MARINE ECOLOGY PROGRESS SERIES Vol. 135: 109-122, 1996 Published May 17 ' Mar Ecol Prog Ser 1 Use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula) J. L. Carballo*, S. A. Naranjo, J. C. Garcia-Gomez Laboratorio de Biologia Marina, Dpto de Fisiologia y Biologia Animal, Facultad de Biologia, Apdo 1095, E-41080 Sevilla, Spain ABSTRACT Infrallttoral sponge fauna was studied as part of a multidisciplinary investigation of ben- thic communities in Algeciras Bay On a monthly basis over 1 year, a senes of environmental vanables were measured (hydrodynamlsm, silting, suspended solids, dissolved organic matter % orgamc matter In silt) The only abiotic vanable that was significantly correlated wlth beta diversity was hydrody- namism, with a linear iegression model between the 2 variables showing a correlatlon coefficient of 0 66 The distributional pattern of the sponges (based on the relative abundance matrix) was correlated with the environmental vanables by matchlng sample simllanties uslng the Spearman rank correlatlon thus showing that the variable combination that best explalns the patterns of distribution is hydrody- namlsm/organlc matter ~n silt (p, = 0 6) Of the species considered, Phorbas fictit~us,Cliona celata, Cl~onav~ndis, Crella elegans. Oscarelld lobular~s,Dysidea fragilis were among those show~ngthe greatest adaptive plast~cityin their relatlonshlp to environmental variables, depth, and selection by substrate, and are categorized as eurytoplc specles present in areas subject to great environmental stress Other species such as Phorbas tenacior, Ren~erafulva Renjera mucosa Cliona rhodensis proved to be much more sensitive to these vanables and were categonzed as stenotop~cspecies lndi- cators of normal conditions Due to the part~cularenvironmental cond~tionswhere it is located, A4ycale rnicracanthoxea was categonzed as a good ind~catorspecies in port environments Others such as Dysidea avara, Halichondna bower bank^ 01 Crella elegans presented morphological differentiations which have permitted them to adapt to sedimentary environments KEY WORDS. Sponge communit~es. Abiotic environment . Bioindicator species. Stress. Port environ- ments INTRODUCTION rera 1987, Muricy 1989, 1991, Carballo et al. 1994). There is now widespread recognition that chemical Sponges are dominant members of many benthic monitoring alone is not enough and that pollution IS communities and, from the autoecological point of essentially a biological phenomenon because its im- view, individual sponge species can have very specific pact is on hving organisms (Mlright et al. 1994). Stress requirements for substrate quality, food particles, light, operates on individual organisms, but its effects may current regime (Reiswig 1971, Wilkinson & Vacelet be recognised at population and ecosystem levels. 1979). Moreover, sponges are strongly associated with Stress induces qualitative and quantitative changes in the abiotic environment and are therefore very sensi- the structure of communities which can usually be tive to environmental stress, which is why some assessed by analysing diversity, relative abundance authors have suggested them as useful tools for envi- (Hawkins et al. 1994). ronmental monitoring (Alcolado 1978, Alcolado & Her- Sponge communities can provide us with important information about the temporal behaviour of the abi- otic factors which affect them; hence, it is feasible to interpret the environment by studying this ecological O Inter-Research 1996 Resale of full article not permitted Mar Ecol Prog Ser 135: 109-122, 1996 structure (Alcolado & Herrera 1987).However, the use codes which permitted us to objectively compare the of sponges in monitoring studies is still limited by the information obtained at the various sampling stations little knowledge available on biotic and abiotic factors (Table 1). Coding usually tends to have the effect of affecting the structure of these communities. normalising data, and subsequent transformation is Algeciras Bay, Spain, is characterised by a great then unnecessary (Field et al. 1982). patchwork of small homogeneous environments, and In order to monitor water quality we analysed hydro- along its 30 km coastline there are important industrial dynamism, dissolved organic matter, suspended solids, areas with chemical industries, refineries, thermal silting and % organlc matter in the silt gathered in col- power plants, ironworks, paper mills, and shipyards, lecting bottles (SOM]. These parameters were mea- along with a major port. All of this activity may in some sured on a monthly basis for l yr at 8 of the 12 stations. way influence the sessile benthic organisms found in To measure silting and hydrodynamism a set of bot- the bay. The amount of urban sewage