Taxonomy and Life History of the Acropora-Eating Flatworm Amakusaplana Acroporae Nov. Sp. (Polycladida: Prosthiostomidae)
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/225666939 Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae) Article in Coral Reefs · September 2011 DOI: 10.1007/s00338-011-0745-3 CITATIONS READS 22 467 4 authors, including: Kate A Rawlinson Andrew Gillis Dalhousie University University of Cambridge 18 PUBLICATIONS 483 CITATIONS 20 PUBLICATIONS 531 CITATIONS SEE PROFILE SEE PROFILE All content following this page was uploaded by Andrew Gillis on 13 February 2015. The user has requested enhancement of the downloaded file. Coral Reefs DOI 10.1007/s00338-011-0745-3 REPORT Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae) K. A. Rawlinson • J. A. Gillis • R. E. Billings Jr. • E. H. Borneman Received: 10 January 2011 / Accepted: 9 March 2011 Ó Springer-Verlag 2011 Abstract Efforts to culture and conserve acroporid corals notch at the midline of the anterior margin. Nematocysts in aquaria have led to the discovery of a corallivorous and a Symbiodinium sp. of dinoflagellate from the coral are polyclad flatworm (known as AEFW – Acropora-eating abundantly distributed in the gut and parenchyma. Indi- flatworm), which, if not removed, can eat entire colonies. vidual adults lay multiple egg batches on the coral skele- Live observations of the AEFW, whole mounts, serial ton, each egg batch has 20–26 egg capsules, and each histological sections and comparison of 28S rDNA capsule contains between 3–7 embryos. Embryonic sequences with other polyclads reveal that this is a new development takes approximately 21 days, during which species belonging to the family Prosthiostomidae Lang, time characteristics of a pelagic life stage (lobes and ciliary 1884 and previously monospecific genus Amakusaplana tufts) develop but are lost before hatching. The hatchling is (Kato 1938). Amakusaplana acroporae is distinguished capable of swimming but settles to the benthos quickly, from Amakusaplana ohshimai by a different arrangement and no zooxanthellae were observed in the animal at this and number of eyes, a large seminal vesicle and dorso- stage. We suggest that intracapsular metamorphosis limits ventrally compressed shell gland pouch. Typical of the the dispersal potential of hatchlings and promotes recruit- genus, A. acroporae, lacks a ventral sucker and has a small ment of offspring into the natal habitat. The evolutionary and ecological significance of retaining lobes and ciliary tufts in the embryo are discussed. Camouflage, high Communicated by Biology Editor Dr. Ruth Gates fecundity and possible dispersal dimorphisms probably K. A. Rawlinson (&) explain how Amakusaplana acroporae can cause Acropora Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, sp. mortality in aquaria where natural predators may be FL 34949, USA absent. e-mail: [email protected] Present Address: Keywords Coral predator Á Acropora-eating flatworm Á K. A. Rawlinson Polyclad Á Amakusaplana acroporae Á Intracapsular larva Á Department of Genetics, Evolution and Environment, University 28S rDNA phylogeny College London, Gower Street, London WC1E 6BT, UK J. A. Gillis Department of Physiology, Development and Neuroscience, Introduction University of Cambridge, Anatomy Building, Downing Street, Cambridge CB2 3DY, UK The interactions of polyclad flatworms (Platyhelminthes) R. E. Billings Jr. and their prey often come to light when the prey is of 9901 Jay Lane, Bristow, VA 20136, USA interest to humans. For example, predation of the bivalves Crassostrea rhizophorae and Mytilus galloprovincialis by E. H. Borneman Stylochus (Stylochus) frontalis and Stylochus mediterran- Department of Biology, University of Houston, Science and Research Building II, 4800 Calhoun Rd., eus, respectively, leads to increased mortality rates in these Houston, TX 77204, USA commercially important species (Galleni et al. 1980; 123 Coral Reefs Littlewood and Marsbe 1990). Similarly, coral biologists, crustaceans (Murina et al. 1995) and cnidarians (Kawaguti aquarists and conservationists are concerned by an 1944; Jokiel and Townsley 1974; Poulter 1975). While Acropora-eating flatworm (commonly referred to as some show prey preference, e.g. Maritigrella crozieri the ‘‘AEFW’’). The AEFW is found on several species (Crozier 1917) and Prostheceraeus roseus (Perez-Portela of Acropora in aquaria (so far reported or observed on and Turon 2007), little is known about prey specificity. Acropora valida, A. pulchra, A. millepora, A. tortuosa, Several polyclad species have been found living in various A. nana, A. tenuis, A. formosa, A. echinata and A. yongei— degrees of association with cnidarians (Table 1), but pre- Nosratpour 2008; R. Billings