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Cole, ES, LA Hahn, J Choquette, and M Thacker. Natural History Characteristics of Synaptula Hydriformis, An PROCEEDINGS OF THE SECOND JOINT SYMPOSIUM ON THE NATURAL HISTORY AND GEOLOGY OF THE BAHAMAS Edited by Tina M. Niemi and Kathleen Sullivan Sealey ORGANIZER: Troy A. Dexter Executive Director Gerace Research Centre University of The Bahamas San Salvador, The Bahamas 2020 iii Copyright 2020, Gerace Research Centre All rights reserved. No part of this work may be reproduced or transmitted in any form by any means, electronic or mechanical, including photocopying, recording, or any data storage or retrieval system without the express written permission of the Gerace Research Centre. ISBN: 978-0-935909-67-8 iv The 2nd Joint Symposium on the Natural History and Geology of The Bahamas NATURAL HISTORY CHARACTERISTICS OF SYNAPTULA HYDRIFORMIS, AN APODID SEA CUCUMBER FROM OYSTER POND, SAN SALVADOR ISLAND, THE BAHAMAS Eric S. Cole, Leigh Anne Hahn, Jessica Choquette, and Miranda Thacker Biology Department, St. Olaf College Northfield, MN 55057 ABSTRACT for colonizing the island’s inland, anchialine Synaptula hydriformis (Echinodermata, pond communities. Holothuroidea, Apodida, Synaptidae: Lesueur, 1824) is a small, hermaphroditic sea cucumber INTRODUCTION commonly found creeping over the benthic pearl oyster communities in Oyster Pond, San Salva- While investigating invertebrate communi- dor Island, The Bahamas. Unusual features in- ties in the anchialine ponds of San Salvador Island clude possession of an ovo-testis; internal self- in The Bahamas, we frequently encountered a fertilization; embryonic brooding accompanied small, "naked sea cucumber" identified as Synap- by matrophagy (juveniles feed on their mother’s tula hydriformis living in Oyster Pond. These soft- coleomic cells and tissues); and viviparous, live- bodied echinoderms bear little resemblance to birth of juveniles with adult characteristics. other, hard-bodied members of the phylum, (sea Through live-culture and paraffin histology, life stars, brittle stars, and urchins) and have adapted a history stages were characterized. The ovo-testis life style that seems to have converged with that of was found to contain both sperm and eggs sup- small benthic worms. At first viewed as a nuisance porting its characterization as a simultaneous (they clung to wetsuits and booties with minute, hermaphrodite. Three unique color morphs were hook-like ossicles embedded in their gelatinous described: solid brown, brown striped, and trans- skins), we soon became fascinated by their natural lucent. In living transparent specimens, we are history and set out to investigate (and manipulate) able to observe juveniles ambulating and feeding their reproductive life cycle. within the mother’s body cavity. Autogamy Synaptula hydriformis was first described (self-fertilization) and vivipary (live-birth) mark by the accomplished French naturalist Charles-Al- the synaptid family as unusual among sea cucum- exandre Lesueur in 1824 during his association bers. Other families of sea cucumber tend to re- with William Maclure and Robert Owen, the re- lease gametes into the water column where they markable founders of an intellectual commune es- undergo external fertilization and develop into tablished in New Harmony, Indiana. Lesueur first free-swimming planktonic larvae. We developed encountered Synaptula hydriformis on an expedi- a method for inducing both synchronous spawn- tion he made with William Maclure in the winter ing and birthing. Subsequently, a successful of 1815-1816 to the West Indies, in a rich man- technique for culturing juvenile sea cucumbers grove community on the north side of the island of was established. Developmental stages were Guadeloupe. The species has been referred to by characterized for the larvae. We found evidence many different names, including Holuthuria hydri- for direct development, bypassing both auricu- formis, Holuthuria viridis, Synaptula vivipara, laria and doliolarian stages and skipping the met- Synapta viridis, Synapta pourtalesii, Leptosynapta amorphosis typical of other holothuroideans. We hydriformis, Leptosynapta pourtalesii, Heter- discuss Synaptula in the context of other her- osynapta viridis, Synapta vivipara, Synapta picta, maphroditic organisms that seem well-adapted and Chondrocloea vivipara (Heding, 1928). 