Suberites Aurantiaca</I>

BULLETIN OF MARINE SCIENCE, 75(3): 487–497, 2004

PERSISTENCE OF THE SPONGE SUBERITES AURANTIACA (DUCHASSAING AND MICHELOTTI, 1864) IN AN ESTUARINE ECOSYSTEM (PACIFIC COAST, MEXICO)

José Luis Carballo, Benjamín Yáñez, and Héctor Nava

Suberites aurantiaca (Duchassaing and Michelotti, 1864) is a common and abundant sponge in many shallow water estuaries along the Pacific coast of Mexico, yet little is known about its ecology. In this study, the temporal variation in abundance and biomass, and their relationship to several environmental factors, was measured in the Urías estuary (Mexico), from February 2002–October 2003, in an attempt to define aspects of the life history of this sponge. Although population size and biomass varied considerably over time, from 35–96 ind 75 m−2; and from 13.3–30 g wet weight m−2 on average, S. aurantiaca was a permanent species in the Urías estuary. The mean abundance increased progressively from spring to summer, and decreased from autumn to winter in both years, but true seasonality was not evident, suggesting the influence of local factors on the population dynamics of this species. The persistence of S. aurantiaca may be due to its tolerance to a highly fluctuating environment (water temperature ranged from 17–33 −1 ºC, dissolved oxygen from 2–5.4 mg 02 L , salinity from 33–38, and pH from 6.9–8), and resistance to desiccation. Experimental results demonstrated that S. aurantiaca can tolerate water loss > 20 %, and salinity in the interstitial water of 51.2. This study is among the first to characterize the environment affecting a sponge population in an estuarine environment. Estuaries are highly fluctuating environments characterized by ample tidal changes and highly variable salinity, water temperature, oxygen, and turbidity (Sfriso et al., 1988). They are also highly productive ecosystems that support numerous organisms adapted to this environment. Sponges are one of the major phyla found in the marine hard-substrate benthos (Sarà and Vacelet, 1973), and some species constitute important populations in estuaries. However, only a few studies of the life history of sponges inhabiting estuaries have been attempted (de Laubenfels, 1947; Hopkins, 1956; Wells, 1959; Wells et al., 1964; Fell, 1978; Fell and Lewandrowski, 1981; Fell et al., 1984). The sponge Suberites aurantiaca (Duchassaing and Michelotti 1864), a species dis- tributed along both the eastern Pacific and western Atlantic coasts (Rützler and Smith, 1993), is one of the most typical components of shallow water estuaries and harbors along the Pacific Mexican coast. Despite its ubiquity, nothing is known about its abundance, biomass, or the role it plays in these ecosystems. The Urías estuary is an internal coastal lagoon that is permanently connected to the ocean via a wide mouth. This ecosystem is exposed to human activity, which causes an over-enrichment of anthropogenic nutrients, altering its properties and functions (Páez-Osuna et al., 1998). Previous studies have shown elevated levels of contaminants in sediment, waters, and biota in this area (Páez-Osuna and Marmolejo-Rivas, 1990). Recently, it was suggested that pollution from the estuary coupled with natural stress due to the highly contrasting seasons, has had severe consequences on the algal (Ochoa-Izaguirre et al., 2002) and polychaete communities (Méndez, 2002). In this estuary, only a few sponge species occur, and some of them, such as S. aurantiaca, are periodically exposed during low tides. The high abundance of S. aurantiaca may be partly due to their relative tolerance to these fluctuating and stressful environments (pers. obs). In the present study, we studied the

Figure 1. (A) Distribution of Suberites aurantiaca in the Paciﬁc Mexican coast (black points). (B) Location of study area showing the sampling stations 1 and 2 at Urías estuary (C). variation in the abundance and biomass of S. aurantiaca over time, together with the ﬂuctuation in several environmental parameters. In addition, we examined the sponge’s tolerance to desiccation when it is exposed to air.

