Reprinted from: -------------- ------ J. exp. mar. Biol. Ecol., 1976, Vol. 25, pp. 109-122; ©North-Holland Publishing Company SPONGE PREDATION IN THE OYSTER REEF COMMUNITY AS DEMONSTRATED WITH CL/ONA CELATA Grant VINCENT G. GUIDA Department of Zoology, North Carolina State University, Raleigh, North Carolina, U.S.A. Abstract: Predation by various invertebrates on the burrowing sponge, Cliona celata Grant, wa investigated both in the laboratory and field, in order to determine the importance of predation t ' snonge nonulation and the adaptive advantage of burrowing to escape predators. Thirty-one sper NORTH HOLLAND AMSTERDAM J. exp. mar. Biol. Ecol., 1976, Vol. 25, pp. 109-122; © North-Holland Publishing Company SPONGE PREDATION IN THE OYSTER REEF COMMUNITY AS DEMONSTRATED WITH CLIONA CELATA Grant VINCENT G. GUIDA Department of Zoology, North Carolina State University, Raleigh, North Carolina, U.S.A. Abstract: Predation by various invertebrates on the burrowing sponge, Cliona celata Grant, was investigated both in the laboratory and field, in order to determine the importance of predation to a sponge population and the adaptive advantage of burrowing to escape predators. Thirty-one species -0fmolluscs, crustaceans, polychaetes, and echinoderms commonly found on oyster beds in Beaufort, North Carolina were tested for their ability to prey on C. celata. Gastropods Diodora cayenensis Lamarck, Seila adamsi, H. C. Lea and Doriopsilla pharpa Marcus, isopod Cilicaea caudata (Say), decapods Alpheus heterochaelis Say, Panopeus herbsti Milne Edwards, Neopancpe sayi (Smith) Eurypanopeus depressus (Smith), Menippe mercenaria (Say) and Pilumnus sayi Rathbun, and echinoids Arbacia punctulata (Lamarck) and Lytechinus variegatus (Lamarck) were all found to ingest sponge. Diodora, Seila, Doriopsilla, Cilicaea, Alpheus and Arbacia frequently eat sponges in nature. All sponge predators were able to obtain sponge ventilation papillae, which ex.tend beyond the surface -0f the shell housing the sponge. Papillae lost to predation were regenerated within 12 days in Cliona celata; little regeneration was noted in predator-damaged Haliclona permollis (Bowerbank), a non­ burrowing sponge. Only Arbacia was able to breach sponge galleries in the shell and destroy Cliona celata 2 to 3 times faster than growth could replace lost sponge tissue. The paucity of subtidal shelly bottom sponge fauna and cryptic or high intertidal habits of oyster bed sponges in Beaufort Harbor :suggest at least partial control of populations of several common sponges by predators. INTRODUCTION This work was undertaken to investigate predation on the burrowing sponge, Cliona celata Grant, by common invertebrates in the oyster reef community at Beau­ fort, North Carolina, to determine whether the burrowing habit of C. celata is an adaptation for reduction of predation and to consider the controlling influence of predation on sponge populations. Until recently, the role of sponges in marine benthic communities has received little attention despite the prominence of the Porifera among the benthos. There are several reasons for the dearth of information. Being less obvious and perhaps having few predators, sponges have been considered of minor importance to energy cycling and community structure. Difficulty with sponge taxonomy has necessitated that most poriferan ecology be done by sponge taxonomists (Annandale, 1915; Laubenfels, 1947; Hartman, 1957; Wells, Wells & Gray, 1964; Riitzler, 1965, 1970; Sara, 1970). As a result, the interaction of sponges with animals other than sponges has been largely ignored. Only Dayton, Robilliard, Paine & Dayton (1974), in their study of an antarctic benthic habitat, have successfully integrated sponge ecology into that of of the community. They showed that sponge-eumetazoan interactions can be im­ portant in energy flow and community structure by virtue of the role of sponges as a 109 110 VINCENT G. GUIDA food source for several common predators and the role of predators as disturbance factors for the sponge populations. The burrowing habit of C. celata suggests protection against some kind of distur­ bance. Clionid sponges, although in many respects typical demosponges, are peculiar in that they live within galleries which they excavate in hard, calcareous substrata, e.g., shell, coral, and limestone. Laubenfels (1947) thought that clionid burrowing may be an adaptation for surviving periods of low salinity, but offered no supporting evidence. Since infaunal habits of prey species often serve to reduce predation, the burrowing habit of Clione may well serve this same purpose. C. celata is one of several common intertidal sponges in Beaufort Harbor (Lauben­ fels, 1947). Sub3tantial populations of several species of sponge within the