Deep-Sea Research II 92 (2013) 207–213 Contents lists available at SciVerse ScienceDirect Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2 Bathyal sea urchins of the Bahamas, with notes on covering behavior in deep sea echinoids (Echinodermata: Echinoidea) David L. Pawson n, Doris J. Pawson National Museum of Natural History, Smithsonian Institution, WA DC 20013-7012, USA article info abstract Available online 24 January 2013 In a survey of the bathyal echinoderms of the Bahama Islands region using manned submersibles, Keywords: approximately 200 species of echinoderms were encountered and documented; 33 species were Echinodermata echinoids, most of them widespread in the general Caribbean area. Three species were found to exhibit Echinoidea covering behavior, the piling of debris on the upper surface of the body. Active covering is common in at Bathyal least 20 species of shallow-water echinoids, but it has been reliably documented previously only once Covering in deep-sea habitats. Images of covered deep-sea species, and other species of related interest, are Bahamas provided. Some of the reasons adduced in the past for covering in shallow-water species, such as Caribbean reduction of incident light intensity, physical camouflage, ballast in turbulent water, protection from desiccation, presumably do not apply in bathyal species. The main reasons for covering in deep, dark, environments are as yet unknown. Some covering behavior in the deep sea may be related to protection of the genital pores, ocular plates, or madreporite. Covering in some deep-sea species may also be merely a tactile reflex action, as some authors have suggested for shallow-water species. Published by Elsevier Ltd. 1. Introduction body. The pedicellariae apparently do not play a significant role in the process of covering, or in retention of the debris (Reese, 1966; During the years 1983–1989, a collaborative effort involving Coppard et al., 2010). In shallow-water taxa the debris usually the National Museum of Natural History (NMNH), Smithsonian consists of shells, or seagrass, and other material picked up from Institution, Washington DC, and the Harbor Branch Oceano- the ocean floor, and it may frequently include pieces of drift algae graphic Institution, Inc. (HBOI), Fort Pierce, Florida, resulted in a that come in contact with the urchin, and are captured by the tube series of dives in Harbor Branch’s Johnson-Sea-Link submersibles feet. In the deep sea, debris may include shell fragments, bryozoan (JSL-I and JSL-II) around the Bahamas in bathyal depths. The main colonies, pteropod skeletons—apparently, whatever is readily objective of these dives was to study the composition and biology available to the animal. of the echinoderm fauna of the region. Approximately 200 species In this paper, we list the species of echinoids encountered in of echinoderms were encountered and documented. Thirty three the bathyal of the Bahamas, along with their depth ranges, and species of echinoids, none of them new to science, were photo- identify the species that cover themselves. Covering in the deep- graphed and videotaped, and voucher specimens were collected. sea is discussed, and compared and contrasted with covering in Some aspects of the biology of the sea urchins proved to be of shallow-water species. special interest. We were astonished to find that even in bathyal depths some species exhibited so-called covering behavior (cover- ing reaction, covering response, heaping, masking), which has been 2. Materials and methods reported only once in the deep sea, as far as we can determine (Levin et al., 2001). David et al. (2003) reported on ‘‘conveying’’ by For the Bahamas study, the research group comprised John another deep-sea species of sessile or sedentary organisms which E. Miller (Leader), Harbor Branch Oceanographic Institution, Inc.; may merely have settled on the host animals. Typically, covering Gordon Hendler, formerly Smithsonian Institution and then, from involves coordinated action on the part of the tube feet and spines 1985, Los Angeles County Museum of Natural History; Porter M. Kier (Millott, 1955, 1956) to heap debris on the upper surface of the and David L. Pawson, Smithsonian Institution. Under an agreement between the Smithsonian Institution and Harbor Branch Oceano- graphic Institution, Inc., the submersibles Johnson-Sea-Link I and II n Corresponding author. Tel.: þ1 202 633 1757. were made available to us between 1983 and 1989. A total of 106 E-mail address: [email protected] (D.L. Pawson). dives were made, 102 in daylight hours and 4 at night, at a variety of 0967-0645/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.dsr2.2013.01.023 208 D.L. Pawson, D.J. Pawson / Deep-Sea Research II 92 (2013) 207–213 sites