:203–213

    Article  Google Scholar 

  • Poloczanska E, Portner HO, Mintenbeck K. 2020. The IPCC Special Report on Ocean and Cryosphere in a Changing Climate–a view from the mountains tops to the deepest depths. Ocean Sciences Meeting 2020, AGU.

  • Post E, Pedersen C (2008) Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci 105:12353–12358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Przeslawski R, Ahyong S, Byrne M, Worheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Global Change Biol 14:2773–2795

    Article  Google Scholar 

  • Purcell SW, Conand C, Uthicke S, Byrne M (2016) Ecological roles of exploited sea cucumbers. Oceanogr Mar Biol Annu Rev 54:367–386

    Google Scholar 

  • Purcell SW, Lovatelli A, Pakoa K (2014) Constraints and solutions for managing Pacific Island sea cucumber fisheries with an ecosystem approach. Mar Policy 45:240–250

    Article  Google Scholar 

  • Purcell SW, Mercier A, Conand C, Hamel JF, Toral-Granda MV, Lovatelli A, Uthicke S (2013) Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish 14:34–59

    Article  Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rao AMF, Polerecky L, Ionescu D, Meysman FJR, de Beer D (2012) The influence of pore-water advection, benthic photosynthesis, and respiration on calcium carbonate dynamics in reef sands. Limnol Oceanogr 57:809–825

    Article  CAS  Google Scholar 

  • Roberts D, Bryce C (1982) Further observations on tentacular feeding mechanisms in holothurians. J Exp Mar Biol Ecol 59:151–163

    Article  Google Scholar 

  • Romanek CS, Grossman EL (1989) Stable isotope profiles of Tridacna maxima as environmental indicators. Palaios:402–413

  • Rossoll D, Bermúdez R, Hauss H, Schulz KG, Riebesell U, Sommer U, Winder M (2012) Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7:e34737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samyn Y, Tallon I (2005) Zoogeography of the shallow-water holothuroids of the western Indian Ocean. J Biogeogr 32:1523–1538

    Article  Google Scholar 

  • Sarmento VC, Pinheiro BR, Montes MDF, Santos PJP (2017) Impact of predicted climate change scenarios on a coral reef meiofauna community. ICES J Mar Sci 74:1170–1179

    Article  Google Scholar 

  • Sarmento VC, Souza TP, Esteves AM, Santos PJP (2015) Effects of seawater acidification on a coral reef meiofauna community. Coral Reefs 34:955–966

    Article  Google Scholar 

  • Schneider K, Silverman J, Kravitz B, Rivlin T, Schneider-Mor A, Barbosa S, Byrne M, Caldeira K (2013) Inorganic carbon turnover caused by digestion of carbonate sands and metabolic activity of holothurians. Estuar Coast Shelf S 133:217–223

    Article  CAS  Google Scholar 

  • Schneider K, Silverman J, Woolsey E, Eriksson H, Byrne M, Caldeira K (2011) Potential influence of sea cucumbers on coral reef CaCO3 budget: A case study at One Tree Reef. J Geophys Res-Biogeo 116:G04032

    Article  CAS  Google Scholar 

  • Scoffin TP, Tudhope AW (1985) Sedimentary environments of the central region of the Great Barrier Reef of Australia. Coral Reefs 4:81–93

    Article  CAS  Google Scholar 

  • Semprucci F, Colantoni P, Baldelli G, Sbrocca C, Rocchi M, Balsamo M (2013) Meiofauna associated with coral sediments in the Maldivian subtidal habitats (Indian Ocean). Mar Biodivers 43:189–198

    Article  Google Scholar 

  • Semprucci F, Frontalini F, Losi V, du Chatelet EA, Cesaroni L, Sandulli R, Coccioni R, Balsamo M (2018) Biodiversity and distribution of the meiofaunal community in the reef slopes of the Maldivian archipelago (Indian Ocean). Mar Environ Res 139:19–26

    Article  CAS  PubMed  Google Scholar 

  • Service SK, Feller RJ, Coull BC, Woods R (1992) Predation effect of three fish species and a shrimp on macrobenthos and meiobenthos in microcosms. Estuar Coast Shelf Sci 34:277–293

