Marine Biology

, 165:157 | Cite as

Diet-induced shifts in the crown-of-thorns (Acanthaster sp.) larval microbiome

  • Tyler J. CarrierEmail author
  • Kennedy Wolfe
  • Karen Lopez
  • Mailie Gall
  • Daniel A. Janies
  • Maria Byrne
  • Adam M. Reitzel
Original paper


Predation by the crown-of-thorns seastar (CoTS; Acanthaster sp.) is a pervasive stressor attributing to the decline of coral reefs. These outbreaks are suggested to be linked to eutrophy-driven recruitment pulses, where increased nutrients enhance larval success. CoTS larvae, however, are tolerant of oligotrophic conditions typical of tropical ecosystems and outbreaks occur in regions isolated from eutrophy, highlighting the resilience of these larvae to oligotrophic conditions. Here, we test the hypothesis that CoTS larvae associate with bacterial communities that are dynamic across an oligotrophic–eutrophic continuum and are specific to each feeding regime. Our analysis of the CoTS larval microbiome suggests that CoTS larvae associate with a bacterial community distinct from the environmental microbiota and that this community experiences a community-level shift in response to differential feeding that is maintained over development. Symbioses with a diverse and dynamic, and a potentially phototrophic, bacterial community may contribute to resilience of CoTS larvae that enable the success of CoTS and, perhaps, other tropical marine larvae in oligotrophic seas.


CoTS larvae Oligotrophic Planktotrophic Bacteria Gut microbiota Great Barrier Reef 



We thank Anne Hoggett, Lyle Vail, Morgan Pratchett, Vanessa Messmer, Ciemon Caballes, Shawna Foo, and Richard Chi for their assistance with specimen collection, laboratory cultures, sampling, and imaging.


T.J.C was supported by an NSF Graduate Research fellowship; A.M.R. was supported by Human Frontier Science Program Award RGY0079/2016; KW was supported by a PhD scholarship from the University of Sydney; M.B. was supported by an Ian Potter Foundation Grant from Lizard Island Research Station, a facility of the Australian Museum; and D.A.J. and K.L. were supported by NSF DEB1036416 and the Department of Bioinformatics and Genomics in the College of Computing and Informatics at UNC Charlotte.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

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Supplementary material 1 (XLSX 11 kb)
227_2018_3416_MOESM2_ESM.pdf (114 kb)
Supplementary material 2 (PDF 113 kb)
227_2018_3416_MOESM3_ESM.pdf (65 kb)
Supplementary material 3 (PDF 64 kb)


