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 with the non-burrowing sponge Haliclona permollis (Bowerbank) instead of C. celata to compare the effects of echinoid on both burrowing and non-burrowing sponges. Confirmation of sponge predation in the field for the same species which ate sponges in the laboratory was made by analysis of feces of freshly-collected animals. Potential predators were weighed, placed in finger bowls and their feces removed daily until there had been no defecation for 24 h. Feces were treated with HN03 and inspected. Distinction between individual predators that had eaten sponge and those that had obtained spicules from sediments or detritus in the field analysis was made based on comparative spicule content of sediment and sponge tissue samples. Both sediment and sponge tissue samples were treated with HN03 and spicules counted as before. Digested sponge tissue required a I: 2500 or I: 5000 dilution for counting at x 20. Mean spicule or spicule fragment lengths were calculated from measurement of 50 ran­ dom spicules at x 200. Mean lengths of spicules from fecal samples were similarly deter­ mined. Since sponge tissue contains 10 3 to 104 times as much spicule material/g dry weight as sediments, an adequate criterion for predation on sponges for individual predators was based on the amount of spicule material (count x mean length) in the feces. I assume that an animal would not ingest more than its own weight in sediment; if its feces contained more than enough spicules to account for its own live weight in dry sediment, the animal was presumed to have eaten sponge, not sediment.

DETERMINATION OF THE EFFECTIVENESS OF SPONGE PREDATORS Transects were established and sampled on the Sluiceway oyster reefs in October 1974 and February 1975 to estimate the population densities of clionid sponges and their predators near the ends of the warm and cold seasons. Transects were set up SPONGE PREDATION ON OYSTER REEFS 113 perpendicular to the shoreline at randomly chosen sites. Six or seven quadrats, 50 x 25 cm, were arranged end to end along transect lines and all material above the sediment-water interface removed. Spongiovores were removed from the oyster shell and identified. The volume of C. celata tissue in the shell was determined by the method of Warburton (1958). The population density of the sea urchin Arbacia was determined in three 1 x 2 m quadrats along the shore of Pivers Island during December 1975. Assessment of predator disturbance effects in the field was made by comparing the growth and survival of C. celata with and without predators. Predator-free growth studies were made using individually tagged C. ce/ata-riddled shells. I placed these in two perforated aluminum cages (round holes, 4 mm diam.), each with a retaining screen near the bottom to prevent burial in silt and a screen top to exclude predators. Both screens were of DuPont Vexar (mesh size 11x15 mm). Cages were suspended from a dock at Pivers Island a few centimeters below the level of the lowest annual low tide. Growth under predation was studied by placing tagged, sponge-riddled shells in an open fiber glass pan (60 x 50 x 8 cm) resting on the bottom at the same tidal level as the cages and about 3 m away from them. Shells from cages and pans were removed monthly, cleaned of accumulated 'fouling', and weighed underwater. This method allows shells to be weighed independently of mollusc (and sponge) tissues (Andrews, 1961). From the changes in shell weight in shells of dead oysters containing Cliona the growth of the sponges may be estimated from the loss in shell weight which is due to new gallery excavation.

RESULTS

IDENTIFICATION OF SPONGIOVORES AND TESTING OF ADAPTIVENESS OF BURROWING Of thirty species of molluscs, crustaceans, polychaetes and echinoderms tested, gut spicule counts showed the keyhole limpet Diodora cayenensis Lamarck, the cerithid snail Seila adamsi H. C. Lea, the isopod Cilicaea caudata (Say), the snapping shrimp Alpheus heterochaelis Say, the grass shrimp Palaemonetes vulgaris (Say), the xanthid crabs Panopeus herbsti Milne Edwards and Neopanope sayi (Smith), the sea urchins Arbacia punctulata (Lamarck) and Lytechinus variegatus (Lamarck), and possibly the brittle star Ophiothrix angulata (Say) had eaten C. celata made readily available by exposure (Tables I and II). The sea urchins Arbacia and Lytechinus were the most destructive spongiovores, completely consuming the sponges and part of the surrounding shell (Table II). Of the nine species tested in the detritus-free exposed sponge predation test, seven ate C. celata (Table III, column 1). Cilicaea, Alpheus, Palaemonetes, Panopeus and Neopanope, which consumed sponge tissue in the exposed test, were also found to ingest sponge tissue in the detritus-free study, suggesting that these species consumed tissue and not detritus during both tests. Two new additions to the list of possible spongiovores, Menippe and Pilumnus, ate Cliona in· the detritus-free test. One 114 VINCENT G. GUIDA