    Article  Google Scholar 

  • Shaver EC, Silliman BR (2017) Time to cash in on positive interactions for coral restoration. Peerj 5:e3499

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaw EC, Phinn SR, Tilbrook B, Steven A (2015) Natural in situ relationships suggest coral reef calcium carbonate production will decline with ocean acidification. Limnol Oceanogr 60:777–788

    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

  • Smith LD, Coull BC (1987) Juvenile spot (Pisces) and grass shrimp predation on meiobenthos in muddy and sandy substrata. J Exp Mar Biol Ecol 105:123–136

    Article  Google Scholar 

  • Snelgrove PV (1997) The importance of marine sediment biodiversity in ecosystem processes. Ambio 26:578–583

    Google Scholar 

  • Solan M, Bennett E, Mumby P, Leyland J, Godbold J (2020) Benthic-based contributions to climate change mitigation and adaptation. Philos T R Soc B 375:20190107

    Article  Google Scholar 

  • Solan M, Cardinale BJ, Downing AL, Engelhardt KA, Ruesink JL, Srivastava DS (2004) Extinction and ecosystem function in the marine benthos. Science 306:1177–1180

    Article  CAS  PubMed  Google Scholar 

  • Souza-Santos L, Ribeiro V, Santos P, Fonseca-Genevois V (2003) Seasonality of intertidal meiofauna on a tropical sandy beach in Tamandaré Bay (Northeast Brazil). J Coastal Res:369–377

  • St John J, Jones GP, Sale PF (1989) Distribution and abundance of soft-sediment meiofauna and a predatory goby in a coral reef lagoon. Coral Reefs 8:51–57

    Article  Google Scholar 

  • Steiner Z, Turchyn AV, Harpaz E, Silverman J (2018) Water chemistry reveals a significant decline in coral calcification rates in the southern Red Sea. Nat Commun 9:3615

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sunday JM, Fabricius KE, Kroeker KJ, Anderson KM, Brown NE, Barry JP, Connell SD, Dupont S, Gaylord B, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2017) Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat Clim Change 7:81–85

    Article  CAS  Google Scholar 

  • Tilbrook B, Van Oiijen E, Neill C, Berry K, Akl J, Passmore A, Lenton A, Richardson AJ (2020) Ocean acidification. In: Richardson AJ, Eriksen R, Moltmann T, Wallis JR, Hodgson-Johnston I (eds) State and trends of Australia’s ocean report. Integrated Marine Observing System (IMOS), Hobart, pp 49–52

    Google Scholar 

  • Tita G, Desrosiers G, Vincx M, Nozais C (2000) Predation and sediment disturbance effects of the intertidal polychaete Nereis virens (Sars) on associated meiofaunal assemblages. J Exp Mar Biol Ecol 243:261–282

    Article  Google Scholar 

  • Uthicke S (1999) Sediment bioturbation and impact of feeding activity of Holothuria (Halodeima) atra and Stichopus chloronotus, two sediment feeding holothurians, at Lizard Island, Great Barrier Reef. B Mar Sci 64:129–141

    Google Scholar 

  • Uthicke S (2001a) Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement. Mar Ecol Prog Ser 210:125–138

    Article  CAS  Google Scholar 

  • Uthicke S (2001b) Nutrient regeneration by abundant coral reef holothurians. J Exp Mar Biol Ecol 265:153–170

    Article  CAS  Google Scholar 

  • Uthicke S, Klumpp DW (1998) Microphytobenthos community production at a near-shore coral reef: seasonal variation and response to ammonium recycled by holothurians. Mar Ecol Prog Ser 169:1–11

    Article  CAS  Google Scholar 

  • Vidal-Ramirez F, Dove S (2016) Diurnal effects of Holothuria atra on seawater carbonate chemistry in a sedimentary environment. J Exp Mar Biol Ecol 474:156–163

    Article  CAS  Google Scholar 

  • Walter LM, Morse JW (1984) Reactive surface area of skeletal carbonates during dissolution; effect of grain size. J Sediment Res 54:1081–1090

    CAS  Google Scholar 

  • Walther BD, Kingsford MJ, McCulloch MT (2013) Environmental records from Great Barrier Reef corals: inshore versus offshore drivers. Plos One 8:e77091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wefer G, Berger WH (1991) Isotope paleontology: growth and composition of extant calcareous species. Mar Geol 100:207–248

