Impacts of necrotising disease on the Endangered cauliflower soft coral (Dendronephthya australis)
Rosemary Kate Steinberg A B C , John Turnbull A D , Tracy D. Ainsworth A * , Katherine A. Dafforn C , Alistair G. B. Poore A and Emma L. Johnston A DA
B
C
D
Abstract
Diseases have affected coral populations worldwide, leading to population declines and requiring active restoration efforts.
Describe population and individual impacts of necrotising disease in the Endangered octocoral Dendronephthya australis.
We quantified population loss and recruitment by using reference photos, survey and GPS mapping and described disease lesions by using histopathology.
From December 2019 to January 2020, we observed polyp loss, necrotic lesions and loss of large colonies of D. australis at Botany Bay, New South Wales, Australia. By September 2020, only a few scattered recruits remained, and all large colonies were lost. Histopathology of colonies sampled in January 2020 confirmed that the disease had resulted in necrosis, gastrovascular canal collapse and internal colony integrity loss, leading to mortality. New recruits were recorded within 10 months of disease onset, and large colonies within 18 months.
Although the necrotising disease had significant impacts on both the individual and population level, natural recruitment began quickly. As such, unlike in other populations, restoration is not currently required in the Bare Island D. australis population.
The extent of disease impact at the individual and population levels suggests that monitoring for lesions should be undertaken before developing conservation and restoration strategies for this species.
Keywords: alcyonacea, Botany Bay, coral disease, disease, disease histology, marine disease, octocoral, temperate, temperate reef.
References
Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Global Change Biology 13, 2078-2088.
| Crossref | Google Scholar |
Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, McQuaid S, Gray RT, Murray LJ, Coleman HG, James JA, Salto-Tellez M, Hamilton PW (2017) QuPath: open source software for digital pathology image analysis. Scientific Reports 7, 16878.
| Crossref | Google Scholar |
Barneah O, Malik Z, Benayahu Y (2002) Attachment to the substrate by soft coral fragments: desmocyte development, structure, and function. Invertebrate Biology 121, 81-90.
| Crossref | Google Scholar |
Barros TL, Bracewell SA, Mayer-Pinto M, Dafforn KA, Simpson SL, Farrell M, Johnston EL (2022) Wildfires cause rapid changes to estuarine benthic habitat. Environmental Pollution 308, 119571.
| Crossref | Google Scholar | PubMed |
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1-48.
| Crossref | Google Scholar |
Bowden BF, Coll JC, Hicks W, Kazlauskas R, Mitchell SJ (1978) Studies of Australian soft corals. X. The isolation of epoxyisoneocembrene-A from Sinularia grayi and isoneocembrene-A from Sarcophyton ehrenbergi. Australian Journal of Chemistry 31, 2707-2712.
| Crossref | Google Scholar |
Bracewell SA, Barros TL, Mayer-Pinto M, Dafforn KA, Simpson SL, Johnston EL (2023) Contaminant pulse following wildfire is associated with shifts in estuarine benthic communities. Environmental Pollution 316, 120533.
| Crossref | Google Scholar | PubMed |
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378-400.
| Crossref | Google Scholar |
Bruckner AW (2009) Rate and extent of decline in Corallium (pink and red coral) populations: existing data meet the requirements for a CITES Appendix II listing. Marine Ecology Progress Series 397, 319-332.
| Crossref | Google Scholar |
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5, e124.
| Crossref | Google Scholar | PubMed |
Calderón-Hernández A, Urbina-Villalobos A, Mora-Barboza C, Morales JA, Fernández-García C, Cortés J (2021) Lesions in octocorals of the Costa Rican Caribbean during the 2015–2016 El Niño. Coral Reefs 40, 1167-1179.
| Crossref | Google Scholar |
Campbell AH, Marzinelli EM, Vergés A, Coleman MA, Steinberg PD (2014) Towards restoration of missing underwater forests. PLoS ONE 9, e84106.
| Crossref | Google Scholar |
Case RJ, Longford SR, Campbell AH, Low A, Tujula N, Steinberg PD, Kjelleberg S (2011) Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environmental Microbiology 13, 529-537.
| Crossref | Google Scholar | PubMed |
Coll JC, Tapiolas DM, Bowden BF, Webb L, Marsh H (1983) Transformation of soft coral (Coelenterata: Octocorallia) terpenes by Ovula ovum (Mollusca: Prosobranchia). Marine Biology 74, 35-40.
| Crossref | Google Scholar |
Concepcion GT, Kahng SE, Crepeau MW, Franklin EC, Coles SL, Toonen RJ (2010) Resolving natural ranges and marine invasions in a globally distributed octocoral (genus Carijoa). Marine Ecology Progress Series 401, 113-127.