  1. Adams DK, Sewell MA, Angerer RC, Angerer LM (2011) Rapid adaptation to food availability by a dopamine-mediated morphogenetic response. Nat Commun 2:592CrossRefGoogle Scholar
  2. Babcock RC, Dambacher JM, Morello EB, Plagányi ÉE, Hayes KR, Sweatman HPA, Pratchett MS (2016) Assessing different causes of crown-of-thorns starfish outbreaks and appropriate responses for management on the Great Barrier Reef. PLoS One 11:e0169048CrossRefGoogle Scholar
  3. Birkeland C (1982) Terrestrial runoff as a cause of outbreaks of Acanthaster planci (Echinodermata: Asteroidea). Mar Biol 69:175–185CrossRefGoogle Scholar
  4. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  5. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13:e1002226CrossRefGoogle Scholar
  6. Bosch I (1992) Symbiosis between bacteria and oceanic clonal sea star larvae in the western North Atlantic Ocean. Mar Biol 114:495–502CrossRefGoogle Scholar
  7. Brodie J, Rabricius K, De’ath G, Okaji K (2005) Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence. Mar Pollut Bull 51:266–278CrossRefGoogle Scholar
  8. Byrne M (1994) Ophiuroidea. In: Harrison FW, Chia FS (eds) Microscopic Anatomy of Invertebrates. Wiley, New York, pp 247–343Google Scholar
  9. Caballes CF, Pratchett MS, Buck ACE (2017) Interactive effects of endogenous and exogenous nutrition on larval development for crown-of-thorns starfish. Diversity 9:15CrossRefGoogle Scholar
  10. Cameron RA, Holland ND (1983) Electron microscopy of extracellular materials during the development of a seastar, Patiria miniata (Echinoderm: Asteroidea). Cell Tissue Res 243:193–200Google Scholar
  11. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  12. Carrier TJ, Reitzel AM (2017) The hologenome across environments and the implications of a host-associated microbial repertoire. Front Microbiol 8:802CrossRefGoogle Scholar
  13. Carrier TJ, Reitzel AM (2018) Convergent shifts in host-associated microbial communities across environmentally elicited phenotypes. Nat Commun 9:952CrossRefGoogle Scholar
  14. Carrier TJ, King BL, Coffman JA (2015) Gene expression changes associated with the developmental plasticity of sea urchin larvae in response to food availability. Biol Bull 228:171–180CrossRefGoogle Scholar
  15. Cerra A, Byrne M, Hoegh-Guldberg O (1997) Developments of the hyaline layer around the planktonic embryos and larvae of the asteroid Patiriella calcar and the presence of associated bacteria. Invertebr Reprod Dev 31:337–343CrossRefGoogle Scholar
  16. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the great barrier reef and its causes. Proc Natl Acad Sci USA 109:17995–17999CrossRefGoogle Scholar
  17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  18. Fabricius KE, Okaji K, De’ath G (2010) Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29:593–605CrossRefGoogle Scholar
  19. Fenaux L, Strathmann MF, Strathmann RR (1994) Five tests of food-limited growth of larvae in coastal waters by comparison of rates of development and form of echinoplutei. Limnol Oceanogr 39:84–98CrossRefGoogle Scholar
  20. Galac MR, Bosch I, Janies DA (2016) Bacterial communities of oceanic sea star (Asteroidea: Echinodermata) larvae. Mar Biol 163:162CrossRefGoogle Scholar
  21. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341CrossRefGoogle Scholar
  22. Gilbert SF, Bosch TCG, Ledon-Rettig C (2015) Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat Rev Genet 16:611–622CrossRefGoogle Scholar
  23. Haszprunar G, Vogler C, Wörheide G (2017) Persistent gaps of knowledge for naming and distinguishing multiple species of crown-of-thorns-seastar in the Acanthaster planci species complex. Diversity 9:22CrossRefGoogle Scholar
  24. Høj L, Levy N, Baillie BK, Clode PL, Strohmaier RC, Siboni N, Webster NS, Uthicke S, Bourne DB (2018) Crown-of-thorns sea star, Acanthaster cf. solaris, have tissue-characteristic microbiomes with potential roles in health and reproduction. Appl Environ Microbiol 84:e00181-18CrossRefGoogle Scholar
  25. Holland ND, Nealson KH (1978) The fine structure of the echinoderm cuticle and subcuticular bacteria of echinoderms. Acta Zool 59:169–185CrossRefGoogle Scholar
  26. Kelly MS, McKenzie JD (1995) Survey of the occurrence and morphology of sub-cuticular bacteria in shelf echinoderms from the north-east Atlantic Ocean. Mar Biol 123:741–756CrossRefGoogle Scholar
  27. Kelly MS, Barker MF, McKenzie JD, Powell J (1995) The incidence and morphology of subcuticlar bacteria in the echinderm fauna of New Zealand. Biol Bull 189:91–105CrossRefGoogle Scholar
  28. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucl Acids Res 41:e1CrossRefGoogle Scholar
