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Did the historic overharvesting of sea cucumbers make coral more susceptible to pathogens?

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Abstract

Detritivore sea cucumbers appear to have been abundant on historic tropical reefs, but (1) have been heavily exploited since at least the mid-1800s, (2) often show minimal recovery post-harvest, and (3) are relatively depleted from modern marine communities. Because they were more abundant, fed on bacteria, microalgae, and other organics, and processed tremendous masses of sediments, removing these detritivores from tropical seas may have suppressed removal of sedimentary pathogens, and impacted co-occurring species in ways that are not documented. We conducted enclosure and exclosure experiments of the sea cucumber Holothuria atra in a back reef lagoon in Moorea, French Polynesia and found that excluding this sea cucumber increased a measure of sediment surface pigmentation by about 10 × but also decreased the potency of extracts from a co-occurring coral (Acropora cytherea) against the heat-activated coral pathogen Vibrio coralliilyticus by a significant 52%. This suggests that the large-scale removal of detritovores from shallow tropical seas may make some co-occurring foundation species more susceptible to pathogens during periods of elevated temperatures or other stresses.

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References

  • Allgeier JE, Burkepile DE, Layman CA (2017) Animal pee in the sea: consumer-mediated nutrient dynamics in the world’s changing oceans. Glob Chang Biol 23:2166–2178

    Article  Google Scholar 

  • Anderson SC, Flemming JM, Watson R, Lotze HK (2011) Serial exploitation of global sea cucumber fisheries. Fish Fish 12:317–339

    Article  Google Scholar 

  • Bakus GJ (1968) Defensive mechanisms and ecology of some tropical holothurians. Mar Biol 2:23–32

    Article  Google Scholar 

  • Beatty DS, Valayil J, Clements CS, Ritchie K, Stewart FJ, Hay ME (2019) Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen. Sci Adv 5(10):eaay1048

    Article  CAS  Google Scholar 

  • Boyero L, López-Rojo N, Tonin AM, Pérez J, Correa-Araneda F, Pearson RG, Bosch J (2021) Impacts of detritivore diversity loss on instream decomposition are greatest in the tropics. Nat Commun 12:3700

    Article  CAS  Google Scholar 

  • Clements CS, Hay ME (2019) Biodiversity enhances coral growth, tissue survivorship and suppression of macroalgae. Nat Ecol Evol 3:178–182

    Article  Google Scholar 

  • Conand C (1990) The fishery resources of the Pacific island countries, Part 2. Holothurians. FAO Fish Tech Pap 272:2

    Google Scholar 

  • Eriksson H, Friedman K, Amos M, Bertram I, Pakoa K, Fisher R, Andrew N (2017) Geography limits island small-scale fishery production. Fish Fish 19:308–320

    Article  Google Scholar 

  • Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jasckson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple W, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soule ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–316

    Article  CAS  Google Scholar 

  • Genin A, Levy L, Sharon G, Raitsos DE, Diamant A (2020) Rapid onset of warming events trigger mass mortality of coral reef fish. Proc Nat Acad Sci USA 117:25378–25385

    Article  CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Ecology, climate warming and disease risk for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  Google Scholar 

  • Harvell CD, Montecino-Latorre D, Caldwell JM, Burt JM, Bosley K, Keller A, Heron SF, Salomon AK, Lee L, Pontier O, Pattengill-Semmens C, Gaydos JK (2019) Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Sci Adv 5:eaau7042

    Article  CAS  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    Article  CAS  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal K, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hugher TP, Kidwell S, Lang CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  CAS  Google Scholar 

  • Kinch J, Purcell J, Uthicke S, Friedman K (2008) Population status, fisheries and trade of sea cucumbers In the western Central pacific. In: Toral-Grande V, Lovatelli A, Vasconcellos M (Eds) Sea cucumbers: a global review of fisheries and trade.FAO Fisheries and Aquaculture Technical Paper # 516. Rome, FAO. Pp. 7–55.