111 The 2nd Joint Symposium on the Natural History and Geology of The Bahamas The second significant mention of Synap- and parturition developed, this organism offers tula hydriformis involves a specimen collected by promise as a novel model organism for the study of the U.S. Fish Commission on an expedition to The invertebrate (echinoderm) embryology. Their abil- Bahamas in 1886 from the very first ship ever de- ity to undergo live-birth also provides an intriguing signed specifically for marine research, the USS Al- novelty rarely seen outside of the chordate phylum: batross. While exploring San Salvador Island (for- a mechanism by which juveniles living within the merly Watling’s Island), the Albatross obtained a mesoderm-lined coelomic space of their mothers second specimen of this sea cucumber. This was are shunted to the animal’s posterior, expressed stored in the Smithsonian Museum, and later iden- into the outside world within a mesoderm/ecto- tified as Synaptula hydriformis (Lesueur 1824) derm “birthing sac”, and released through a devel- when Hubert Clark uncovered it in the 1900s. opmentally programmed (reversible?) rupture of Clark performed extensive (beautifully illustrated) that sac during birth. It seems likely that juveniles research on this self-fertilizing, internally brooding from multiple, asynchronous reproductive cohorts species and wrote prolifically of its physiology, are delivered (exhibiting “superfetation”) as evi- taxonomy, and embryology (Clark, 1897, 1907). denced by varying sizes and states of development The Smithsonian obtained a more recent sample of the progeny expressed at the time of birth from from The Bahamas in 1996, collected by Charlene a single individual. It would be interesting to learn D. Long (American Natural History Museum). whether or not larval forms can be sorted and re- The most-studied specimens were collected from tained when older juveniles are birthed, or if they Bermuda, Panama, Jamaica, and the Florida Keys. too are discharged without regard to their develop- Since Clark’s impressive monograph, there are mental maturity. only modest references to the species until Jennifer Frick (Smithsonian Marine Station, Fort Piece, FL) METHODS took up the study of their ovo-testis and matroph- agy (or matrotrophy: feeding on, or deriving nour- Collection and laboratory culture of ishment from ones' mother) in the late 1990s for Synaptula hydriformis her Ph.D. Frick collected specimens from Indian River Lagoon and Lake Surprise on Key Largo Specimens were collected by hand while (Frick et al., 1996; Frick, 1998). snorkeling over beds of scaly pearl oysters in Synaptids are interesting from a variety of Oyster Pond, San Salvador Island, The Bahamas. perspectives. Unlike most other sea cucumbers, It is perhaps worth noting, that synaptids insinu- the apodid species lack tube feet for motility. They ate themselves deeply into the internal spaces of adhere to the substrate through surprisingly clingy calcareous-algal aggregates that form biotic out- dermal hooks called ossicles and ambulate using crops which also house a variety of bivalves and their feeding tentacles to pull themselves along, living sponge. It is often, unfortunately neces- while feeding on the substrate. As self-fertilizing sary to open such outcrops in order to extract liv- hermaphrodites, they are well-adapted for colo- ing specimens. We would endorse an attitude of nizing novel habitats. A single specimen could the- respectful prudence when it is necessary or desir- oretically establish an entire population without a able to collect living specimens. Individual mating partner. This has implications for genetic specimens were isolated and maintained in finger diversity. It is possible that the entire population bowls with seawater, and fed small droppers-full within our field site is comprised of only a few ge- of sedimentary floc collected from Oyster Pond netic “clones”. The life-style of embryonic brood- (a loose bottom sediment rich in microbial mate- ing and matrophagy is also interesting. If labora- rial that the Synaptula appear to feed on). Floc tory cultures of the transparent adults can be estab- was maintained under full-spectrum lights to pro- lished, and experimental triggers for fertilization mote algal growth. 112 The 2nd Joint Symposium on the Natural History and Geology of The Bahamas Induction of birthing and spawning Olympus BH40 microscope using bright field op- tics and a DP-71 digital camera. Fixed histological Adult Synaptula were placed in 90 mm pe- specimens were examined using the Olympus tri dishes half-filled with seawater and floated on BH40 microscope. an ice-water bath for ten minutes. These gave birth within 6-18 hours (exhibiting a lot of individual variation). Juveniles of numerous developmental Paraffin Histology stages from a single adult were observed, confirm- ing “superfetation” (multiple broods maintained Sea cucumbers were collected in January within the same adult). We also used this cold- 2017. Specimens were fixed in Bouin’s fixative, shock treatment to induce ovulation and internal dehydrated, and embedded in paraffin as described spawning, which we confirmed by subsequently by Humason (1979). Eight to nine micron-thick decapitating and expressing the coelomic contents sections were
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