pers. obs.) and, if unchecked, dation has been inferred in only a few instances by the its corallivory can lead to the death of entire colonies presence of cnidae (nematocysts, spirocysts and ptycho- (Nosratpour 2008). Based on external morphology, the cysts) in the epithelium and/or gut (Bock 1922; Karling AEFW was identified as a Platyhelminthe of the order 1966; Poulter 1975; Holleman 1998). Polycladida and was tentatively assigned to the acotylean Knowledge of the life history strategies of polyclads is genus Apidioplana (Nosratpour 2008). However, to date, a the key to understanding their population dynamics and detailed morphological, histological and molecular analysis therefore may also be useful in managing their predatory of AEFW taxonomic affinity has been lacking. Whether the impact. Polyclads are the only free-living platyhelminth AEFW is as destructive an acroporid predator in the wild as clade in which members exhibit a gradient of develop- it is in aquaria is not known. However, given the threatened mental modes, from ‘direct’ development (i.e. embryos or vulnerable status of many of the AEFW-affected hatching as a benthic juvenile) through ‘intermediate’ acroporids (IUCN 2010) – and the importance of aquarium- development (i.e. intracapsular larva – larva with lobes and reared acroporids to the sustainable hobby trade, education ciliary band retained within an egg case, and hatching as a and reef restoration efforts (Yates and Carlson 1993; benthic juvenile – Kato 1940) to ‘indirect’ development Borneman and Lowrie 2001; Carlson 1999) – a careful (i.e. with a planktonic life history stage with lobes and study of the AEFW’s phylogenetic affinity and natural ciliary band, e.g. Go¨tte’s and Mu¨ller’s larvae). Indirect history is urgently needed. development has been described in both suborders of Polyclad flatworms prey on a variety of marine inver- polyclads – the Cotylea and Acotylea – while intracapsular tebrates, including molluscs (Pearse and Wharton 1938; larva and direct development have, until now, been found Littlewood and Marsbe 1990; Ritson-Williams et al. 2006), exclusively within the Acotylea (Smith et al. 2002). urochordates (Crozier 1917; Millar 1971; Newman and The aims of this study were to identify the AEFW Cannon 1994; Baeza et al. 1997; Newman et al. 2000), species using morphological, histological and molecular Table 1 Associations of polyclads with cnidarian taxa Polyclad species Cnidarian taxa (Order) Association Reference Notes Apidioplana mira Melitodes sp. (Alcyonacea) ? Bock (1926) Apidioplana okadai Melithaea flabellifera ?? (Alcyonacea) Unknown planarians Montipora sp. (Scleractinia) ? Kawaguti (1944) Lobophyllia sp. Stylophora sp. Hydroplana sp. Prosthiostomum (P.) Montipora verrucusa Obligate ectoparasite Jokiel and Townsley No cnidae observed in montiporae (Scleractinia) symbiont (1974) polyclad gut (Poulter, 1975) Stylochoplana tarda ? Karling (1966) Nematocysts in gut Stylochoplana inquilina Calliactis armillatus, Predator Poulter (1975) Nematocysts in gut (Actiniaria) Anonymus virilis ? Predator Karling (1966) Nematocysts in gut Anonymus multivirilis ? Predator Holleman (1998) Nematocysts in gut and dorsal epidermis Anonymus kaikourensis ? Predator Holleman (1998) Nematocysts in gut and dorsal epidermis Chromoplana bella Hydrozoa Predator Karling (1966) Nematocysts in gut Amyella lineata Hydrozoa Predator Bock (1922) Nematocysts in gut 123 Coral Reefs characters and to collect the first data on AEFW develop- Histoclear (National Diagnostics) for 24 h, infiltrated with ment and life history, as a foundation for future predator 1:1 histoclear/paraffin for 24 h and equilibrated in molten management efforts. We have determined that the AEFW paraffin for 24 h (all steps performed in a 60°C paraffin is a new species, belonging to the suborder Cotylea, the oven, with several changes at each step). Specimens were family Prosthiostomidae and the previously monospecific then embedded in fresh paraffin and left to harden at room genus Amakusaplana (Kato 1938). This species exhibits a temperature for 24 h prior to sectioning. Entire specimens number of interesting morphological and life history con- were sectioned in the cross- or sagittal plane at 6 lMona ditions – including intra-capsular metamorphosis – that rotary microtome. Sections were mounted on glass slides may represent adaptations to a corallivorous existence. and stained with Mayer’s haematoxylin and eosin Y as follows: 2 9 5 min in histosol (National Diagnostics), 2 9 2 min in 100% ethanol, 2 min in 70% ethanol, 2 min Materials and methods in 30% ethanol, 2 min in distilled water, 15 min in Mayer’s haematoxylin, 20 min in running tap water, 1 min in eosin Collection Y, 2 9 2 min in 95% ethanol,