Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae)

Abstract

Efforts to culture and conserve acroporid corals in aquaria have led to the discovery of a corallivorous polyclad flatworm (known as AEFW – Acropora-eating flatworm), which, if not removed, can eat entire colonies. Live observations of the AEFW, whole mounts, serial histological sections and comparison of 28S rDNA sequences with other polyclads reveal that this is a new species belonging to the family Prosthiostomidae Lang, 1884 and previously monospecific genus Amakusaplana (Kato 1938). Amakusaplana acroporae is distinguished from Amakusaplana ohshimai by a different arrangement and number of eyes, a large seminal vesicle and dorsoventrally compressed shell gland pouch. Typical of the genus, A. acroporae, lacks a ventral sucker and has a small notch at the midline of the anterior margin. Nematocysts and a Symbiodinium sp. of dinoflagellate from the coral are abundantly distributed in the gut and parenchyma. Individual adults lay multiple egg batches on the coral skeleton, each egg batch has 20–26 egg capsules, and each capsule contains between 3–7 embryos. Embryonic development takes approximately 21 days, during which time characteristics of a pelagic life stage (lobes and ciliary tufts) develop but are lost before hatching. The hatchling is capable of swimming but settles to the benthos quickly, and no zooxanthellae were observed in the animal at this stage. We suggest that intracapsular metamorphosis limits the dispersal potential of hatchlings and promotes recruitment of offspring into the natal habitat. The evolutionary and ecological significance of retaining lobes and ciliary tufts in the embryo are discussed. Camouflage, high fecundity and possible dispersal dimorphisms probably explain how Amakusaplana acroporae can cause Acropora sp. mortality in aquaria where natural predators may be absent.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Baeza JA, Veliz D, Pardo LM, Lohrmann K, Guisado C (1997) A new polyclad flatworm, Tytthosoceros inca (Platyhelminthes: Polycladida: Cotylea: Pseudocerotidae) from Chilean coastal waters. Proc Biol Soc Wash 110:476–482

    Google Scholar 

  2. Bock S (1922) Two new cotylean polyclads from Japan. Ark Zool 14:1–31

    Google Scholar 

  3. Bock S (1923) Boninia, a new polyclad genus from the Pacific. Nov Act R Soc Sci Uppsala 6: 32 pp

    Google Scholar 

  4. Bock S (1926) Eine Polyclade mit muskuloesen druesenorganen rings um dem koerper. Zool Anz 66:133–138

    Google Scholar 

  5. Borneman EH, Lowrie J (2001) Advances in captive husbandry and propagation: an easily utilized reef replenishment means from the private sector? Bull Mar Sci 69(2):897–913

    Google Scholar 

  6. Carlson BA (1999) Organism responses to rapid change: what aquaria can tell us about nature. Am Zool 39:44–55

    Article  Google Scholar 

  7. Crozier WJ (1917) On the pigmentation of a Polyclad. Proc Am Acad Arts Sci 50:725–730

    Article  Google Scholar 

  8. Faubel A (1984) The Polycladida, Turbellaria. Proposal and establishment of a new system. Part II. The Cotylea. Mitt Hamb Zool Mus Inst 81:189–259

    Google Scholar 

  9. Galleni L, Tongiorgi P, Ferrero E, Salghetti U (1980) Stylochus mediterraneus (Turbellaria: Polycladida), predator of the mussel, Mytilus galloprovincialis. Mar Biol 55:317–326

    Article  Google Scholar 

  10. Holleman JJ (1998) Two new species of the genus Anonymus from New Zealand (Polycladida, Cotylea). Hydrobiologia 383:61–67

    Article  Google Scholar 

  11. Hyman LH (1959) A further study of Micronesian polyclad flatworms. Proc US Natl Mus 108:543–597

    Article  Google Scholar 

  12. IUCN (2010) IUCN Red List of Threatened Species. Version 2010.4

  13. Jokiel PL, Townsley SJ (1974) Biology of the polyclad Prosthiostomum (Prosthiostomum) sp., a new coral parasite from Hawaii. Pac Sci 28:361–373

    Google Scholar 

  14. Karling TG (1966) On nematocysts and similar structures in turbellarians. Acta Zool Fenn 116:1–28

    Google Scholar 

  15. Kato K (1938) Polyclads from Amakusa, Southern Japan. Jpn J Zool 7:559–576

    Google Scholar 

  16. Kato K (1940) On the development of some Japanese polyclads. Jpn J Zool 8:537–573

    Google Scholar 

  17. Kawaguti S (1944) Zooxanthellae as a factor of positive phototropism in those animals containing them. Palao Trop Biol Stn Stud 2:681–682

    Google Scholar 

  18. Krug PJ (2009) Not my “type”: larval dispersal dimorphisms and bet-hedging in Opisthobranch life histories. Biol Bull 216:355–372

    Article  PubMed  Google Scholar 

  19. Lang A (1884) Die Polycladen (Seeplanarien) des Golfes von Neapel und der angrenzenden Meeresabschnitte. Fauna und Flora des Golfes von Neapel Monogr 11:688 pp

