Aggregated clumps of lithistid sponges: a singular, reef-like bathyal habitat with relevant paleontological connections

Abstract

The advent of deep-sea exploration using video cameras has uncovered extensive sponge aggregations in virtually all oceans. Yet, a distinct type is herein reported from the Mediterranean: a monospecific reef-like formation built by the lithistid demosponge Leiodermatium pfeifferae. Erect, plate-like individuals (up to 80 cm) form bulky clumps, making up to 1.8 m high mounds (1.14 m on average) on the bottom, at a 760 m-deep seamount named SSS. The siliceous skeletal frameworks of the lithistids persist after sponge death, serving as a complex 3D substratum where new lithistids recruit, along with a varied fauna of other sessile and vagile organisms. The intricate aggregation of lithistid mounds functions as a "reef" formation, architecturally different from the archetypal "demosponge gardens" with disaggregating siliceous skeletons. Leiodermatium pfeifferae also occurred at two additional, close seamounts (EBJ and EBS), but, unlike at SSS, the isolated individuals never formed accretive clumps. The general oceanographic variables (temperature, salinity, dissolved nutrients, chlorophyll, and oxygen) revealed only minimal between-seamount differences, which cannot explain why sponge abundance at SSS is about two orders of magnitude higher than at EBJ or EBS. Large areas of the dense SSS aggregation were damaged, with detached and broken sponges and a few tangled fishing lines. Satellite vessel monitoring revealed low fishing activity around these seamounts. In contrast, international plans for gas and oil extraction at those locations raise serious concerns over the need for protecting urgently this unique, vulnerable habitat to avoid further alteration. Modern lithistids are a relict fauna from Jurassic and Cretaceous reefs and the roots of the very genus Leiodermatium can be traced back to those fossil formations. Therefore, understanding the causes behind the discovered lithistid aggregation is critical not only to its preservation, but also to elucidate how the extraordinary Mesozoic lithistid formations developed and functioned.

Fig 1. Study site location.

The inset shows the location of the Western Mediterranean surveyed area. The large map indicates the location of the 32 ROV transects. The framed squares (Stone Sponge Seamount = SSS; Emile Baudot Jr. Seamount = EBJ; Emile Baudot South Seamount = EBS) indicate the 3 seamounts reported in this study where the lithistid sponges grew abundantly.

Fig 2. Features of Leiodermatium pfeifferae.

(A) In situ view of an isolated, small group of individuals. (B) Detail of the convex, inhalant side of a dried individual, showing punctiform ostioles (ot). (C) Detail of the concave, exhalant side, showing small elevated oscules (os). (D) General view of the framework of spiny rhizoclone desmas. At the internal (en = endosome) region of the body plate, packs of oxeas (ox) and the aquiferous canals (ac) run from side to side of the sponge, passing through the network of desmas (rh). Note that at the inhalant side (in), desmas are thinner and smaller, making a more denser network that functions as a dermal skeleton among the ostia (ot). (E) Detail of rhizoclones (rh) around an aquiferous canal, showing large spines (sp). (F) Detail of contacts (z = zygoses) between adjacent desmas. (G) SEM view of the inhalant side of a dried specimen, showing abundant hispidating oxeas (ox) and ostia (ot) provided with a poral membrane (mb) that allows these pores to be closed if required. (H) Detail of hispidating oxeas forming a subterminal fringe at the free edge of the plates.

Fig 3. Skeletal details of Leiodermatium pfeifferae.

(A) General view of the desma (rh) network, with oxeas (ox) and aquiferous canals (ac) passing through. (B) Pack of oxeas (ox) running through the desma (rh) network. (C-D) Detail of the round, spiny (sp) ends of the thickest strongyloxeas occurring in the marginal fringe. (E) Detail of a very thin oxea (ox) on the typical multifurcated spine (sp) of a rhizoclon desma. (F) View of the triangular axial canal (ax) at the core of a broken oxea. (G-H) Broken arms (ba) of desma showing no internal axial canal.

Fig 4. ROV track at the Stone Sponge Seamount (SSS).

Substrate coverage by lithistid sponges along the track is indicated by the color scale. A and B sites refer to the two areas where the lithistid reef was intersected by the track.

Fig 5. Views of lithistid reef at Stone Sponge Seamount (SSS).

(A-B) General view of the lithistid mounds, showing intertwined growth and a complex 3D structure. Translucent "a-b" and "c-d" lines indicate sponge clumps measuring respectively 118 cm and 94 cm, relative to sediment bottom. Note the occurrence of dead sponges (d) and bare skeletal remains (sr) buried in the sediment. A squat lobster (s) is also shown. (C) View of sponge plates, showing how the sediment rain accumulates on the convex (in = inhalant) side, while the concave (ex = exhalant) side has no silt. The abundant hispidating spicules on the inhalant side appear to facilitate the accumulation of sediment on the sponges. Note the presence of the starfish Peltaster placenta, thought to be also a suspension feeder. (D) Common invertebrates growing on the lithistid are hydroids (h), the alcyonacean octocoral Muriceides lepida (m), and the scleractinian coral Desmophyllum dianthus (c) with abundance of newly settled recruits (r). (E) Group of lithistid individuals laying on the sediment. Note the superimposing structure of the clump. One of the individuals is already dead (d), buried in sediment. On the other sponges, growth marks (g) are seen on the bodies, probably reflecting periodical pulses of food and silicate in the sponge habitat. (F) Aggregation area seriously damaged, with large sponges broken and laying on the side (arrows) while being buried under the sediment rain.

Fig 6. General oceanographic features.

(A) Silicate concentration (μM) at the -800 m isobath of the Balearic Sea. (B-C) Chlorophyll concentration (mg m^-3) at the -800 m and -300 m isobaths; the latter one indicates the coastal origin of the sinking phytoplankton. (D) Oxygen concentration (ml l^-1) at the -800 m isobath. To illustrate between-mountain comparisons in the various variables of interest, we are depicting only the spatial distribution during the season in which differences between the SSS area and the EBJ-EBS area were the greatest for each variable. In general, between seamount differences were very small over the year cycle, with the winter season causing the larger differences, except for oxygen concentration, which took place in summer.

Fig 7. Spatial distribution of demersal fishing activities.

Summary of a vessel monitoring system (VMS) analysis involving the fishing activity of 1045 vessels geared with otter trawls, set gillnets, set longlines, and/or traps during the 2007–2010 period. Results are expressed as relative (%) fishing effort (i.e., comparative numbers of fishing hours at a 5' x 5' grid cell). Crosses (+) refer to the location of the seamounts of interest (SSS, EBJ, EBS), each being surrounded by a 20 x 20 nautical mile quadrat.