Caribbean and Pacific stocks invaded the market with cheapest low quality products ... the sheltered Bay of Vathi, hosting 30 floating cages for fish farming and.
5th INTERNATIONAL SPONGE SYMPOSIUM 1998 BRISBANE, AUSTRALIA SPONGE FARMING IN THE MEDITERRANEAN SEA: NEW PERSPECTIVES ROBERTO PRONZATO1, GIORGIO BAVESTRELLO4 CARLO CERRANO1, GIUSEPPE MAGNINO1, RENATA MANCONI3, JANNIS PANTELIS2 ANTONIO SARA1, MARZIA SIDRI1 1. Istituto di Zoologia, Universita, V. Balbi 5, 16126 Genova, Italy. 2. Secretariat of Fishery and Sponge fishery Municipality of Kalymnos, GR 85200, Greece. 3. Dipartimento di Zoologia ed Antropologia Biologica dell'Universita, V. Muroni 25, I 07100 Sassari, Italy. 4. Istituto di Scienze del Mare dell'Universita,Via Brecce Bianche 1, 68031 Ancona, Italy Some Mediterranean sponge species, belonging to the genera Spongia and Hippospongia are characterised by a soft and absorbent skeleton and usually harvested for commercial purposes. Recently, the synergetic action of a widespread epidemic together with overfishing, strongly reduced the density of sponge banks, leading these species into the brink of extinction. Moreover the recovery of banks needs a long time and now, after several years, sponge density is still very low. A simple solution to this problem is sponge-farming. Sponges are sessile filter feeding organisms and because of their pumping activity they are able to retain bacteria and suspended organic matter (SOD) from the entire water-column in littoral marine environments. This ability could be basic for an integrated aquaculture of sponges and fish in coastal areas: floating-cage fish farms release a lot of organic wastes that can be recycled as a rich source of food for surrounding commercial sponge intensive cultures. Besides, the interest shown by chemists and pharmacologists in regards of natural products extracted from sponges, could create new possibilities in sponge famming. Aquaculture, organic pollution, overfishing, bath sponges, natural prod,ucts, cicatrisation. INTRODUCTION Commercial horny sponges have been harvested and utilised as bath sponges since ancient times: Phoenicians and Egyptians used to collect stranded sponges along the seashores, while the millenary history of sponge fishery take roots in the ancient Greek civilisation. With the traditional fishing method, fishermen utilised an heavy stone as ballast to reach easily the sea bottom and a net basket to gathered sponges. At the end of the last century, this harvesting system was replaced by divingsuits. The introduction of this device strongly increased the fishing effort, but many divers also died because of the decompression illness: as a consequence many Government forbade it. Only hyperbaric medicine and modern diving equipment solved this problem. Sponge banks density is continuously decreasing both for overfishing and the socalled sponge disease. Oldest professional divers relate the incredible abundance of commercial species in the thirties along the coasts of Cyprus, Crete and Sardinia: more than 200-300 specimens/100 m2. Before the epidemic, not-exploited commercial sponge banks reached densities of about 100 specimens/100 m2 but, at present, the mean density does not exceed in 50 specimens/100 m2 (Pronzato et al, 1996. Pronzato et al, in press). Sponge illnesses do not occur frequently but in the past sponge populations contracted the sponge disease both in the Mediterranean and in the Caribbean Sea. From 1985 to 1988, commercial sponges practically disappeared in a lot of areas, especially in the Eastern Mediterranean Basin, with heavy economic
consequences. Sick sponges are easily recognisable for the exposition of their internal skeleton. Sponge disease is due to invasive pathogenic micro-organisms: first they destroy the sponge external fibrous layer, then they proceed rapidly into the sponge body destroying living tissues. Fibres become fragile and flake off, loosing their characteristic endurance and softness 1989. Pronzato & Gaino, 1991 ; Gaino et al., 1992).There is a synergetic effect, of overfishing on sponge disease because overexploitation might be responsible of the lowering of self-defence mechanisms, increasing the risk of environmental aggressions. Because of the banks impoverishment, from the sixties till 1990, many producers have gone out of business breaking-down to zero the exportation from many Mediterranean countries. The decrease of catches has been directly connected to a sharp increase in price for Mediterranean sponges and, as a consequence, Caribbean and Pacific stocks invaded the market with cheapest low quality products (Verdenal & Vacelet, 1990). Sponge banks recovery is a long lasting process (Rizzitello et al., 1997) infact, ten years after the mediterranean sponge disease, commercial sponges are still rare in many sites as we observed during our experiments. In the last few years, chemical researchers showed an interest in sponge culture because of the presence of natural products useful in pharmacology. Metabolites extracted from Porifera are giving promising results in prevention and treatment of tumours (De Flora et al, 1995) and as antiphlogistic compounds (De Rosa et al., 1995). Moreover, sponge extracts appear in catalogues of laboratory products with very high prices. Our goal is to face the market request of these products without reducing natural populations. This paper reports the preliminary results of two different experiences of sponge-farming. The first one aims to reconvert sponge fishery toward more profitable and environmentally sustainable