    Article  CAS  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Global Change Biol 18:1491–1498

    Article  Google Scholar 

  • Werner U, Blazejak A, Bird P, Eickert G, Schoon R, Abed RMM, Bissett A, de Beer D (2008) Microbial photosynthesis in coral reef sediments (Heron Reef, Australia). Estuar Coast Shelf S 76:876–888

    Article  Google Scholar 

  • Whiteley N (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271

    Article  CAS  Google Scholar 

  • Widdicombe S, Dashfield S, McNeill C, Needham H, Beesley A, McEvoy A, Øxnevad S, Clarke K, Berge J (2009) Effects of CO2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar Ecol Prog Ser 379:59–75

    Article  CAS  Google Scholar 

  • Wolanski E (2000) Physics–biology links in the Great Barrier Reef. Oceanographic Processes of Coral Reefs. CRC Press, pp 27–38

  • Wolfe K, Anthony K, Babcock RC, Bay L, Bourne D, Burrows D, Byrne M, Deaker D, Diaz-Pulido G, Frade PR, Gonzalez-Rivero M, Hoey A, Hoogenboom M, McCormick M, Ortiz J-C, Razak T, Richardson AJ, Roff G, Sheppard-Brennand H, Stella J, Thompson A, Watson S-A, Webster N, Audas D, Beeden R, Carver J, Cowlishaw M, Dyer M, Groves P, Horne D, Thiault L, Vains J, Wachenfeld D, Weekers D, Williams G, Mumby PJ (in press) Priority species to support the functional integrity of coral reefs. Oceanography and Marine Biology: An Annual Review 58

  • Wolfe K, Byrne M (2017) Biology and ecology of the vulnerable holothuroid, Stichopus herrmanni, on a high-latitude coral reef on the Great Barrier Reef. Coral Reefs 36:1143–1156

    Article  Google Scholar 

  • Wolfe K, Vidal-Ramirez F, Dove S, Deaker D, Byrne M (2018) Altered sediment biota and lagoon habitat carbonate dynamics due to sea cucumber bioturbation in a high-pCO(2) environment. Global Change Biol 24:465–480

    Article  Google Scholar 

  • Wolkenhauer SM, Uthicke S, Burridge C, Skewes T, Pitcher R (2010) The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds. J Mar Biol Assoc Uk 90:215–223

    Article  Google Scholar 

  • Woods RE, Coull BC (1992) Life history responses of Amphiascus tenuiremis (Copepoda, Harpacticoida) to mimicked predation. Mar Ecol Prog Ser 79:225–234

    Article  Google Scholar 

  • Yamamuro M, Kayanne H, Minagawao M (1995) Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol Oceanogr 40:617–621

    Article  CAS  Google Scholar 

  • Yohannes E, Hansson B, Lee RW, Waldenström J, Westerdahl H, Åkesson M, Hasselquist D, Bensch S (2008) Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia 158:299–306

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a PhD scholarship from the University of Sydney and grants from the Mohammed bin Zayed Species Conservation Fund, the Great Barrier Reef Foundation, the Great Barrier Reef Marine Park Authority and the Holsworth Wildlife Research Endowment. The authors thank Dr. Sebastian Holmes and Dr. Mallie Gall for assistance with isotopic methodology and sample preparation, and Dr. Francisco Vidal-Ramirez, Aaron Chai, Giovanni Bernal Carrillo and the Coral Reef Ecosystems Laboratory (University of Queensland) for support with climate change experiments on Heron Island. Additionally, they thank Camila Ayroza, Dr. Shawna Foo, Luca Palazzo and Louise Wolfe for assistance in the field, and the staff of One Tree, Heron and Orpheus Island Research Stations. This is contribution number 261 from the Sydney Institute of Marine Science. On behalf of all authors, the corresponding author states that there is no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kennedy Wolfe.

Additional information

Publisher's Note

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

Topic Editor: Alastair Harborne

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wolfe, K., Deaker, D.J., Graba-Landry, A. et al. Current and future trophic interactions in tropical shallow-reef lagoon habitats. Coral Reefs 40, 83–96 (2021). https://doi.org/10.1007/s00338-020-02017-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-02017-2

Keywords

Navigation