  • Lamb JB, Van De Water JAJM, Bourne DG, Altier C, Hein MY, Fiorenza EA, Abu N, Jompa J, Harvell CD (2017) Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355:731–733

    Article  Google Scholar 

  • Lawrence JM (1979) Numbers and biomass of the common holothuroids on the windward reef flat at Enewetak atoll. In: Echinoderms Present and Past. Edited by M. Jangoux. Rotterdam, Balkema, pp. 201–204

    Google Scholar 

  • Lee S, Ford AK, Mangubhai S, Wild C, Ferse SCA (2018) Effects of sandfish (Holothuria scabra) removal on shallow-water sediments in Fiji. PeerJ 6:e4773. https://doi.org/10.7717/peerj.4773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  CAS  Google Scholar 

  • Moriarty DJW (1982) Feeding of Holoturia atra and Stichopus chloronotus on bacteria, organic carbon and organic nitrogen in sediments of the Great Barrier Reef. Aust J Mar Freshw Res 33:255–263

    Article  Google Scholar 

  • Moriarty DJW, Pollard PC, Hunt WG, Moriarty CM, Wassenberg TJ (1985) Productivity of bacteria and microalgae and the effect of grazing by holothurians in sediments on a coral reef. Mar Biol 85:293–300

    Article  Google Scholar 

  • Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46:609–620

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Richmond R (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. In C. Birkeland (Ed.), Life and death of coral reefs (pp. 175–196). New York: Chapman and Hall

    Chapter  Google Scholar 

  • Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343: Article number 1241484. https://doi.org/10.1126/science.1241484

  • Seale A (1911) The fishery resources of the Philippine Islands. Part IV, miscellaneous marine products. Philipp J Sci 6:283–289

    Google Scholar 

  • Stein A (2018) Development and application of sea cucumber fishery regulations in French Polynesia. SPC Fisheries Newsletter 157:40–59

    Google Scholar 

  • Steneck RS, Bellwood DR, Hay ME (2017) Herbivory in the marine realm: shaping ecosystems and colliding with the Anthropocene. Curr Biol 27:R484-489

    Article  CAS  Google Scholar 

  • Taylor BW, Flecker AS, Hall RO (2006) Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–836

    Article  CAS  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. Bull Mar Sci 64:129–141

    Google Scholar 

  • Uthicke S (2001) 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, Welch D, Benzie JAH (2004) Slow growth and lack of recovery in overfished Holothurians on the Great Barrier Reef: evidence from DNA fingerprints and repeated large-scale surveys. Conserv Biol 18:1395–1404

    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-pCO2 environment. Glob Chang Biol 24:465–480

    Article  Google Scholar 

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Acknowledgements

Financial support came from U.S. National Science Foundation Grant OCE 1947522, the National Geographic Society (Grant No. NGS-57078R-19), the Teasley Endowment, and the Anna and Harry Teasley Gift Fund. This work represents a contribution of the Moorea Coral Reef (MCR) LTER Site supported by U.S. National Science Foundation Grant OCE 16-37396. We thank the French Polynesian Government (Délégation à la Recherche) and the Haut-commissariat de la République en Polynésie Française (DTRT) for relevant permits (Protocole d'Accueil 2017–2020).

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  1. Deanna S. Beatty

    Present address: Department of Evolution and Ecology, University of California, Davis, Davis, CA, 95616, USA

Authors and Affiliations

  1. Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, CA, 92093, USA

    Natalie Grayson

  2. School of Biological Sciences and Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Cody S. Clements, Alexandra A. Towner, Deanna S. Beatty & Mark E. Hay

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  1. Natalie Grayson
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  2. Cody S. Clements
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Correspondence to Mark E. Hay.

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Grayson, N., Clements, C.S., Towner, A.A. et al. Did the historic overharvesting of sea cucumbers make coral more susceptible to pathogens?. Coral Reefs 41, 447–453 (2022). https://doi.org/10.1007/s00338-022-02227-w

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