activity. It has been placed in Kalymnos Island (Dodecanese, Greece) during March of 1998. A second experimental sponge culture for the sake of pharmacology has began in Mediterranean (Paraggi, Ligurian Sea), testing the survival of different non commercial sponge species in farming conditions. MATERIAL AND METHODS The plant of Kalymnos (Dodecanese, Greece: 36058' N; 27°2' E) was situated in the sheltered Bay of Vathi, hosting 30 floating cages for fish farming and placed at 15 m of depth, on a flat bottom,500 m far from the floating cages (Fig. 1). Four metallic horizontal structures were moored to the bottom (Fig. 2); some specimens of Spongia offcinalis var. adriatica and Hippospongia communis were cut into 4 X 4 cm fragments and fixed on a nylon line as pearls in a necklace (Fig. 3A, B). Totally, 350 fragments were spaced out with plastic tubes (7 X 0.6 cm) (Fig. 2). A team of operators controlled every day the plant of Kalymnos for the first week and every ten days for the successive five months. With the same method the plant of Paraggi (Ligurian Sea, Italy. 44°18' N. 9°9' E) was settled on a, flat bottom, at a depth of 25 m. 50 fragments obtained from each of the following species: Agelas oroides, Axinella damicornis, Cacosspongia mollior, Chondrosia reniformis, Ircinia variabilis,Petrosia ficiformis, Spongia agaricina and Spongia offcinalis var. adriatica have been fixed onto the horizontal structures described before; these species are mainly the most common in the rocky cliffs of the Ligurian Sea. During the first week, samples of the cut surfaces were daily collected from both plants (Paraggi and Kalymnos), fixed in Glutaraldheyde 2.5% in ASW, dehydrated in a graded series of ethanol, critical point dried using a Pabish CPD 750, coated with gold using a Balzers SCD 004 and observed using a scanning electron microscope Philips EM 515.
RESULTS AND DISCUSSION Many experimental approaches to the problem of a profitable sponge culture have been performed since the beginning of the century and, at present, some data are irrecusable (See Pronzato, in press,for a review). On the average, in more than two years sponges increase their volume of 100/200 % and generally, smallest fragments show the higher growth rate (Verdenal & Vacelet, 1985). Kalymnos plant. Mortality, lower than 20%, was limited to the first 48 hours after transplantation and Hippospongia communis seems more resistant than Spongia officinalis. In fact, Spongia officinalis shows a survival rate of 69.4% but Hippospongia communis gives excellent results with a percentage of survival of 100% (Table 1). The regenerative process starts immediately and in two-three days sponges rebuild their external protective layer: after 24 hours a thin transparent cell layer covers the cut surfaces (Fig 3C, D) and after one week, also the characteristic dark external pigmentation of the sponge was restored. In one month sponge fragments assumed a rounded shape: the external fibrous layer and the aquiferous system of cutting surfaces are completely reorganised (Fig 3E). Mortality could be due to high sedimentation rates which favours bacterial proliferation: only naked skeletons of dead fragments remain onto the rope (Fig 3F). In agreement with modern integrated aquaculture systems, the association of sponge culture with floating cage fish farms can reduce the environmental impact on coastal areas due to the pollution produced by intensive fish farming (Pronzato et al. 1998). The major impact is on the sea bottom, just under floating cages, where a real 'rain of particles' falls on benthic organisms causing a rapid euthrophisation (decrease of dissolved oxygen and increase of nutrient levels) (Wu, 1995). Food wastes and faecal pellets released by bred fish are rapidly colonized and degraded by bacteria (Honjo and Roman, 1977). Filtering activity of sponges could contribute to reduce this pollution in the boundaries of fish farms as under the cages sedimentation rate is too high. Sponges can retain about 80 % of organic particulate material suspended in the water and about 70 % of bacteria (Reiswig, 1971; 1975) filtering the entire water column in a day (Reiswig, 1974). This integrated aquaculture gives a double result: depurated water and commercial bath sponges. At present the Municipality of Kalymnos, after our first attempt, is planning to farm many thousands sponges in the boundaries of lack floating cages fish farm present along the is1and's coasts. Paraggi plant Among the tested species, Chondrosia reniformis is completely unsuitable for our experimental conditions. The collagen's matrix of this species cut by itself the body on the thread and the sponge 'drips down' in one-two days. This behaviour, recalling that of the collagen's tissue with a variable structure of Echinoderms (Candia Carnevali et al, 1990) is very interesting and is the topic of a recent study (Bavestrello et al , 1998). Axinella damicornis and Ircinia variabilis show a high mortality rate, probably because of the damaging during the cutting phase. In fact Axinella damicornis is very fragile and must be handled with care, while Ircinia is so compact that it is difficult to cut it without squeezing (Table 1). Petrosia ficiformis is the most reactive species. The cut surface produced new pinacoderm in 4-5 days and the survival of the fragments is very close to 100% (Table 1). Percentages of survival of Spongia officinalis and Cacospongia mollior are satisfactory (about 60-80% in two months) and data about Spongia offcinalis are concordant in both of our plants (Table 1).