  20. Littlewood DTJ, Marsbe LA (1990) Predation on cultivated oysters, Crassostrea rhizophorae (Guilding), by the polyclad turbellarian flatworm, Stylochus (Stylochus) frontalis Verrill. Aquaculture 88:145–150

    Article  Google Scholar 

  21. Littlewood DT, Curini-Galletti M, Herniou EA (2000) The interrelationships of proseriata (Platyhelminthes: seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466

    CAS  Article  PubMed  Google Scholar 

  22. Litvaitis MK, Bolanos DM, Quiroga SY (2010) When names are wrong and colours deceive: unravelling the Pseudoceros bicolor species complex (Platyhelminthes: Polycladida). J Nat Hist 44:829–845

    Article  Google Scholar 

  23. Millar RH (1971) The biology of ascidians. In: Russell FS, Yonge M (eds) Advances in marine biology, 9. Academic Press, New York, pp 1–100

    Google Scholar 

  24. Murina G-V, Grintsov V, Solonchenko A (1995) Stylochus tauricus, a predator of the barnacle Balanus improvisus in the Black Sea. Hydrobiologia 305:101–104

    Article  Google Scholar 

  25. Newman LJ, Cannon LRG (1994) Pseudoceros and Pseudobiceros (Platyhelminthes, Polycladida, Pseudocerotidae) from eastern Australia and Papua New Guinea. Mem Qld Mus 37:205–266

    Google Scholar 

  26. Newman LJ, Norenburg JL, Reed S (2000) Taxonomic and biological observations on the tiger flatworm, Maritigrella crozieri (Hyman, 1939), new combination (Platyhelminthes, Polycladida, Euryleptidae) from Florida waters. J Nat Hist 34:799–808

    Article  Google Scholar 

  27. Nosratpour F (2008) Observations of a polyclad flatworm affecting acroporid corals in captivity. In: Leewis RJ, Janse M (eds) Advances in coral husbandry in public aquariums. Public Husbandry Series 2:37–46

  28. Pearse AS, Wharton GW (1938) The oyster “leech” Stylochus inimicus Palombi, associated with oysters on the coasts of Florida. EcoI Monogr 8:605–655

    CAS  Article  Google Scholar 

  29. Perez-Portela R, Turon X (2007) Prey preferences of the polyclad flatworm Prostheceraeus roseus among Mediterranean species of the ascidian genus Pycnoclavella. Hydrobiologia 592:535–539

    Article  Google Scholar 

  30. Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700–W703

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Poulter JL (1975) Hawaiian polyclads: Prosthiostomids I. Pac Sci 29:317–339

    Google Scholar 

  32. Prudhoe S (1985) A monograph on Polyclad Turbellaria. Oxford University Press, London, p 259

    Google Scholar 

  33. Rawlinson KA (2010) Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits. Front Zool 7:12

    Article  PubMed  PubMed Central  Google Scholar 

  34. Rawlinson KA, Litvaitis MK (2008) Cotylea (Platyhelminthes, Polycladida): a cladistic analysis of morphology. Invertebr Biol 127:121–138

    Article  Google Scholar 

  35. Ritson-Williams R, Yotsu-Yamashita M, Paul VJ (2006) Ecological functions of tetrodotoxin in a deadly polyclad flatworm. Proc Natl Acad Sci USA 103:3176–3179

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  Article  PubMed  Google Scholar 

  37. Smith NF, Johnson KB, Young C (2002) Phylum platyhelminthes. In: Young CM, Sewell MA, Rice ME (eds) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 123–148

    Google Scholar 

  38. Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU D1–D2 sequences for their use in species identification. Front Zool 4:6

    Article  PubMed  PubMed Central  Google Scholar 

  39. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4.10b. Sinauer Associates, Sunderland, MA

    Google Scholar 

  40. Teshirogi W, Ishida S, Jatani K (1981) On the early development of some Japanese polyclads. Rep Fukara Mar Biol Lab 9:2–31

    Google Scholar 

  41. Yates KR, Carlson BA (1993) Corals in aquarium: How to use selective collecting and innovative husbandry to promote reef conservation. Proc 7th Int Coral Reef Symp 2: 1091–1095

    Google Scholar 

Download references

Acknowledgments

We thank Greg Rouse, Fernando Nosratpour, Bruce Wilfong, Alan Flojo and Randy Donowitz for providing additional AEFW specimens. We thank Bernhard Egger and Peter Ladurner for providing samples of Prosthiostomum siphunculus and Macrostomum lignano, respectively. We thank John Chuk for help with collection and identification of Australian polyclad species, Nicolette Craig of Practical Fish Keeping magazine and Mary Hagerdorn for helpful discussion. This work was funded by a Smithsonian Marine Science Network fellowship to KAR and a Smithsonian Link Foundation Fellowship to JAG. Smithsonian Marine Station contribution number 842.

Author information

Affiliations

Authors

Corresponding author

Correspondence to K. A. Rawlinson.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rawlinson, K.A., Gillis, J.A., Billings, R.E. et al. Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae). Coral Reefs 30, 693 (2011). https://doi.org/10.1007/s00338-011-0745-3

Download citation

Keywords

  • Coral predator
  • Acropora-eating flatworm
  • Polyclad
  • Amakusaplana acroporae
  • Intracapsular larva
  • 28S rDNA phylogeny