An Extraordinary New Carnivorous Sponge, Chondrocladia Lyra, in the New Subgenus Symmetrocladia
Total Page:16
File Type:pdf, Size:1020Kb
See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/260103802 An extraordinary new carnivorous sponge, Chondrocladia lyra, in the new subgenus Symmetrocladia... Article in Invertebrate Biology · December 2012 DOI: 10.2307/23352690 CITATIONS READS 10 199 4 authors, including: Lonny Lundsten Monterey Bay Aquarium Research Institute 27 PUBLICATIONS 471 CITATIONS SEE PROFILE All content following this page was uploaded by Lonny Lundsten on 22 April 2014. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately. Invertebrate Biology 131(4): 259–284. © 2012, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12001 An extraordinary new carnivorous sponge, Chondrocladia lyra, in the new subgenus Symmetrocladia (Demospongiae, Cladorhizidae), from off of northern California, USA Welton L. Lee,1,a Henry M. Reiswig,2,3 William C. Austin,4 and Lonny Lundsten5 1 Department of Invertebrate Zoology, California Academy of Sciences, San Francisco, California 94118, USA 2 Department of Biology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada 3 Natural History Section, Royal British Columbia Museum, Victoria, British Columbia V8W 9W2, Canada 4 Khoyatan Marine Laboratory, North Saanich, British Columbia V8L 5G5, Canada 5 Monterey Bay Aquarium Research Institute, Moss Landing, California 95039, USA Abstract. Chondrocladia (Symmetrocladia) lyra subgen. nov., sp. nov., is described from northeast Pacific sites at Escanaba Ridge and Monterey Canyon at depths of 3316–3399 m. Two retrieved specimens are described in detail, while variations are described in ten photo- graphed or videotaped specimens. The basic structure, termed a vane, is harp- or lyre-shaped. From 1 to 6 vanes extend by radial growth from the organism’s center. The orientation among the vanes is approximately equiangular, such that together they display pentaradiate, tetraradiate, triradiate, or biradiate symmetries. Each vane is formed by a horizontal stolon supporting a series of upright, equidistantly spaced branches each of which terminates at its apex in a swollen ball in all observed specimens except the para- type. Swellings occur midway along the branches in the holotype, but not in the paratype. A linear row of filaments project from the sides, front, and back of each branch, and also from the tops of each stolon. The terminal balls are the sites of spermatophore production and release; mid-branch swellings are sites of oocyte maturation. The two megasclere spicule types have specific distributions; styles support rhizoids, stolons, and branches, while subtylo- styles support filaments and terminal balls. Anchorate isochelae cover all surfaces. Enclosed crustacean prey on branches and stolons provide direct evidence of carnivory. The structure of the vanes maximizes surface area for passive suspension feeding. Increased surface area could also maximize spermatophore capture, with the sigmas projecting from the spermato- phore surface being caught by projecting isochelae on filaments. Swellings on filaments are snared spermatophores, firmly fused to recipient tissues and undergoing destruction. Sperma- tophores on filaments are present in branch swellings containing early and mature oocytes. Oogenesis and maturation occur only in proximity to branch swellings, suggesting that devel- opment is induced by spermatophore reception. Symmetrical development of uniserial branched stolons (the vanes) characterized members of the new subgenus Symmetrocladia. Additional key words: Porifera, northeast Pacific, spicules, spermatophores, radial symmetry It has been 17 years since incontrovertible proof fare in substrate competition with other sessile of carnivory by sponges was published by Vacelet & organisms (Jackson & Buss 1975; Pawlik et al. 2007) Boury-Esnault (1995). Before that major discovery, and in antipredatory defense against mobile animals sponges were generally regarded as rather simple, (Wulff 2002; Pawlik 2011). It had been known that filter-feeding bacterivores and herbivores, restricted some sponges aggressively kill corals at the scale of in their aggressive activities to waging chemical war- single coral heads (e.g., Cliona delitrix PANG 1973: Chaves-Fonnegra & Zea 2007), and occasionally aAuthor for correspondence. over a larger reef-wide scale (e.g., Terpios hoshinota E-mail: [email protected] RU¨ TZLER &MUZIK 1993), but they had not been 260 Lee, Reiswig, Austin, & Lundsten known to pose a threat to mobile animals. Our ditions conducted by the Monterey Bay Aquarium understanding of sponge biology changed signifi- Research Institute (MBARI) using the remotely