| Crossref | Google Scholar |
Corry M, Harasti D, Gaston T, Mazumder D, Cresswell T, Moltschaniwskyj N (2018) Functional role of the soft coral Dendronephthya australis in the benthic food web of temperate estuaries. Marine Ecology Progress Series 593, 61-72.
| Crossref | Google Scholar |
Dahan M, Benayahu Y (1997) Clonal propagation by the azooxanthellate octocoral Dendronephthya hemprichi. Coral Reefs 16, 5-12.
| Crossref | Google Scholar |
Davis TR, Harasti D, Smith SDA (2015) Extension of Dendronephthya australis soft corals in tidal current flows. Marine Biology 162, 2155-2159.
| Crossref | Google Scholar |
Davis TR, Harasti D, Smith SDA (2018) Responses of Dendronephthya australis to predation by Dermatobranchus sp. nudibranchs. Marine and Freshwater Research 69, 186-190.
| Crossref | Google Scholar |
Dennis MM, Becker AAMJ, Freeman MA (2020) Pathology of multifocal purple spots, a nonspecific lesion morphology of Caribbean sea fans Gorgonia spp. Diseases of Aquatic Organisms 141, 79-89.
| Crossref | Google Scholar | PubMed |
Epstein HE, Kingsford MJ (2019) Are soft coral habitats unfavourable? A closer look at the association between reef fishes and their habitat. Environmental Biology of Fishes 102, 479–497. 10.1007/s10641-019-0845-4
Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: a review. Marine Pollution Bulletin 64, 1737-1765.
| Crossref | Google Scholar | PubMed |
Finlay-Jones H, Raoult V, Harasti D, Gaston TF (2021) What eats a cauliflower coral? An assessment of predation on the endangered temperate soft coral, Dendronepthya australis. Marine and Freshwater Research 73, 307-318.
| Crossref | Google Scholar |
Garra S, Hall A, Kingsford MJ (2020) The effects of predation on the condition of soft corals. Coral Reefs 39, 1329-1343.
| Crossref | Google Scholar |
Gissing A, Timms M, Browning S, Crompton R, McAneney J (2022) Compound natural disasters in Australia: a historical analysis. Environmental Hazards 21, 159-173.
| Crossref | Google Scholar |
Griffith JK (1994) Predation on soft corals (Octocorallia: Alcyonacea) on the Great Barrier Reef, Australia. Marine and Freshwater Research 45, 1281-1284.
| Crossref | Google Scholar |
Harasti D (2016) Declining seahorse populations linked to loss of essential marine habitats. Marine Ecology Progress Series 546, 173-181.
| Crossref | Google Scholar |
Harasti D, Martin-Smith K, Gladstone W (2014) Ontogenetic and sex-based differences in habitat preferences and site fidelity of White’s seahorse Hippocampus whitei. Journal of Fish Biology 85, 1413-1428.
| Crossref | Google Scholar | PubMed |
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328, 1523-1528.
| Crossref | Google Scholar |
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547-1551.
| Crossref | Google Scholar |
Hwang S-J, Song J-I (2007) Reproductive biology and larval development of the temperate soft coral Dendronephthya gigantea (Alcyonacea: Nephtheidae). Marine Biology 152, 273-284.
| Crossref | Google Scholar |
Jones R, Fisher R, Bessell-Browne P (2019) Sediment deposition and coral smothering. PLoS ONE 14, e0216248.
| Crossref | Google Scholar |
Larkin MF, Davis TR, Harasti D, Cadiou G, Poulos DE, Smith SDA (2021a) The rapid decline of an Endangered temperate soft coral species. Estuarine, Coastal and Shelf Science 255, 107364.
| Crossref | Google Scholar |
Larkin MF, Harasti D, Davis TR, Smith SDA (2021b) If you plant it, they will come: rapid recruitment of habitat-dependent marine invertebrates to transplanted fragments of an endangered soft coral species. Diversity 13, 79.
| Crossref | Google Scholar |
Larkin MF, Davis TR, Harasti D, Benkendorff K, Smith SDA (2023a) Substantial advancement in aquaria rearing methods to assist recovery of an Endangered soft coral. Aquatic Conservation: Marine and Freshwater Ecosystems 33, 1-14.
| Crossref | Google Scholar |
Larkin MF, Davis TR, Harasti D, Smith SDA, Ainsworth TD, Benkendorff K (2023b) A glimmer of hope for an Endangered temperate soft coral: the first observations of reproductive strategies and early life cycle of Dendronephthya australis (Octocorallia: Malacalcyonacea). Marine Biology 170, 146.
| Crossref | Google Scholar |
Losey GS, Balazs GH, Privitera LA (1994) Cleaning symbiosis between the wrasse, Thalassoma duperry, and the green turtle, Chelonia mydas. Copeia 1994, 684-690.