Material and Methods

Study Area and Meteorological Conditions.—The study area is located along the south- east coast of the Gulf of California and includes the lagoon system known as Estero de Urías between 23º 10′ 36″ and 23º 13′ 00″ N and 106º 20′ 00″ and 106º 25′ 35″ W (Fig. 1). Estero de Urías is 17 km long and has a surface area of 18 km2, connecting to the ocean via a wide mouth. There is no continuous supply of fresh water, and physical-chemical characteristics are highly influenced by the contrasting weather in this region where there are distinct rainy (July–October) and drought (November–June) seasons. This body of water can be considered estuarine during the rainy season and anti-estuarine in the drought season (Pritchard, 1967). Moreover, the estuary is exposed to intensive human activity (harbors, fishing fleet, urban waste, thermoelectrical power plant, and fishing industries), which produce great quantities of organic waste (Ochoa-Izaguirre et al., 2002). The estuary consists mainly of soft bottoms, but the margin of most of the estuary is surrounded by manmade piles of rocks of different diameters, and multiple harbor buildings. Most of these rocky substrates are fully covered with silt. There are several patches of mangroves and small sand-mud beaches in the upper part of the estuary. The tides are mixed semidiurnal, and the maximum range > 1.4 m. NOTES 489

Sampling Procedure.—Preliminary SCUBA dives were undertaken to identify the broad distributions of S. aurantiaca in the Urías estuary. After locating the main populations, two replicate sampling stations with similar hard-bottom substrates and depths (2–4 m depth) were selected (Fig. 1). The artificial rocks in this zone form a gently sloping platform from the surface to the bottom at a depth of 6 m. Abundance estimations were made monthly at each of the two sampling stations from February 2002–October 2003. A permanent 50 m transect was established at each of the stations, running parallel to the margin and at 1–3 m depth. To assess the abundance, a 1.5 m bar was moved along the transect line and all the individuals observed within the area were counted. An individual was defined as being any sponge growing independently (without contact) of its neighbors. The total area sampled monthly in each sampling station was 75 m2 (50 m long × 1.5 m width), thus abundance was expressed as individual sponges 75 m−2. Two additional transects in a neighbor- ing area were used to estimate the biomass and the volume of S. aurantiaca. Sampling for these estimates was undertaken only twice each year (March and July) so as not to reduce the natural population. Biomass was estimated by collecting all sponges found inside an aluminum frame of 1 m2 (1 × 1 m), placed every 2 m along 20 m transect lines (total surface sampled 10 m2). In the laboratory wet weight (g) was determined using an analytical scale, and the biomass calculated as g wet weight m−2. Volume was estimated by fluid displacement (Rützler, 1978), and the relationship between wet weight and volume were fitted by linear regression analysis. Environmental Variables.—We recorded the oxygen concentration, salinity, pH, and water temperature in an area located between the two transects on a monthly basis using a Hydrolab Datasonde Multiprobe. The Hydrolab was suspended approximately 1 m above the bottom, and calibrated against standards several times during the study. Water temperature was measured with a maximum/minimum thermometer permanently placed at a depth of 5 m on the seafloor. Rainfall data were provided by the National Water Commission. Spearman rank correlation was used to assess relationship between sponge abundance and environmental variables. Resistance to Desiccation.—To determine resistance to desiccation, 45 specimens of S. aurantiaca of similar size were collected from the Urías estuary in the vicinity of the Instituto of Ciencias del Mar and Limnología, and moved to small seawater tanks at the Institute. The sponges were continually submerged, supplied with changes of seawater, and shaded while in transit to the laboratory. Groups of five specimens were exposed to air to determine water loss rates for 0 hrs (control), 1, 2, 3, 4, 5, 6, 7, and 8 hrs. This procedure allowed rigorous control of exposure time. These time periods were selected on the basis of previous observations indicating that S. aurantiaca can survive at least 5 hrs emerged (unpubl. data). The specimens were suspended in the open shade (air flow, 0–1.8 ms−1; relative humidity, 69%). The initial (after quick external blot with tissue paper) and final wet weight (to 0.001 g) after the different treatments was calculated between 1000 and 1200 hrs. The difference between both weights was used to determine water loss over time. Salinity in the interstitial water retained by the sponge was also measured in five replicates with a refractometer.

Description and Distribution

Suberites aurantiaca (Duchassaing and Michelotti, 1864)

Suberites aurantiaca (Duchassaing and Michelotti 1864), Terpios aurantiaca Duchassaing and Michelotti, 1864; Laxosuberites zeteki de Laubenfels, 1936; Terpios zeteki (de Laubenfels, 1936).