TABLE I

Exposed sponge predation tests: spicules in guts of various invertebrates provided with exposed C. celata tissue.

No. No. cont. Major taxon Species tested 50 spicules

Amphineura: Chaetopleura apiculata Sa) 4 0 Gastropoda: Diodora cayenensis Lamarck 12 +a Bittium varium Pfeiffer 71 0 Cantharus tinctus Conrad 10 0 Seila adamsi H. C. Lea 21 +a Mitrella lunata Say 12 0 Fasciolaria hunteria (Perry)' 10 0 Crassispira ostrearum Stearns 22 0 Odostomia seminuda C. B. Adams 26 0 Doriopsilla pharpa Marcus 3 0 Isopoda: Cilicaea caudata (Say) 3 Amphipoda: Lembcs sp. 6 0 Melita nitida Smith 2 0 Melita appendiculata (Say) 4 0 Decapoda: Alpheus heterochaelis Say 16 13 Palaemonetes vulgaris (Say) 3 Clibanarius vittatus (Bose) 2 0 Panopeus herbsti Milne Edwards 28 9 Neopanope sayi (Smith) 2 2 Eurypanopeus depressus (Smith) 8 0 Pilumnus sayi Rathbun 1 0 Polychaeta: Nereiphylla fragilis (Webster) 8 0 Lepidonotus sublevis Verrill 3 0 Eunice rubra Grube 7 0 Marphysa sanguinea (l'vfontagu) 6 0 Nereis succinea (Frey & Leuckhart) and N. occidentalis Hartman 5 0 Ophiuroidea: Ophiothrix angulata (Say) 10

1 Only immature animals. a Gut contents of individuals pooled for counting; several with > 50 spicules.

TABLE II

Exposed sponge predation test for echinoids Arbacia punctulata (Lamarck) and Lytechinus variegatus (Lamarck): loss of wet weight.

No. % wt loss Sponge Predator individuals (shell +sponge)

Al A. punctulata 8 21 A2 A. punctulata 8 21 LI L. variegatus 4 18 c Control 0 SPONGE PREDATION ON OYSTER REEFS 115 individual each of Alpheus and Menippe were observed ingesting pieces of sponge. The failure of Ophiothrix to ingest C. celata in the detritus-free test indicated that it had not obtained spicules from sponge in the exposed test, but rather from detritus: this species was not, therefore. tested further.

TABLE III

Detritus-free exposed and unexposed sponge predation tests and field fecal analysis results: no. of spongiovores tested and those positive for sponge ingestion based on spicule content of guts/feces.

2 3 Detritus-free Unexposed Field fecal Major !axon/species ------No. No. No. No. No. No. tested + tested + tested ' Gastropoda Diodora cayenensis 6 6 8 8 Seila adamsi 6 5 Doriopsilla pharpa 6 0 11 9 Isopoda Cilicaea caudata 9 3 6 0 12 12 Decapoda Alpheus heterochaelis 1 4 2 9 7 Palaemonetes vulgaris 2 15 0 Panopeus herbsti 8 5 5 31 6 Neopanope sayi 5 2 I 0 2 0 Eurypanopeus depressus 7 2 7 3 Menippe mercenaria 1 3 2 3 0 7 2 Pilumnus sayi 2 2 2 2 Echinoidea Arbacia punctulata 3 3 8 8 Lytechinus variegatus 2 2 6 Ophiuroidea Ophiothrix angulata 3 0

1 Immature animals only: a unavailable at time of test: b inflicted obvious damage on sponges: test unnecessary: c eliminated due to failure to demonstrate predation in previous test.