| Crossref | Google Scholar |
Lourie SA, Randall JE (2003) A new pygmy seahorse, Hippocampus denise (Teleostei: Sygnathidae), from the Indo-Pacific. Zoological Studies 42, 284-291.
| Google Scholar |
Maggioni D, Montano S, Voigt O, Seveso D, Galli P (2020) A mesophotic hotel: the octocoral Bebryce cf. grandicalyx as a host. Ecology 101, e02950.
| Crossref | Google Scholar |
Mandelberg Y, Benayahu D, Benayahu Y (2016) Octocoral Sarcophyton auritum Verseveldt & Benayahu, 1978: microanatomy and presence of collagen fibers. The Biological Bulletin 230, 68-77.
| Crossref | Google Scholar | PubMed |
Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evolution & Development 9, 355-367.
| Crossref | Google Scholar | PubMed |
Maynard J, van Hooidonk R, Eakin CM, Puotinen M, Garren M, Williams G, Heron SF, Lamb J, Weil E, Willis B, Harvell CD (2015) Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nature Climate Change 5, 688-694.
| Crossref | Google Scholar |
Montero-Serra I, Garrabou J, Doak DF, Figuerola L, Hereu B, Ledoux JB, Linares C (2018) Accounting for life-history strategies and timescales in marine restoration. Conservation Letters 11, e12341.
| Crossref | Google Scholar |
Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS ONE 3, e1811.
| Crossref | Google Scholar |
Nicolet KJ, Hoogenboom MO, Gardiner NM, Pratchett MS, Willis BL (2013) The corallivorous invertebrate Drupella aids in transmission of brown band disease on the Great Barrier Reef. Coral Reefs 32, 585-595.
| Crossref | Google Scholar |
Nicolet KJ, Chong-Seng KM, Pratchett MS, Willis BL, Hoogenboom MO (2018) Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease. Scientific Reports 8, 5258.
| Crossref | Google Scholar |
NSW Fisheries Scientific Committee (2021) Final determination: cauliflower soft coral Dendronephthya australis. (Fisheries Scientific Committee) Available at https://www.dpi.nsw.gov.au/__data/assets/pdf_file/0007/1277782/Final-determination-D.australis-.pdf
Permata WD, Kinzie RA, Hidaka M (2000) Histological studies on the origin of planulae of the coral Pocillopora damicornis. Marine Ecology Progress Series 200, 191-200.
| Crossref | Google Scholar |
Peters EC, Oprandy JJ, Yevich PP (1983) Possible causal agent of ‘white band disease’ in caribbean acroporid corals. Journal of Invertebrate Pathology 41, 394-396.
| Crossref | Google Scholar |
Poore AGB, Watson MJ, de Nys R, Lowry JK, Steinberg PD (2000) Patterns of host use among alga- and sponge-associated amphipods. Marine Ecology Progress Series 208, 183-196.
| Crossref | Google Scholar |
Poulos DE, Harasti D, Gallen C, Booth DJ (2013) Biodiversity value of a geographically restricted soft coral species within a temperate estuary. Aquatic Conservation: Marine and Freshwater Ecosystems 23, 838-849.
| Crossref | Google Scholar |
Poulos DE, Gallen C, Davis T, Booth DJ, Harasti D (2016) Distribution and spatial modelling of a soft coral habitat in the Port Stephens-Great Lakes Marine Park: implications for management. Marine and Freshwater Research 67, 256-265.
| Crossref | Google Scholar |
Pratchett MS (2007) Dietary selection by coral-feeding butterflyfishes (chaetodontidae) on the great barrier reef, Australia. The Raffles Bulletin of Zoology 2014, 171-176.
| Google Scholar |
Qiu Z, Coleman MA, Provost E, Campbell AH, Kelaher BP, Dalton SJ, Thomas T, Steinberg PD, Marzinelli EM (2019) Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp. Proceedings of the Royal Society B: Biological Sciences 286, 20181887.
| Crossref | Google Scholar |
Raymundo LJ, Work TM, Miller RL, Lozada-Misa PL (2016) Effects of Coralliophila violacea on tissue loss in the scleractinian corals Porites spp. depend on host response. Diseases of Aquatic Organisms 119, 75-83.
| Crossref | Google Scholar | PubMed |
Rodríguez-Villalobos JC, Work TM, Calderon-Aguilera LE (2016) Wound repair in Pocillopora. Journal of Invertebrate Pathology 139, 1-5.
| Crossref | Google Scholar | PubMed |
Ruiz Allais JP, Amaro ME, McFadden CS, Halasz A, Benayahu Y (2014) The first incidence of an alien soft coral of the family Xeniidae in the Caribbean, an invasion in eastern Venezuelan coral communities. Coral Reefs 33, 287.