Material Examined.—Laxosuberites zeteki de Laubenfels, 1936; Holotype USNM 22212, from Balboa, Paciﬁc coast of Panama, Suberites gadus de Laubenfels, 1926 Ho- lotype USNM 21489, and diverse material from the Mexican Paciﬁc coast. 490 BULLETIN OF MARINE SCIENCE, VOL. 75, NO. 3, 2004

Description of Mexican Material.—Suberites aurantiaca is a very distinctively marked massive sponge which can be very large. It can occasionally grow vertically with digitate projections emerging from an encrusting base, with branches up to 1–4 cm long, which can coalesce in part of their length. The maximum height measured was 15 cm with up to 14 × 18 cm in coverage. Encrusting and cushion-shaped specimens (1–4 mm thick) were found which were interpreted as juvenile forms. The color of live sponges is quite variable: specimens are ochre-yellow or ochre-yellow tinged with greenish or reddish color. Some specimens have crimson color on the tips of branches that turns to orange in the rest of the body. The sponge is relatively soft, and the surface is almost smooth, but frequently the top parts of the sponge are slightly verrucose. The oscules are contractile (0.5–1.5 mm in diameter). Spicule armament consists of tylostyles with well-formed heads (sometimes slightly subterminal), which can be separated in two size classes. The larger class measures 700 × 14 µm on average (head 12.5 µm), and the smaller class measures 200 × 4.5 µm on average (head 6 µm). In the specimens with digitate projections the skeletal arrangement is an axial condensation of reticulate tracks (30–150 µm wide), linked by spongin. The extra-axial skeleton is composed of radial tracks with perpendicular ectosomal brushes of small tylostyles sometimes pro- truding from the sponge surface. In the encrusting forms the skeletons consist of a dense structure, formed by bundles of tylostyles arranged in confused or ill defined bundles of spicules. Distribution.—An intensive survey carried out along the Pacific Mexican coast during the last 6 yrs determined that S. aurantiaca is one of the most typical sponges living in inner shallow estuaries and semi-enclosed bays. The species was found exclusively in these habitats, and despite numerous dives along the open coast, S. aurantiaca was found only once outside this typical habitat. So far, it has been found in the states of Sinaloa, Nayarit, Jalisco, Colima, and Baja California (Fig. 1). Environment.—The natural environment of the Urías estuary fluctuates throughout the year, during contrasting drought and rainy seasons. Salinity and water temperature varies accordingly. (Fig. 2). Although these values represent one observation per month, they are considered fairly representative of conditions in the estuary. Thus, the highest measures of salinity occurred from February–May (38), and the minimum from June–September (33; Fig. 2). Water temperature also fluctuated from 17 ºC in February to 33ºC in August 2003, reflecting seasonal changes (Fig. 2). Other variables, such as the dissolved oxygen and pH, did not have a clear seasonal pattern: dissolved oxygen values −1 −1 varied from 2 mg 02 L in April 2002, to 5.3 mg 02 L in July 2003, and pH ranged from 6.9–8 (Fig. 2). Abundance and Biomass.—In the course of this study large fluctuations in abundance were apparent through time, including an abrupt change in abundance between February and March 2003 when the number of individuals decreased by 67.5%, and overall higher abundance and biomass in 2002 than during the same months in 2003 (Fig. 3). In 2002, the highest mean abundance (96 ind 75 m−2) was detected in summer and early autumn, with the minimum values occurring in early spring (70 ind 75 m−2) and winter (67 ind 75 m−2; Fig. 3). The increase in the mean abundance from spring to summer did not represent an increase in the biomass or volume. In fact, both stayed almost constant over time, ranging between 29.5–27.5 g m−2 and 31–34 ml m−2, respectively (Fig. 3). The same tendency (peak in summer–early autumn) was detected in 2003, but in summer 2003 the mean abundance (37.5–45.5 ind 75 m−2) was lower than in 2002 (90–96.5 ind 75 m−2). In March 2003 a marked decline in population was detected (from NOTES 491

Figure 2. (A) Maximum (black circles) and minimum (white circles) water temperature over time, (B) Monthly precipitation (black circles, left axis) and salinity (white circles, right axis) over time, and (C) Monthly dissolved oxygen (black circles, left axis) and pH (white circles, right axis) over time. Data from October were not available. 74–40 ind 75 m−2; Fig. 3), and the biomass and the volume m−2 were also affected. The biomass ranged between 13.3– 15.2 g m−2, which represented a loss of 43–55% with re- spect to the previous year, and the volume varied between 11.9–12.5 ml m−2; a decrease of 61–63%. 492 BULLETIN OF MARINE SCIENCE, VOL. 75, NO. 3, 2004