cantly when Vacelet and Boury-Esnault showed that operated vehicles (ROVs) Tiburon (in 2000, 2005– sponges without choanocyte chambers passively 2007) and Doc Ricketts (in 2009). These ROVs are ensnared zooplankton, aggressively enclosed them in equipped with studio-quality digital video cameras, a cavity by cell migration, and effectively dismem- digital still cameras, a variety of sensors (e.g., CTD, bered them into small particles, which could be O2), and sampling gear (e.g., manipulator arm, suc- phagocytosed and digested intracellularly. tion sampler). Observations were recorded to digital The great majority of known or suspected carnivo- video tape and later analyzed using the Video Anno- rous sponges belong to the demosponge family Clad- tation and Reference System (VARS: Schlining & orhizidae (all members of the presently recognized Jacobsen Stout 2006), a software interface and data- seven genera); a few members of the closely related base that contains over 4,000,000 observations of families Esperiopsidae and Guitarridae are also sus- organisms, geologic features, and equipment pected to be carnivorous by similarity of body form deployed during MBARI’s 25 years of deep-sea and the presence of erected chelate microscleres on research. For each observation of C. lyra, associated their external surface (Vacelet 2007). When carnivory fauna, substrate features, and other ecological was first proven, there were 84 species in the family parameters were annotated within VARS. Observa- Cladorhizidae, a group dominated in form by small, tions were merged with physical data collected by thin, bottle-brush sponges with little or no “body.” the ROV so that position, depth, and water chemis- Intense interest in documenting the variety and ubiq- try are known for each specimen. Parallel red lasers uity of this group has seen 24 new species described (640 nm), spaced 29 cm apart, were used to estimate in the intervening period of 18 years (1995–2012), organism size for observations where no physical compared with only six species described in the previ- collection was made. ous 18 years (1977–1994). In spite of the increase in During the encounters with C. lyra, large frag- taxonomic activity, there is still relatively little known ments of two specimens were collected, one in 2000 about details of body organization, reproduction, and the other in 2005, from the South Escanaba and cytology of the carnivorous sponges. Only five Ridge (Gorda Ridge) off northern California at species can be considered known in any significant about 3300 m depth (Fig. 1). Both were observed detail: Asbestopluma hypogea VACELET &BOURY- on soft abyssal plain sediment with their root struc- ESNAULT 1996; A. occidentalis (LAMBE 1893) (Riesgo tures (rhizoids) mostly buried. Collected specimens et al. 2007), Cladorhiza methanophila VACELET &BOU- were preserved in 70% ethanol, which proved suffi- RY-ESNAULT 2002; C. pteron REISWIG &LEE 2007; and cient for routine taxonomy and light microscopy of Chondrocladia gigantea (HANSEN 1885) (Ku¨ bler & cells in one specimen, the holotype, but too poor for Barthel 1999). Members of the last genus retain examination of cells by transmission electron aquiferous canals and choanocyte chambers that, at microscopy (TEM). The remaining ten video obser- least in some species, function in maintaining water vations were made in 2006, 2007, and 2009, all in a pressure for inflation of spectacular terminal globes. region south of the Monterey Canyon (Fig. 1). Here, we report the results of our examination of two recently collected specimens and ten additional imaged specimens of a spectacular and large new spe- Spicule examination cies of Chondrocladia from deep water in the northeast Pacific Ocean. We provide a taxonomic description of Spicules from fragments of each body part were this species, summarize variation in its body form, disassociated, either in sodium hypochlorite or in and describe details of cellular organization, including concentrated nitric acid. They were then rinsed and its feeding and reproductive systems. We also extrapo- mounted on glass microscope slides. A compound late from the reproductive evidence to suggest pro- microscope fitted with an ocular micrometer or com- cesses that maintain this species in nature. puter digitizer was used to measure the length, and, where appropriate, the width of 50 spicules of each Methods spicule type within each body part. Exceptionally, in some cases, fewer than 50 spicules were found and measured. Anomalies were noted, but not necessarily Specimens enumerated. Immature spicules were deemed to be In situ observations of twelve individuals of those of similar or lesser length than the mean length, Chondrocladia