At first glance, C. celata's burrowing habit did not appear to deter seven of the ten spongiovores studied in the unexposed sponge predation test (Table III, column 2). Diodora, Alpheus, Panopeus, Eurypanopeus, Pilumnus, Arbacia and Lytechinus were able to consume sponge tissue despite Cliona's infauna] habit. Small predator sample size may account for the failure of Cilicaea, Neopanope and Menippe to ingest Cliona in this test. Close examination of the sponge-riddled shells from the unexposed sponge test shows, however, that the shell does afford Cliona some protection. Sponge oscular and ostial papillae, which normally extend ::::::' 1 mm beyond the surface of the shell, were eaten down to the shell surface by Alpheus, the xanthid crabs, Arbacia and Lytechinus and to just below the surface by Diodora. Only Arbacia breached 116 VINCENT G. GUIDA

the gallery roof in one instance to take a small part of the contained sponge. Com­ pared to complete destruction of Cliona by Arbacia and Lytechinus in the exposed test, the damage done to unexposed Cliona by these species was slight. The adaptiveness of having only ventilation structures exposed, as in the case of Cliona, relative to their being entirely exposed to predation as is the case for Haliclona permollis, depends to some extent on the rate of recovery from damage. C. celata papillae lost to predation in the unexposed sponge predation test regenerated com­ pletely after 12 days in running sea water, but H. permollis, a non-burrowing sponge exposed to Arbacia predation (data not included in Table III), showed little regenera­ tion and soon died. Predation on Cliona, though not prevented, is inhibited by the burrowing habit, and sponge survival is enhanced. Analysis of the feces of spongiovores collected in the field indicated that all species, except Palaemonetes and Neopanope, found to eat burrowing sponges in the labora­ tory did so in the field (Table III, column 3). I suspect the predator sample size was inadequate in the two exceptions. Doriopsilla, a nudibranch which failed to eat C. celata in laboratory tests, was, however, found to ingest sponges in the field. Either experimental conditions in the laboratory were unsuitable for the mollusc or C. celata is not a preferred prey species. Prey species were not identifiable from predator gut contents, since spicules in the guts were fragmented and whole spicules are necessary for sponge identification. The results of the field study allow separation of sponge predators into two groups, namely, those which frequently have spicules in their guts (> 60 % of the individuals were positive for spicules) e.g., Diodora, Seila, Doriopsilla, Cilicaea, Alpheus, and Arbacia, and those which occasionally have spicules in their guts ( < 25 % of the individuals were positive for spicules) e.g., the xanthids and Lytechinus. The first category represents those animals for which sponges are important as an energy source and the second those which consume sponges but for which the latter are only an incidental food source.

DETERMINATION OF EFFECTIVENESS OF SPONGE PREDATORS The relative importance of various predators to the C. celata population is depen­ dent on the densities of the predators and their feeding rates. High year-round densities of Diodora, Alpheus, and Panopeus suggest the possibility of an appreciable predation effect (Table IV). Around Pivers Island, where meanArbacia density was 3.7 m2 (s.D. = ± 0.3, n = 3), an appreciable predation effect also is anticipated. This population density remained nearly constant throughout 1975. Although feeding rates are not available for most sponge predators, an estimate of in situ predation on C. celata by Arbacia was made based on the amount of shell destroyed by this echinoid's attempts to obtain the sponge from the galleries (see p. 113). Arbacia sponge feeding rates were compared to calculated growth potentials for the damaged sponges and for all the sponges in the experimental pans. The SPONGE PREDATION ON OYSTER REEFS 117

TABLE IV

2 Densities of spongiovores (no./m ) from October and February on Sluiceway transects.

Density Species 15.x.74 26.ii.75

Diodora cayenensis 34.3 24.0 Seila adamsi 5.7 8.0 Doriopsilla pharpa 2.3 8.0 Cilicaea caudata 1.1 <0.8 Alpheus heterochaelis 19.4 18.7 Panopeus herbsti 51.4 32.0 Neopanope sayi 2.3 <0.8 Eurypanopeus depressus 18.3 <0.8 Menippe mercenaria 1.1 <0.8 Pilumnus sayi 1.1 <0.8 Unidentified xanthids 1 26.3 6.7 Arbacia punctulata 1.1 <0.8 Lytechinus variegatus <0.8 <0.8