Figure 3. Variation in the mean abundance (lines, left axis) and biomass (bars, right axis) of Su- berites aurantiaca over time. Vertical lines indicate standard error. The trend in the patterns of sponge abundance was similar to that of pH (Fig. 2), while the decrease in mean sponge abundance occurred with an abrupt drop in the water temperature during February–March 2003 (from 24–17 ºC). The abundance following this time period did not return to high levels. A signiﬁcant linear relationship was found between wet weight and volume per individual, which may be useful in future studies to estimate the biomass of the population (Fig. 4). Effects of Exposure to Air.—Field observations have shown that the low tides usually result in prolonged exposures of up to 5 hrs for S. aurantiaca. The effect of exposure to air was measured as water loss and as increase in the salinity of interstitial water through time (Fig. 5). Water loss increased constantly from 5% after 1 hr of exposure, to 33% after 8 hrs. A similar effect was observed in the salinity of the interstitial water retained by S. aurantiaca, which rose from 39 (control specimens that were never exposed to air), to 57 by the end of the study 8 hrs later. A typical in situ exposure time of 5 hrs is equivalent to a loss of interstitial water of more than 20% and an increase in the salinity of up to 51.2.

Discussion

The assessment and monitoring of sponge populations through the number of individuals alone has been claimed to be an unstable measure that does not reﬂect the number of larval recruitment events (Wulff, 2001). Natural fragmentation and the process of ﬁssion and fusion would also cause changes in abundance that are not linked to the mortality of adults and recruitment of juveniles (Wulff, 1985). However, S. aurantiaca NOTES 493

Figure 4. Relationship between wet weight and volume for Suberites aurantiaca from the Paciﬁc Mexican Coast.

does not seem to be susceptible to these processes, and no unattached fragments of this species were ever observed in the course of this study. Thus, the changes in the sponge abundance probably reﬂect important ecological events for this species: mortality of adult sponges and variation in the number and survival of sexual recruits produced by larval settlement. The highest abundances (and biomass) of some sponge populations generally occur during the highest water temperatures (Rader and Winget, 1985; Barthel, 1991; Meroz and IIan, 1995; Turon et al., 1998), and sponges in the Urías estuary appear to follow this pattern: the abundance increased progressively from spring to summer, and decreased

Figure 5. Water loss (solid bars, left axis), and salinity increase in interstitial water (white bars, right axis) of Suberites aurantiaca over time. Vertical lines indicate standard error. The shad- owed area is the maximum time S. aurantiaca has been observed emerged in the study area. 494 BULLETIN OF MARINE SCIENCE, VOL. 75, NO. 3, 2004