| Crossref | Google Scholar |
Ruiz-Allais JP, Benayahu Y, Lasso-Alcalá OM (2021) The invasive octocoral Unomia stolonifera (Alcyonacea, Xeniidae) is dominating the benthos in the southeastern Caribbean Sea. Memoria de la Fundación La Salle de Ciencias Naturales 79, 63-80.
| Crossref | Google Scholar |
Sánchez JA, Ballesteros D (2014) The invasive snowflake coral (Carijoa riisei) in the tropical eastern Pacific, Colombia. Revista de Biología Tropical 62, 199-207.
| Crossref | Google Scholar |
Sharp W, Maxwell K, Smith K, Hunt J (2020) Investigating the ongoing coral disease outbreak in the Florida Keys: continued SCTLD monitoring at middle and lower Florida Keys, experimental coral restoration of SCTLD-susceptible coral species, and assessing the prevalence of SCTLD on intermediate reef habitat. Florida Department of Environmental Protection Award 24, Florida Fish & Wildlife Conservation Commission.
Slattery M, Renegar DA, Gochfeld DJ (2013) Direct and indirect effects of a new disease of alcyonacean soft corals. Coral Reefs 32, 879-889.
| Crossref | Google Scholar |
Smith HA, Moya A, Cantin NE, van Oppen MJH, Torda G (2019) Observations of simultaneous sperm release and larval planulation suggest reproductive assurance in the coral Pocillopora acuta. Frontiers in Marine Science 6, 362.
| Crossref | Google Scholar |
Steinberg RK (2023) Histological slides of Dendronephthya australis. V2. (Science Data Bank) [Data files, updated 2023-11-03] doi:10.57760/sciencedb.09644
Steinberg RK, Dafforn KA, Ainsworth T, Johnston EL (2020) Know thy anemone: a review of threats to octocorals and anemones and opportunities for their restoration. Frontiers in Marine Science 7, 590.
| Crossref | Google Scholar |
Tracy AM, Weil E, Harvell CD (2018) Octocoral co-infection as a balance between host immunity and host environment. Oecologia 186, 743-753.
| Crossref | Google Scholar | PubMed |
Tracy AM, Weil E, Burge CA (2021) Ecological factors mediate immunity and parasitic co-infection in sea fan octocorals. Frontiers in Immunology 11, 608066.
| Crossref | Google Scholar |
Tsounis G, Rossi S, Gili J-M, Arntz W (2006) Population structure of an exploited benthic cnidarian: the case study of red coral (Corallium rubrum L.). Marine Biology 149, 1059-1070.
| Crossref | Google Scholar |
Wada N, Pollock FJ, Willis BL, Ainsworth T, Mano N, Bourne DG (2016) In situ visualization of bacterial populations in coral tissues: pitfalls and solutions. PeerJ 4, e2424.
| Crossref | Google Scholar |
Wainwright D (2011) Halifax Park/Fly Point sand accumulation study. R.N2128.001.01, prepared for Port Stephens – Great Lakes Marine Park, BMT WBM Pty Ltd, Newcastle, NSW, Australia Available at https://indopacificimages.com/wp-content/uploads/2021/09/Halifax-Fly-Point-Sand-Accumulation-Study.pdf
Wendt PH, van Dolah RF, O’Rourke CB (1985) A comparative study of the invertebrate macrofauna associated with seven sponge and coral species collected from the South Atlantic Bight. Journal of the Elisha Mitchell Scientific Society 101, 187-203.
| Google Scholar |
Wickham H (2011) ggplot2. WIREs Computational Statistics 3, 180-185.
| Crossref | Google Scholar |
Work TM, Aeby GS (2011) Pathology of tissue loss (white syndrome) in Acropora sp. corals from the Central Pacific. Journal of Invertebrate Pathology 107, 127-131.
| Crossref | Google Scholar | PubMed |
Work TM, Aeby GS (2014) Microbial aggregates within tissues infect a diversity of corals throughout the Indo-Pacific. Marine Ecology Progress Series 500, 1-9.
| Crossref | Google Scholar |
Work T, Meteyer C (2014) To understand coral disease, look at coral cells. EcoHealth 11, 610-618.
| Crossref | Google Scholar | PubMed |
Work TM, Russell R, Aeby GS (2012) Tissue loss (white syndrome) in the coral Montipora capitata is a dynamic disease with multiple host responses and potential causes. Proceedings of the Royal Society of London – B. Biological Sciences 279, 4334-4341.
| Crossref | Google Scholar |
Zannella C, Mosca F, Mariani F, Franci G, Folliero V, Galdiero M, Tiscar PG, Galdiero M (2017) Microbial diseases of bivalve mollusks: infections, immunology and antimicrobial defense. Marine Drugs 15, 182.
| Crossref | Google Scholar |