corresponds to a tom-mounted frames was placed along the Algeciras population of approximately 205000 inhabitants; in- Bay littoral, each one having 6 sediment collecting bot- dustrial contamination corresponds to 150000 inhabi- tles (Moore 1972), which remained for a month at each tants (Wait et al. 1990). Into the bay's center flow 2 sampling station (Carballo et al. 1994). To estimate the rivers, the Palmones and the Guadarranque, each with water movement we used the method of plaster disso- an amount of sewage corresponding to 15000 inhabi- lution described by Gambi et al. (1989). The hydrody- tants, and industrial contamination corresponding to namism was calculated in water speed equivalents (V) 15000 inhabitants for the former and 2500 for the latter according to the formula suggested by Bailey-Brock (Wait et al. 1990). (1979).The suspended solids, dissolved organic matter The composition and abundance of the benthic com- and SOM (silt which remained in the sediment traps) munities situated in Algeciras Bay are conditioned by were measured using methods described by Strickland their level of adaptation to general environmental & Parsons (1960).All environmental variables were log factors and to factors of a more local character, such transformed to normality, the latter confirmed by as organic material, contamination, and deep water means of a chi-squared test. movement. These physico-chemical factors generally Similarities among the sampling stations were estab- have a great influence on the distribution of the major- lished by means of a classification analysis, using as ity of filtering sessile invertebrates. In this sense, we variables the species present in the established zones. have related the distnbution patterns of sponges to a The similarity matrix for the classification was calcu- series of abiotic variables (water movement, sus- lated by means of the Bray-Curtis index (Bray & Curtis pended solids), which are considered by the majority 1957). This index was chosen as it does not consider of authors as responsible, along with a series of other biotic factors (type of substrate, epibiotic relationships, symbiosis, etc.), for the presence/absence of a species in a given habitat (Sara & Vacelet 1973, Wilkinson & Cheshire 1989). MATERIAL AND METHODS The sampling stations inside Algeciras Bay were cho- sen on the basis of the heterogeneity of the environ- ment at depths between 5 and 30 m. In this way, sta- tions were set up at the main port constructions, .,,,,,,-, shipyards, piers, natural rock formations, etc. Fig. 1 ,!?:E;=:) shows the various sampling areas. The specimens were D (R.&S-C-J E (%awld vrlfi~lr& collected by SCUBA diving along permanent transects wide he pan d ,q~rru) D in order to ensure sampling reproducibility. Each tran- ~,~u~,~~~ioal,b,nhehmour R sect (approximately 50 m long) was sampled at least ~.dmd.lbrthrm~mpr~~) L ISaluml ad .ntTmrl nxks m rhr rd* hubour) 4 times a year with a similar immersion time at all the N (c,,, ~b,~, stations (there were no replicates on each occasion).All g :~~~y-&~"~&ludr~~,huhvhovl sponges sighted at a distance of 1 m at either side of the R Eu-) transects were collected and/or photographed. We _)B used semi-quantitative sampling, which is more appro- priate for our subject, and we established abundance Fig. 1. Locatlon of the sampling stations in the study area Carballo et al.. Marine sponges as stress indicators 111 double absences, frequently found in our data base, in its calculations. The results were then graphically de- scribed using dendrogranls with the UPGMA ('un- weighted pair-group method using centroids') aggre- gation algorithm (Sneath & Sokal 1973). The species mainly responsible for the dissimilarity between sam- pling stations were determined using the computer program SIMPER (Clarke 1993). The ordination analyses were carried out by means of an MDS ('non-metric multi-dimensional scaling pro- gram') based on the similarity matrix between stations. In order to individually relate environmental variables to sampling stations, the letters of the stations, propor- tional in size to the numerical value of each variable, were superimposed on a 2-dimensional MDS configu- Fig 2. Beta diversity (P,,) of sponge comlnunities at sampling ration to provide a 'visual correlation' (Field et al. Stns A to R 1982). In this manner we were able to study the influ- ence of different environmental variables on the vari- tion of the common species showed 3 basic distiibu- ous areas of study. In addition we carried out a factor- tional patterns: ial analysis in order to explore the relationship patterns - Species found throughout the Bay: Cliona celata, which group the various species together. Cliona viridis, Crambe crarnbe, Crella