  29. Lesser MP, Walker CW (1992) Comparative study of the uptake of dissolved amino acids in sympatric brittle stars with and without endosymbiotic bacteria. Comput Biochem Physiol 101:217–223Google Scholar
  30. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefGoogle Scholar
  31. Lucas J (1982) Quantitative studies of feeding and nutrition during larval development of the coral reef asteroid Acanthaster planci (L.). J Exp Mar Biol Ecol 65:173–193CrossRefGoogle Scholar
  32. McAlister JS, Miner BG (2018) Phenotypic plasticity of feeding structures in marine invertebrate larvae. In: Carrier TJ, Reitzel AM, Heyland A (eds) Evolutionary Ecology of Marine Invertebrate Larvae. Oxford University Press, OxfordGoogle Scholar
  33. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236CrossRefGoogle Scholar
  34. McKenzie JD (1994) Using the very small to comment on the very large: can ultra-structure be of use in phylongeny? In: David B, Guille A, Feral J-P, Roux M (eds) Echinoderms Through Time. Balkema, Rotterdam, pp 73–85Google Scholar
  35. Mies M, Sumida MYG, Rädecker N, Voolstra CR (2017) Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Front Ecol Environ 5:56CrossRefGoogle Scholar
  36. Nakajima R, Nakatomi N, Kurihara H, Fox MD, Smith JE, Okaji K (2016) Crown-of-thorns starfish larvae can feed on organic matter released from corals. Diversity 8:18CrossRefGoogle Scholar
  37. Olson R (1987) In situ culturing as a test of the larval starvation hypothesis for the crown-of-thoms starfish, Acanthaster planci. Limnol Oceanogr 32:895–904CrossRefGoogle Scholar
  38. Olson RR, Olson MH (1989) Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Annu Rev Ecol Syst 20:225–247CrossRefGoogle Scholar
  39. Pratchett M, Caballes C, Wilmes J, Matthews S, Mellin C, Sweatman H, Nadler L, Brodie J, Thompson C, Hoey J, Bos A, Byrne M, Messmer V, Valero-Fortunato S, Chen C, Buck A, Babcock R, Uthicke S (2017) Thirty years of research on crown-of-thorns starfish (1986–2016): scientific advances and emerging opportunities. Diversity 9:41CrossRefGoogle Scholar
  40. Roche RC, Pratchett MS, Carr P, Turner JT, Wagner D, Head C, Sheppard CRC (2015) Localized outbreaks of Acanthaster planci at an isolated and unpopulated reef atoll in the Chagos Archipelago. Mar Biol 162:1695–1704CrossRefGoogle Scholar
  41. Rosenberg E, Sharon G, Zilber-Rosenberg I (2009) The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol 11:2959–2962CrossRefGoogle Scholar
  42. Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385CrossRefGoogle Scholar
  43. Soars NA, Prowse TAA, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus transversus’ type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125CrossRefGoogle Scholar
  44. Strathmann MF, Strathmann RR (2007) An extraordinarily long larval duration of 4.5 years from hatching to metamorphosis for teleplanic veligers of Fusitriton oregonenis. Biol Bull 213:152–159CrossRefGoogle Scholar
  45. Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986CrossRefGoogle Scholar
  46. Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein SR (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1:e00028-00016CrossRefGoogle Scholar
  47. Uthicke S, Schaffelke B, Byrne M (2009) A boom and bust phylum? Ecological and evolutionary consequences of large population density variations in echinoderms. Ecol Monogr 79:3–24CrossRefGoogle Scholar
  48. Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2:16CrossRefGoogle Scholar
  49. Walker CW, Lesser MP (1989) Nutrition and development of brooded embryos in the brittlestar Amphipholis squamata: do endosymbiotic bacteria play a role? Mar Biol 103:519–530CrossRefGoogle Scholar
  50. Wolfe K, Graba-Landry A, Dworjanyn S, Byrne M (2015a) Larval phenotypic plasticity in the boom-and-bust crown-of-thorns seastar, Acanthaster planci. Mar Ecol Prog Ser 539:179–189CrossRefGoogle Scholar
  51. Wolfe K, Graba-Landry A, Dworjanyn S, Byrne M (2015b) Larval starvation to satiation: influence of nutrient regime on the success of Acanthaster planci. PLoS One 10:e0122010CrossRefGoogle Scholar
  52. Wolfe K, Graba-Landry A, Dworjanyn S, Byrne M (2017) Superstars: assessing nutrient thresholds for enhanced larval success of Acanthaster planci, a review of the evidence. Mar Pollut Bull 116:307–314CrossRefGoogle Scholar
  53. Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30:614–620CrossRefGoogle Scholar
  54. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of North Carolina at CharlotteCharlotteUSA
  2. 2.School of Medical SciencesThe University of SydneySydneyAustralia
  3. 3.Department of Bioinformatics and GenomicsUniversity of North Carolina at CharlotteCharlotteUSA
  4. 4.School of Environmental and Life SciencesThe University of SydneySydneyAustralia

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