It is important to underline that environmental conditions, health state of mother sponge and the techniques utilised for transplantation influence survival and growth rate of farmed specimens as suggested in Verdenal & Vacelet (1990). For instance, in their Marseilles farm, the authors found out that Spongia agaricina showed a survival of 100% while we obtained a mortality rate of about 60%.
KALYMNOS ( DODECANESE , GREECE ) S p e c ie s S p o n g ia o f f ic in a lis H ip p o s p o g ia c o m m u n is
n 75 252
S u r v iv a l a f te r 4 8 h o u r s ( % ) S u r v iv a l a f te r 2 m o n th s ( % ) 6 9 .4 6 9 .4 100 100
PARAGGI ( LIGURIAN SEA , ITALY ) Agelas oroides Axinella damicornis Cacospongia mollior Ircinia variabilis Petrosia ficiformis Spongia officinalis Spongia agaricina
46 50 60 50 40 50 49
45.8 0 83.3 2 100 66 42.8
44 0 83.3 1 98 66 40
TABLE 1: percentages of survival of the monitored specimens farmed in Kalymnos and in Paraggi: Hippospongia communis, Petrosia ficiformis and Cacospongia mollior are perfectly suited, while Axinella damicornis and Ircinia variabilis are unsuitab1e. “n” indicates the number of transp1anted fragments. The recovering of the exposed choanosome starts from the borders of the cut and increases concentrically. The reconstruction process differs if the external layer is a real pinacoderm or, as for bath sponges, a fibrous layer without cells. Our experience shows that in Agelas oroides (Fig. 4A,B) and Petrosia ficiformis (Fig. 4E, F) the restoration of the exopinacoderm is completed in two/three days while in Axinella damicornis (Fig. 4C, D) this does not happen. Commercial bath sponges show a lowest mortality rate probably due to their external fibrous layer whose recovering is different. Spherical cells, with long pseudopodia, go along cutting edges producing collagen fibrils and completing the cicatrization process in few days (Fig. 5). The quickness of reconstitution of the new external layer on the cut portions is variable from species to species (2-3 days in Agelas oroides and Petrosia ficiformis; about 10 days in Cacospongia mollior). CONCLUSIONS Commercial sponges are practically disappeared in the Eastern Mediterranean Sea owing to overfishing and sponge disease: spongeculture could decrease the fishing pressure, helping a natural repopulation of these areas. Pharmacological researches on products extracted from sponges are giving promising results, opening new perspectives in the exploitation of new species of Porifera. Data about density of wild sponge banks are not available for the moment and the risk of overfishing on species that could have, in the future, a commercial value could become real. A valuation of the adaptability of the most common Mediterranean species to farming conditions could give a choice to an indiscriminate exploitation of these species too.
