Hofstenia Spp., Acoela), with Notes on Color Variation and Genetic Variation Within the Genus
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Hydrobiologia (2007) 592:439–454 DOI 10.1007/s10750-007-0789-0 PRIMARY RESEARCH PAPER A revision of the systematics of panther worms (Hofstenia spp., Acoela), with notes on color variation and genetic variation within the genus Matthew Hooge Æ Andreas Wallberg Æ Christiane Todt Æ Aaron Maloy Æ Ulf Jondelius Æ Seth Tyler Received: 28 July 2006 / Revised: 12 May 2007 / Accepted: 17 May 2007 / Published online: 31 July 2007 Ó Springer Science+Business Media B.V. 2007 Abstract Species of the genus Hofstenia are islands of Bermuda and the Bahamas, and the voracious predators and among the largest and Caribbean and in a variety of habitats includ- most colorful of the Acoela. They are known ing the rocky intertidal, among Thalassia sea from Japan, the Red Sea, the North Atlantic grass, on filamentous algae and decaying man- grove leaves. Certain color morphs associated with each of these habitats seem to have confused the taxonomy of the group. While Handling editor: K. Martens brown-and-white banding and spotting patterns of Hofstenia miamia and Hofstenia giselae are Electronic supplementary material The online version of this article (doi:10.1007/s10750-007-0789-0) contains distinctive for species associated with mangrove supplementary material, which is available to authorized leaves and Thallasia sp. and are likely to be users. cryptic for these specific environments, we find some evidence to suggest that the coloration is M. Hooge (&) S. Tyler Department of BiologicalÁ Sciences, The University of mimicry of a nudibranch with aposematic Maine, Orono, ME 04469-5751, USA coloration. The common plan in these patterns e-mail: [email protected] is one with three variously solid or spotted lighter cross bands on a dark background. Our A. Wallberg Department of Systematic Zoology, Evolutionary examination of museum type material and live Biology Centre, Uppsala University, Norbyva¨gen specimens of Hofstenia collected from Baha- 18D, 752 36 Uppsala, Sweden mas, Belize, Bermuda, and Panama revealed no internal morphological differences between C. Todt Department of Biology, University of Bergen, the Hofstenia species occurring in the Carib- Thormøhlensgate 55, 5007 Bergen, Norway bean. Similarly, our analyses of 18S and 28S molecular sequence data revealed no significant A. Maloy differences among specimens. Accordingly, we Centre of Applied Marine Biotechnology, Letterkenny Institute of Technology, Letterkenny, declare that Hofstenia giselae is a junior syn- County Donegal, Ireland onym of Hofstenia miamia, the three-banded panther worm. U. Jondelius Department of Invertebrate Zoology, Swedish Keywords Platyhelminthes Turbellaria Museum of Natural History, POB 50007, 104 05 Á Á Stockholm, Sweden Mangrove Caribbean Intraspecific variation Á Á 123 440 Hydrobiologia (2007) 592:439–454 Introduction with sclerotized needles. Species of Hofstenia lack a female gonopore, but the sharp needles of the Species of the genus Hofstenia are among the everted penis can penetrate the body wall of the largest and most distinctive of the Acoela. They receiving worm and deposit sperm directly are voracious predators of micrometazoans, suck- beneath its epidermis (Bock, 1923); sperm then ing in prey with a capacious muscular pharynx at apparently migrate through the parenchymal the anterior tip of the body. Mature specimens tissue to the oocytes. are typically 4–9 mm in length and, rather than Such distinctive features made it difficult for being colorless and having the teardrop body early systematists to place Hofstenia among other shape of most acoel species, Hofstenia species are platyhelminths. The first described species, Hof- darkly pigmented, with patterns of white bands stenia atroviridis Bock, 1923, attracted consider- and spots, and nearly cylindrical in shape, often able attention for the primitive features of its with a small pointed tail (Fig. 1). Their carnivory nervous system and gut relative to those of other and color patterns, reminiscent of panthers in platyhelminths and for features of its reproduc- general, inspires their common name. tive system that seemed to be intermediate The large, muscular, anteriorly directed phar- between those of other primitive and the more ynx simplex is one-third to one-half the length of derived flatworms (Bock, 1923; Steinbo¨ ck, 1924; the entire worm (Fig. 2) and is used to suck up Bresslau, 1933; Karling, 1940). At first, similarity copepods, ostracods, and turbellarians. Also dis- of its reproductive organs and pharynx to those of tinctive of Hofstenia is its anteriorly positioned prolecithtophoran and some lecithoepitheliate male copulatory organ (Fig. 2). Located ventral turbellarians was weighed heavily in placing it to the pharynx, the copulatory organ is composed among such so-called ‘‘alloeocoels,’’ even though of a highly muscular, eversible penis equipped its affinity to the Acoela was recognized (Stein- Fig. 1 Dorsal aspect of eight specimens of Hofstenia miamia from Curac¸ao (from Correˆa, 1963) 123 Hydrobiologia (2007) 