1 Too small for accurate identification.

results indicate that the urchins ate several times as much sponge as the prey popula­ tion could produce during September and October 1975 (Table V) so that a high density Arbacia population could control a Cliona population. Population density of C. celata at the start of this experiment was 400-500 ml sponge m - 2 and decreased at a rate of 12 % per month as a result of predation. Densities on the Sluiceway reef transects, where Arbacia are scarce (Table IV), were 1700 and 1300 ml sponge m - 2 for October 1974 and February 1975, respectively. Such a dense prey population could not have developed at Pivers Island where even much more rarified prey densities are unstable due to heavy sea urchin predation.

TABLE V

Cliona growth under predation experiment: rates of consumptian of C. celata by Arbacia compared with potential rates of growth of the sponges in experimental pan (area= 0.3 m 2 ): estimates of total sponge and sponge consumption rates assuming that sponges occupy 30 % of the volume of the shells they inhabit and, therefore, 30 % of the volume of shell destroyed by Arbacia: estimates of growth potential calculated by using % growth of sponges from the predator-free sponge growth study to the attacked sponges only, and to all sponges in the growth under predation study, respec- tively.

Estimated Estimated Estimated Estimated total sponge sponge sponge growth sponge growth present at consumption potential for potential for Month beginning of rate preyed-upon all sponges in period sponges study (ml) (ml/month) (ml/month) (ml/month)

9/75 146.3 17.9 3.7 6.7 10/75 128.4 15.5 2.0 4.8 118 VINCENT G. GUIDA

DISCUSSION

Predation on sponges is vitally important to our understanding of the food resources in benthic systems and of sponge population control, yet this phenomenon has been overlooked or underestimated because of the assumption that few animals eat sponges. Predation on sponges has been attributed to a few specialized gastropods, dorid nudibranches (e.g. Doriopsilla) and cerithid snails (e.g. Seila) (Wells, Wells & Gray, 1964 ), and some grazing molluscan generalists, such as chitons, littorines, patellid limpets and fissurellid limpets (e.g. Diodora) (Hartman, 1958; Hyman, 1967). No previous report has been found in the literature of detritivorous and/or carniv­ orous crustaceans eating sponges. Some symbiotic associations between sponges and alpheid shrimp are known, but predation has not been suggested (Knowlton, 1970). Powell & Gunter (1968) worked on feeding habits of Menippe, but no mention was made of sponges. Patton (1974), although he did not state that the alpheids and xanthids he studied ate sponges, mentioned that sponge spicules were the second most common item in the animal guts. Echinoids have been known to eat sponges, even destroying limestone to obtain the burrowing sponges within (Neumann, 1966), but urchin predation has been treated only sporadically. Eucidaris tribuloides was found to prefer Cliona lampa to fish or algae as food (McPherson, 1968). Reiswig (1974) also mentioned the spongiovorous habits of this echinoid. Arbacia punctulata showed a preference for the sponges Microciona prolifera and Haliclona canaliculata over various nonsponge 'fouling' organisms (Karlson, 1975). The data I have presented clearly indicate that sponges are not eaten by only a a few rare specialists, but also by common generalists. The Porifera have an im­ portant role in the diets of the generalists Diodora, Cilicaea, Alpheus and Arbacia as well as the specialists Seila and Doriopsilla, so that sponges are potentially quite important to community structure and energy flow in the oyster reef community. Some qualitative statements here are possible. Arbacia is by far the most voracious predator of C. celata and probably of other sponges as well. This one predator maintains the densities of burrowing sponges on Pivers Island well below those possible in its virtual absence the Sluiceway reef. Because it is a generalist, capable of eating almost any 'fouling' organism (Karlson, 1975), Arbacia can rely on other sources of nutrition if sponges are too scarce or too difficult to obtain. This allows the pori­ feran prey to survive at a low population density or in places difficult of access. One such habitat is in lightly-burrowed shells, and Arbacia appears to prefer heavily­ burrowed shells as a source of burrowing sponges. These shells are easier for the echinoid to break since the sponge has already weakened the shell with extensive galleries, and they would yield more nutritive material for the amount of non-nutritive shell material ingested. Clionids, then, probably grow with little threat of complete destruction by urchins until they have weakened the shell they inhabit sufficiently to allow easy access to Arbacia. Beyond this point these sponges incur increasing risk of predation as they slowly destroy the shell. SPONGE PREDATION ON OYSTER REEFS 119