LITERATURE CITED BAVESTRELLO G., BENATTI U, CALCINAI B., CATTANEO-VIETTI R., CERRANO C., FAVRE A., GIOVINE M., LANZA S., PRONZATO R. & SARA' M. 1998. Body polarity and mineral selectivity in the Demosponge Chondrosia reniformis. Biological Bulletin 195. in press. CANDIA CARNEVALI M.D., BONASSORO F., WILKIE I.C., ANDRIETTI F. & MELONE G. 1990. Functional morphology of the peristomial membrane of regular sea-urchins: structural organisation and mechanical properties in Paracentrotus lividus in Echinoderm research. Balkema, Rotterdam: 207-216. DE FLORA S., BAGNASCO M., BENNICELLI C., CAMOIRANO A., BOJNEMIRSKI A. & KURLEC B. 1995. Biotransfommation ofgenotoxic agents in marine sponges. Mechanisms and modulation. Mutagenesis 10(4): 357-364. DE ROSA S., CRISPINO A., DE GIULIO A., IODICE C., PRONZATO R. & ZAVODNIK N. 1995. Cacospongionolide B, a new sesterterpene from the sponge Fasciospongia cavernosa. J Nat. Prod. 58. 1776-1780. GAINO E. & PRONZATO R. 1989. Ultrastructural evidence ofbacterial damage to Spongia officinalis fibres (Porifera, Demospongiae). Diseases Aquatic organisms 6: 67)74. GAINO E., PRONZATO R., CORRIERO G. & BUFFA P. 1992. Mortality of commercial sponges: incidence in two Mediterranean areas. Bollettino di Zoologia 59. 79-85. HONJO S. & ROMAN M.R. 1978. Marine copepod faecal pellets: production, preservation and sedimentation. Journal of Marine Research 36(1): 45)57. PRONZATO R. & GAINO E. 1991. La malattia delle spugne commerciali: considerazioni storico) economiche. Bollettino dei Musei degli Istituti di Biologia dell'Universita di Genova 55 : 17)25. PRONZATO R., RIZZELLO R., DESSY E., CORRIERO G., SCALERA LIACI L. 1996. Distribuzione e pesca di Spongia officinalis lungo il litorale Ionico Pugliese. Bollettino dei Musei degli Istituti di Biologia dell'Universita. 60-61: 79)89. RONZATO R., BAVESTRELLO G. & CERRANO C. 1998. Morphofunctional adaptations of three species of Spongia (Porifera, Demospongiae) from a mediterranean vertical cliff Bulletin of Marine Science, in press. PRONZATO R., CERRANO C., CUBEDDU T , LANZA S., MAGNINO G., MANCONI R., PANTELIS J., SARA' A. & SIDRI M. 1998. Sustainable development in coastal areas: role of sponge farming in integrated aquaculture. Aquaculture and water. fishculture, shellfish culture and water usage. Abstracts. EAS special publication. 26. 231)232. PRONZATO R. 1998. State of the art of sponge fishery, disease and farming in the Mediterranean Sea. Aquatic Conservation: in press. REISWIG H.M. 1971. Particle feeding in natural populations of three marine Demosponges. Biological Bulletin 141 : 568-591. REISWIG H.M 1974. Water transport, respiration and energetic of three tropical marine sponges. Journal of Experimental Marine Biology and Ecology 14: 231-249. REISWIG H.M. 1975. Bacteria as food for temperate water marine sponges. Canadian Journal of Zoology 53(5): 582-589.
RIZZITELLO R., CORRIERO G., SCALERA LIACI L., PRONZATO R. 1997 Estinzione e ricolonizzazione di Spongia offcinalis nello Stagnone di Marsala. Biologia Marina Mediterranea 4(1): 443-444. VERDENAL B., VACELET J. 1985. Sponge culture on vertical ropes in the northwestern Mediterranean sea. In: K. Rutzler (Ed.), New perspectives in Sponge Biology. Smithsonian Inst. Press, Washington D.C. 416-424. WU R.S.S. 1995. The environmental impact ofmarine fish sustainable future. Marine Pollution Bulletin 31: 159)166.
culture:
towards
a
Special thanks to Mr. Emanuele Bruzzone and Mr. Carlo Grattarola for their technical support. FIG. 1. the plant project in Kalymnos. FIG. 2: the horizontal structures moored to the bottom with fragments fixed onto.
FIG. 3. A, fragments of Hippospongia communis and B, Spongia offιcinalis just after transplantation: portions of the dark original external fibrous layer are maintained. C, particular of the thin cell layer after 24 hours in Hippospongia communis and, D, in Spongia offιcinalis. E, Spongia offιcinalis three weeks after transplantation: the characteristic dark pigmentation and the rounded shape have been restored. F, a dead specimen of Spongia officinalis. Death, that occurs mainly the first 48 hours after transplantation, has due to high sedimentation rates and bacterial attack.Marker bars: 1 cm. FIG. 4. The cicatrizating process of some species. Agelas oroides: A, the cut surface the day of transplantation and B, after three days when the exopinacoderm is completely restored. C, Axinella damicornis the first day and D, the third day. the external layer has not rebuilt. E, Petrosia fιciformis just after the cutting and F, after three days: the external cell layer is perfectly reconstructed. Marker bars: A, B, E, F. 100 blm; B: 10 blm; C: 1 mm. FIG. 5. The regenerative process of Spongia agaricina shows the recovering of a new fibrous layer on exposed spongin fibers (A); many globous moving cells occour on the sponge surface (B); elongated pseudopodia actively produce the collagene deposited on the sponge fibers (C); after few days the superficial fibrous layer is more or less completely restored (D). Scale bars: A: 1mm; B, C:100 μm; D. 10 μm.