around the Bahamas, to a maximum depth of approximately Table 1 765 m. Habitats where echinoderms flourished were commonly Bathyal Bahamas echinoids documented during dives of the JSL submersibles, steep rocky slopes with a thin veneer of sandy sediment, and small 1983-1989. almost-flat plains with deeper soft sediments. aDepth range Covered? During the Bahamas investigations, for each echinoderm of (m) interest encountered, attempts were made to briefly videotape the subject and its surroundings, with the scientist/observer Order Cidaroida Cidaris abyssicola (Agassiz, 1869) 633–723 No providing a contemporaneous commentary. Several 35 mm still Cidaris blakei (Agassiz, 1878) 577–902 No color photographs were also taken. As desired, voucher specimens Cidaris rugosa (Clark, 1907) 658–788 No were collected for further study in the laboratory and eventual Calocidaris micans (Mortensen, 1903) 226–624 No incorporation into reference collections at the National Museum Histocidaris nuttingi (Mortensen, 1926) 618–624 No of Natural History, Smithsonian Institution, and Harbor Branch Histocidaris sharreri (Agassiz, 1880) 732–868 No Histocidaris purpurata (Thomson, 1872) 903 No Oceanographic Institution, Inc. Details of collection data for the Stylocidaris lineata (Mortensen, 1910) 240–630 No species listed here can be found at http://collections.nmnh.si.edu/ Tretocidaris bartletti (Agassiz, 1880) 212–305 No search/iz or at the Oceanographic Museum, Florida Atlantic Order Echinothurioida University Harbor Branch Oceanographic Institute, Fort Pierce, Araeosoma belli (Mortensen, 1903) 272–709 No Florida. Araeosoma fenestratum (Thomson, 1872) 703–834 No Recently, we have participated in the Smithsonian Institution’s Hygrosoma petersii (Agassiz, 1880) 403 No Deep Reef Observation Project (DROP) using the submersible Phormosoma placenta (Thomson, 1872) 231–768 No Curasub in June 2011 (4 dives) and in August 2012 (2 dives) to Order Salenioida study echinoderms at Curacao, Netherlands Antilles, down to Salenia goesiana (Loven, 1874) 314–616 No depths of approximately 305 m. At Curacao, individuals of Con- Order Aspidodiadematoida olampas sigsbei were observed and collected and, in August 2012, Aspidodiadema jacobyi (Agassiz, 1880) 411–696 No were maintained alive in aquaria for approximately 36 h while a Order Diadematoida variety of experiments related to the covering reaction were Centrostephanus longispinus rubicingulus (Clark, 54–58 No conducted. Unfortunately, the animals were moribund and unre- 1921) sponsive, and the experiments were unsuccessful. Order Arbacioida Coelopleurus floridanus (Agassiz, 1872) 291–404 No Order Camarodonta 3. Results Gracilechinus tylodes (Clark, 1912) 778 No Lytechinus euerces (Clark, 1912) 244–458 Yes/nob c Thirty three species of echinoids were found around the Genocidaris maculata (Agassiz, 1869) 99 Unknown Bahamas in bathyal depths. An annotated list of echinoids is Order Clypeasteroida presented in Table 1. There were no new taxa; all echinoid species Clypeaster cyclopilus (Clark, 1941) 394–487 No Clypeaster subdepressus (Gray, 1825) 226–378 No had been previously described from various areas of the Carib- bean. This result was unexpected, because several new taxa were Order Spatangoida found in all other classes of Echinodermata. Species which Aceste bellidifera (Thomson, 1877) 569 Buried Agassizia excentrica (Agassiz, 1869) 453–455 Buried typically burrow were, of course, seldom encountered. For bur- Brissopsis atlantica (Mortensen, 1907) 613–624 Buried rowing species listed below, the only evidence of the species’ Heterobrissus hystrix (Agassiz, 1880) 237–614 No presence in the area was in the form of a dead test on the Linopneustes longispinus (Agassiz, 1878) 231–700 Buriedd e sediment surface. Palaeobrissus hilgardi (Agassiz, 1880) 598–698 Yes/no Paleopneustes cristatus (Agassiz, 1873) 265–592 No Paleopneustes tholoformis (Chesher, 1968) 236–645 No 3.1. Incidence of covering behavior in bathyal Bahamas Sea Urchins Plagiobrissus grandis (Gmelin, 1788) 392–409 Buried Plethotaenia angularis (Chesher, 1968) 618–645 Buried 3.1.1. Three species exhibited covering behavior Order Echinolampadoida C. sigsbei (A. Agassiz) (Fig. 1A and B). This relatively common Conolampas sigsbei (Agassiz, 1878) 272–540 Yes species was photographed or videotaped in situ on 9 dives, at depths a Depth ranges given here are those encountered during the program of of 272–464 m, but it was observed and ignored, or merely briefly Bahamas submersible dives. For broader depth ranges of most species, see Serafy noted, on many other dives. All individuals documented by imagery (1979) and Pawson et al. (2009). were covered with a topknot of coarse debris. In many cases (see b In Lytechinus euerces, some individuals