Although predators other than Arbacia cannot completely consume Cliona as Arbacia does, these predators may well be able to completely consume non-burrowing sponges, including non-burrowing clionids. Burrowing C. celata (alpha stage) has the potential ability to grow out of its galleries, cover the surface of the shell (beta stage), and eventually destroy the shell completely, becoming a massive, free-living sponge (gamma stage). Neither beta nor gamma stage sponges ever have been observed in Beaufort Harbor by George & Wilson (1919), Laubenfels (1947) or myself. The beginnings of beta stage overgrowth were, however, observed in spring and fall of 1975 in my predator-free sponge growth study, where predators were denied access to the sponges. This would imply that predation prevents development of beta and non­ burrowing gamma stage C. celata. What happens to shells filled with sponge tissue which cannot proceed to the beta stage is not known. No shells from the Sluiceway transects had more than 55 % of their original volume replaced by Cliona tissue, and few had more than 50 %. Prevention by predators of beta stage overgrowth might eventually kill a sponge which cannot continue growing in the alpha mode. The relative importance of predation to Cliona compared with other disturbance factors is substantial. Among biotic factors affecting the C. celata population, competition is unimportant. Five other species of Cliona found on the Sluiceway reef (Wells, 1959) are apparently not serious substratum competitors because they were found to inhabit only about half of the available shell. I have found no signs of competitive interactions between C. celata and other non-sponge shell burrowers (spionid polychaetes and mytilid pelecypods) or surface 'fouling' organisms. Clionid ventilation papillae were seen growing through patches of encrusting sponges of other species without apparent harm to either poriferan, suggesting benign epizoism (Rutzler, 1970). Competition for food between C. celata and other nannoplankton filter feeders is unlikely. Marked stability in the C. celata population on the Sluiceway beds despite wide fluctuations in air and water temperature, wave action, light intensity and tidal range associated with seasonal changes at Beaufort, argues against control of this sponge by physical factors. The October mean burrowing sponge abundance was 55.6 ml sponge tissue kg- 1 shell; in February it was 53.0, a difference of only 4.9 %. If sponges were being killed by some physical agency, a substantially lower sponge population density would be expected in February. Since there is no growth or larval settlement from October to February (Hartman, 1958) to offset mortality, similar densities in these two months must represent a high survival rate in spite of any physical :fluctuations. Karlson (1975) found aperiodic :fluctuations in the abundance of H. canaliculata, M. prol(fera and Halichondria bowerbanki which were independent of Arbacia density and which he suspected were caused by physical-chemical changes. If these fluctuations were decreases in salinity (Laubenfels, 1947), they would not have adversely affected C. celata, since continuous salinity records from Pivers Island show no salinities < 18 °/ 00 for 1972 through 197 5, well within the tolerance of the burrowing sponge (Hartman, 1958). 120 VINCENT G. GUIDA