from autumn to winter in both years. Biomass and volume did not change from spring to summer 2002 even when abundance did. This suggests a shift in the size-frequency distribution of the population probably due to the fact that the changes in sponge volume and the biomass reflected growth more than recruitment. In 2003, the abundance of S. aurantiaca abruptly dropped from February–March when water temperature dropped drastically. This decrease of 7ºC in such a short period of time could have caused a change in the dynamics of S. aurantiaca during 2003. A similar tendency was shown in Halichondria sp. In New England, whose peak in the standing stock biomass during July and early August was followed by a rapid decline of the population (Fell and Lewandroski, 1983). In contrast, Halichondria sp. in the Mystic, Connecticut estuary (Fell and Lewandrowski, 1981), and Halichondria bowerbanki Burton, 1930 at Hatteras Harbor, North Carolina, experienced the highest mortality when water temperatures ap- proached 30ºC during mid-summer (Wells et al., 1964). However, true seasonality was not evident in the dynamics of S. aurantiaca, and high variability in the abundance, especially during autumn 2003, suggests that sponge population dynamics cannot be explained by simple environmental factors alone such as variations in water temperature. Estuaries are also characterized by having fluctuations in salinity following major storms. The influence of the salinity in marine sponges has been documented in a few cases that show that some marine sponges, particularly clion- aids, can live in a salinity of 1.5–2.0, and can recover from several days of exposure to salinities as low as 1 (Hopkins, 1956; Hartman, 1958). The use of free amino acids has been suggested for osmotic compensation in the sponge Microciona prolifera (Ellis and Solander, 1786) (Knight et al., 1992), which occurs naturally in salinities ranging from 7–38 (de Laubenfels, 1947). During the drought season in the Urías estuary, salinities were frequently higher than in the rainy season, but the salinity in our study area did not vary much (33–38), due to the proximity of the mouth of the estuary to the open ocean. Thus this factor probably did not influence the dynamics of S. aurantiaca. Dissolved oxygen is another critical parameter in estuaries. Low levels of oxygen, produced by excessive decomposition of organic matter or by oxygen-consuming chemical wastes, can cause the death of marine organisms (Díaz and Rosenberg, 1995). Con- centrations in the water column of 2 mg L−1 or lower are considered hypoxic and often have deleterious effects on animals (Tyson and Pearson, 1991). In estuaries, hypoxic dis- turbances increase the mortality of epifaunal species living in clumps such as sponges (Stachowitsch, 1984), but our results indicated that S. aurantiaca lives in a range from −1 2–5 mg 02 L , suggesting that it is tolerant of low levels of oxygen. Tolerance to low levels of oxygen by many invertebrate groups such as sponges is unknown; perhaps they can reduce their metabolism during short periods, and recover when oxygen increases (Hochachka and Somero, 1984). Suberites aurantiaca may survive in this environment because low oxygen concentrations are only experienced during short periods of time. pH was the only variable that was roughly correlated with the variation in sponge abundance (R = 0.79, P < 0.0001). As a measure of water acidity, low pH can indicate excessive acidity produced by decomposition of organic matter or industrial wastes. The pH of marine waters is ~8.2, whereas most natural freshwaters have pH values from 6.5–8.0 (Sammut, et al., 1995; Hinga, 2002). The Urías estuary serves as a harbor and waterway to urban and industrial centers, thus lower pH (from 6.9–8) may reflect anthropogenic activities, which may have influenced the dynamics of this species. Estuaries are also characterized by large tidal changes, and sponges generally are not considered resistant to air exposure during low tide (Rützler, 1995). Field observations NOTES 495

have shown that S. aurantiaca can survive exposures of up to 5 hrs, corresponding to a water loss of 20 %. A similar effect was observed in the salinity of the interstitial water retained, which rose from 39–51.2. These data agree with those of Rützler (1995), which suggest that the loss of water by evaporation in some sponges is probably higher than the loss by drainage. However, this species seems more tolerant than those studied by Rützler (1995) in a mangrove community, which resulted in some tissue loss after 4 hrs of exposure, and almost 50% loss after exposures of 6 hrs. The influence of biotic factors such as predation on the dynamics of S. aurantiaca could also be important. The sponge is free of epibiotic fouling, suggesting the presence of inhibitory chemicals, but at least two different groups of predators (two species of angelfishes and a sea urchin) have been identified in the same environment where the sponge lives. Preliminary results (stomach contents analyses) show that these predators consume S. aurantiaca among other sponges (Camacho-Cruz, 2004). The occurrence of these predators could provoke short-term changes in the dynamics of this species, however, without additional data, this is only speculative. There is not much data on the biomass of sponges in the eastern tropical Pacific. The values obtained for S. aurantiaca for biomass (13.3–30 g wet weight m−2) and volume (11.9–34 ml m−2), are lower than those obtained for the association Haliclona caerulea (Hechtel, 1965)/Jania adherens Lamouroux, 1812, which ranged from 11.5–93.4 g wet weight m−2 and from 29.6–289 ml m−2 respectively, through a similar period of time (Avila and Carballo, 2004). Both of these sponges, H. caerulea and S. aurantiaca, are two of the most important species in terms of permanence, distribution, abundance, and biomass in the benthic communities from the Bay of Mazatlán (open water environment) and the Urías estuary, respectively. In summary S. aurantiaca is an important component of the biomass of the estuarine environs in the Mexican Pacific coast. This sponge appears to be confined to shallow water estuarine environs along the Pacific coast of Mexico, and the population in the Urías estuary is persistent over time. The persistence of S. aurantiaca seems to be in part due to their tolerance to contamination and other natural stressors, including their resistance to desiccation. It is possible that a “multixenobiotic resistance pump” that acts to protect the sponge against pollution by extruding potential toxicants from cells (Mül- ler et al., 1996) is present in S. aurantiaca.