diverse oyster reef community at Beaufort (Wells, 1961) parallels the situation in McMurdo Sound (Dayton et al., 1974 ), suggesting a similarity in the factors disturbing sponge populations. Although fluctuations in physical conditions undoubtedly affect sponges more in Beaufort than in McMurdo Sound, biotic factors also may play vital roles at Beaufort. MATERIALS AND METHODS DESCRIPTION OF THE AREA All collections and field studies were made on oyster beds around Pivers Island, in the Sluiceway, and Prytherch's Marsh, all in Beaufort Harbor, North Carolina (Fig. 1). Oyster reefs in this area span the intertidal and shallow subtidal zones (to :::::: 10 cm below M.L.W.) and consist largely of shells of living and dead oysters, Crassostrea virgirdca (Gmelin), with smaller numbers of Ostrea equestris Born and Mercenaria mercenaria (L. ). Concrete rubble and a sea wall surrounding most of Pivers Island also provide settlement space for the hard-bottom community. The underlying substratum is mud or sandy mud. Water temperatures vary from :::::: 2° to 35 °C annually and salinities generally from 20 °I 00 to 35 °I 00 with occasional values < 10 °/ 00 during severe storms. No such storms were encountered during the course of this work. Tides are semidiurnal and have a range of :::::: 1.5 m. A more complete description of the physical and biotic condition on Beaufort oyster reefs may be found in Wells (1961). IDENTIFICATION OF SPONGIOVORES AND TESTING OF THE ADAPTIVENESS OF BURROWING The ability to ingest C. celata was tested in two laboratory experiments. The first was an 'exposed' sponge predation test. Potential spongiovores included all species of small ( < 5 cm in their largest dimension) motile macro-invertebrates found at more than one site during more than one collecting trip together with all echinoids regardless of size. Individuals were first starved until fecal elimination ceased (3-14 days) before being used for the 'exposed' sponge predation test. Large portions of the gallery roofs of shells riddled with C. celata were chipped away with a dissecting SPONGE PREDATION ON OYSTER REEFS 111 needle to render sponge tissue easily acce3sible. Potential spongiovores and oyster shells were placed together in finger bowls of various sizes with aerated sea water and maintained at 20-25 °C under a natural summer light-dark cycle. Except in the case of decapods where to avoid cannibalism single animals were used, several individuals of any species were placed in each bowl. Tests generally lasted 20 to 83 hours. Tests in which species did obvious damage to sponges were terminated earlier. After each experiment, potential spongiovores were superficially cleaned and boiled in concen­ trated nitric acid (15.7 N) to eliminate all organic and calcareous remains, leaving only any siliceous gut contents. The presence of 50 or more siliceous sponge spicules and/or spicule fragments in the residue from a single animal was arbitrarily regarded as evidence of sponge ingestion. Microscopic inspection for spicules was done at x 20 magnification. BOGUE BANKS 1km Atlantic Ocean Fig. l. Map of Beaufort Harbor: 1, Prytherch's Marsh; 2, the Sluiceway; 3, Pivers Island; 4, More­ head City Turning Basin; 5, Taylor Creek. The second laboratory experiment was a detritus-free sponge predation test and was designed to determine whether any detritus-feeders in the previous experiment 112 VINCENT G. GUIDA had ingested spicule-containing detritus from the surface of the shell. Only species ingesting spicules in the first test were further investigated. Doriopsilla pharpa Marcus, a known spongiovore (Marcus, 1961), and xanthid crabs Pilumnus sayi Rathbun and Menippe mercenaria (Say), close relatives of other spicule-ingesting xanthids in the previous experiment, were also tested. Species doing visible damage to C. celata in the exposed test were not subjected to the detritus-free test. This detritus-free experiment was conducted similar to the exposed predation studies, except that the sponge tissue was completely excised from the shell and the predator and sponge held away from the bottom of the test chamber by a fiber glass window screen (0.8 mm mesh openings), so that loose spicules would fall out of reach of the animal. The ability of spongiovores to attack C. celata in its burrowing habit and the capacity of that habit to reduce predation were tested in the unexposed sponge predation test. Species which ingested sponge in the detritus-free test together with those excluded from it because of obvious damage done to sponges in the exposed test were used. The unexposed sponge predation test was conducted much like the exposed test except that sponge galleries were unaltered. Three individuals of the echinoid Arbacia punctulata (Lamarck) were provided