592:439–454 441 Fig. 2 Sagittal histological section of Hofstenia miamia mgp—male gonopore, phm—pharynx musculature, from Belize. cs—Digestive central syncytium, e—egg, st—penis stylets, sv—seminal vesicle gv—granule vesicle, m—mouth, ma—male antrum, bo¨ ck, 1924; Meixner, 1938; Karling, 1940). Not acquired the type material for H. atroviridis, H. until a quarter century after its discovery was its giselae, and H. miamia (Table 2) for comparison. true nature as an acoel established (Papi, 1957). We report here the results of our comparative Currently there are four described species of morphological study of this material. In addition, Hofstenia (see Tyler et al., 2006). The type we document the range in color patterns in species, H. atroviridis, is a dark, blackish green Caribbean specimens, and propose systematic species from the coast of Japan where it is found revision of the genus Hofstenia. Acoels have associated with coralline algae in tide pools and been attributed to possess unusually fast evolving on the holdfasts of Laminaria at subtidal depths nuclear ribosomal genes (Carranza et al., 1997; (Bock, 1923). H. miamia Correˆa, 1960, was Ruiz-Trillo et al., 1999), which may make these described from a single specimen found in algae molecular markers useful for studying closely at Miami, Florida (Correˆa, 1960); however, addi- related acoel lineages (e.g. Tekle et al., 2005). We tional specimens were subsequently found in therefore used 18S and 28S rDNA genes acquired Antigua as well as Curac¸ao (Correˆa, 1963) and from several specimens of Hofstenia from all four were used to document the variation in the dark- collection sites in an attempt to reconstruct a brown, white-banded color patterns within the molecular phylogeny of this taxon and test the species (Fig. 1). Soon thereafter, Steinbo¨ ck traditional classification. (1966) published a monograph on the Hofstenii- dae in which he established two new species: H. beltagii Steinbo¨ ck, 1966, from specimens collected Materials and methods in the Red Sea and first identified by Beltagi (1958) as H. atroviridis, and H. giselae Steinbo¨ ck, Collection and observation of living specimens 1966, collected from a Thalassia bed in the Bahamas. With his specimens of H. giselae, which Approximately 150 living specimens of Hofstenia were lighter-colored than the reported pigmenta- were collected from sites in Bahamas, Belize, tion of H. miamia, Steinbo¨ ck experimented Bermuda, and Panama (Table 1). The majority of extensively on their regenerative capabilities specimens we collected were taken from sub- (Steinbo¨ ck, 1966, 1967). merged, decaying mangrove leaves found in piles Over a 1-year period from April 2004 to May at the base of living mangroves, and had dark 2005, we collected living specimens of Hofstenia coloration that appeared most similar to Correˆa’s from Bahamas, Belize, Bermuda, and Panama (1963) H. miamia specimens (Fig. 1). A single (Table 1). Some of these were light-colored and specimen of H. miamia was also found on associated with Thalassia and filamentous algae, Penicillus attached to a mangrove root at Man- which we identified as H. giselae, and others dark atee Cay, Belize. We collected lightly colored and associated with decaying mangrove leaves, specimens of Hofstenia from a Thalassia sp. bed which we identified as H. miamia. We also at Carrie Bow Cay, Belize, and from filamentous 123 442 Hydrobiologia (2007) 592:439–454 25 20 25 25 25 ~ ~ ~ ~ ~ Stylet number 1 4 10 25 30 90 Specimens ~ ~ ~ ~ m) l 75 40 70 65 70 Stylet length ( (m) 1 1 1 1 Depth <1 <1 Subterminal Subterminal Subterminal Subterminal Subterminal Mouth root leaves leaves leaves Thalassia 0.3 0.4 0.4 0.4 0.5 Pharynx/ body ratio mangrove algae mangrove mangrove mangrove on underlying 1.3 1.0 1.0 1.7 2.1 Pharynx length (mm) Habitat filamentous Penicillus Submerged Submerged Sediment Submerged 4.2 2.5 3.7 3.9 4.2 Body length (mm) 2004 4 2004 2004 2004 2004 2005 assoc. Fig. in Date April April April August April May Thalassia green shown with (W) study Brown/white Brown/white White/brown White/brown Dark Color † † † † those 26 10 54 32 this ¢ ¢ ¢ ¢ ¢ ¢ 06 11 06 04 15 42 in ° ° ° ° ° ° Longitude 76 88 88 88 82 64 used including Corallina , , Thalassia (N) with † † † † algae 26 46 9 46 Hofstenia ¢ ¢ ¢ ¢ ¢ Hofstenia ¢ Laminaria 46 39 49 43 20 of intertidal/subtidal leaves ° ° ° ° ° of 21 submerged among assoc. and ° Latitude 16 9 23 16 32 16 with sections specimens mangrove Thalassia assoc. Low-energy Low-energy Low-energy High-energy Low-energy Habitat for station side side field ao ¸ histological Garden East of North STRI Belize Curac Belize Japan Bahamas Location information Island Pond, Cay, Grouper Toro, Cay 5 miamia giselae atroviridis 2508a Bow del Comparison Sampling Cays, III, Stocking 2 1 1096778 SMNH 74878/9 89913 NMW 12, USNM Paratype SMNH Lectotype Lectotype Lee Manatee Twin Carrie Bocas Walsingham SMNH Hofstenia Hofstenia Hofstenia Specimen Table Table Locality Bahamas Belize Panama Bermuda 123 Hydrobiologia (2007) 592:439–454 443 algae at the surface of a saltwater pond on Lee Gran˜ a’’ (Ferrol, Galiza, Spain) in August 2006 in Stocking Island, Bahamas.