Acknowledgements

The authors are indebted to K. Rützler and J. Clark from the Smithsonian Institution for the loan of the holotypes of Laxosuberites zeketi USNM 22212 and Suberites gadus USNM 21489. The authors also wish to express their gratitude to C. Ramirez Jáuregui, P. Allende and V. Montes (ICML-UNAM) for generous help with the literature and aerial images of the Urías estuary, and to G. Ramirez Reséndiz and C. Suarez (ICML-UNAM) for their computer assistance. The assistance of J. Toto Fiscal during ﬁeld sampling is greatly appreciated. The study was funded in part by the projects “ Biodiversidad de esponjas del Mar de Cortés: bases para su conservación y valoración como recursos marinos,” convenio número FB666/S019/99, and “Actualización e incorporación de nuevos registros a la fauna de esponjas del litoral Paciﬁco de México,” convenio número FB789/AA004/02, both funded by CONABIO (National Commission for Biodiversity Research). This work was supported in part by a grant from the Consejo Estatal de Ciencia y Tecnología del Gobierno de Sinaloa to BY and HN. 496 BULLETIN OF MARINE SCIENCE, VOL. 75, NO. 3, 2004

Literature Cited

Ávila, E. and J. L. Carballo. 2004. Growth and standing stock biomass of a mutualistic association between the sponge Haliclona caerulea and the red algae Jania adherens. Symbiosis 36: 225–243. Barthel, D. 1991. Population dynamics of the sponge Halichondria panicea (Pallas) in Kiel Bight. Pages 203–209 in G. Colombo et al., eds. Marine eutrophication and population dynamics. Olsen and Olsen Fredensborg, Denmark. Camacho-Cruz, L. 2004. Estudio preliminar de la composición faunística de depredadores de esponjas en la bahía de Mazatlán (Sinaloa). Tesis de Licenciatura, UAS, (Mexico), 53 p. de Laubenfels, M. W. 1947. Ecology of the sponges of a brackish water environment at Beaufort, N.C. Ecol. Monograph 17: 31–46. Díaz, R. J. and R. Rosenberg. 1995. Marine benthic hypoxia: A review of its ecological effects and the behavioral responses of benthic macrofauna. Oceanogr. Mar. Biol. 33: 245–303. Fell, P. E. 1978. Variation in the time of annual degeneration of the estuarine sponge, Haliclona loosanoffi. Estuaries 1: 261–264. ______and K. B. Lewandrowski. 1981. Population dynamics of the estuarine sponge, Hali- chondria sp. within a New England eelgrass community. J. Exp. Mar. Biol. Ecol. 55: 49–63. ______and ______. 1983. Seasonal fluctuations in standing stock biomass of Hali- chondria sp. (Porifera: Demospongia) within a New England eelgrass community. J. Exp. Mar. Biol. Ecol. 66: 11–23. ______, E. H. Parry, and A. M. Balsamo. 1984. The life histories of sponges in the Mystic and Thames estuaries (Connecticut) with emphasis on larval settlement and postlarval reproduc- tion. J. Exp. Mar. Biol. Ecol. 78: 127–144. Hartman, W. D. 1958. Natural history of the marine sponges of southern New England. Bull. Pea- body Mus. Nat. Hist. 12: 1–155. Hinga, K. R. 2002. Effects of pH on coastal marine phytoplankton, Mar. Ecol. Prog. Ser. 238: 281–300. Hochachka, P. W. and G. N. Somero. 1984. Biochemical adaptation. Princeton University Press, Princeton. 537 p. Hopkins, S. H. 1956. Notes on the boring sponges in Gulf Coast estuaries and their relation to salinity. Bull. Mar. Sci. Gulf Caribb., 6: 44–58. Knight, P. A., S. H Loomis, and P. E. Fell. 1992. The use of free amino acids compensation by euryhaline sponge Microciona prolifera (Ellis & Solander). J. Exp. Mar. Biol. Ecol. 163: 111– 123. Méndez, N. 2002. Annelid assemblage in soft bottoms subjected to human impact in the Urías estuary (Sinaloa, México). Oceanologica Acta: 139–147. Meroz, E. and M. Ilan. 1995. Life history characteristics of a coral reef sponge. Mar. Biol. 124: 443–451. Muller, W. E. G., R. Steffen, B. Rinkevich, V. Matranga, and B. Kurelec. 1996. The multixenobiotic resistance mechanism in the marine sponge Suberites domuncula; its potential applicability for the evaluation of environmental pollution by toxic compounds. Mar. Biol. 125: 165–170. Ochoa-Izaguirre, M. J., J. L. Carballo, and F. Páez-Osuna. 2002. Qualitative changes in macroal- gae assemblages under two contrasting climatic conditions in a subtropical estuary. Bot. Mar. 45: 130–138. Páez-Osuna, F. and C. Marmolejo-Rivas. 1990. Occurrence and seasonal variation of heavy metals in the oyster Saccostrea iridescens. Bull. Environ. Cont. Tox. 44: 129–134. ______, H. Bojórquez-Leyva, and C. R. Green-Ruíz. 1998. Total carbohydrate: organic carbon ratio in lagoon sediments as an indicator of organic effluents from agriculture and sugar-cane industry. Environ. Poll. 102: 321–326. Pritchard, D. W. 1967. What is an estuary: Physical viewpoint? Pages 3–5 in G. Lauff, ed. Estuar- ies, Pub. 83. American Association for the Advancement of Science, Washington, D.C. NOTES 497