Given the generally superior compet1t1ve pos1t10n of sponges in the 'fouling' community (Hartman, 1958; Goodbody, 1961; Ri.itzler, 1975) and the lack of severe physical disturbance over the last 3 years, a great increase in sponge prominence would be expected, especially in a species as long-lived and influential as C. celata, which can monopolize a shelly bottom (Driscoll 1967, Nicol & Reisman, 1976). Though the possibility of control of sponge populations by some physical factor independent of seasonal and salinity fluctuations has not been ruled out, predation seems a more plausible choice of controlling factors, especially where Arbacia is present. Recogni2fog the importance of predation as a potential controlling factor in sponge populations, a re-examination of the peculiarities of sponge distribution in Beaufort Harbor (Laubenfels, 1947) is in order. Dredgings from the Morehead City Turning Basin and Taylor Creek (Fig. 1) confirm Laubenfel's observations that sponges are notably lacking on subtidal shelly bottoms. Clionids were present, but they were much less frequent than in the intertidal zone. Much bare shell was en­ countered. The occasional freshets mentioned by Laubenfels do not explain this phenomenon, since there have been no freshets for several years. The sponge preda­ tors Arbacia, Lytechinus and xanthid crabs, however, were numerous and could possibly limit sponge populations in these subtidal areas. The distribution of sponge in the intertidal and near subtidal zones also supports the hypothesis that predation limits sponge populations in the Beaufort area. As Laubenfels (1947) noted, sponges are common in these areas. M. prolifera, H. permollis, Adocia tub ifera (George & Wilson) and Haliclona sp. (H. canaliculata and/or H. loosanoffi Hartman) are all small, encrust­ ing forms frequently found in crevices and on undersides of shells and concrete blocks. Cliona spp. were found in their burrowing stages only. M. prolifera was never seen with its typical upright, finger-like adult growth form in the area investigated, but rather, always as a fiat, red crust on the substratum. I suggest that M.prolifera is never allowed to attain its upright form, just as C. celata is never allowed to attain its gamma stage, because any such easily accessible growths are destroyed by predators as they develop, or possibly because the sponges are completely destroyed before they can attain these advanced growth forms. Haliclonids, the only other sponges as ubiquitous as the clionids in the lower harbor, may be afforded protection from predation by their small size and cryptic habits. The same can be said of the clionids. The frequency of intertidal sponges contrasted with the scarcity on shelly bottoms deeper than 10 cm below M.L.W. lends support to the predation control hypothesis. Arbacia and the molluscan spongiovores can graze continuously in subtidal areas, but only intermittently in the intertidal zone because of their inability to withstand prolonged exposure to air. More exposure-tolerant crustacean spongiovores become inactive during low tide. Hymeniacidon heliophila (Parker), the one sponge found that does commonly develop an obvious, exposed, upright growth form, was abundant only in marshes, high up in the intertidal zone, where few predators can venture. Around Pivers Island, where conditions for predators are more favorable, only rare., isolated colonies of H. heliophila were found. SPONGE PREDATION ON OYSTER REEFS 121

ACKNOWLEDGMENTS I wish to gratefully acknowledge the staff of the National Marine Fisheries Service, Atlantic Estuarine Fisheries Center, Beaufort, N. C. for the most generous extension of laboratory space, material, personal aid and editorial services without which this study would not have been possible. Special thanks are due Dr T. G. Wolcott for his aid during the initial organization and planning of this research. Thanks, too, are due the marine ecologists of Duke University Marine Laboratory for so many stimulating discussions of biotic interactions. This research has been supported m part by the Marine Sciences Curriculum of North Carolina State University.