Rader, R. B. and R. N. Winget. 1985. Seasonal growth rate and population dynamics of a freshwa- ter sponge. Hydrobiologia 123: 171–176. Rützler, K. 1978. Sponges in coral reefs. Pages 299–314 in D.R. Stoddart and R.E. Johannes eds. Coral reefs: research methods. Monographs on oceanographic methodology 5. UNESCO, Paris. ______. 1995. Low-tide exposure of sponges in a Caribbean mangrove community. P.S.Z.N.I: Mar. Ecol. 16: 165–179. ______and K. P. Smith. 1993. The genus Terpios (Suberitidae) a new species in the “Lobi- ceps” complex. Pages 381–393 in M.J. Uriz and K. Rützler eds. Recent advances in ecology and systematics of sponges. Sci. Mar. 57. Sammut, J., M. D. Melville, R. B. Callinan, and G. C. Fraser. 1995. Estuarine acidiﬁcation: Im- pacts on aquatic biota of draining acid sulphate soils. Aust. Geograph. Stud. 33: 89–100. Sarà, M. and J. Vacelet. 1973. Écologie des Démosponges. Pages 463–516 in Traité de Zoologie, Anatomie, Systematique, Biologie, Masson et Cie, Paris. Sfriso, A., B. Pavoni, A. Marcomini, and A. Orio. 1988. Annual variations of nutrients in the La- goon of Venice. Mar. Poll. Bull. 19: 54–60. Stachowitsch, M. 1984. Mass mortality in the Gulf of Trieste: the course of community destruc- tion. P.S.Z.N.I. Mar. Ecol. 5: 243–264. Turon, X., I. Tarjuelo, and M. J. Uriz. 1998. Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defense. Funct. Ecol. 12: 631–639. Tyson, R. V. and T. H. Pearson. 1991. Modern and ancient continental shelf anoxia: An overview. Pages 1–26 in R.V. Tyson and T.H. Pearson eds. Modern and ancient continental shelf anoxia. Geological Society Special Publication Nº 58, London. Wells, H. W. 1959. Boring sponges (Clionidae) of Newport River, North Carolina. J. Elisha Mitch- ell Sci. Soc. 75: 168–175. ______, M. J. Well, and I. E. Gray. 1964. Ecology of sponges in Hatteras Harbor, North Carolina. Ecology 45: 752–767. Wulff, J. L. 1985. Dispersal and survival of fragments of coral reef sponges. Pages 119–124 in Proceedings of the 5th Intl. Coral Reef Symp., Tahiti, vol 5. ______. 1997. Causes and consequences of differences in sponge diversity and abundance between the Caribbean and eastern Paciﬁc of Panama. Pages 1377–1382 in Proc. 8th Intl. Coral Reef Sym., vol 2. ______. 2001. Assessing and monitoring coral reef sponges: Why and how? Bull. Mar. Sci. 69: 831–846.

Date Submitted: 29 August, 2003. Date Accepted: 12 April, 2004.

Address: Laboratorio de Ecología del Bentos. Instituto de Ciencias del Mar y Limnología. Universidad Nacional Autónoma de México, Apartado Postal 811, Mazatlán 82000, Mexico. Corresponding Author: (J.L.C.) E-mail: . FAX: +52-669- 9826133.