REFERENCES

ANDREWS, J. D., 1961. Measurement of shell growth in oysters by weighing in water. Proc. natn. Shel~fish. Ass., Vol. 52, pp. 1-11. ANNANDALE, N., 1915. Some sponges parasitic on Clionidae with further notes on that family. Rec. Indian Mus., Vol. 10, pp. 457-478. DAYTON, P. K., G. A. RoBILLIARD, R. T. PAINE & L. B. DAYTON, 1974. Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol .•'lfonogr., Vol. 44, pp. 105-128. DRISCOLL, E. G., 1967. Attached epifauna-substrate relations. Limnol. Oceanogr., Vol. 12, pp. 633-641. GEORGE, W. C. & H. V. WILSON, 1919. Sponges of Beaufort (N.C.) Harbor and vicinity. Bull. Bur. Fish., Wash., Vol. 36, pp. 129-179. GooDBODY, I., 1961. Inhibition of development of a marine sessile community. Nature, Land., Vol. 190, pp. 282-283. HARTMAN, W. D., 1957. Ecological niche differentiation in the boring sponges (Clionidae). Evolution, Lancaster, Pa., Vol. 11, pp. 294-297. HARTMAN, W. D., 1958. Natural history of the marine sponges of southern New England. Bull. Peabody Mus. nat. Hist., No. 12, 155 pp. HYMAN, L. H., 1967. Mollusca I. The Invertebrates, Vol. 6. McGraw-Hill Book Co., New York, 792 pp. KARLSON, R. H., 1975. The effects of predation by the sea urchin Arbacia punctulata on a marine, epibenthic community. Ph.D. thesis, Duke University, Durham, N.C., 133 pp. KNOWLTON, R., 1970. Effects of environmental factors on the larval development of Alpheus hetero­ chaelis Say and Palaemonetes vulgar is (Say) (Crustacea Decapoda Caridea), with ecological notes on larval and adult Alpheidae and Palaemonetidae. Ph.D. thesis, University of North Carolina, Chapel Hill, N. C., 513 pp. Laubenfels, M. W. de, 1947. Ecology of sponges of a brackish water environment, at Beaufort, N. C. Ecol. Monogr., Vol. 17, pp. 32-46. MARCUS, E., 1961. Opisthobranchia from North Carolina. J. Elisha Mitchell scient. Soc., Vol. 77, pp. 141-151. McPHERSON, B. F., 1968. Feeding and oxygen uptake of the tropical sea urchin Eucidaris tribuloides (Lamarck). Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 135, pp. 308-321. NEUMANN, A. C., 1966. Observations on coastal erosion in Bermuda and measurement of the boring rate of the sponge, Cliona lampa. Limnol. Oceanogr., Vol. 11, pp. 92-108. NICOL, W. L. & H. M. REISMAN, 1976. Ecology of the boring sponge (Cliona celata) at Gardiner's Island, New York. Chesapeake Sci., Vol. 17, pp. 1-7. PATTON, W. K., 1974. Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In, Symbiosis in the sea, edited by W. B. Vernberg, Uni­ versity of South Carolina Press, Columbia, South Carolina, pp. 219-243. PowELL, JR, E. H. & G. GUNTER, 1968. Observations on the stone crab Menippe mercenaria Say in the vicinity of Port Aransas, Texas. Gulf Res. Rep., Vol. 2, pp. 285-299. 122 VINCENT G. GUIDA

REISWIG, H. W., 1974. Water transport, respiration and energetics of three tropical marine sponges. J. exp. mar. Biol. Ecol., vol. 14, pp. 231-249. RDTZLER, K., 1965. Substratstabilitat im marinen Benthos als okologischer Faktor, dargestellt am Beispiel adriatischer Porifera. Int. Revue ges. Hydrobiol., Bd 50, pp. 281-292. RVTZLER, K., 1970. Spatial competition among Porifera: solution by epizoism. Oecologia, Berl., Bd 5, S. 85-95. RDTZLER, K., 1975. The role of burrowing sponges in bioerosion. Oecologia, Berl., Bd 19, S. 203-216. SARA, M., 1970. Competition and cooperation in sponge populations. In, The biology cf the Porifera, edited by W. G. Fry, Symp. zool. Soc. Lond., No. 25, pp. 273-284. WARBURTON, F. E., 1958. The effects of boring sponges on oysters. Prag. Rep. Atlant. Cst Stns, No. 68, pp. 3-8. WELLS, H. W., 1959. Boring sponges (Clionidae) of Newport River, North Carolina. J. Elisha Mit­ chell scient. Soc., Vol. 75, pp. 168-173. WELLS, H. W., 1961. The fauna of oyster beds with special reference to the salinity factor. Ecol. Monogr., Vol. 31, pp. 239-266. WELLS, H. W., M. J. WELLS & I. E. GRAY, 1964. Ecology of sponges of Hatteras Harbor, North Carolina. Ecology, Vol. 45, pp. 752-767.